Diagnosis and Treatment of Furcation‐Involved Teeth Diagnosis and Treatment of Furcation‐Involved Teeth
Edited by Luigi Nibali
Senior Clinical Lecturer Centre for Immunobiology and Regenerative Medicine Centre for Oral Clinical Research, Institute of Dentistry Barts and the London School of Medicine and Dentistry Queen Mary University of London (QMUL), London, UK Honorary Associate Professor, University of Hong Kong This edition first published 2018 © 2018 John Wiley & Sons Ltd
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Library of Congress Cataloging‐in‐Publication Data Names: Nibali, Luigi, 1978– editor. Title: Diagnosis and treatment of furcation-involved teeth / edited by Luigi Nibali. Description: Hoboken, NJ : Wiley, [2018] | Includes bibliographical references and index. | Identifiers: LCCN 2018010570 (print) | LCCN 2018011380 (ebook) | ISBN 9781119270669 (pdf) | ISBN 9781119270676 (epub) | ISBN 9781119270652 (hardback) Subjects: | MESH: Furcation Defects–diagnosis | Furcation Defects–therapy | Models, Animal Classification: LCC RK450.P4 (ebook) | LCC RK450.P4 (print) | NLM WU 242 | DDC 617.6/32–dc23 LC record available at https://lccn.loc.gov/2018010570 Cover image: (Main, top left and middle images) © Luigi Nibali; (Top right image) © Roberto Rotundo Cover design: Wiley
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Contents
List of Contributors vii Foreword ix Preface xi About the Companion Website xiii
1 Anatomy of Multi‐rooted Teeth and Aetiopathogenesis of the Furcation Defect 1 Bernadette Pretzl
2 Clinical and Radiographic Diagnosis and Epidemiology of Furcation Involvement 15 Peter Eickholz and Clemens Walter
3 How Good are We at Cleaning Furcations? Non‐surgical and Surgical Studies 33 Jia‐Hui Fu and Hom‐Lay Wang
4 Furcation: The Endodontist’s View 55 Federica Fonzar and Riccardo Fabian Fonzar
5 Why do We Really Care About Furcations? Long‐term Tooth Loss Data 91 Luigi Nibali
6 Regenerative Therapy of Furcation Involvements in Preclinical Models: What is Feasible? 105 Nikolaos Donos, Iro Palaska, Elena Calciolari, Yoshinori Shirakata, and Anton Sculean
7 Regenerative Therapy of Furcations in Human Clinical Studies: What has been Achieved So Far? 137 Søren Jepsen and Karin Jepsen
8 Furcation Therapy: Resective Approach and Restorative Options 161 Roberto Rotundo and Alberto Fonzar
9 Furcation Tunnelling 177 Stefan G. Rüdiger
10 Innovative and Adjunctive Furcation Therapy: Evidence of Success and Future Perspective 191 Luigi Nibali and Elena Calciolari
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11 Furcation: Why Bother? Treat the Tooth or Extract and Place an Implant? 209 Nikos Mardas and Stephen Barter
12 Is it Worth it? Health Economics of Furcation Involvement 229 Falk Schwendicke and Christian Graetz
13 Deep Gaps between the Roots of the Molars: A Patient’s Point of View 249 Luigi Nibali
14 Assessment of Two Example Cases Based on a Review of the Literature 257 Luigi Nibali
15 Furcations: A Treatment Algorithm 269 Luigi Nibali
Index 285 vii
List of Contributors
Dr Stephen Barter Dr Riccardo Fabian Fonzar Private practice, Eastbourne, UK Private practice Udine Dr Elena Calciolari Italy Centre for Immunobiology and Regenerative Medicine Dr Jia‐Hui Fu Centre for Oral Clinical Research Discipline of Periodontics Institute of Dentistry Faculty of Dentistry Barts and the London School of Medicine National University of Singapore and Dentistry Singapore Queen Mary University of London (QMUL) Dr Christian Graetz London, UK Clinic for Conservative Dentistry and Prof. Nikolaos Donos Periodontology Centre for Immunobiology and Regenerative Christian‐Albrechts‐University Medicine Kiel Centre for Oral Clinical Research Germany Institute of Dentistry Barts and the London School of Medicine Dr Karin Jepsen and Dentistry Department of Periodontology Queen Mary University of London (QMUL) Operative and Preventive Dentistry London, UK University of Bonn Prof. Peter Eickholz Germany Poliklinik für Parodontologie Prof. Søren Jepsen Zentrum der Zahn‐ Mund‐ und Department of Periodontology Kieferheilkunde (Carolinum) Operative and Preventive Dentistry Johann Wolfgang Goethe‐Universität University of Bonn Frankfurt Germany Frankfurt am Main Germany Dr Nikos Mardas Dr Federica Fonzar Centre for Immunobiology and Regenerative Medicine Private practice Centre for Oral Clinical Research Udine Institute of Dentistry Italy Barts and the London School of Medicine Dr Alberto Fonzar and Dentistry Private practice Queen Mary University of London (QMUL) Udine London Italy UK
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Dr Luigi Nibali Dr Falk Schwendicke Centre for Immunobiology and Regenerative Department of Operative and Preventive Medicine Dentistry Centre for Oral Clinical Research Charité‐Universitätsmedizin Berlin Institute of Dentistry Berlin Barts and the London School of Medicine Germany and Dentistry Queen Mary University of London (QMUL) Prof. Anton Sculean London Department of Periodontology UK School of Dental Medicine University of Bern Dr Iro Palaska Bern Centre for Immunobiology and Regenerative Switzerland Medicine Centre for Oral Clinical Research Dr Yoshinori Shirakata Institute of Dentistry Department of Periodontology Barts and the London School of Medicine Kagoshima and Dentistry University Graduate School of Medical and Queen Mary University of London (QMUL) Dental Sciences London Kagoshima UK Japan Dr Bernadette Pretzl Prof. Clemens Walter Section of Periodontology Klinik für Parodontologie Department of Operative Dentistry Endodontologie und Kariologie University Clinic Heidelberg Universitätszahnkliniken, Heidelberg Universitäres Zentrum für Germany Zahnmedizin Basel Dr Roberto Rotundo Basel Periodontology Unit Switzerland UCL Eastman Dental Institute Prof. Hom‐Lay Wang London UK Department of Periodontics and Oral Medicine Dr Stefan G. Rüdiger School of Dentistry Department of Periodontology University of Michigan Public Dental Service/Malmö University Ann Arbor Malmö MI Sweden USA ix
Foreword
The preservation of tissues and structures diagnosis and treatment, but includes valua- that support the dentition is a major goal of ble information from a health economics and conservative dentistry for the benefit of our treatment algorithms perspectives on long‐ patients. As dental practitioners, we are term tooth preservation. trained to maintain and restore function, In the first part of the book, a thorough aesthetics, and phonetics for the promotion background on the unique anatomy of multi‐ of oral health. In the development of this rooted teeth and corresponding diagnostic, book, Diagnosis and Treatment of Furcation‐ prognostic, and therapeutic intricacies is Involved Teeth, Luigi Nibali and his presented. The next section provides a strong co‐authors have assembled an excellent text rationale regarding the concept of tooth that comprehensively examines the manage- preservation from the restorative, periodon- ment of the most challenging‐to‐treat teeth tal, and endodontic perspectives, which in the jaws – the molar and premolar teeth highlights the strong evidence base of with furcation involvement. It is clear that treatment success of tooth furcations. This clinicians are continually tested on which are background is important to examine criti- the best approaches to handle these clinical cally, since many oral implantologists in the scenarios that include furcated teeth. The field are not adequately versed on the ramifi- education, skill, and training required to cations of premature tooth removal versus manage furcations are significant given the those teeth that can be predictably retained anatomy, location, and functional biome- for the long‐term success of the patient. The chanical occlusal forces associated with application in clinical practice by those with- posterior teeth that make for complex clinic al out adequate training occasionally errs on decision‐making. the expedience of tooth extraction, without In this text, Dr Nibali has convened inter- pausing to weigh methodically the advan- national experts providing chapters ranging tages and disadvantages of embarking on from the diagnosis of disease to clinical out- comprehensive therapy for furcated teeth. comes from the health policy expert’s, cari- Those without access to this text on the many ologist’s, periodontist’s, and endodontist’s options available to increase the lifespan of perspectives on periodontal‐endodontic‐ molar and premolar teeth may not be pre- restorative dilemmas in patient care. It is pared to treatment plan the complex dental important to recognize that there is a large patient appropriately for the comprehensive evidence base that was initiated from the assessment of restorative, periodontal, endo- ‘pre–dental implant era’ on the long‐term dontic, functional, and aesthetic needs. success in the maintenance of compromised Given practice trends of more common teeth affected by extensive restorative care, extractions of furcated periodontally and periodontal involvement, and/or pulpal endodontically compromised teeth, it sug- pathology. This text not only focuses on gests that ‘the time is right’ to emphasize the
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great potential available in the proper assess- of peri‐implant biological complications in ment and treatment of furcated teeth. This the molar regions, we should re‐examine the section highlights the long‐term success with opportunities for maintaining and treating proper therapy in maintaining furcated teeth. furcated teeth more diligently and more fully. The next part of the text highlights the many The concluding chapters scrutinize the health different therapeutic modalities that are clini- economics opportunities at the patient and cally available to treat multi‐rooted teeth, clinician levels in terms of tooth preservation including non‐surgical maintenance, resective of furcated molars, and in which types of cases procedures (including tunnelling, root resec- which treatment planning approach is indi- tion, and bicuspidization), and reconstructive cated for such advanced clinical scenarios. regenerative therapy using biologics or bioma- Stimulated by the comprehensive approach terials. Other chapters in the book build on in this book, this can be a renaissance period our existing evidence base to examine the in reconstructive dentistry when we firmly cases that can genuinely be retained versus consider the many options available to us as those teeth too compromised as ‘hopeless’ clinicians to better preserve the dentition in that may benefit from extraction, implant site treating furcation‐involved teeth. This text development (bone grafting and alveolar ridge lays out a contemporary and exciting oppor- preservation), followed by dental implant tunity for us as clinicians to provide our reconstruction. Indeed, dental implant ther- patients with state‐of‐the‐art therapy for the apy has revolutionized oral care and clinical betterment of oral health! treatment decision‐making paradigms for advanced reconstructive procedures. It is also William V. Giannobile, DDS, MS, DMedSc crucial for the advanced clinician to under- Najjar Endowed Professor of Dentistry & stand when and when not to attempt to retain Biomedical Engineering advanced disease cases. Large epidemiologi- Departments of Periodontics and Oral cal studies have demonstrated that dental Medicine & Biomedical Engineering, implant therapy is not a ‘panacea’ and that, University of Michigan School of Dentistry and given the significant incidence and prevalence College of Engineering, Ann Arbor, MI, USA xi
Preface
Declare the past, diagnose the present, might find this book useful for the treatment foretell the future. of molars already affected by periodontitis Hippocrates and furcation involvement. Immense thanks go to all the expert collab- Doubt is not a pleasant condition, but orators and friends, Will Giannobile, certainty is an absurd one. Bernadette Pretzl, Peter Eickholz, Clemens Voltaire Walter, Jia‐Hui Fu, Hom‐Lay Wang, Federica, Riccardo, and Alberto Fonzar, Roberto Young and new to a periodontal clinic, I Rotundo, Stefan Rüdiger, Nikos Donos, Toni remember looking at cases of extensive peri- Sculean, Elena Calciolari, Iro Palaska, odontal and bone loss in multi‐rooted teeth Yoshinori Shirakata, Søren and Karin Jepsen, and wondering how the problem could be Nikos Mardas, Steve Barter, Christian Graetz, solved, and if and how the tooth could be and Falk Schwendicke, who all contributed retained. The fascination with the spaces chapters to this book, and to Paul Kletz for created by inter‐radicular bone resorption, kindly proofreading some of the chapters and called ‘furcations’, and the struggle over how for his support throughout my career. Special to manage them in the clinic, continues to thanks go to the patients who over the years occupy large parts of my days and has have been a big source of inspiration with prompted me to write this book. Here, with their interest and commitment, and who the help of several expert colleagues, I have every day make me want to be a better perio- tried to: dontist. I also need to thank my teachers at the University of Catania and at the UCL Eastman ●● Critically appraise the evidence. Dental Institute, who have all contributed, ●● Present expert opinions. some with small and some with larger ●● Show treated cases. ingredients, to the cauldron of periodontal ●● Present useful clinical guidelines, step‐by knowledge from which I drew for the plan- step procedures, and treatment algorithms. ning and editing of this book. The students The emphasis of the book is to try and and staff at Barts and the London School of maintain molars affected by furcation involve- Medicine and Dentistry, Queen Mary ment and regenerate the lost support, when University of London (QMUL), are gratefully possible, accepting that this is not always pos- acknowledged. But most of all, I would like to sible in the long term. It goes without saying thank my family, Daniela, Domenico, Lorenzo, that primary prevention of periodontitis Delia, and my parents and in‐laws, for their remains the best way to prevent tooth loss. continued support of my work. I hope that periodontists, dental/postgraduate students, hygienists, and general dentists Luigi Nibali
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About the Companion Website
Don’t forget to visit the companion website for this book:
www.wiley.com/go/nibali/diagnosis
There you will find valuable material designed to enhance your learning, including: ●● video clips ●● additional treated cases Scan this QR code to visit the companion website
Chapter No.: 1 Title Name:
Chapter 1
Anatomy of Multi‐rooted Teeth and Aetiopathogenesis of the Furcation Defect Bernadette Pretzl
Section of Periodontology, Department of Operative Dentistry, University Clinic Heidelberg, Heidelberg, Germany
1.1 Introduction: Why unique anatomy of molars, poses a challenge Focus on Molars? for all dentists focusing on molar retention.
Dentists generally agree on three statements 1.2 The ‘Special’ Anatomy about molars: of Molar Teeth ●● They play an important role in the dentition. The essential knowledge of molar root anat- ●● They are difficult to reach for self‐performed omy for every periodontist is stressed in a as well as professional cleaning due to their review by Al‐Shammari et al. (2001). Due to posterior position in the mouth. the higher mortality and compromised ●● They pose some challenges due to their diagnoses of furcation‐involved molars, and unique anatomy. likewise to the reduced efficacy of perio- The important role of molar teeth in the den- dontal therapy in multi‐rooted teeth, the tition mainly consists in their contribution to authors suggest a thorough engagement mastication, because they carry a considera- with possibly decisive tooth factors such as ble part of the occlusal load. Hiiemäe (1967) furcation entrance area, (bi)furcation focused on the masticatory function in mam- ridges, root surface area, root separation, mals and molars grinding the food, and in and root trunk length, because they may 1975 Bates et al. reviewed the literature on critically affect the diagnosis and therapy the masticatory cycle in natural and artificial of multi‐rooted teeth (Leknes 1997; Al‐ dentitions of men, attributing a fundamental Shammari et al. 2001). role to our posterior teeth regarding the For centuries, scientists have concerned intake and preparation of nutrition. Thus, a themselves with the human teeth, their anat- focus on molars and the endeavour to retain omy, evolution, function, histology, and our posterior teeth in a healthy functional histogenesis. Almost 3000 years ago, the state seems justified. Etruscans populating the northern and cen- This chapter will reveal how the posterior tral part of what is now Italy from 900 to 100 position of molars makes them less accessi- bc recognized the importance of teeth and ble for cleaning, whether it may be self‐ fabricated quite delicate dental prostheses, performed or carried out by a dental which Loevy and Kowitz (1997) compared to professional. This fact, combined with the prostheses from the mid‐twentieth century.
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
The formation and genesis of teeth have the dental papilla as well as the buccal and been studied in more detail during the last lingual epithelial elements and described the three and a half centuries, starting with the development as follows: The first epithelial works of the so‐called father of microscopic elements, which later evolve into the bifurca- anatomy and histology, Marcello Malpighi tion, appear at the 24‐week stage of gesta- (1628–1694) from Italy (Rifkin and tional age. At that time, the crown formation Ackerman 2011), who referred to an ‘invo- of the molar is not complete and Hertwig’s lucrum externum’ describing the outer part root sheath has not developed yet (Bhussry of the tooth, which is today known as 1980; Bower 1983). Thus, the author suggests enamel. More than a century later the that the epithelial elements form extensions formation of cementum (1798–1801) and of the epithelium of the developing crown dentine (1835–1839) was described (e.g. rather than the root (Bower 1983). Blake 1801; Bell 1835). Written in 1935, Additionally, he detected stellate reticulum Meyer’s Normal Histology and Histogenesis (which is essential for the formation of of the Human Teeth and Associated Parts ameloblasts) in the furcation area. The (Churchill 1935) builds the foundation of author speculated about a possible mecha- our understanding regarding the anatomy nism of enamel formation due to the presence of teeth. Orban and Mueller (1929), who of stellate reticulum in the region of the studied the development of furcations in furcation, which develops into ameloblasts, multi‐rooted teeth, set a focus on molars for example resulting in cervical projections using graphic reconstructions as early as of enamel. 1929. Their three‐dimensional illustrations allow a detailed impression of the root area comparable to those documented by Svärdström and Wennström (1988). In later 1.3 Anatomical Factors years, scientists focused more and more on in Molar Teeth micro‐anatomical and histological research. Based on the knowledge thus created, the In 1988, Svärdström and Wennström plotted sequence of molar development can be three‐dimensional contour maps in order to divided into three phases analogous to the describe the topography of the furcation area development of all teeth (Thesleff and and compared drawings of maxillary and Hurmerinta 1981): initiation, morphogene- mandibular molars. These show a complex sis, and cell differentiation. The evolution of area with small ridges, peaks, and pits, and more than one root sets molars apart from the authors summarize that the complexity the rest of the dentition: in multi‐rooted of the furcation topography evidently teeth the enamel organ expands with increases the difficulties with respect to projections of Hertwig’s root sheath (an epi- proper debridement once the periodontal thelial diaphragm). These expansions were pocket reaches the furcation entrance and described as lobular growing inwards runs into the furcation area. Thus, in addi- between the lobes. Depending on the num- tion to the aforementioned potentially deci- ber of lobes, two to three (in rarer cases four) sive factors – furcation entrance area, roots develop as soon as the projections have bifurcation ridges, root surface area, and fused (Bhussry 1980). In an investigation by root trunk length – it has to be kept in mind Bower (1983) of furcation development, that the complexity of the furcation area evolving mandibular molars from 13 foetuses itself poses a challenge to the dental practi- between 17 and 38 weeks of gestation were tioner (Svärdström and Wennström 1988). fixed, sectioned, and stained, giving a unique Figure 1.1 shows a diagram of a mandibular and detailed impression of furcation devel- molar, highlighting the main anatomical opment. The author measured the base of features. Anatomy of Multi-rooted Teeth 3
Crown
Root trunk Fornix
Degree of Root complex separation Bone loss
Root cone
Divergence
Figure 1.1 Drawing of mandibular molar with furcation involvement, showing the main anatomical features, including root trunk (part of the root from the cemento‐enamel junction [CEJ] to the furcation entrance) and root cones, and pointing at root divergence and degree of separation between roots. The ‘bone loss’ is schematically indicated as the distance between the CEJ and the most apical part of the bone. Source: Courtesy of Dr Aliye Akcali.
1.3.1 Furcation Entrance Area 0.63 mm, respectively), which was con- The furcation entrance area was measured firmed by Svärdström and Wennström by Bower (1979a) in 114 maxillary and 103 (1988) and dos Santos et al. (2009). mandibular first molars. The diameter of In mandibular molars the results differed, the entrance area was smaller than a curette with wider entrance areas in buccal furca- blade in more than 50% of the examined fur- tions of first and second molars (b: 0.88 mm cations, with the smallest average diameter and 0.73 mm; l: 0.81 mm and 0.71 mm, in buccal (b) sites of maxillary as well as respectively). Nonetheless, the furcation mandibular first molars. No correlation entrance area was < 1 mm in the majority of between the size of the tooth and its furca- molars and < 0.75 mm in 58%, 49%, and 52% tion entrance area could be detected (Bower of molars, respectively (Bower 1979a; Chiu 1979a). Hou et al. (1994) studied 89 et al. 1991; Hou et al. 1994). Thus, the stand- extracted maxillary and 93 extracted man- ard width of curettes (0.75–1.0 mm) is dibular first and second molars microscopi- mostly too large to access, let alone properly cally. In their Chinese population sample, clean, a furcation entrance. Hou et al. (1994) they concurred with the results presented concluded that in order to achieve complete by Bower (1979a) in the maxilla and found a debridement of root surfaces within furca- larger diameter in mesio‐ (mp) and disto‐ tions, an appropriate selection and combi- palatal (dp) furcation entrances for first and nation of ultrasonic tips (diameter 0.56 mm) second molars (mp: 1.04 mm and 0.90 mm; and periodontal curettes should be consid- dp: 0.99 mm and 0.67 mm; b: 0.74 mm and ered. A recent study by dos Santos et al. 4 Chapter 1
(2009) analysed 50 maxillary and 50 man- to studies in extracted molars (Bower 1983, dibular molars and confirmed the afore- 1979b). Secondly, the exclusion of ectomes- mentioned findings, concluding that some enchyme between the lobes described by molar furcation entrances could not be Bhussry (1980) may explain the large quanti- adequately instrumented with curettes and ties of cementum in the furcation area of the suggesting the use of alternative hand mature tooth corresponding to bifurcation instruments. In a review, Matthews and ridges (Bower 1983). In general, two types of Tabesh (2004) stressed the importance of bifurcation ridge are known: one in the the diameter of the furcation entrance in bucco‐lingual direction, the other in the order to judge the effect of professional mesio‐distal direction (intermediate = IBR). cleaning, and thus the probable success of Everett et al. (1958) detected buccal and lin- periodontal therapy. The challenges of fur- gual ridges, mainly constituting of dentine, in cation cleaning are discussed by Fu and 63% of mandibular first molars and IBRs, Wang in Chapter 3. mainly composed of cementum, in 73%. The findings of Burch and Hulen (1974), Dunlap 1.3.2 (Bi)furcation Ridges and Gher (1985), and Hou and Tsai (1997a) concur, with a prevalence of 76.3%, 70%, and In early morphological studies of extracted 67.9%, respectively, in mandibular first first molar teeth, cementum was found in the molars. furcation area in a ridge, building the furca- Gher and Vernino (1980) suggest a connec- tion region in mandibular molars, and was tion between the presence of an IBR and the called an intermediate bifurcation ridge progression of the furcation defect due to the (IBR), with a high presence of cementum morphology and location of IBRs. Hou and adjacent to the furcation entrance (Everett Tsai (1997a) confirmed this correlation. et al. 1958; Bower 1979a, b; see Figure 1.2). Additionally, they stated that an even higher In a study on developing first mandibular significant correlation exists between the molars sectioned at different gestational simultaneous presence of IBRs combined ages, the lingual element was found to be with cemento‐enamel projections and furca- wider in a mesio‐distal dimension comparable tion involvement (FI).
Figure 1.2 Furcation ridge. Source: Courtesy of Dr Nicola Perrini. Anatomy of Multi-rooted Teeth 5
1.3.3 Root Surface Area Anderson et al. (1983). They concluded that the mesial root showed a statistically signifi- A team of researchers (Hermann et al. 1983; cant greater RSA than the distal root, which Dunlap and Gher 1985; Gher and Dunlap should be taken into consideration when 1985) focused on the topic of root surface planning treatment, especially regarding area (RSA) in maxillary and mandibular first resective approaches. Dunlap and Gher molars. In a meta‐analysis derived of data (1985) dissected 20 extracted mandibulary from 22 original articles, Hujoel (1994) com- first molars and cross‐sectioned them in puted a total RSA (corresponding to the 1 mm increments. They too observed that periodontal surface area) for the complete the distal root had a significantly smaller dentition of 65–86 cm2, excluding third RSA than the mesial one, but stressed that molars. In maxillary first molars a mean of the shapes of the roots (conical for the distal 4.5 cm2 (second: 4.0 cm2) and in mandibular one; hour‐glass shaped for the mesial one) first molars a mean of 4.2 cm2 (second: should be taken into consideration as well. In 3.4 cm2) were calculated. In molars, it is often contrast to their findings in the maxilla, the difficult to judge the extent of FI clinically root trunk surface area was not larger than (Bower 1979b) and thus to determine the the surface of the individual roots, and aver- RSA exactly. aged 30.5% of the total RSA of the mandibu- lary first molar. They found a mean root 1.3.3.1 RSA in the Maxilla length of 14.4 ± 1.1 mm and a total RSA of Hermann et al. (1983) as well as Gher and 4.37 ± 0.64 cm2. In other studies (Jepsen 1963; Dunlap (1985) dissected 20 extracted first Anderson et al. 1983), the total RSA varied maxillary molars and cross‐sectioned them in from 4.31 to 4.7 cm2. 1 mm increments. Molars with fused roots were excluded. They observed that the disto‐ buccal root had a significantly smaller RSA 1.3.4 Root Trunk Length than either the mesio‐buccal or palatal root, The portion of multi‐rooted teeth located api- confirming the results of Bower (1979b). The cal to the cemento‐enamel junction (CEJ) is root trunk surface area was significantly larger called the ‘root complex’ and is divided into than any surface of the three individual roots, root trunk and root cones. The root trunk is and averaged 32% of the total RSA of the max- generally defined as the area of the tooth from illary first molar (Hermann et al. 1983). Gher the CEJ to the furcation fornix. In a study by and Dunlap (1985) measured a mean root Gher and Dunlap (1985), the distance between length of 13.6 mm (ranging from 10.5 to the CEJ and the furcation entrance in maxil- 16 mm) and a total RSA of 4.77 cm2 (ranging 2 lary molars differed considerably between the from 3.36 to 5.84 cm ). Additionally, a ‘bal- mesial (3.6 ± 0.8 mm) and the distal entrance looning’ of the RSA percentage in the furca- (4.8 ± 0.8 mm), whereas the buccal entrance tion area of maxillary molars was described, was detected 4.2 ± 1.0 mm apical to the CEJ. which could not be detected in other teeth. These findings led to the conclusion that the Accordingly, the importance of periodontal clinician should suspect a through‐and‐ support in the furcation area of maxillary through furcation (degree III according to molars was stressed, concluding that a rela- Hamp et al. 1975) in maxillary molars once a tively small attachment gain or loss may have loss of 6 mm in vertical attachment occurred. a significant impact on the stability of the In more than 50% of the dissected maxillary maxillary first molar (Gher and Dunlap 1985). molars, the furcation roof was found coronal of the root separations and formed a concave 1.3.3.2 RSA in the Mandible dome between the three roots. For a study on mandibular first molars, It should be emphasized that the dome‐like 10 teeth were hemisected and measured by anatomy further complicates therapy and 6 Chapter 1
maintenance of maxillary first molars (Gher Al‐Shammari et al. 2001). Thus, Al‐ and Dunlap 1985). Hou and Tsai (1997b) Shammari et al. (2001) summarized that the measured the root trunk in 166 extracted root trunk length significantly relates to the first and second maxillary and 200 extracted prognosis and treatment of molars. A short first and second mandibular molars of a root trunk worsens the prognosis with regard Taiwanese tooth sample. In the maxilla, short to a more likely FI, but once periodontal root trunks were more commonly found destruction has occurred, it improves the buccally, whereas long root trunks were more chances of a successful treatment (Horwitz commonly found mesially (Hou and Tsai et al. 2004). 1997b). The authors found generally longer root trunks in second molars than in first molars in both jaws, and additionally stated 1.4 Anatomical Aetiological that long root trunks are associated with Factors short root cone length (Hou and Tsai 1997b). In 134 extracted first and second mandibu- 1.4.1 Cervical Enamel Projections lar molars, Mandelaris et al. (1998) detected longer root trunks in lingual molar surfaces Enamel surfaces do not allow for the attach- when compared to buccal surfaces (mean: ment of connective tissue and represent an 4.17 mm and 3.14 mm, respectively), confirm- anatomical abnormality in the root area. ing the results of Hou and Tsai (1997b). The Thus, cervical enamel projections (CEP) may mean distance between the CEJ and the furca- contribute to the development of a furcation tion entrance was 4.0 ± 0.7 mm in mandibular defect (Al‐Shammari et al. 2001). The first to molars (4.6 ± 0.6 mm in maxillary first molars; report a possible connection between CEPs Dunlap and Gher 1985; Gher and Dunlap and periodontal destruction in molars was 1985), whereas no root trunk of > 6 mm could Atkinson in 1949. According to Masters and be found (Dunlap and Gher 1985; Mandelaris Hoskins (1964), CEPs can be classified in et al. 1998). Like in maxillary molars, it can be three grades (Table 1.1). concluded that a through‐and‐through furca- Different prevalences of CEPs have been tion (Hamp et al. 1975) should be expected in documented so far. Masters and Hoskins the mandible once a loss of 6 mm in vertical (1964) found CEPs in 29% of mandibular and attachment was reached on both sides (buccal 17% of maxillary molars. In Egyptian skulls, and lingual). On the other hand, it has to be Bissada and Abdelmalek (1973) detected a kept in mind that a furcation defect has a CEP prevalence of 8.6%. In the 1138 molars horizontal component as well. Santana et al. studied, a higher incidence of CEPs in the (2004) measured 100 extracted first and sec- ond mandibular molars and their findings Table 1.1 Classification of cervical enamel projections. suggest that a horizontal attachment loss of 4.3–6.9 mm is essential in order to allow com- munication between the buccal and lingual Grade I The enamel projection extends from the cemento‐enamel junction of the furcation entrance. Complete or partial fusion tooth towards the furcation entrance of roots is also not unusual in multi‐rooted (<1/3 of the root trunk). teeth. Some 40% of maxillary premolars are Grade II The enamel projection approaches two‐rooted and the entrance to the furcation the furcation entrance but does not is located an average 8 mm from the CEJ, well enter it. No horizontal component is into the middle third of the root complex present (>1/3 of the root trunk). (Bower 1979a). See Figure 1.3a. A clinically evident FI correlates with the Grade III The enamel projection extends vertical length and type of the root trunk horizontally into the furcation. Compare Figures 1.3b and 1.3c. (Carnevale 1995; Hou and Tsai 1997b, Anatomy of Multi-rooted Teeth 7
Figure 1.3a Cervical enamel projection grade II (>1/3 of root trunk; Masters and Hoskins 1964) on upper right first molar (REM microscope). Source: Eickholz and Hausmann 1998.
mandible could be confirmed. A study in 200 confirmed that CEPs are found more fre- East Indian skulls with 2000 molars reported a quently in the mandible and are significantly 32.6% incidence rate of CEPs (Swan and Hurt associated with the occurrence of FI. The 1976). They were most often reported in man- incidence ranged from 14.7% in mandibular dibular second molars (51.0%), followed by second molars to 5.5% in wisdom teeth. The maxillary second molars (45.6%), mandibular most recent study was performed using cone‐ first and maxillary first molars (13.6%). Grade beam computed tomography data in a Korean I enamel projections (Masters and Hoskins population analysing 982 mandibular molars 1964) were detected most frequently. These (Lim et al. 2016) and reported an overall could not be significantly related to furcation prevalence rate of CEP of 76%. Grade I CEPs involvement, as could grade II and III CEPs were the most common, followed by CEPs of (Swan and Hurt 1976). An observation in 78 grades II and III (Lim et al. 2016). Taiwanese individuals reported detection of The huge variations can partly be explained CEPs in 49.3% of second and 62.3% of first by different study objects: in human skulls maxillary and 51.2% of second and 73.9% of healthier periodontal conditions can be first mandibular molars (Hou and Tsai 1987). assumed, while extracted molars most prob- A study by the same authors in furcation‐ ably show worse conditions, and Hou and involved mandibular molars reported even Tsai (1987, 1997a) as well as Mandelaris et al. higher CEP percentages: 71% of second and (1998) studied furcation‐involved molars in 92.9% of first mandibular molars showed periodontal patients. Additionally, a higher enamel projections (Hou and Tsai 1997b). prevalence of CEPs in Oriental subjects than Mandelaris et al. (1998) documented CEPs in in Caucasians is suspected (Hou and Tsai 66.4% of mandibular molars (61.9% of buccal 1987; Lim et al. 2016). and 50.8% of lingual surfaces) ranging from Nonetheless, it can be concluded that CEPs 0.98 to 1.33 mm in diameter. Current research are a common problem which must be on CEPs was published in 2013 and 2016. addressed by clinicians when treating molar Bhusari et al. (2013) investigated their inci- teeth. They are more prevalent than enamel dence on the buccal surface of 944 upper and pearls and prevent connective tissue attach- lower first, second and third permanent ment, thus contributing to the aetiology of molars from 89 Indian dry human skulls, and furcation defects, possibly resulting in localized additionally measured FI. Again, it could be chronic periodontitis and FI in molars (Leknes 8 Chapter 1
Figure 1.3b Cervical enamel projection on lower left first molar; grade III (reaching furcation entrance area; Masters and Hoskins 1964). Source: Eickholz 2005.
Figure 1.4a Macroscopic image of an enamel pearl on an extracted molar. Source: Courtesy of Prof. Dr. H.-K. Albers.
Figure 1.3c Cervical enamel projection on extracted lower right first molar; grade III (reaching furcation entrance area; Masters and Hoskins 1964). Source: Eickholz and Hausmann 1998.
1997; Al‐Shammari et al. 2001; Bhusari et al. 2013). Additionally, significantly higher plaque and gingivitis index values have been reported in the presence of CEPs (Carnevale et al. 1995).
1.4.2 Enamel Pearls
Enamel pearls (see Figure 1.4) were first described in an article in the American Figure 1.4b Microscopic image of an enamel pearl. Journal of Dental Science in 1841 (Moskow Source: Courtesy of Prof. Dr. H.-K. Albers. Anatomy of Multi-rooted Teeth 9
Figure 1.4c Orthopantomogram showing enamel pearls on upper right and left second molars. Source: Eickholz and Hausmann 1998. and Canut 1990). They are ectopic globules in molars. Akgül et al. (2012) evaluated the consisting mostly of enamel, often contain- presence of enamel pearls using cone‐beam ing a core of dentine, and they adhere to the computed tomography in 15 185 teeth (4334 tooth root surface, with a distinct predilec- molars). An incidence of enamel pearls of tion for the furcation areas of molar teeth, 0.83% in molars and 4.69% per subject with no particularly maxillary third and second gender differences was reported. Again, the molars. In a review from 1990, an incidence incidence was significantly higher in the max- of 2.6% (ranging from 1.1 to 9.7%) was illa. Colak et al. (2014) studied the prevalence reported, with differences among racial of enamel pearls in Turkish dental patients groups and a greater incidence in histological and detected them in 0.85% of teeth and 5.1% studies (Moskow and Canut 1990). Like of subjects, with a contradictory higher inci- CEPs, enamel projections prevent connec- dence in the mandible and in male patients. tive tissue attachment and thus contribute to Although lower in incidence than enamel the aetiology of periodontal destruction. projections, it can be summarized that They usually occur singularly, but up to four enamel pearls play an important role in the enamel pearls have been observed on the aetiology of furcation defects, and it is con- same tooth (Moskow and Canut 1990). sidered essential to diagnose enamel pearls More recent research demonstrates an early on to allow for an adequate prognosis of incidence within the range documented by molar retention and probably alter the thera- Moskow and Canut (1990). Darwazeh and peutic approach. Hamasha (2000) evaluated the presence of enamel pearls in a Jordanian patient sample, studying 1032 periapical radiographs. An 1.5 Periodontal Aetiological incidence of 1.6% of enamel pearls in molars Factors in Molar Teeth and 4.76% per subject with no gender differences was reported. Chrcanovic et al. (2010) evalu- Aetiological factors interact with the previ- ated the prevalence of enamel pearls in ously described anatomical factors and may 45 539 permanent teeth (20 218 molars) from lead to periodontal destruction and attach- a human tooth bank in Brazil. They con- ment loss in molars, and thus result in a fur- firmed the predominant presence in the cation defect. According to Al‐Shammari maxilla and reported an incidence of 1.71% et al. (2001), plaque‐associated inflammation, 10 Chapter 1
trauma from occlusion, pulpal pathology, tional occlusal load. Even before that, vertical root fractures, and iatrogenic factors Glickman et al. (1961) compared the effect of need to be taken into consideration. occlusal force on splinted and non‐splinted teeth in rhesus monkeys, and suggested that 1.5.1 Plaque‐associated the fibre orientation in the furcation area Inflammation makes multi‐rooted teeth more susceptible to increased functional forces. More recently, The reader of this book will surely be well Nakatsu et al. (2014) confirmed the afore- accustomed to plaque formation and the mentioned findings in an observation in rats. inflammatory component of gingivitis and On the other hand, Waerhaug (1980) con- periodontitis. What is special about molars cluded from his observations of 46 human in this context? In general, it can be stated molars (extracted because of advanced peri- that furcations are more prone to plaque odontal destruction) that increased mobility adhesion and less likely to stay plaque free. and occlusal trauma are not involved in the The anatomy of the furcation favours reten- aetiology of the FI and are instead a late tion of bacterial deposits and renders hygiene symptom of periodontal disease. Thus, the procedures difficult (Matthews and Tabesh impact of occlusal forces in the aetiology of 2004). In 1987, Nordland et al. monitored periodontitis in general and FI in particular 2472 sites in 19 periodontal patients for remains controversial (Al‐Shammari et al. 24 months after periodontal therapy, and 2001; Reinhardt and Killeen 2015). In a reported that furcation sites responded less review, Harrel (2003) suggest that occlusal favourably to therapy and were more likely to interferences should be regarded as a poten- exhibit higher plaque and gingivitis scores. tial risk factor comparable to smoking, rather Apart from that, it is assumed that furcation than a causative or aetiological factor. areas are an extension of periodontal pock- ets, because unique histological features are 1.5.3 Vertical Root Fractures lacking (Glickman 1950; Al‐Shammari et al. 2001). Thus, plaque formation follows the It is generally agreed that vertical root frac- same process in molars and their furcations tures, which can occur in a longitudinal as in the remaining dentition (Leknes 1997). direction on any surface of the root, are dif- ficult to diagnose because they share symp- 1.5.2 Occlusal Trauma toms with other dental conditions (Matthews and Tabesh 2004). Additionally, in most cases Trauma from occlusion is suspected to mild pain or a dull discomfort is the only be another aetiological factor contributing clinical symptom of a vertical root fracture to periodontal destruction in molars. (Meister at al. 1980). They result in rapid Two groups of researchers, Glickman and localized loss of attachment and bone co‐workers as well as Lindhe and co‐workers, (Walton et al. 1984) and can lead to FI focused on this topic in animal studies apply- depending on their position. Mostly, a poor ing excessive occlusal forces on molars. In prognosis is assigned to teeth exhibiting ver- their classic studies on beagle dogs, Lindhe tical root fractures (Al‐Shammari et al. 2001; and Svanberg (1974) and Nyman et al. (1978) Matthews and Tabesh 2004). reported significant alterations in tooth mobility combined with angular bony defects 1.5.4 Endodontic Origin and loss of periodontal support in artificially and Pulpal Pathology created, gingivally inflamed multi‐rooted teeth carrying splints, compared to teeth Accessory canals are quite common in molar with inflammation but carrying no addi- teeth. A study of 46 extracted molars of both Anatomy of Multi-rooted Teeth 11 jaws found accessory canals in 59% of exam- composition characteristically found in peri- ined teeth (Lowman et al. 1973). Burch and odontitis. Thus, the authors concluded that Hulen (1974) reported ‘openings’ in 76% of the changes observed in the subgingival the furcations of maxillary and mandibular microflora document a potential mechanism molars. These canals allow for products of for the initiation of periodontal disease asso- pulpal necrosis to enter the furcation area ciated with iatrogenic factors. Wang et al. and cause an inflammatory lesion (Carnevale (1993) focused on molars and assessed the et al. 1995). Thus, a pulpal pathosis can result correlation between FI and the presence of a in FI. Carnevale et al. (1995) reported that crown or proximal restoration in 134 perio- proximal and inter‐radicular bone destruc- dontal patients during maintenance therapy. tion of endodontic origin is reversible after Their results showed a significant associa- root canal treatment. Periodontal therapy tion between FI as well as periodontal attach- only becomes necessary in the case of a ment loss and the presence of a crown or persistent lesion after the endodontic treat- restoration. ment. A more detailed description of the Additionally, Matthews and Tabesh (2004) associations between FI and endodontic commented that overhangs not only build a pathology is provided in Chapter 4. plaque retention niche, but also impinge on the biological width (between the depth of a 1.5.5 Iatrogenic Factors healthy sulcus and the alveolar crest) and thus cause damage. They report ranges of Generally, overhanging dental restorations overhangs in restored teeth from 18 to 87% or discrepancies of the subgingival margin in (Matthews and Tabesh 2004). In general, the any kind of restoration or even orthodontic placement of restorative margins subgingi- bands allow for adhesion of plaque and show vally results in more plaque, more gingival detrimental effects on adjacent gingival tis- inflammation and deeper periodontal sues; additionally, the fit of pro sthetic resto- pockets. rations is mostly less than perfect (Leknes It can be concluded that special care needs to 1997) and builds a niche, where plaque be taken when placing restorations, and over- formation is facilitated and cleansing diffi- hangs need to be diagnosed and removed as cult. According to a study by Lang et al. early as possible. Should a restoration margin (1983) in dental students with healthy gingi- need to be placed subgingivally, the biological vae who received proximal inlays with 1 mm width has to be kept in mind and crown length- overhangs, the microbial composition of the ening considered. Thus, a dento‐gingival attach- subgingival biofilm shifted from healthy to a ment may be achieved (Herrero et al. 1995).
Summary of Evidence
●● Numerous anatomical factors like furca- impact on the prognosis and therapeutic tion entrance area, bifurcation ridges, outcome of multi‐rooted teeth. root surface area, and root trunk length ●● Iatrogenic factors should be tackled early need to be considered in the diagnosis and on (at the beginning of periodontal ther- periodontal treatment of molars. The apy), thus allowing for improvement of periodontist should be aware of these fac- gingival and periodontal conditions. tors because they may have a significant 12 Chapter 1
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Lim, H.‐C., Jeon, S.‐K., Cha, J.‐K. et al. (2016). debridement in molar teeth. Journal of Prevalence of cervical enamel projection Clinical Periodontology 14, 231–236. and its impact on furcation involvement in Nyman, S., Lindhe, J., and Ericsson, I. (1978). mandibular molars: A cone‐beam computed The effect of progressive tooth mobility on tomography study in Koreans. The destructive periodontitis in the dog. Journal Anatomical Record 299, 379–384. of Clinical Periodontology 5, 213–225. Lindhe, J., and Svanberg, G. (1974). Influence Orban, B., and Mueller, E. (1929). The of trauma from occlusion on progression of development of the bifurcation of experimental periodontitis in the beagle dog. multirooted teeth. Journal of the American Journal of Clinical Periodontology 1, 3–14. Dental Association 16, 297–319. Loevy, H.T., and Kowitz, A.A. (1997). The Reinhardt, R.A., and Killeen, A.C. (2015). Do dawn of dentistry: Dentistry among the mobility and occlusal trauma impact Etruscans. International Dental Journal 47, periodontal longevity? Dental Clinics of 279–284. North America 59, 873–883. Lowman, J.V., Burke, R.S., and Pelleu, G.B. Rifkin, B.A., and Ackerman, M.J. (2011). (1973). Patent accessory canals: Incidence in Human Anatomy: A Visual History from the molar furcation region. Oral Surgery Oral Renaissance to the Digital Age. New York, Medicine Oral Pathology 38, 451–455. NY: Abrams Books. Mandelaris, G.A., Wang, H.L., and MacNeil, Santana, R.B., Uzel, I.M., Gusman, H. et al. R.L. (1998). A morphometric analysis of the (2004). Morphometric analysis of the furcation region of mandibular molars. furcation anatomy of mandibular molars. Compendium of Continuing Education in Journal of Periodontology 75, 824–829. Dentistry 19, 113–120. Svärdström, G., and Wennström, J.L. (1988). Masters, D.H., and Hoskins, S.W. (1964). Furcation topography of the maxillary and Projection of cervical enamel into molar mandibular first molars. Journal of Clinical furcations. Journal of Periodontology 35, Periodontology 15, 271–275. 49–53. Swan, R.H., and Hurt, W.C. (1976). Cervical Matthews, D., and Tabesh, M. (2004). enamel projections as an etiologic factor in Detection of localized tooth‐related factors furcation involvement. Journal of the that predispose to periodontal infections. American Dental Association 93, 342–345. Periodontology 2000 34, 136–150. Thesleff, I., and Hurmerinta, K. (1981). Tissue Meister, F., Lommel, T.J., and Gerstein, H. interactions in tooth development. (1980). Diagnosis and possible causes of Differentiation 18, 75–88. vertical root fractures. Oral Surgery, Oral Waerhaug, J. (1980). The furcation problem: Medicine, Oral Pathology 49, 243–253. Etiology, pathogenesis, diagnosis, therapy Moskow, B.S., and Canut, P.M. (1990). Studies and prognosis. Journal of Clinical on root enamel. Journal of Clinical Periodontology 7, 73–95. Periodontology 17, 275–281. Walton, R.E., Michelich, R.J., and Smith, G.N. Nakatsu, S., Yoshinaga, Y., Kuramoto, A. et al. (1984). The histopathogenesis of vertical (2014). Occlusal trauma accelerates root fractures. Journal of Endodontics 10, attachment loss at the onset of experimental 48–56. periodontitis in rats. Journal of Periodontal Wang, H.L., Burgett, F.G., and Shyr, Y. (1993). Research 49, 314–322. The relationship between restoration and Nordland, P., Garrett, S., Kiger, R.D. et al. furcation involvement on molar teeth. (1987). The effect of plaque control and root Journal of Periodontology 64, 302–305. 15
Chapter 2
Clinical and Radiographic Diagnosis and Epidemiology of Furcation Involvement Peter Eickholz1 and Clemens Walter 2
1 Poliklinik für Parodontologie, Zentrum der Zahn‐ Mund‐ und Kieferheilkunde (Carolinum), Johann Wolfgang Goethe‐Universität Frankfurt, Frankfurt am Main, Germany 2 Klinik für Parodontologie, Endodontologie und Kariologie, Universitätszahnkliniken, Universitäres Zentrum für Zahnmedizin Basel, Basel, Switzerland
2.1 Introduction furcation‐involved molars, recurrent perio- dontal infection, and as a result an inferior In single‐rooted teeth, periodontal destruc- long‐term prognosis of these teeth (McGuire tion proceeds from the cemento‐enamel and Nunn 1996; Dannewitz et al. 2006, 2016; junction (CEJ) apically, predominantly in a Pretzl et al. 2008; Salvi et al. 2014; Graetz vertical direction. The vertical attachment et al. 2015). Furcation‐involved molars loss is assessed as vertical probing attach- respond less favourably to periodontal ther- ment loss (PAL‐V) from the CEJ, or if the CEJ apy than molars without furcation involve- is destroyed by a restoration from the resto- ment or single‐rooted teeth, and are at ration margin (RM) to the bottom of the per- greater risk for further attachment loss iodontal pocket. Vertical bone loss is assessed (Nordland et al. 1987; Loos et al. 1989; Wang radiographically or by vertical probing bone et al. 1994) than other teeth. Addressing this level (PBL‐V) from the CEJ or RM to the issue, Kalkwarf et al. (1988) reported the suc- alveolar crest. If periodontitis affects multi‐ cess of different surgical and non‐surgical rooted teeth, the tissues are not only treatment modalities in 158 molars. destroyed vertically but also horizontally Irrespective of the therapy performed, the between the roots, creating furcation involve- horizontal defect in the furcation area ment. This dimension of periodontal increased during the two‐year follow‐up. destruction (horizontal attachment and bone Thus, reliable diagnosis of incidence and loss) may be assessed as horizontal probing extent of furcation involvement is decisive attachment loss (PAL‐H) or horizontal for prognosis and treatment planning. probing bone level (PBL‐H). Horizontal probing attachment loss and bone loss in the furcation area create a niche 2.2 Clinical Furcation (furcation involvement), which impedes Diagnosis accessibility for individual oral hygiene in the molar region (Lang et al. 1973) and profes- Furcation involvement can only be found in sional root debridement (Fleischer et al. multi‐rooted teeth (Table 2.1). More than 1989). This adds to the factors contributing one root is regularly found in maxillary and to more severe disease progression in mandibular molars as well as in first maxillary
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
Table 2.1 Regularly multi‐rooted teeth with location of roots and location of furcation entrances.
Location of Location of furcation Tooth type roots entrance
Maxillary molars Mesio‐buccal Buccal Disto‐buccal Mesio‐palatal Palatal Disto‐palatal Maxillary premolars Buccal Mesial Palatal Distal Mandibular molars Mesial Buccal Distal Lingual
premolars (see Chapter 1). However, two‐ bizarre anatomy of furcations (Schroeder rooted variants may be found in second max- and Scherle 1987), their curved course, and illary premolars and mandibular anteriors. the fact that the furcation entrances of maxil- Rarely, three‐rooted variants may be found in lary premolars and molars open into inter- mandibular molars and maxillary premolars proximal spaces require the use of particular (Mohammadi et al. 2013). Those sites at curved furcation probes in furcation diagno- which furcation entrances are regularly sis (e.g. Nabers probe; Figure 2.1). The probe expected have to be examined for furcation is placed onto the tooth surface coronally of involvement on a regular basis in the course the gingival margin at the site where a furca- of periodontal examination. Search for and tion entrance is expected (e.g. lingual of a scoring of furcation involvement are funda- mandibular molar). Then the probe is pushed mental elements of periodontal examination. apically, gently displacing the gingiva in Particularly in untreated periodontal zigzag movements until the bottom of the patients, furcation entrances do not lie open. sulcus or pocket is reached. If the probe falls In most cases they are covered by gingiva. into a pit horizontally, in most cases furca- Thus, furcation involvement cannot be seen tion involvement has been detected. simply with the naked eye, but has to be Straight rigid periodontal probes (e.g. probed below the gingival margin. The PCPUNC15) are inappropriate for furcation
Figure 2.1 Curved furcation probes: Nabers probes (left: without markings; right: marked in 3 mm steps up to 12 mm). Clinical and Radiographic Diagnosis and Epidemiology 17 diagnosis because they fail to follow the rigid curved probe (e.g. Nabers probe) and curved course of most furcations. Their use measuring the distance from the probe tip to bears a high risk of underestimating the a virtual tangent to the root convexities adja- extent of the furcation involvement (Eickholz cent to the furcation (Figure 2.2). Measuring and Kim 1998). this distance allows assessment of different degrees of furcation involvement or the 2.2.1 Classification of Furcation amount of horizontal attachment loss in mil- Involvement limetres (horizontal probing/clinical attach- ment level: PAL‐H/CAL‐H; Figures 2.2–2.4). Besides the simple fact of the existence of a Whereas assessment of the continuous vari- furcation involvement and its location, the able horizontal attachment loss provides severity of furcation involvement is of major information on small changes of inter‐radicular significance. Severity of furcation involve- tissues (since they are relevant after regener- ment is assessed by probing the respective ative therapy), the categorical classification furcation in a horizontal direction using a of inter‐radicular tissue destruction as degree
(a) (b)
(c) (d)
Figure 2.2 Furcation involvement degree I (Eickholz and Staehle 1994; Table 2.4): horizontal loss of periodontal tissue support up to 3 mm: (a) schematic (maxillary molar, buccal furcation entrance): horizontal probing/clinical attachment level 2.5 mm; (b) mesial tooth 24 with neighbouring tooth; (c) buccal tooth 46: the probe does not penetrate more than 3 mm between the two buccal roots; (d) disto‐palatal tooth 16 with neighbouring tooth. 18 Chapter 2
(a) (b)
Figure 2.3 Furcation involvement degree II (Hamp et al. 1975; Tables 2.3 and 2.4): horizontal loss of support exceeding 3 mm, but not encompassing the total width of the furcation area: (a) schematic (maxillary molar, buccal furcation entrance): horizontal probing/clinical attachment level 5 mm; (b) tooth 47: the 9 mm marking is at the gingival margin. However, the 6 mm marking is at the height of the virtual tangent placed to the roots adjacent to the furcation. Source: Eickholz (2010).
of furcation involvement provides suffi- and II according to Hamp et al. (1975); that ciently relevant information for prognosis is, horizontal loss of periodontal tissue sup- and decision regarding therapy of the respec- port less than 3 mm (degree I) or exceeding tive multi‐rooted tooth. 3 mm (degree II). Degrees III and IV of the The different classifications of furcation Glickman classification describe two severity involvement basically exhibit differences grades of the situation where the desmodon- only in the details (Tables 2.2–2‐3). The clas- tal fibres are detached from the furcation sification by Glickman (1953) provides some- fornix/dome throughout the diameter of what vague criteria to distinguish classes of the tooth; that is, horizontal ‘through‐ furcation involvement, and also considers and‐through’ destruction of the periodontal radiographic information which is known to tissue in the furcation (degree III according be of low reliability (Table 2.2; Ammons and to Hamp et al. 1975). Harrington 2006). The criteria for the Hamp The criteria for assigning a degree III et al. (1975) classification are based on meas- (Hamp et al. 1975) to a furcation have also urements (threshold: PAL‐H = 3 mm). The been modified. For Graetz et al. (2014), it was colour‐coded version of the Nabers probe, required to see the tip of the furcation probe marked in 3 mm steps (PQ2N; Figure 2.1), is (Nabers) at the opposite furcation opening to particularly suitable for scoring degrees of assign a degree III. For all other cases of deep furcation involvement, according to Hamp but not completely penetrating horizontal et al. (1975; Eickholz and Kim 1998). probing, a degree II was assigned (Graetz However, there exist also furcation probes et al. 2014). Walter et al. (2009) created a with 2 mm markings (Zappa probe ZA 2). degree II–III for the situation of horizontal The distinction between degrees I and II of probing of more than 6 mm, but not com- the Glickman classification is not as clear or pletely penetrating to the opposite furcation definite as the distinction between degrees I entrance (Table 2.3). This at least partially (a) (b)
(c)
(e)
(d)
(f) (g) (h)
Figure 2.4 Furcation involvement degree III (Ammons and Harrington 2006): horizontal ‘through‐and‐through’ destruction of the periodontal tissue in the furcation: (a) schematic (maxillary molar, buccal to interproximal furcation entrance); (b) tooth 46 (occlusal view); (c) lingual view; (d) tooth 14; (e) tooth 16 without neighbouring tooth from mesio‐palatal to disto‐palatal; (f) respective radiograph; (g) tooth 46: the interdental bone is destroyed, and the soft tissues have receded apically so that the furcation opening is clinically visible. A tunnel therefore exists between the roots of such an affected tooth (Glickman degree IV); (h) respective radiograph. Source: d and e, Eickholz (2010).
Chapter No.: 1 Title Name:
Degree 0 No furcation involvement. Degree I Early/incipient stage of furcation involvement. The pocket is suprabony and primarily affects the soft tissue. Early bone loss may have occurred with an increase in probing depth. Radiographic changes are not usually found. Degree II Can affect one or more of the furcations of the same tooth. The furcation lesion is essentially a cul‐de‐sac with a definite horizontal component. If multiple defects are present, they do not communicate with each other because a portion of alveolar bone remains attached to the tooth. The extent of the horizontal probing of the furcation determines whether the defect is early or advanced. Vertical bone loss may be present and represents a therapeutic complication. Radiographs may or may not depict the furcation involvement, particularly with maxillary molars because of the radiographic overlap of the roots. In some views, however, the presence of furcation ‘arrows’ indicates possible furcation involvement. Degree III The bone is not attached to the dome of the furcation. In early degree III involvement, the opening may be filled with soft tissue and may not be visible. The clinician may not even be able to pass a periodontal probe completely through the furcation because of interference with the bifurcational ridges or facial/lingual bony margins. However, if the clinician adds the buccal and lingual probing dimensions and obtains a cumulative probing measurement that is equal to or greater than the buccal/ lingual dimension of the tooth at the furcation orifice, the clinician must conclude that a degree III furcation exists (Figure 2.5). Properly exposed and angled radiographs of early degree III furcations display the defect as a radiolucent area in the crotch of the tooth. Degree IV The interdental bone is destroyed, and the soft tissues have receded apically so that the furcation opening is clinically visible. A tunnel therefore exists between the roots of such an affected tooth. The periodontal probe passes readily from one aspect of the tooth to another.
Source: Ammons and Harrington (2006).
Table 2.3 Classification of furcation involvement according to Hamp et al. (1975).
Degree 0 No furcation involvement. Degree I Horizontal loss of periodontal tissue support less than 3 mm (Figure 2.2). Modifications by: ●● Eickholz and Staehle (1994): horizontal loss of periodontal tissue support up to 3 mm. ●● Carnevale et al. (1995): horizontal loss of periodontal support not exceeding one‐third of the width of the tooth. Degree II Horizontal loss of support exceeding 3 mm, but not encompassing the total width of the furcation area (Figure 2.3). Modifications by: ●● Carnevale et al. (1995): horizontal loss of periodontal support exceeding one‐ third of the width of the tooth, but not encompassing the total width of the furcation area. ●● Walter et al. (2009): degree II – horizontal loss of support exceeding 3 mm, but no more than 6 mm. Degree II–III ●● Walter et al. (2009): horizontal loss of support exceeding 6 mm, but no detectable ‘through‐and‐through’ destruction. Degree III Horizontal ‘through‐and‐through’ destruction of the periodontal tissue in the furcation (Figure 2.4). Modification by: ●● Graetz et al. (2014): through‐and‐through furcation (requiring seeing the tip of the Nabers probe at the contralateral furcation opening).
Source: Hamp et al. (1975).
Chapter No.: 1 Title Name:
Table 2.4 Recommended classification of furcation involvement.
Degree 0 No furcation involvement. Degree I Horizontal loss of periodontal tissue support up to 3 mm (Eickholz and Staehle 1994). Degree II Horizontal loss of support exceeding 3 mm, but not encompassing the total width of the furcation area (Hamp et al. 1975). Degree III Horizontal ‘through‐and‐through’ destruction of the periodontal tissue in the furcation. In early degree III involvement, the opening may be filled with soft tissue and may not be visible. The clinician may not even be able to pass a periodontal probe completely through the furcation because of interference with the bifurcational ridges or facial/lingual bony margins. However, if the clinician adds the buccal and lingual probing dimensions and obtains a cumulative probing measurement that is equal to or greater than the buccal/ lingual dimension of the tooth at the furcation orifice, the clinician must conclude that a degree III furcation exists (Ammons and Harrington 2006).
Sources: Hamp et al. (1975); Eickholz and Staehle (1994); Ammons and Harrington (2006). 22 Chapter 2
(Tables 2.2 and 2.4). Thus, underestimation Intrarater reproducibility in disto‐lingual of furcation involvement as observed by furcations is significantly worse than for all Walter et al. (2009) and Graetz et al. (2014) other locations. In mesio‐buccal furcations, a can be avoided. neighbouring tooth is associated with higher variability (Eickholz and Staehle 1994; Eickholz 2.2.3 The Vertical Dimension and Kim 1998). Interproximal furcations, in of Furcation Involvement particular the disto‐lingual site and in the pres- ence of a neighbouring tooth, are more difficult The central problem about furcation involve- to access and to measure than the other loca- ment is the difficult‐to‐access horizontal tions. This fact has to be kept in mind when niche between the roots of multi‐rooted the clinical examiner scores maxillary molars teeth. Thus, the classifications referred to in particular. consider mainly the horizontal component of How accurately does the clinical measure- attachment/bone loss. However, it is plausi- ment assess the intrasurgically measured fur- ble that in addition to horizontal attachment/ cation involvement (PBL‐H)? Disto‐lingual bone loss, vertical attachment/bone loss in location and a neighbouring tooth are also the furcation area plays a role. It has been associated with less accuracy. Furthermore, a demonstrated that survival of molars after curved rigid furcation probe (Nabers probe) furcation therapy does not only depend on demonstrated better accuracy than a straight baseline furcation involvement, but also on rigid (PCPUNC 15) and flexible plastic (TPS) baseline bone loss (Dannewitz et al. 2006; probe (Eickholz and Kim 1998). Interestingly, Park et al. 2009). Thus, a subclassification clinical PAL‐H measurements on average has been proposed that measures the probe- overestimated intrasurgically measured able vertical depth from the roof of the furca- PBL‐H. However, the difference was only sig- tion apically. Subclass A indicates a probeable nificant for measurements with a Nabers vertical depth of 1–3 mm, B 4–6 mm, and C probe in degree I furcation lesions (Eickholz 7 mm or more of probeable depth from the 1995; Eickholz and Kim 1998). roof of the furcation apically. Furcations would thus be classified as IA, IB, IC, IIA, 2.2.5 Documentation IIB, IIC, and IIIA, IIIB, IIIC (Tarnow and of Furcation Involvement Fletcher 1984). The more severe the vertical As documented in Chapter 5, differentiated component the worse is long-term prognosis documentation of furcation involvement of molars with degree II furcation involve- according to extent (degree) and location is a ment (Tonetti et al. 2017). Prognosis also prerequisite for proper prognosis and treat- depends on the remaining circular attach- ment planning (Figure 2.5). In the meantime, ment of each root (Walter et al. 2009). many computer programs for dental patient charting provide the necessary differentiated 2.2.4 Reproducibility and Validity digital documentation (Florida probe chart; of the Assessment of Furcation Figure 2.6). Involvement
Furcation involvement is difficult to access for 2.3 Radiographic Diagnosis hygiene. How reliably can furcation lesions be of Furcation Involvement diagnosed; that is, scored? Whereas for buccal, lingual, and mesio‐lingual scoring of furcation In general, radiographs provide information degrees excellent intrarater reproducibility is on the translucency to X‐rays of different tis- reported, disto‐lingual furcation lesions pro- sues. The denser a tissue (e.g. compact vide only moderate reproducibility. Similar bone) is, the less translucent it is for X‐rays. results are reported for PAL‐H measurements Thus, both two‐ and three‐dimensional radi- (excluding degree III furcation involvement). ographic images primarily provide information Clinical and Radiographic Diagnosis and Epidemiology 23
(a) (b)
Figure 2.5 Furcation probing at tooth 16: (a) from mesio‐palatal – probing (PAL‐H)/clinical horizontal attachment loss (CAL‐H) = 9 mm; (b) from disto‐palatal – probing (PAL‐H)/clinical horizontal attachment loss (CAL‐H) = 6 mm. In tooth 16 the PAL‐H/CAL‐H measurements add up to 15 mm. At the furcation entrances tooth 16 has a width less than 15 mm. Thus the furcation is through and through (degree III; Table 2.4). Source: Eickholz (2010).
on bone in contrast to soft tissue. However, only to a very limited extent. Only in man- furcation involvement is not only a matter of dibular molars is the fur cation channel bone, but also of connective tissue attach- located perpendicularly to the plane of the ment. Therefore, radiographs tell a substan- film/sensor and parallel to the central beam. tial part of but not the whole story about Therefore, under conditions of orthoradial furcation involvement. This is particularly projection, inter‐radicular bone may be true after regenerative treatment, where assessed in mandibular molars. However, there may be a new connective tissue attach- radiographs only provide information on ment without new bone formation within a resorption or density of bone. Reduced bone furcation. density may be due to periodontal destruc- Using two‐dimensional radiographic tech- tion or reduced bone density caused by loose niques (projection radiography: periapical spongeous structure. Thus, conventional and panoramic radiographs), reliable diagno- radiographs may only provide hints for a sus- sis of furcation involvement is not provided picion of furcation involvement; this suspi- (Topoll et al. 1988). For maxillary premolars, cion has to be confirmed or rejected by the furcation channel is oriented perpendic- furcation probing using a curved probe. ularly to the central beam. Thus, furcation Additional to degree of furcation involve- involvement in maxillary premolars cannot ment, radiographs may provide information be visualized using projection radiography. In to judge whether a buccal or lingual degree II three‐rooted maxillary molars, the furcation furcation may benefit from regenerative channel between mesio‐ and disto‐palatal therapy. In molars with class II furcation furcation entrances also runs parallel to the involvement, a long root trunk, a furcation plane of the radiographic film or sensor and fornix located coronally of the adjacent inter- perpendicular to the central beam. The buc- proximal alveolar crest, and a wide furcation cal furcation entrance is in most cases over- are associated with less favourable horizontal lapped by the palatal root. Thus, in maxillary attachment gain after regenerative therapy molars inter‐radicular bone can be judged (Horwitz et al. 2004). 24 Chapter 2
(a)
b Furkation 0 b
AL
0 b
ST/LG
0
(b) Right
Recession 222 1 3 1 111 10–1 Depth 6 3 8 3 6 3 443344
1 3 1
GM
Tooth #12345 3 33 33
GM
Depth 7 2 6 4 3 7 435435 Recession 012 131 400 000 Mobility 0 0 0 0
Figure 2.6 Differentiated documentation of furcation scores: (a) periodontal chart from the Department of Periodontology of the Johann Wolfgang Goethe‐Universität, Frankfurt am Main: tooth 17 – buccal degree I furcation; through‐and‐through furcation from mesio‐palatal to disto‐palatal (Grade III); tooth 16 – through‐ and‐through furcation at all furcation entrances; tooth 14 – distal degree I furcation. (b) Florida Probe: tooth 17 – buccal degree I furcation; through‐and‐through furcation from mesio‐palatal to disto‐palatal (Grade III); tooth 16 – through‐and‐through furcation at all furcation entrances; tooth 14 – distal degree I furcation. Clinical and Radiographic Diagnosis and Epidemiology 25
2.3.1 Digital Subtraction baseline radiograph are inverted (white to Radiography black, black to white) and added to those of the follow‐up radiograph. In two completely A highly specialized and technically sensitive identical radiographs that overlap perfectly, a radiographic method may be used to follow middle grey value will result. An increase of up changes of inter‐radicular bone in molar bone density (bony fill) results in lighter grey furcations: digital subtraction radiography values, a decrease of bone density (bone loss) in (DSR; (Eickholz and Hausmann 1997). Two darker grey values (Eickholz and Hausmann consecutively obtained radiographs (e.g. prior 1997; Figure 2.7). However, DSR requires strict to and 12 months after therapy) of the same standardization of projection geometry and is tooth are overlapped in such a way that cor- highly sensitive to misalignment. Thus, the responding structures are positioned exactly technique is rarely applied in clinical practice. over one another. The grey values of the
(a) (b)
(c) (d)
Figure 2.7 Follow‐up of inter‐radicular bone at teeth 46 and 47 using digital subtraction radiography (DSR): (a) standardized radiograph of teeth 46 and 47 prior to regenerative therapy; (b) intrasurgical view – buccal degree II furcation involvement at both teeth; (c) standardized radiograph six months after regenerative therapy; (d) subtraction image – increase of bone density within the furcations of 46 and 47. Source: Eickholz (2010). 26 Chapter 2
2.3.2 Three‐dimensional ment in maxillary molars (Walter et al. 2009, Radiography 2010, 2016). In addition, the three‐dimensional images revealed several findings, such as the Since conventional two‐dimensional radio- surrounding bony support of each maxillary graphic imaging may have some clinically rel- molar root, fusion or proximity of roots, evant drawbacks, it might be useful to analyse periapical lesions, root perforations, and/or distinct clinical situations, particularly in missing bony walls (Walter et al. 2009). The maxillary molar teeth, with a suitable three‐ clinical relevance of these radiographic data dimensional diagnostic approach with appro- was analysed regarding the decision‐making priate exposure to radiation (Laky et al. 2013; process for resective or non‐resective thera- Walter et al. 2016). Cone Beam Computed pies (Figures 2.8 and 2.9). These treatment Tomography (CBCT) has been validated in options were classified according to their vivo for the assessment of furcation‐involved graduation of invasiveness (GoI), ranging maxillary molars (Walter et al. 2016). CBCT from minimally invasive SPT to maximally data were found to be accurate in assessing invasive extraction and implant restoration: the amount of periodontal tissue loss and in GoI 0 = supportive periodontal treatment classifying the degree of furcation involve-
Figure 2.8 Diagnosis and treatment planning using cone‐beam computed tomography (CBCT). CBCT images with horizontal, sagittal, and transversal sections of first and second left maxillary molars. According to the bone loss around the disto‐buccal root and the remaining periodontal attachment around the mesio‐buccal and palatal root, it was decided to extract the distobuccal root. Source: Walter et al. (2010). Clinical and Radiographic Diagnosis and Epidemiology 27
(a) (b)
(c) (d)
(e)
Figure 2.9 Root resection in a maxillary first molar: (a) pre‐surgical view; (b) tri‐section of the distobuccal root; (c) the flap is fixed with monofil synthetic sutures 5 × 0; (d) four months post‐operation, the wound healing was uneventful; (e) a crown with an extended metal margin is placed and the patient is introduced to meticulous oral hygiene.
(SPT); GoI 1 = open flap debridement with or the entire tooth. Significant discrepancies without gingivectomy or apic ally repositioned between conventional and CBCT‐based flap and/or tunnelling; GoI 2 = root separa- treatment approaches were found in most tion; GoI 3 = amputation/trisection of one situations, which possibly necessitates intras- root (with or without root separation or tun- urgical changes in the treatment plan in those nel preparation; GoI 4 = amputation/trisec- cases where no CBCT is available (Walter tion of two roots; and GoI 5 = extraction of et al. 2009). 28 Chapter 2
However, the findings from a cost-benefit furcation involvement differentiated accord- analysis indicate the need for a critical ing to degree are rare and relatively small. appraisal of CBCT applications in upper For the third National Health and Nutrition molars (Walter et al. 2012). In most cases Examination Survey (NHANES III), 9689 with clinically based GoI ≤ 1, CBCT imaging individuals representative of the US popula- seems to have no or only minor impact on tion received periodontal examinations economic benefit and to reduce treatment including furcation scores. Partial furcation time only slightly, if at all. With more inva- involvement was scored in sites where the sive clinically based treatment decisions explorer was definitely catching into but did (GoI > 1), however, the benefits of using not pass through the furcation. This repre- CBCT were greater, probably because the sents degrees I and II of the Hamp et al. indication for tooth extraction is clarified. (1975) classification (Table 2.3). Total furca- On the one hand, a straightforward tooth tion involvement was assigned when the extraction followed by implant placement explorer could be passed between the roots and restoration is feasible, thereby avoiding and through the entire furcation. This repre- explorative periodontal surgeries when the sents degree III of the Hamp et al. (1975) tooth is not maintainable. On the other classification (Table 2.3). The prevalence of hand, unnecessary tooth extractions and furcation involvement for all age groups was implant placement in sites where teeth 13.7%, and the extent was 6.8% of posterior would be maintainable may be avoided. teeth per person. The prevalence of through‐ Moreover, root canal treatments in sites and‐through furcation involvement was 0.9% planned for GoI degrees 2, 3, or 4 may be (extent: 0.5%). The prevalence of furcation‐ prevented, when CBCT reveals morphologi- involved teeth (all/through‐and‐through) cal variations such as root proximities or increased with age (60–69 years: 27.6/2.1%; root fusions, which preclude clinically based 70–79: 31.7/3.2%; 80–89: 37.9/3.4%) and was resective treatment planning. higher in males (17.8/1.2%) than in females The main goal of diagnostic radiology is to (11.3/0.7%; Albandar et al. 1999). keep the radiation dose as low as reasonably For a sample of 71 periodontally diseased achievable (ALARA), and this should also be patients in Germany, Dannewitz et al. (2006) a prerequisite for CBCT application in den- reported tooth‐based furcation involvement; tistry, since increased radiation in the dental that is, they assigned to each molar the most office may potentially cause malignancies, severe furcation involvement that was including thyroid cancer or intracranial observed within the particular tooth. Using meningioma (Hallquist and Näsman 2001; this mode, the information relevant for prog- Longstreth et al. 2004; Hujoel et al. 2006). nosis is given for each molar. However, the The potential risks associated with additional frequency of less severe furcation degrees is radiation exposure are only justified in single underestimated. They observed degree I cases and have to be evaluated in each indi- furcation lesions in 23%, and degree II and III vidual situation. furcation lesions in 24% and 13% of all molars, respectively. No furcation involve- ment at all was exhibited in 40% of all molars. 2.4 Epidemiology of Premolars were not scored (Dannewitz et al. Furcation Involvement 2006). In a sample of 345 periodontitis patients How frequent is furcation involvement? (Eickholz et al. 2016), the degree of furcation There exists only one population‐representative involvement of all sites was reported (site study from the USA on the frequency of based). This enlarges the proportion of less furcation involvement. Even in periodontitis severe furcation lesions in comparison to patients, studies reporting the frequency of reporting tooth‐based furcation involvement. Clinical and Radiographic Diagnosis and Epidemiology 29
There was no furcation involvement in 45% 1996). Furcation involvement was found of all furcation sites, which approximately more frequently in the maxilla than in the confirms the frequency reported for molars mandible (Svärdström and Wennström 1996; (Dannewitz et al. 2006). The study observed Dannewitz et al. 2006). However, this may be degree I furcation lesions in 36%, and degree due simply to the fact that maxillary molars II and III furcation lesions in 13.5% and 5.5% have more sites at risk than mandibular of all molars and first maxillary premolars, molars (maxillary molars with three, man- respectively. Considering this and the fact dibular with two furcation entrances). that Dannewitz et al. (2006) did not report At least in periodontitis patients, furcation premolars, the data on frequency of furcation involvement is a frequent finding. In perio- lesions roughly confirm the earlier findings in dontally diseased patients, roughly one‐third a much larger sample (Eickholz et al. 2016). of all molars and almost one‐fifth of all In individuals aged 40 years or older, every furcation sites exhibit degree II and III furca- second molar was affected by advanced peri- tion involvement, which affects prognosis odontal destruction (score 2–3) in at least one and choice of therapy for the respective furcation site (Svärdström and Wennström multi‐rooted teeth.
Summary of Evidence
●● Reliable clinical furcation diagnosis involvement. However, this suspicion has requires a rigid curved furcation probe to be confirmed or rejected by furcation (e.g. colour‐coded Nabers probe). probing using a curved probe. CBCT may ●● The distinction between degree II (Hamp provide additional information for deci- et al. 1975) and through‐and‐through fur- sion-making particularly in maxillary cation (degree III) is as difficult as it is of molars if periodontal surgery is required. decisive significance for either prognosis ●● In periodontally diseased patients, roughly as well as choice of therapy. one‐third of all molars and almost one‐ ●● A modified classification of furcation fifth of all furcation sites exhibit degree II involvement is recommended. and III furcation involvement. ●● Conventional radiographs may only pro- vide hints for a suspicion of furcation
References
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Mohammadi, Z., Shalavi, S., and Jafarzadeh, H. furcation involvement. Journal of (2013). Extra roots and root canals in Periodontology 55, 283–284. premolar and molar teeth: Review of an Tonetti, M.S., Christiansen A.L., and endodontic challenge. Journal of Cortellini, P. (2017). Vertical Contemporary Dental Practice 14, 980–986. subclassification predicts survival of molars Nordland, P., Garrett, S., Kriger, R. et al. with class II furcation involvement during (1987). The effect of plaque control and root supportive periodontal care. J Clin debridement in molar teeth. Journal of Periodontol 44, 1140–1144. Clinical Periodontology 14, 231–236. Topoll, H.H., Streletz, E., Hucke, H.P., and Park, S.Y., Shin, S.Y., Yang, S.M., and Kye, S.B. Lange, D.E. (1988). Furkationsdiagnostik: (2009). Factors influencing the outcome of Ein Vergleich der Aussagekraft von OPG, root‐resection therapy in molars: A 10‐year Röntgenstatus und intraoperativem Befund. retrospective study. Journal of Deutsche Zahnärztliche Zeitschrift 43, Periodontology 80, 32–40. 705–708. Pretzl, B., Kaltschmitt, J., Kim, T.‐S. et al. Walter, C., Kaner, D., Berndt, D.C. et al. (2009). (2008). Tooth loss after active periodontal Three‐dimensional imaging as a pre‐ therapy. 2: Tooth‐related factors. Journal of operative tool in decision making for Clinical Periodontology 35, 175–182. furcation surgery. Journal of Clinical Salvi, G.E., Mischler, D.C., Schmidlin, K. et al. Periodontology 36, 250–257. (2014). Risk factors associated with the Walter, C., Schmidt, J.C., Dula, K. et al. (2016). longevity of multi‐rooted teeth: Long‐term Cone beam computed tomography (CBCT) outcomes after active and supportive for diagnosis and treatment planning in periodontal therapy. Journal of Clinical periodontology: A systematic review. Periodontology 41, 701–707. Quintessence International 47, 25–37. Sanz, M., Jepsen, K., Eickholz, P., and Jepsen, Walter, C., Weiger, R., Dietrich, T. et al. (2012). S. (2015). Clinical concepts for regenerative Does three‐dimensional imaging offer a therapy in furcations. Periodontology 2000 financial benefit for the treatment of 68, 308–332. maxillary molars with furcation involvement? Schroeder, H.E., and Scherle, W.F. (1987). A pilot clinical case series. Clinical Oral Warum die Furkation menschlicher Zähne Implants Research 23, 351–358. so unvorhersehbar bizarr gestaltet ist. Walter, C., Weiger, R., and Zitzmann, N.U. Schweizerische Monatsschrift für (2010). Accuracy of three‐dimensional Zahnmedizin 97, 1495–1508. imaging in assessing maxillary molar Svärdström, G., and Wennström, J.L. (1996). furcation involvement. Journal of Clinical Prevalence of furcation involvements in Periodontology 37, 436–441. patients referred for periodontal treatment. Wang, H.L., Burgett, F.G., Shyr, Y., and Journal of Clinical Periodontology 23, Ramfjord, S. (1994). The influence of molar 1093–1099. furcation involvement and mobility on Tarnow, D., and Fletcher, P. (1984). future clinical periodontal attachment loss. Classification of the vertical component of Journal of Periodontology 65, 25–29. 33
Chapter 3
How Good are We at Cleaning Furcations? Non‐surgical and Surgical Studies Jia‐Hui Fu1 and Hom‐Lay Wang2
1 Discipline of Periodontics, Faculty of Dentistry, National University of Singapore, Singapore 2 Department of Periodontics and Oral Medicine, School of Dentistry, University of Michigan, Ann Arbor, MI, USA
3.1 Introduction bone, leading to established periodontitis lesions (Page and Kornman 1997). The An experimental gingivitis model in humans microbial nature of periodontitis is very established that microbial plaque is the aetio- complex; it is thought that alterations in the logical factor of gingivitis (Loe et al. 1965). composition of the subgingival biofilm (dys- A 26‐year longitudinal study on well‐maintained biosis) involving ‘accessory’ and ‘keystone’ Norwegian males found that sites with per- pathogens and pathobionts drive periodonti- sistent plaque‐induced gingival inflamma- tis in a susceptible host (Hajishengallis and tion had 70% more clinical attachment loss Lamont 2012). (odds ratio [OR] = 3.22) compared to sites In order to arrest the initiation and pro- that were always healthy, thereby supporting gression of periodontitis, its management is the concept that gingivitis is a prerequisite predominantly focused on removing micro- for the inception of periodontitis (Schatzle bial plaque and its retentive factors from root et al. 2003). Microbial plaque exists in the surfaces and gingival sulci. This is primarily oral cavity as biofilms, which are consortia of achieved by professional supra‐ and subgin- micro‐organisms interacting with the sur- gival mechanical debridement, with the aim rounding environment in a dynamic manner. of disrupting the microbial biofilm growing Subgingival plaque samples from 588 patients on the root surface. Subgingival tooth with chronic periodontitis demonstrated debridement has traditionally been referred that with increasing probing depth, there was to as ‘scaling and root planing’, although the a significant increase in the ‘orange’ and ‘red importance of necessarily planing or smooth- complex’ microbes (Socransky and Haffajee ening the root surface has been questioned 2005). These Gram‐negative bacteria release (Checchi and Pelliccioni 1988; Smart et al. molecules such as lipopolysaccharide and 1990). Microbial biofilm disruption leads to a extracellular proteolytic enzymes, which reduction of the host response cascade, interact with the innate host inflammatory which halts periodontal destruction and thus surveillance system to mount an immune results in improvement of the clinical signs of response against the invading bacteria disease. Immediately after scaling and root (Darveau et al. 1997). The inflammatory planing, the denuded root surface will be response results in breakdown of the con- partially covered by fibrin and polymorpho- nective tissue attachment and supporting nuclear leukocytes. The junctional epithelium
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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will start to migrate apically towards the per- non‐surgical and surgical debridement of iodontal ligament. Granulation tissue will furcal areas, using instruments such as form in the transseptal fibre region. By the curettes, ultrasonic scalers, lasers, photody- third week, the apical migration of the junc- namic therapy, and interdental brushes. tional epithelium will terminate at the apical end of the root instrumentation, with the periodontal ligament fibres oriented parallel 3.2 Longitudinal Studies to the root surface. Some root resorption or even crestal bone loss may occur along the on Management of root surface at areas that are not covered by Furcation‐involved Teeth the long junctional epithelium. As a result, the healing after scaling and root planing is Ramfjord and colleagues first introduced therefore mainly by periodontal repair, with the concept of longitudinal studies in 1968, the formation of the long junctional epithe- where they compared different treatment lium and gingival recession (Tagge et al. modalities in a large subject population over 1975; Biagini et al. 1988). time using the split‐mouth design. This It is relatively straightforward to debride approach allowed clinicians to better appre- single‐rooted teeth; however, in multi‐rooted ciate the possible treatment outcomes that teeth the furcal areas are anatomically chal- will arise over time with minimal host varia- lenging to access because of their configura- bility. Subsequently, several research groups tions. Several anatomical factors related to have adopted this approach to evaluate the furcations and roots, covered by Pretzl in treatment outcomes of non‐surgical and Chapter 1, contribute to the aetiology and surgical debridement of single‐ and multi‐ compromised prognoses of furcation‐ rooted teeth. These studies are generally involved teeth. These factors include furca- described based on geographical locations tion entrance width, root trunk length, and and treatment modalities performed, the presence of root concavities, cervical including scaling and root planing, subgingi- enamel projections, bifurcation ridges, and val curettage, modified Widman flap, modi- enamel pearls. An evaluation of 50 mandibu- fied Kirkland’s flap, pocket elimination, and lar molars revealed variations in the furca- apically positioned flap with and without tion area, with 48%, 34%, and 18% having flat, osseous resection. Clinical parameters, such convex, and concave domes, respectively as clinical attachment level gain, probing (Matia et al. 1986). Therefore, it has been depth reduction, bleeding on probing, and reported that complete plaque and calculus plaque index, were used to determine the removal in the furcation is highly unlikely outcome of the treatment rendered. Table 3.1 (Matia et al. 1986; Parashis et al. 1993a, b; shows a summary of longitudinal studies that Kocher et al. 1998a, b). The imperfect reported data on multi‐rooted teeth. The debridement can be attributed to the pres- results described the treatment outcomes ence of difficult‐to‐reach root concavities, specific to multi‐rooted teeth. which are commonly found in the furcal Results from the Michigan longitudinal areas, with an incidence of 100% in maxillary studies reported more tooth loss in teeth premolars, 17–94% in maxillary molars, and with baseline furcation involvement (FI) 99–100% in mandibular molars (Bower despite surgical interventions, thus imply- 1979a, b; Booker and Loughlin 1985). In ing that the quality of surgical debridement addition, furcation entrances are generally or post‐surgical home or professional care narrower (less than 0.75 mm) than the blade did not deter disease progression in the long of conventional curettes (0.75–1.10 mm; term (Ramfjord et al. 1968, 1987; Wang Bower 1979a, b; Chiu et al. 1991; dos Santos et al. 1994). The authors believed that et al. 2009). Therefore, this chapter attempts although flap elevation would improve to provide an overview of the efficacy of access to the furcation areas, complete Table 3.1 Summary of some longitudinal studies that evaluated multi‐rooted teeth.
Author/ Sample No. of Follow‐Up Group Year Size Teeth Treatment Modalities Years SPT ProtocolResults
Michigan Ramfjord et al. 1968 32 729 Initial SRP with curettes. 23 monthsBaseline FI did not significantly affect CAL in molars in Subgingival curettage vs the short term. gingivectomy/APF with osseous resection as needed. Ramfjord et al. 1987 72 1881 Initial SRP with curettes. 53 months Out of 17 teeth that were lost due to periodontal reasons: Surgical pocket elimination ● 16 had FI at baseline. vs MWF vs subgingival ● 15 were treated with surgical interventions and 2 were curettage vs SRP treated with SRP. Wang et al. 1994 24 165 Initial SRP with curettes. 83 months FI molars had 2.54 times greater risk of being lost. Surgical pocket elimination vs MWF vs subgingival curettage vs SRP. Minnesota Pihlstrom et al. 1984 10 266 SRP alone vs SRP with 6.5 3–4 monthsCompar ed to non‐molars: MWF vs subgingival ● Molars with baseline PPD 4–6 mm: significantly deeper curettage vs SRP residual PPD (1.05 mm) and greater apical CAL (0.54 mm) after SRP alone. ● Molars with baseline PPD of 4–6 mm: significantly deeper residual PPD (1.02 mm) and greater apical CAL (1.27 mm) after SRP with MWF. ● Molars with baseline PPD ≥ 7 mm: no significant difference in PPD or CAL, for both treatment modalities. 9/11 teeth lost after completion of treatment were molars. Loma LindaNordland et al. 1987 19 Initial SRP with curettes 23 monthsCompar ed to non‐molar or non‐furcation sites, molar FI and ultrasonic scaler sites had: ● More bleeding on probing. ● Higher bleeding scores of 60% to 70% and > attachment loss (1 out of 5 molars) when PPDs were 7 mm or more. ● Lowest post‐treatment reduction was in PPD (1.0 mm). ● 0.5 mm loss of CAL instead of attachment gain.
(Continued)
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Author/ Sample No. of Follow‐Up Group Year Size Teeth Treatment Modalities Years SPT ProtocolResults
Loos et al. 1988 11 43 Initial SRP with ultrasonic 1.1 3 months Compared to non‐molar sites, molar FI sites had: scaler. ● Greater tendency to rebound after treatment. ● Mean probing attachment level gain of 0.1 mm (0.7 mm at non‐molar sites). ● Significantly higher microbial count. Loos et al. 1989 12 1682 Initial SRP with ultrasonic 23 months Molar FI sites: or sonic scaler. ● Similar PPD and CAL pre‐ and post‐treatment. ● With at least 7.0 mm PPD had lower PPD reduction after treatment. ● Did not have significant changes in CAL. ● Had greater percentage of sites worsening over time (38.5%). Nebraska Kalkwarf et al. 1988 82 1394 Initial scaling with curettes 23 months ● FI sites tended to progress with horizontal probing and ultrasonic scaler. attachment loss irrespective of treatment. Coronal scaling only vs SRP ● Periodontal breakdown rate was 2.6% for sites that had vs SRP with MWF vs SRP osseous resection, 5.9% for sites that had MWF, 8.4% with flap and osseous for sites that had SRP, and 8.3% for sites that had resection. coronal scaling only. North Hirschfeld and 600 15 666 SRP, gingivectomy, 15 4–6 months ● 19.3% of FI molars were lost compared to 1.7% of Carolina Wasserman 1978 gingivoplasty, and APF incisors in a well‐maintained population. with osseous surgery. McFall 1982 100 2627 SRP, curettage, gingivectomy, 15 3–6 months ● 27.3% of FI molars were lost compared to 0.6% of gingivoplasty, and APF with incisors in a well‐maintained population. osseous surgery. Wood et al. 1989 63 1607 SRP. 13.6 6–9 months ● 23.2% of FI molars were lost compared to 0.8% of incisors in a well‐maintained population.
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debridement was difficult to achieve and treatment with regular maintenance maintain post‐surgically due to the complex (Hirschfeld and Wasserman 1978; McFall configurations of the furcal area; therefore, 1982; Wood et al. 1989). furcation‐involved teeth had a poorer long‐ A group in New Jersey evaluated 384 term prognosis. In addition, it was hard to maxillary molars with varying degrees of FI maintain furcated molars, thus they had a over 5–24 years. They used a combination 2.54 times greater susceptibility of being of scaling, curettage, gingivectomy and/or lost during the periodontal maintenance gingivoplasty, and apically positioned flap phase (Wang et al. 1994). A longitudinal to manage the furcation‐involved maxillary study by the Minnesota group demonstrated molars. Their results showed that the ther- that molars compared to non‐molars had apies rendered were able to maintain maxil- significantly greater post‐treatment pocket lary molars with FI over that period, with depth and clinical attachment level changes only 12% of molars being lost over time. at sites with baseline pocket depths of However, the therapies did not have any 4–6 mm, regardless of the treatment ren- effect on the bone support, as 75% of the dered. However, at deeper sites (pocket molars had no significant changes in bone depth of 7 mm or more), no significant dif- levels. On the contrary, 11% had detectable ferences were detected between molars and bone loss and 12% were extracted (Ross and non‐molars in the long term. Although the Thompson 1978). A German group evalu- authors did not report the severity of FI in ated only molars in 136 patients over a the molars in their study, 9 out of the 11 mean follow‐up period of 13 years. They teeth that were extracted at the end of treat- reported that similar percentages of molars ment were molars (Pihlstrom et al. 1984). were lost when treated with both closed‐ The Loma Linda group evaluated the and open‐flap scaling and root planing effectiveness of plaque control and subgin- (Dannewitz et al. 2006, 2016). A group in gival root debridement of non‐molar, molar Sweden too found that reduction in the non‐furcation, and molar furcation sites mean plaque index score was greater in over a two‐year period and found that non‐molars compared to molars (Lindhe molar furcation sites had persistent inflam- et al. 1982). mation, the poorest response to treatment A review of the longitudinal studies seemed in terms of pocket depth reduction and to show that debridement of the furcation clinical attachment gain, and a significant areas during root planing or with a surgical tendency to rebound to baseline status after procedure, for instance apically positioned treatment (Nordland et al. 1987; Loos et al. flap with osseous surgery, did not signifi- 1988, 1989). The Nebraska group compared cantly improve the long‐term prognosis of coronal scaling alone, complete scaling these teeth. Although furcation‐involved and root planing alone and followed by teeth might survive in the long term, their modified Widman flap or osseous‐respec- survival rates were substantially lower than tive surgery in the management of molars single‐rooted teeth such as incisors. The with FI. Their results showed that osseous authors alluded that the anatomy of the fur- resection had the greatest probing depth cation area complicated both professional reduction with the least tendency for fur- debridement and patient home care, imply- ther breakdown (Kalkwarf et al. 1988). The ing that the quality of debridement might not North Carolina group evaluated patients be ideal and thereby indicating that molar over 13–15 years and found that molars teeth are tougher to maintain successfully with FI were lost 10–27 times more fre- over time. A summary on the long‐term sur- quently compared to incisors, despite hav- vival of molars with FI is provided in ing non‐surgical and surgical periodontal Chapter 5. How Good are We at Cleaning Furcations? 39
3.3 Professional thus could debride the hard‐to‐reach areas Debridement (Matia et al. 1986; Sugaya et al. 2002). In addition, they were able to significantly Conventionally, scaling and root planing are reduce the bacterial counts for all degrees of carried out using manual instruments, such FI and were more effective in debriding the as curettes, sickles, chisels, hoes, and files, or class II and III furcations compared to power‐driven scalers, for example sonic or curettes (Leon and Vogel 1987). A study that ultrasonic scalers. These instruments can be evaluated the efficacy of four ultrasonic used in both the non‐surgical and surgical sharp tips (Cavitron TFI 10 tip, Cavitron phases of periodontal therapy. Curettes, for EWPP [Probe] tip, Titan‐S Universal tip, and instance universal and Gracey, are double‐ Titan‐S Sickle tip) showed that there were no ended instruments with customized cutting significant differences in calculus removal edges, shank lengths, blade lengths, and when different tips were used (Patterson angulations. Therefore, each one of the nine et al. 1989). When sharp tips were compared standard Gracey curettes is designed to scale to ball tips, the Titan sonic scaler with uni- and root plane a specific area in the mouth. versal tip and Cavitron with ball tip were the These curettes have a blade width of at least most efficient at debriding both maxillary 0.76 mm and a blade length of 5 mm (Oda and mandibular molars, especially the furca- et al. 2004). tion roofs (Takacs et al. 1993). Other similar Powered scalers are either sonic or ultra- studies evaluated modified sonic tips with sonic. In sonic scalers, compressed air causes different angulations, and found that angu- the working tip to vibrate in an elliptical fash- lated tips provided a more thorough debride- ion at frequencies of 2000 to 6000 Hz under a ment because the tips could better access the water spray. Ultrasonic scalers, on the other furcations (Kocher et al. 1996, 1998a, b). In hand, are subclassified into magnetostrictive addition, some of the sonic tips had an ellip- and piezoelectric scalers. The magnetostric- soidal terminal end of 0.8 mm in diameter, tive scalers, such as Cavitron® (Dentsply, which would provide more intimate contact USA), work by creating a magnetic field with the root concavities and the furcation where an expanding and contracting coil, dome, thus improving the quality of the together with an alternating current, results instrumentation. Diamond‐coated ultra- in vibrations that are transmitted to the sonic and sonic scaler tips were found to working tip. The tip moves in an elliptical remove calculus 2–3.3 times faster than motion, thus all sides of the tip are active. In manual curettes, but they were prone to the piezoelectric scalers, such as Piezon remove cementum and dentine during Master® (EMS, Switzerland), reactive ceramic debridement (Kocher and Plagmann 1999; crystals undergo dimensional changes when Scott et al. 1999). subjected to an alternating electrical current. A study that investigated the quality of the The expansion and contraction result in mechanical and chemical debridement of root vibrations that are transmitted to the work- surfaces on 90 periodontally involved ing tip, which moves in a linear manner, thus extracted teeth found that with unlimited only the lateral sides of the tip act as the access to the root surfaces, all mechanical active sides. The average ultrasonic scaler tip debridement methods – that is, curettes, and width is 0.55 mm (Oda et al. 2004). ultrasonic with regular or diamond‐coated A comparison between the use of hand P‐10 tip – were equally effective. Thus, this instruments and ultrasonic scalers showed study suggested that access was the main criti- that the latter were better suited for the cal factor that affected the quality of root sur- debridement of narrow furcation areas, as face debridement (Eschler and Rapley 1991). their tips were narrower than curettes and In addition, it was reported that interproximal 40 Chapter 3
FIs responded less favourably to mechanical open approach, experienced periodontists debridement compared to their buccal and had 68% calculus‐free furcation surfaces lingual counterparts. This phenomenon compared to 44% with a closed approach. could be due to the increased difficulty in Although the percentages were not statisti- accessing the interproximal furcations for cally significant, they were clinically impor- debridement (Del Peloso Ribeiro et al. tant, because almost a quarter of the root 2007). surfaces had residual calculus when the Besides modifying the scaler tips, root closed approach was used. However, despite surface debridement can be performed the increased visibility with the open through a non‐surgical (closed) or surgical approach, the use of hand instruments at the (open) approach. It was reported that sig- furcal areas was ineffective (Fleischer et al. nificantly more residual calculus was found 1989; Wylam et al., 1993). in groups that had the closed approach Figure 3.1 shows an extracted maxillary (34.1–37.0%) compared to the open first molar which had received what was approach (1.0–2.7%; Matia et al. 1986). In defined as ‘deep cleaning’ by a general dental addition, clinical experience and proficiency practitioner. The tooth was extracted, since it did significantly affect the quality of debride- was deemed hopeless due to bone loss to the ment at the furcations. Less experienced apex and mobility degree III. The images residents left significantly more calculus‐ show very extensive deposits of calculus in free surfaces with the open approach (43%) the furcation region. compared to the closed approach (8%). This Table 3.2 shows a summary of the studies percentage of only 8% calculus‐free furca- that evaluated the effectiveness of mechanical tion surfaces for less experienced operators and chemical debridement at multi‐rooted with a closed approach was particularly teeth. It is obvious that there is a paucity of striking. On the other hand, there was no available literature on the effectiveness of significant difference between the open and mechanical debridement in furcation areas. closed approaches for experienced perio- A systematic review of 13 randomized dontists (Fleischer et al. 1989). Using the controlled clinical trials revealed that there
(a)
(b) (c)
Figure 3.1 The upper right maxillary molar (UR6) of a 53‐year‐old female patient affected by generalized advanced chronic periodontitis, extracted as deemed hopeless due to bone loss to the apex and mobility degree III. This tooth had received what was defined as ‘deep cleaning’ by a general dental practitioner. However, the images show very extensive deposits of calculus in the furcation region, testifying to the difficulty of achieving good subgingival debridement in furcation regions. Table 3.2 Summary of studies that evaluated efficacy of mechanical debridement.
Author/ Sample Year SizeNo. of Teeth Study DesignResults
Matia et al. 48 50 mandibular Curette (closed approach) vs curette ● Closed approach: ultrasonic scaler and curette had 1986 molars with class II (open approach) vs ultrasonic (closed 37.7% and 34.1% of residual calculus, respectively. or III FI approach) vs ultrasonic (open approach) ● Open approach: ultrasonic scaler and curette had vs no treatment. 1.0% and 2.7% of residual calculus, respectively. ● More calculus was removed with the open approach. ● Ultrasonic scaling removed more calculus in narrow furcations (<2.3 mm) compared to curette. Leon and 6 33 maxillary and Gracey curettes vs ultrasonic scaler ● Ultrasonic scaling was significantly more effective Vogel 1987 mandibular molars (Cavitron® with P‐10 tip) vs no than curettes in reducing the bacterial counts for all (class I, II, and III FI) treatment. degrees of FI. ● Ultrasonic scaling was more effective in the class II and III FI. Oda and – 120 extracted Gracey curettes #11/12 and #13/14 vs ● Mean % of residual marks that represents calculus: Ishikawa maxillary and standard tip for ultrasonic scaler (ST‐08) 15.1%, 50.3%, and 61.1% for newly designed tip, 1989 mandibular molars vs newly designed spherical tip (0.8 mm conventional ultrasonic scaler tip, and Gracey diameter). curettes, respectively, in maxillary molars (16.7%, 44.1%, and 39.5%, respectively, in mandibular molars). ● The newly designed tip produced surfaces that were as smooth as those produced by the Gracey curettes. ● The newly designed tip was more effective in debriding the furcation area. Patterson – 24 extracted Cavitron TFI 10 tip vs Cavitron EWPP ● Mean % of residual calculus: 13 mm2 , 11 mm2 , et al. 1989 mandibular molars (Probe) tip vs Titan‐S Universal tip vs 9 mm2 , and 8 mm2 for Cavitron TFI 10 tip, Cavitron mounted on a Titan‐S Sickle tip. EWPP (Probe) tip, Titan‐S Universal tip, and typodont Titan‐S Sickle tip (no significant differences). ● On average 25–30% of calculus remained after debridement. ● No significant differences between the efficacy of the four ultrasonic tips.
(Continued) Table 3.2 (Continued)
Author/ Sample Year SizeNo. of Teeth Study DesignResults
Scott et al. – 60 extracted Cavitron TFI‐10 tip vs Gracey curettes ● Ultrasonic scaling was significantly faster than 1999 mandibular molars vs fine‐ or medium‐grit diamond‐coated hand curettes in calculus removal. ultrasonic tips. Parashis 23 30 mandibular SRP with closed approach vs SRP with ● The use of the rotary diamond tip significantly et al. 1993b molars (60 open approach vs SRP with open removed more calculus in the furcation area. furcations) approach + rotary diamond instrumentation. Kocher – 24 acrylic molars Universal curettes vs sonic scaler vs ● Ultrasonic scaling was more effective than hand et al. 1996 modified sonic scaler with bud‐shaped instrumentation. tips and different angulations vs ● Specific angulations of the scaler tips were more modified sonic scaler tips with plastic suited for distal furcations or the root of the coating. furcations. ● Sonic scaler tips with plastic coatings appeared to remove only plaque and thus were not suitable for furcation debridement. Kocher – 15 extracted Curettes vs diamond bur and curettes vs ● Ultrasonic and sonic scalers cleaned only 70% of et al. 1998a maxillary and ultrasonic scaler vs sonic scaler vs the root surfaces compared to the other groups mandibular molars diamond‐coated sonic scaler tips (85%). placed in a dummy (angulated like Gracey curette #13/14 ● Only the diamond‐coated sonic scaler managed to model with 1.5 mm diameter and 45 microns effectively clean the maxillary molars (85% of the diamond grit size). root surfaces were clean compared to 75% by curettes). Kocher – 15 extracted Curettes vs diamond‐coated sonic scaler ● Mandibular molars were better debrided compared et al. 1998b maxillary and tips (angulated like Gracey curette to maxillary molars. mandibular molars #13/14 and universal curette, with 1 mm ● Diamond‐coated sonic scalers do damage the root placed in a dummy diameter and 15 microns diamond grit surfaces to the same degree as hand curettes (more model size). definitive notches were seen on the palatal roots). ● Diamond‐coated sonic scaler tips with varying angulations did improve root surface debridement.
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(Continued)
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Author/ Sample Year SizeNo. of Teeth Study DesignResults
Takacs – 100 extracted molars Cavitron® ultrasonic with 0.8 mm ball tip ● On average 74.2% of calculus was left behind at the et al. 1993 with FI vs Cavitron ultrasonic with furca roof of mandibular molars after debridement EWP12R/12 L pointed tip vs ENAC (the pointed tip and universal tip removed the most ultrasonic with furcation 0.8 mm ball tip calculus). vs EVA contra‐angle reciprocating ● On average 76.4% of calculus was left behind at the handpiece with Per‐Io‐Tor #1 and #2 tips furca roof of maxillary molars after debridement (similar to threaded fissure bur) vs (Cavitron ball tip and universal tip removed the Titan‐S sonic scaler with universal tip. most calculus). ● Titan sonic scaler with universal tip and Cavitron with ball tip were the most efficient at debriding molars. Wylam 26 60 molars with class Curettes (closed approach) vs curettes ● Molars after non‐surgical SRP: significantly greater et al. 1993 II or III FI (open approach) vs no treatment. residual calculus (54.3%) vs open approach (33.0%). ● At the furcal area, molars after non‐surgical SRP: slightly greater residual calculus (93.2%) vs open approach (91.1%). ● Hand instrumentation was unable to effectively clean the furcal area. Otero‐ – 100 artificial teethCurettes (Vision curvettes #11/12 and ● Debridement with curettes had significantly less Cagide and #13/14) vs ultrasonic with EWP‐12 L‐R residual calculus compared to ultrasonics. Lang scaler tip. 1997
FI = furcation involvement; OFD = open‐flap debridement; SRP = scaling and root planing.
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was no evidence on the efficacy of powered Other authors have also proposed the use scalers in debriding multi‐rooted teeth. This of chemotherapeutics, such as chlorhexidine, outcome needs to be interpreted with ca ution, essential oils, locally delivered tetracycline, because out of the 13 studies, 7 evaluated and doxycycline, to facilitate microbial only single‐rooted teeth, and the remaining biofilm removal at the furcation areas, with 6 studies focused on patient healing out- contradictory results. A more detailed review comes. In addition, the instruments used in of this topic is provided in Chapter 10. the studies were conventional Gracey and Figures 3.6 and 3.7 show two cases of FI Columbia curettes and Cavitron ultrasonic with pre‐, intra‐, and post‐treatment views, tips, which have thicker blade widths than the showing limitations in non‐surgical debride- instruments that are available today. The ment of furcation defects and tools used for evidence, however, did show that powered intrasurgical furcation debridement. Table 3.2 (Continued) scalers debride faster than hand curettes (Tunkel et al. 2002). Author/ Sample Year SizeNo. of Teeth Study DesignResults In recent years, advancements in material 3.4 Patient Home Care
Takacs – 100 extracted molars Cavitron® ultrasonic with 0.8 mm ball tip ● On average 74.2% of calculus was left behind at the science have allowed curettes and ultrasonic et al. 1993 with FI vs Cavitron ultrasonic with furca roof of mandibular molars after debridement tips to be stronger and thinner than in past It has been shown that poor plaque control EWP12R/12 L pointed tip vs ENAC (the pointed tip and universal tip removed the most ultrasonic with furcation 0.8 mm ball tip calculus). decades. Gracey curettes are available in results in suboptimal treatment outcome vs EVA contra‐angle reciprocating ● On average 76.4% of calculus was left behind at the handpiece with Per‐Io‐Tor #1 and #2 tips furca roof of maxillary molars after debridement different angulations, for example Gracey (Rosling et al. 1976). The clinician can (similar to threaded fissure bur) vs (Cavitron ball tip and universal tip removed the curette #17/#18, or blade widths, for instance perform effective instrumentation, but the Titan‐S sonic scaler with universal tip. most calculus). ● Titan sonic scaler with universal tip and Cavitron Micro Mini Five® Gracey curettes. The newer patient must be able to maintain the root with ball tip were the most efficient at debriding molars. Micro Mini Five curettes have a shorter blade surface free of microbial biofilm. Numerous Wylam 26 60 molars with class Curettes (closed approach) vs curettes ● Molars after non‐surgical SRP: significantly greater length (2 mm) and thinner blade width tools are available for the patient to clean et al. 1993 II or III FI (open approach) vs no treatment. residual calculus (54.3%) vs open approach (33.0%). (0.6 mm) compared to regular Gracey their furcation‐involved multi‐rooted teeth. ● At the furcal area, molars after non‐surgical SRP: slightly greater residual calculus (93.2%) vs open curettes, with a blade length and width of These are manual and powered toothbrushes, approach (91.1%). ● Hand instrumentation was unable to effectively 5mm and 0.9mm respectively. A study of 100 interspace brushes, interdental brushes, and clean the furcal area. artificial teeth used Vision curvettes that had the WaterPik®. A recent Cochrane systematic Otero‐ – 100 artificial teethCurettes (Vision curvettes #11/12 and ● Debridement with curettes had significantly less Cagide and #13/14) vs ultrasonic with EWP‐12 L‐R residual calculus compared to ultrasonics. 50% shorter blades and increased blade cur- review conducted a meta‐analysis on 51 clini- Lang scaler tip. vature to debride the furcation of mandibular cal trials concluded that powered tooth- 1997 molars. The authors reported that the modi- brushes, compared to manual ones, were FI = furcation involvement; OFD = open‐flap debridement; SRP = scaling and root planing. fied blades were more effective than ultra- more effective in reducing plaque and gingi- sonic scalers in the debridement of the val inflammation in both the short and long furcation area (Otero‐Cagide and Long term (Yaacob et al. 2014). Powered tooth- 1997). Besides curettes, ultrasonic tips are brushes have different modes of action, now slimmer with improved angulations. namely side to side, counter‐oscillation, rota- For example, the Cavitron ultrasonic tips tion oscillation, multi‐dimensional, and cir- THINserts® are 47% thinner than the cular. The rotating oscillating powered Slimline® inserts (diameter 0.5 mm), with an toothbrushes were found to significantly additional 9° backbend to gain better access reduce plaque and gingivitis in the short and to the subgingival areas. The EMS Piezon long term, with the greatest benefit at the lin- Master universal ultrasonic tips are 0.6 mm gual surfaces (Klukowska et al. 2014a, b). in diameter, and are thus able to access most Another Cochrane review evaluated 17 rand- furcation areas (<0.75 mm). Certain systems, omized controlled trials comparing the effi- such as Kavo®, have an inbuilt light‐emitting cacy of powered toothbrushes with different diode (LED) to improve visibility in the more modes of action (Deacon et al. 2010). It was posterior areas of the oral cavity. All these reported that powered toothbrushes with modifications aim to improve the access the rotation oscillation motion performed of instruments into the furcation area better than those with the side‐to‐side action. (Figures 3.2–3.5). However, limited studies with short follow‐up 46 Chapter 3
(a) (b)
(c)
Figure 3.2 (a) Mini Five® Gracey curettes #11/12 and #13/14 with blade width of 0.76 mm; (b) Micro Mini Five® Gracey curettes #11/12 and #13/14 with blade width of 0.6 mm; (c) difference in the blade widths of the Micro Mini Five Gracey curette #11/12 (left) and Mini Five Gracey curette #11/12 (right).
periods (three months or less) and unclear There is only one study that evaluated the risk of bias were included. Therefore, the efficacy of brushing instruments at the furcal results of the review should be interpreted areas (Bader and Williams 1997). The authors with caution. compared a pointed‐end tufted powered brush and a small‐head powered toothbrush, and found that the former was more effective in removing plaque at the furcal area. The pointed tip is able to fit into the furcal area to remove the plaque. As the end‐tufted brush looks simi- lar to the interspace brush, it might be inferred that the interspace brush will be effective in maintaining the furcation area free of biofilm. Interdental brushes come in various sizes and shapes. They can be conical or cylindrical in shape, have angled or straight handles, Figure 3.3 Traditional piezoelectric ultrasonic scaler have regular nylon bristles or rubber bristles, tips with a diameter of 0.7–0.8 mm. and be of different sizes. They are used to How Good are We at Cleaning Furcations? 47
Figure 3.4 EMS Piezon® Master ultrasonic scaler and tips: (a) PL1 tip with a diameter of 0.5 mm for debridement of hard‐to‐reach interproximal areas; (b) PL5 tip with a ball end of diameter 0.8 mm for debridement of furcations and concavities; (c) PS universal tip with a diameter of 0.6 mm for debridement of (a) (b) deep pockets.
(c)
The WaterPik is an oral irrigator introduced in 1962 that uses pulsating hydrodynamic force to remove food debris from the tooth surface. Its clinical benefits include removal of subgingival bacteria, clinical and histological reduction in gingival inflammation, down‐ Figure 3.5 Cavitron® Slimline™ insert with a regulation of pro‐inflammatory cytolines, diameter of 0.5 mm. reduction of probing depths, improvement of clinical attachment loss, being safe for gingival tissues, and minimal bacteremia (Jolkovsky clean the interproximal surfaces or furcation and Lyle 2015; Cutler et al. 2000). Therefore, areas. A comparison between dental floss in patients with less than ideal oral hygiene, and the interdental brush showed that the supragingival irrigation will flush out the sub- latter was significantly more effective in gingival bacteria, reducing gingival inflamma- removing plaque (mean proximal plaque tion to a degree greater than toothbrushing score: 1.22 for interdental brush and 1.71 for alone (Research, Science and Therapy dental floss; Kiger et al. 1991), hence it is Committee of the American Academy of better suited for cleaning proximal surfaces. Periodontology 2001). In comparison to the As evidenced by the significantly higher Sonicare Airfloss®, which uses a fluid spray of bleeding and plaque scores, a short‐term micro‐bubbles to disrupt the plaque, the study found that conical interdental brushes WaterPik may be more effective in terms of did not clean the lingual proximal surface as removing plaque and consequently reducing well as their cylindrical counterparts (Larsen the bleeding score (Goyal et al. 2015). et al. 2017). Also, straight brushes can clean Evidence on home care of furcations is better than angled ones (Jordan et al. 2014). scarce. As such, results from studies that It seemed that rubber‐bristled interdental assessed interproximal cleaning was used to brushes were as effective as regular interden- infer the effectiveness of these brushes in tal brushes in terms of plaque removal and removing plaque from the tooth surfaces. It patients found them more comfortable to use appears that powered toothbrushes with the (Abouassi et al. 2014). Therefore, in patients rotation oscillation action, interspace with periodontitis, and possibly interproxi- brushes, straight cylindrical interdental mal FI, interdental brushes remove more brushes with rubber or nylon bristles, and plaque than flossing or brushing alone the WaterPik are effective in cleaning inter- (Christou et al. 1998). proximal areas and potentially furcations. (a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 3.6 (a) The maxillary right first molar presented with a Grade I cervical enamel projection, 6 mm pockets, and a class II furcation. (b) Periapical radiograph showed radiolucency in the furcation area. (c) Cervical enamel projection was evident and seen protruding into the furcation. (d) Furcal area was debrided with After‐5 Gracey curettes (Hu‐Friedy, USA) and Piezo ultrasonic scalers (EMS, Switzerland). (e) Newmeyer’s rotary bur was used to remove the cervical enamel projection and any remaining granulomatous tissue. (f) Clinical photo showed the defect after cleaning. (g) Defect was grafted with human cancellous allograft (LifeNet, USA). (h) The graft was then protected with a well‐trimmed collagen membrane (2–3 mm beyond the defect margin all around).
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(i) (j)
(k) (l)
(m)
Figure 3.6 (Continued) (i) The flap was then coronally advanced and sutured. (j) At the two‐year post‐surgery follow‐up visit, the probing pocket depth at the furcation area was reduced to 3 mm and (k) radiographic bone fill was observed. (l) The furcation area remained stable clinically and (m) radiographically even at the four‐year post‐ surgery follow‐up visit. Further details and indications of furcation regenerative therapy are given in Chapter 7. 50 Chapter 3
(a) (b)
(c) (d)
Figure 3.7 The mandibular left second molar presented with a grade III cervical enamel projection, 6–8 mm pockets, and a class III furcation. (a) Residual calculus observed on flap elevation, reflecting the ineffectiveness of non‐surgical debridement. (b) Surgical open‐flap scaling and root planing with fine ultrasonic inserts (Cavitron®, Dentsply, USA) and Gracey curettes (Hu‐Friedy, USA) were performed to achieve a smooth root surface. The flap was repositioned and sutured apically, exposing the class III furcation involvement. (c) At the two‐year post‐surgery follow‐up visit, there was recurrence of the pocket to 5 mm at the midlingual site (d) with bleeding on probing, despite the patient using an interdental brush of the appropriate size and being on a strict three‐monthly periodontal maintenance regimen. This therefore concurs with the literature that plaque removal at the furcation area is unpredictable, even when exposed and visible.
Summary of Evidence
●● Longitudinal studies show that, compared ●● There is limited evidence on home care of to single‐rooted teeth, furcation‐involved furcations, however tools such as pow- teeth respond poorly to non‐surgical and ered toothbrushes, interspace brushes, surgical treatment. Improvements in the interdental brushes, and the WaterPik furcation area, if any, are also less sustain- may be useful in removing plaque from able over time. the furcation area. ●● Finer and angulated ultrasonic tips can better debride the furcation area than hand instruments, e.g. Gracey curettes. How Good are We at Cleaning Furcations? 51
References
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Chapter 4
Furcation: The Endodontist’s View Federica Fonzar and Riccardo Fabian Fonzar
Private practice, Udine, Italy
4.1 Introduction considering the inter‐radicular space only. Therefore, the present chapter aims to com- To avoid contact with the exogenous sub- prehensively detail the aetiology and devel- stances of the oral cavity, pulp and dentine are opment of endodontic‐periodontal lesions, genetically protected by the overlying enamel with particular emphasis on the diagnosis, and cementum. Despite these defensive phys- management, and long‐term prognoses of ical barriers, the pulp can be threatened by the affected teeth, especially when the furca- manifold insults, such as caries, restorative tion region is involved. procedures, and mechanical, chemical, and thermal trauma. In periodontitis‐affected 4.2 Pathways Between patients, periodontal pathogens can induce pulp infection because of the vascular inter- Endodontium and connections between periodontium and Periodontium: Anatomical endodontium. Through the accessory canals Considerations or exposed dentinal tubules, bacteria and tox- ins might gain the access to the pulp. The Because of the anatomical and vascular inter- effect is generally atrophy and is comparable connections, periodontium and endodon- with ‘pulp aging’. Likewise, endodontic infec- tium can influence each other during tions can influence periodontal health. When function and should therefore be considered the noxae of degenerated pulp involve the as one biological unit. The main pathways supporting periodontium, rapid inflamma- involved in the development of endodontic‐ tory responses, characterized by bone loss, periodontal lesions are the dentinal tubules, tooth mobility, and/or sinus tract formation, the lateral and accessory canals, and the might develop. These clinical conditions apical foramen or foramina (Seltzer et al. 1963). where both endodontium and periodontium are simultaneously affected in what appears 4.2.1 Dentinal Tubules to be a single periodontal lesion are known as endodontic‐periodontal lesions. Crown and root dentinal tubules, which Despite the topic of the book regarding extend from the pulp to the amelodentinal exclusively furcation pathology, the ethi- and dentinocemental junctions, respectively, opathogenesis of endodontic‐periodontal are permeable structures. Their permeability disease cannot be described by merely varies with regard to the dentine type, tooth
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
area, and functional tubular diameter layer that commonly shows surface defects, (Pashley 1990). for instance in the sites where Sharpey’s The root dentine is less patent than the fibres attach to its matrix (Adriaens et al. coronal. The number of tubules generally 1987). Its exposure to crevicular fluid, bacte- ranges from approximately 42 000/mm2 in rial enzymes, or acidic metabolites might the cervical area to about 8000/mm2 in the induce physicochemical and structural alter- radicular. By the lower permeability, roots ations, such as localized resorptive lacunae and furcation dentine act as a real protective or demineralization (Daly et al. 1982; barrier (Rapp et al. 1992). From the outer to Adriaens et al. 1987). It can be speculated, the closer surfaces to the pulp, tubules, which therefore, that cementum might be structur- follow an S‐shaped path, are denser, wider, ally damaged by physiological, bacterial, and more patent, and therefore greater in flow environmental factors, and that this altera- rate (Ghazali 2003). With ageing or as a tion might facilitate bacterial penetration response to continuous low‐grade stimuli, within the exposed root of periodontally diameters and patency might decrease diseased teeth. through the apposition of highly mineralized The vitality of the tooth is another variable peritubular dentine. that might play an important role in hinder- On healthy teeth, enamel and cementum ing bacteria migration towards the pulp. By usually prevent the pulpo‐dentinal complex exposing the dentine surface to the oral envi- from contact with the oral cavity micro‐ ronment for 150 days, bacterial invasion organisms. Owing to developmental defects, occurs faster in non‐vital rather than vital caries, trauma, restorative procedures, or teeth (Nagaoka et al. 1995). A possible expla- periodontal disease, cementum might not nation of this finding might be sought in the cover the underlying dentine any longer, and resistance offered by outward dentinal fluid the exposed dentinal tubules might serve as movement and the presence of odontoblast communication pathways between the endo- processes in the tubules of vital teeth dontium and periodontium (Adriaens et al. (Vongsavan and Matthews 1991, 1992; 1988; Love and Jenkinson 2002). Bacteria and Pashley et al. 2002). In addition, antibodies bacterial products can therefore induce and anti‐microbial components contained pulpal reactions by migrating towards the within the dentinal fluid might also help the pulp (Langeland et al. 1974; Bergenholtz vital teeth to be more properly defended 1981; Adriaens et al. 1988). By colonizing the (Hahn and Overton 1997). root dentine tubules of periodontally diseased teeth, pathogens might act as a reservoir for 4.2.2 Lateral and Accessory pocket recolonization after debridement Canals (Adriaens et al. 1987). As proof of this, micro- biological investigations revealed the presence An accessory canal is any branch starting of Gram‐negative and Gram‐positive species from the pulp chamber or the main root in the root dentine (Adriaens et al. 1988; canal that communicates with the external Guiliana et al. 1997). surface of the root. When the location is While it has been proved that bacteria are the coronal or middle third of the root, able to invade radicular dentine from the and the orientation is horizontal with respect periodontal pocket, it remains unclear to the main canal, accessory canals are named whether bacteria invade the healthy cemen- lateral canals (American Association of tum before penetrating the dentine, or reach Endodontists 2015). the root dentine through breaches in the It is estimated that 30–40% of teeth exhibit cementum layer (Adriaens et al. 1987, 1988; accessory canals, most of which are found in Guiliana et al. 1997; Love and Jenkinson the apical third of the root (De Deus 1975). 2002). Cementum is a thin, often discontinuous Their prevalence might vary within the teeth, The Endodontist’s View 57 and was seen to be greater in mandibular prevalence generally ranges from 23 to 76% molars and premolars than in maxillary (Lowman et al. 1973; Burch and Hulen 1974; molars and lateral incisors (Kirkham 1975). Goldberg et al. 1987), but the extension rarely In addition, it can also change according to covers the entire distance between the pulp the root third analysed. In fact, De Deus chamber and the furcation floor (Goldberg (1975) found that 17%, 9%, and less than 2% et al. 1987) and only 30–60% of molars have of teeth showed accessory canals in the api- patent canals connecting the main root canal cal, middle, and coronal third, respectively. system and the periodontal ligament (see With regard to the number of accessory Figure 4.1). In particular, mandibular molars canals per tooth, 17% and 6% of teeth have have a higher incidence (56%) than maxillary one or two accessory canals (Kirkham 1975). (48%) (Lowman et al. 1973; Gutmann 1978; Despite these anatomical considerations, the Vertucci 2005). Because of these interconnec- prevalence of periodontal disease associated tions, pulp inflammation might have detr imental with accessory canals seems to be relatively consequences on the furcation by inducing low (Rotstein and Simon 2004). inflammatory responses on the inter‐radicular In multi‐rooted teeth, furcation dentine periodontal tissues (Seltzer et al. 1963). might represent a communication pathway between endodontium and periodontium. In 4.2.3 Apical Foramen or Foramina fact, the vascular system of the pulp is con- nected to that of periodontium through the The major connections between periodontal accessory canals. At the furcation, their and pulp tissues are the apical foramina. The
(a) (b)
(c) (d)
Figure 4.1 Accessory canal located distally to the mesial root on 4.6 (LR6) (a). Interradicular radiolucency on 3.6 (LL6) (b). After root canal therapy, the accessory canal located distally to the mesial root was filled with cement (c). Complete remineralization after four‐year follow‐up (d). 58 Chapter 4
morphology of the apex might be quite varia- sealant. The faster the sealing, the more con- ble. All the teeth have at least one accessory trolled the infection. Hence, time elapsed foramen. Generally, there are fewer primary before treatment seems to be crucial for dentinal tubules in the apical root third than success. Among sealants, reinforced zinc in the coronal dentine. Their direction and oxide‐eugenol cements and bioceramic mate- density might be somewhat irregular, and rials, such as mineral trioxide aggregate, are some areas can be completely free of tubules used most for this purpose (Weldon et al. (Mjör et al. 2001). Maxillary premolars have 2002; Parirokh and Torabinejad 2010; the most complicated apical morphology with Haapasalo et al. 2015; Gorni et al. 2016). the largest accessory foramina, followed by Vertical root fractures (see Figures 4.2 and maxillary and mandibular molars (Marroquin 4.3) are generally caused by loading trauma et al. 2004), and this makes the prognosis of and occur more frequently in non‐vital teeth endodontic therapy in premolars and molars (Chan et al. 1999; Sugaya et al. 2015). In vital more uncertain than for other teeth. teeth, vertical fractures can initiate coronally in ‘cracked tooth syndrome’ (Cameron 1964) 4.2.4 Non‐physiological or can involve the root only (Chan et al. 1999; Communications Sugaya et al. 2015). While in the past endo- dontically treated teeth were considered to Root perforation, vertical root fracture, and be weaker due to structural changes in den- inflammatory root resorption are artificial tine composition, such as water and collagen pathways between periodontal and pulpal cross‐linking loss, currently it is believed that tissues. the greater brittleness is linked to the loss of Iatrogenic root canal perforations are structural integrity. In fact, the extension serious complications that originate from of cavity access might influence the degree of manual/rotatory instrumentation or post‐ cuspal deflection during function, increasing space preparation, and can threaten the the risk of fracture. Furthermore, a history of prognosis of the tooth (Tsesis et al. 2010; extensive restorations, especially in mandib- Gorni et al. 2016). The treatment outcome ular posterior teeth, might make the tooth depends on several factors that should be even more susceptible to fracture, especially evaluated early, such as the size and position in elderly patients (Lewinstein and Grajower of the root per foration, the time elapsed 1981; Huang et al. 1992; Cheron et al. 2011; before making the diagnosis and treatment, Faria et al. 2011). the degree of periodontal involvement, and Root resorption is a pathological process the sealing ability and biocompatibility of the associated with dentine, cementum, and/or (a) (b)
Figure 4.2 Vertical root fracture starting from the apex on 2.7 (UL7). The lesion resembled an endodontic infection (a). Complete failure after two years follow‐up (b). Root resection was not possible due to unfavourable anatomy. The Endodontist’s View 59
(a) (b) (c)
Figure 4.3 Vertical fracture of the distal root on 3.6 (LL6) (a). Rizectomy of the distal root (b) and after healing (c). bone loss. It can be external or internal, Similarly, endodontic infection has an anaer- depending on whether the origin is the peri- obic nature. Most of the species found in odontium or the pulp. The aetiopathogenesis infected root canals are also present in perio- is far from being completely understood. dontal pockets. However, the endodontic Mechanical and infective factors such as biofilm seems to be less complex than the orthodontic treatment, trauma, intracoronal periodontal biofilm (Trope et al. 1988; bleaching, periodontitis, and thermal stimuli Kobayashi et al. 1990; Sundqvist 1994; might be considered as predisposing factors. Kurihara et al. 1995; Zehnder et al. 2002). The presence of profuse bleeding on prob- Root canal infection is a dynamic process, ing, granulation tissue, and hard cavity and different bacterial species can apparently bottom might confirm the diagnosis of exter- prevail at different stages. The most prevalent nal inflammatory root resorption. Electric named species detected in primary endodon- and cold pulp tests might be positive. tic infections, including abscessed cases, However, sensitivity tests alone do not differ- belong to diverse genera of Gram‐negative entiate this pathological process from dental (Fusobacterium, Dialister, Porphyromonas, caries or internal resorption. Radiographic Prevotella, Tannerella, Treponema, evaluation reveals that the canal profile is Campylobacter, and Veillonella) and Gram‐ well defined in internal resorption, and positive bacteria (Parvimonas, Filifactor, rather undefined and faded in external. Pseudoramibacter, Olsenella, Actinomyces, External resorption progression (see Peptostreptococcus, Streptococcus, Propioni Figure 4.4) can lead to the invasion of the bacterium, and Eubacterium). Conversely, pulp space as a last resort. Likewise, untreated the microflora changes if endodontic therapy internal resorption can establish a communi- fails. Several culture and molecular biology cation between endodontium and periodon- studies revealed that Enterococcus faecalis is tium by breaking the external root surface the most frequent species in root canal– (Tronstad 1988; Trope 1998; Andreasen and treated teeth, with a prevalence of up to 90% Andersson 2007; Patel et al. 2010). of cases and a strong association with persis- tent infections (Rôças et al. 2004; Mohammadi et al. 2013). Canals that are apparently well 4.3 Bacteria Involved in treated might contain from 1 to 5 bacterial Endodontic‐periodontal Disease species; however, in those not properly treated, the number might vary from 10 to 30, Periodontal diseases are mixed anaerobic which is very similar to that of untreated infections, modulated by a complex interplay canals (Sundqvist et al. 1998; Pinheiro et al. between local and host factors (Page 1999). 2003; Sakamoto et al. 2008). 60 Chapter 4
Figure 4.4 Disto‐lingual external progressive root resorption on 4.7 (LR7). Initally, the invisible resorption induced pulpitis and root canal therapy was performed.
4.4 Relationship Between towards the pulp, inducing hystological Periodontal Disease and changes (Rubach and Mitchell 1965; see Histological Pulp Changes Figure 4.5). However, the deposition of repara- tive dentine (Bergenholtz and Lindhe 1978; Many controversies still exist about the rela- Nilvéus and Selvig 1983; Hattler and Listgarten tionship between periodontal inflammation 1984), the outward movement of the dentinal and pulp health (see Table 4.1). However, it fluid (Vongsavan and Matthews 1991, 1992; seems to be widely accepted that periodontitis Pashley et al. 2002), the presence of odonto- and periodontal therapy can induce pathologi- blast processes in the tubules (Nagaoka et al. cal changes in the pulp. Periodontal disease 1995; Pasley et al. 2002), and the presence of progression can lead to the exposure and bacte- antibodies and anti‐microbial components rial contamination of the accessory canals, within the dentinal fluid (Hahn and Overton more frequent in the apical third of the tooth 1997) can act as a defense system, preventing and at the furcation (Seltzer et al. 1963; Rubach the bacteria from reaching the pulp. In refer- and Mitchell 1965), or it can reach the root ence to this, we should stress that, as mentioned apex with subsequent neuro‐vascular bundle in Chapter 3, subgingival debridement is now damage (Langeland et al. 1974; De Deus 1975). moving away from the concept of ‘root planing’ Cementum removal, resulting from scaling and and ‘removal of all diseased cementum’ (Aleo root planing, can expose the dentinal tubules et al. 1974) towards an emphasis on disruption and accessory canals (Adriaens et al. 1988), of the subgingival biofilm, with minimal altera- therefore the micro‐organisms can migrate tion to the cementum (Nibali et al. 2015). Table 4.1 Effect of periodontal disease on pulp tissue.
Do progressive periodontitis and periodontal treatment affect the pulp? Pulp damage Pulp response
Progressive Yes Apex Neuro‐vascular Irreversible Inflammatory Complete necrosis periodontal Apical foramen bundle damage Degenerative disease (Langeland et al. 1974 ; Main canal involved (Rubach and Mitchell 1965 ; Zehnder 2001 ; Harrington et al. 2002 ; Sheykhrezaee et al. 2007 ; Aguiar et al. 2014 ; Sheykhrezaee et al. 2007 ; Rathod et al. 2014 ) Aguiar et al. 2014 ; Rathod et al. 2014 ) Apical root third Bacteria and toxins Irreversible Inflammatory Fibrosis (Rubach and Mitchell 1965 ; migrate towards the or Degenerative Calcification Adriaens et al. 1988 ; pulp through the Reversible (Rubach and Mitchell 1965 ; Sheykhrezaee et al. Inflammation Sheykhrezaee et al. 2007 ; accessory canals 2007 ; Rathod et al. 2014 ) Odontoblast integrity loss Zuza et al. 2012 ) Neuro‐vascular alteration Partial/complete necrosis Furcation Reparative Calcification ≈ pulp ageing (Rubach and Mitchell 1965 ; (Mazur and Massler 1964 ; Bender and Seltzer Fibrosis Bender and Seltzer 1972 ; 1972 ; Langeland et al. 1974 ; Lantelme et al. Vascular Adriaens et al. 1988 ; Zuza 1976 ; Bergenholtz and Lindhe 1978; Ross and alteration et al. 2012 ) Thompson 1978 ; Czarnecki and Schilder 1979 ; Nerve Torabinejad and Kiger 1985 ; Cortellini and alteration Tonetti 2001 ; Harrington et al. 2002 ; Aguiar et al. 2014) Periodontal Yes Neuro‐vascular Irreversible Inflammatory Complete necrosis treatment (Rubach and Mitchell 1965 ; bundle damage Degenerative (scaling and Adriaens et al. 1988 ) Main canal involved (Rubach and Mitchell 1965 ; Sheykhrezaee et al. root planing) 2007 ; Rathod et al. 2014 ) (Continued )
Chapter No.: 1 Title Name:
Do progressive periodontitis and periodontal treatment affect the pulp? Pulp damage Pulp response
Cementum removal: Irreversible Inflammatory Fibrosis bacteria and toxins or Degenerative Calcification migrate towards the Reversible (Rubach and Mitchell 1965 ; Sheykhrezaee et al. Inflammation pulp through the 2007 ; Rathod et al. 2014 ) Odontoblast integrity loss accessory canals and Vascular alteration the exposed dentinal Partial/complete necrosis tubules Reparative Calcification ≈ pulp ageing (Mazur and Massler 1964 ; Bender and Seltzer Fibrosis 1972 ; Langeland et al. 1974 ; Lantelme et al. 1976 ; Vascular Bergenholtz and Lindhe 1978 ; Ross and alteration Thompson 1978 ; Czarnecki and Schilder 1979 ; Nerve Torabinejad and Kiger 1985 ; Cortellini and alteration Tonetti 2001 ; Harrington et al. 2002 ; Aguiar et al. 2014 ) No No bacteria and Reversible Reparative dentine (Bergenholtz and Lindhe 1978 ; Hattler and Listgarten 1984 ; (Bergenholtz and Lindhe toxins migrate Vongsavan and Matthews 1991 ) 1978; Nilvéus and Selvig towards the pulp + 1983; Hattler and through the Dentinal fluid (Vongsaven and Matthews 1991, 1992; Pashley et al. 2002 ) Listgarten 1984 ; Nagaoka accessory canals and + et al. 1995 ; Hahn and the exposed dentinal Odontoblast processes (Nagaoka et al. 1995 ; Pashley et al. 2002 ) Overton 1997; Pashley tubules Antibodies/antimicrobial components within the dentinal fluids et al. 2002 ) (Hahn and Overton 1997 )
Chapter No.: 1 Title Name:
Figure 4.5 Pulp necrosis on 3.6 (LL6) after deep root debridement. Source: Courtesy Dr Cristiano Luciano. Table 4.1 (Continued)
Do progressive periodontitis and periodontal treatment affect the pulp? Pulp damage Pulp response Pulp response might vary, from normal pulp fixation is challenging and artifacts result- Cementum removal: Irreversible Inflammatory Fibrosis (Mazur and Massler 1964; Smukler and ing from improper specimen preparation bacteria and toxins or Degenerative Calcification migrate towards the Reversible (Rubach and Mitchell 1965 ; Sheykhrezaee et al. Inflammation Tagger 1976; Czarnecki and Schilder 1979; might lead to misjudgements (Harrington pulp through the 2007 ; Rathod et al. 2014 ) Odontoblast integrity loss accessory canals and Vascular alteration Torabinejad and Kiger 1985) to reparative et al. 2002; Sheykhrezaee et al. 2007). the exposed dentinal Partial/complete necrosis (Mazur and Massler 1964; Langeland et al. At the current stage of scientific knowl- tubules Reparative Calcification ≈ pulp ageing 1974; Czarnecki and Schilder 1979; edge, we could summarize that periodontal (Mazur and Massler 1964 ; Bender and Seltzer Fibrosis Torabinejad and Kiger 1985; Harrington disease might induce reparative or degenera- 1972 ; Langeland et al. 1974 ; Lantelme et al. 1976 ; Vascular Bergenholtz and Lindhe 1978 ; Ross and alteration et al. 2002) or degenerative (Rubach and tive pulp changes. Pulp necrosis is rather rare Thompson 1978 ; Czarnecki and Schilder 1979 ; Nerve Torabinejad and Kiger 1985 ; Cortellini and alteration Mitchell 1965; Sheykhrezaee et al. 2007; and occurs when the defect is up to the apical Tonetti 2001 ; Harrington et al. 2002 ; Aguiar et al. Zuza et al. 2012; Aguiar et al. 2014; Rathod third of the tooth and the neuro‐vascular 2014 ) No No bacteria and Reversible Reparative dentine (Bergenholtz and Lindhe 1978 ; Hattler and Listgarten 1984 ; et al. 2014). Repaired vital pulp is calcificated, bundle is involved. If the blood supply (Bergenholtz and Lindhe toxins migrate Vongsavan and Matthews 1991 ) fibrotic, and has fewer blood vessels and through the apical foramen remains intact, 1978; Nilvéus and Selvig towards the pulp + 1983; Hattler and through the Dentinal fluid (Vongsaven and Matthews 1991, 1992; Pashley et al. 2002) nerve fibres (Mazur and Massler 1964; the pulp is usually able to withstand the Listgarten 1984 ; Nagaoka accessory canals and + et al. 1995 ; Hahn and the exposed dentinal Odontoblast processes (Nagaoka et al. 1995; Pashley et al. 2002 ) Langeland et al. 1974; Czarnecki and Schilder physiological insults induced by both perio- Overton 1997 ; Pashley tubules Antibodies/antimicrobial components within the dentinal fluids et al. 2002 ) 1979; Torabinejad and Kiger 1985; Harrington dontal disease and therapy. (Hahn and Overton 1997) et al. 2002). Conversely, degenerated pulp exhibits fibrosis, calcification, inflammation, vascular alteration, loss of odontoblast integ- 4.5 Endodontic‐periodontal rity, and partial necrosis (Rubach and Disease Mitchell 1965; Aguiar et al. 2014; Rathod et al. 2014). Complete necrosis seems to only Because of their anatomical and functional occur if the apical neuro‐vascular bundle is interconnection, pulp and periodontium can involved (Langeland et al. 1974; Zehnder be simultaneously affected in what appears 2001; Harrington et al. 2002; Sheykhrezaee to be a single periodontal lesion. This clinical et al. 2007; Aguiar et al. 2014; Rathod et al. scenario, known as ‘endodontic‐periodontal 2014). lesion’ (Bergenholtz and Hasselgreen 2008) The lack of randomized clinical trials with was first described by Simring and Goldberg test and control groups prevents a clear asso- in 1964. ciation between progressive periodontal disease and pulp alterations being established. 4.5.1 Classification Data have to be carefully interpreted, since pulpal alterations might be the result of multi- Despite the many attempts to classify endo- ple factors, such as periodontal disease, history dontic‐periodontal lesions, the Simon, Glick, of caries, physiological pulp ageing, previous and Frank (1972) classification remains the ignored trauma, or pulp tissue fixation. Indeed, most widely accepted point of reference (see 64 Chapter 4
also Gargiulo 1984; Guldener 1985; Abbott can be positive because of the partial necrosis. and Salgado 2009; Kerns and Glickman As the lesion has an endodontic origin, root 2011). According to Simon et al., endodon- canal treatment (European Society of tic‐periodontal lesions are classified as: Endodontology 2006) is mandatory for sinus tract resolution without any associated peri- ●● Primary endodontic lesion. odontal therapy (Zehnder et al. 2002; ●● Primary periodontal lesion. Bergenholtz and Hasselgreen 2008; Shenoy ●● Primary endodontic lesion with secondary and Shenoy 2010; Kerns and Glickman 2011). periodontal involvement. Sometimes, a period of up to four or five ●● Primary periodontal lesion with secondary years might be required for the complete endodontic involvement. radiographic healing of the periapical lesion ●● True combined lesion. (Ng et al. 2007; Zitzmann et al. 2009). Incongruous root canal treatment or 4.5.1.1 Primary Endodontic Lesion untreated canals (i.e. MB2 in first maxillary Primary endodontic lesions (Box 4.1 and molars or D2 in lower molars) might prevent Table 4.2) mostly involve decayed, restored, or the lesion from healing, because of the traumatized teeth. As a result of the endodon- high residual bacterial load within the tic inflammatory process, bone resorption endodontium. occurs at the apex, along the lateral aspect of the root, or at the furcation area when multi‐ 4.5.1.2 Primary Periodontal Lesion rooted teeth are affected (see Figures 4.6 and 4.7). Periodontitis (Box 4.2 and Table 4.3) is a pro- Because of the suppurative process, the sinus gressive inflammatory process that starts in tract can develop through the periodontal lig- the sulcus and moves towards the apex due ament space or the cortical bone in accord- to the accumulation of plaque and calculus ance with the locus minoris resistentiae (place on the root surface. The final effect is the loss of least resistance) principle. For multi‐rooted of alveolar bone and supporting tissues teeth, the tract can drain off into the furcation around the teeth. This process can also be area, resembling a class III periodontal defect. accompanied by periodontal abscess in the Pain, tooth mobility, tenderness to pres- acute phases of the disease (Toto and sure and percussion, and periodontal Gargiulo 1970; Hoffman and Gold 1971). abscess‐like swelling can be the related clini- Clinical examination reveals soft‐tissue cal inflammatory signs. inflammation, tooth mobility, bleeding on Sensitivity tests show necrotic pulp, even probing, and the presence of wide pockets though in multi‐rooted teeth the response (i.e. accessible at different points on the
Box 4.1 Primary endodontic lesion.
●● Tooth history: caries, cracks, extensive restoration, crown or bridge abutment, incongruous root canal treatment, dental trauma,* root resorption.** ●● Root surface: smooth on probing. No presence of subgingival calculus. ●● Pocket conformation: narrow if the pocket is present. ●● Sensitivity pulp test response: generally negative. However, it might be positive in multi‐rooted teeth. ●● Radiographic sign: lateral, apical and/or inter‐radicular radiolucency. ●● Treatment: root canal treatment.
* Post‐traumatic pulp healing, especially after luxation injuries, is characterized by temporary loss of sensitivity. All sensitivity tests show low reliability right after the trauma (Bastos et al. 2014). ** Root resorption might affect the external surfaces of the tooth (external resorption) or the internal dentine (inter- nal resorption) after being started in the periodontium or within the pulp space, respectively. The Endodontist’s View 65
Table 4.2 Primary endodontic lesions.
Diagnostic Elements Findings Clinical Management
Presence of caries/restorations/cracks + Anamnesis Clinical examination Subgingival calculus − Periodontal probing History of trauma +/− Radiographic examination Sensitivity tests Abscess +* Endodontic treatment Narrow deep pocket +/− Re‐evaluation after a few months Bleeding on probing − Thermal test −/+** Electric test −/+** Radiolucency + Mobility +/− Palpation test + Percussion test + * In the acute phase. ** The test is negative if all the pulp tissue is necrotic, except in case of gases‐related thermal expansion. The test could be positive in case of partial necrosis.
Differential Diagnosis Vertical root fractures Primary periodontal lesions Favourable Endodontic Congruous endodontic treatment Prognostic Factors No symptoms No probing within 30 days Fistular track closure within 30 days Radiolucency improvement within 6 months
Source: Adapted from AIE – Collana di Monografie Piccin Nuova Libraria S.p.A 2014.
Figure 4.6 Pulpitis on 3.6 (LL6). Inter‐radicular and periapical radiolucencies due to bacterial toxins. Five‐year follow‐up after root canal therapy. 66 Chapter 4
Figure 4.7 Primary endodontic lesion with inter‐radicular and apical involvement on 4.6 (LR6). No furcation probing after three months and partial healing after one‐year follow‐up.
On the basis of the previous considera- Box 4.2 Primary periodontal lesion. tions, the prognosis would mainly depend on ●● Tooth history: periodontal pocket, attach- the extension of the periodontal disease, the ment loss, bleeding on probing. outcome of the periodontal therapy, and the ●● Root surface: rough on probing because patient’s ability to comply with potential of subgingival plaque and calculus. long‐term maintenance (Bergenholtz and ●● Pocket conformation: wide, often multiple Hasselgreen 2008; Kerns and Glickman pockets. 2011). ●● Sensitivity pulp test response: generally positive. Primary Endodontic Lesion with Secondary ●● Radiographic sign: lateral and/or inter‐ Periodontal Involvement radicular radiolucency, apical radiolu- Periodontal pathogens might induce perio- cency in advanced disease. dontitis by migrating apically into the patent ●● Treatment: oral hygiene instructions (OHI) sinus tract when the endodontic infection is and root debridement. not treated or persists after root canal ther- apy. At the radiographic evaluation, angular intrabony or inter‐radicular osseous defects tooth) supported by plaque and calculus are appreciated. Plaque and calculus are along the root. It should be noted that perio- detected on probing, therefore healing dontal pockets might also originate from requires both endodontic and periodontal anomalies in the root development (Rotstein therapies for necrotic pulp removal and root and Simon 2004). During the diagnostic debridement. Since root canal treatment phase, pulp sensitivity tests generally reveal resolves only a part of the defect (European positive responses. However, negative Society of Endodontology 2006; Shenoy and responses can also be recorded and do not Shenoy 2010), dental prognosis relies on the necessarily account for pulp necrosis. Owing extent and severity of the osseous defect, and to dystrophic calcifications, the pulp space on the efficacy of the periodontal therapy. might be reduced and the tooth might not For suppurative processes fistulizing respond to the sensitivity tests despite its through the cortical bone, bacteria from the vitality (Abou‐Rass 1982). oral cavity might colonize first the fistula and The Endodontist’s View 67
Table 4.3 Primary periodontal lesions.
Diagnostic Elements Findings Clinical Management
Presence of caries/restorations/cracks +/− Anamnesis Clinical examination Subgingival calculus + Periodontal probing History of trauma +/− Radiographic examination Sensitivity tests Abscess +* Splinting of mobile teeth (if needed) Wide, not isolated, deep pocket/furcation + Oral hygiene instructions and periodontal Bleeding on probing + non‐surgical therapy Periodontal re‐evaluation after a few months Thermal test + Periodontal surgical therapy (if needed) Electric test + Lateral/interradicular radiolucency + Mobility + Palpation test +* Percussion test +* * In the acute phase.
Differential Diagnosis Endodontic‐periodontal lesions Favourable No symptoms Prognostic Factors Pulpal vitality No bleeding on probing Probing pocket depth reduction Mobility reduction Radiographic bone remineralization in the apical part of the defect
Source: Adapted from AIE – Collana di Monografie Piccin Nuova Libraria S.p.A 2014. then the apex, affecting the tooth prognosis. Primary endodontic lesion with secondary Box 4.3 Primary endodontic lesion periodontal involvement (Box 4.3 and with secondary periodontal involvement.
Table 4.4) might also occur in endodontically ●● Tooth history: caries, cracks, extensive treated teeth because of root perforation restoration, crown or bridge abutment, and/or fracture. Once the communication incongruous root canal treatment, dental between endodontium and periodontium is trauma. established, the secondary periodontal lesion ●● Root surface: rough on probing because can develop as a result of the micro‐organ- of subgingival plaque and calculus. isms’ migration from the root canal to the ●● Pocket conformation: narrow to wide, periodontium. depending on the exposition time The clinical signs may range from local of the sinus tract to periodontal periodontal pocket deepening to abscess for- pathogens. mation associated with pain, exudate, and ●● Sensitivity pulp test response: negative. tooth mobility. In single‐rooted teeth, the ●● Radiographic sign: lateral, apical, and/or prognosis is usually poor if the defect is close inter‐radicular radiolucency. to the apex. In multi‐rooted teeth, the prog- ●● Treatment: root canal treatment, oral nosis might be better, since the tooth can be hygiene instructions (OHI), and root maintained by resecting the affected root, if debridement. the anatomy is indicated for this procedure 68 Chapter 4
Table 4.4 Primary endodontic lesions with secondary periodontal involvement.
Diagnostic Elements Findings Clinical Management
Presence of caries/restorations/cracks + Anamnesis Clinical examination Subgingival calculus + Periodontal probing History of trauma +/− Radiographic examination Sensitivity tests Abscess +* Splinting of mobile teeth (if Narrow to wide deep pocket + needed) Bleeding on probing + Oral hygiene instructions and non‐surgical periodontal therapy§ Thermal test − Endodontic treatment Electric test − Re‐evaluation after a few months Surgical periodontal therapy (if Radiolucency + needed) Mobility + Palpation test + Percussion test + * In the acute phase § Deep Root Debridement Should Be Avoided Before Determining The Endodontic Component Of The Defect (See Section 4.5.3) Differential Diagnosis Primary periodontal lesion with secondary endodontic involvement Vertical root fracture Root/furcation perforation in endodontically treated teeth Favourable Endodontic Congruous endodontic treatment Prognostic Factors No symptoms Partial probing depth reduction within 30 days Fistular track closure within 30 days Mobility reduction Partial radiolucency improvement within 6 months
Source: Adapted from AIE – Collana di Monografie Piccin Nuova Libraria S.p.A 2014.
(Cameron 1964; Chan et al. 1999; Zehnder Box 4.4 Primary periodontal lesion with et al. 2002; Sunitha et al. 2008; Kerns and secondary endodontic involvement.
Glickman 2011; Sugaya et al. 2015; see also ●● Tooth history: probing pocket depth Chapter 8). deepening, bleeding on probing. ●● Root surface: rough on probing because Primary Periodontal Lesion with Secondary of subgingival plaque and calculus. Endodontic Involvement ●● Pocket conformation: wide, often multiple Primary periodontal lesion with secondary pockets. endodontic involvement (Box 4.4 and ●● Sensitivity pulp test response: generally Table 4.5) differs from primary endodontic negative. lesion with secondary periodontal involve- ●● Radiographic sign: lateral, apical, and/or ment only in the temporal sequence of the inter‐radicular radiolucency. disease processes. If periodontitis remains ●● Treatment: root canal treatment, oral hygiene untreated, periodontal pathogens can reach instructions (OHI), and root debridement. the pulp through the accessory canals or The Endodontist’s View 69
Table 4.5 Primary periodontal lesions with secondary endodontic involvement.
Diagnostic Elements Findings Clinical Management
Presence of caries/restorations/cracks +/− Anamnesis Clinical examination Subgingival calculus + Periodontal probing History of trauma +/− Radiographic examination Sensitivity tests Abscess +* Splinting of mobile teeth (if Not isolated, wide deep pocket/furcation + needed) Bleeding on probing + Oral hygiene instructions and non‐surgical periodontal therapy§ Thermal test −** Endodontic treatment Electric test −** Periodontal re‐evaluation after a few months Lateral/apical/inter‐radicular radiolucency + Surgical periodontal therapy (if Mobility + needed) Palpation test + Percussion test + * In the acute phase. ** The test is negative if all the pulp tissue is necrotic, except in case of gases‐related thermal expansion. The test could be positive in the case of partial necrosis. § Deep Root Debridement Should Be Avoided Before Determining The Endodontic Component of The Defect (See Section 4.5.3) Differential Diagnosis Primary endodontic lesions with secondary periodontal involvement Favourable Endodontic Congruous endodontic treatment Prognostic Factors No symptoms Partial probing depth reduction within 30 days Fistular track closure within 30 days Mobility reduction Partial radiolucency improvement within 6 months
Source: Adapted from AIE – Collana di Monografie Piccin Nuova Libraria S.p.A 2014.
apical foramina. Pulp necrosis occurs and an generalized periodontitis might suggest a endodontic‐periodontal lesion develops primary periodontal origin. The number and (Rubach and Mitchell 1965; Aguiar et al. conformation of pockets can help in the 2014). Periodontal therapy can also lead to diagnosis. Wider or narrower defects gener- secondary pulp involvement. By exposing ally suggest a periodontal or endodontic lateral canals and dentine during scaling and origin of the lesions, respectively (Zehnder root planing or surgical flap procedures, et al. 2002; Sunitha et al. 2008; Kerns and blood supply might be interrupted and Glickman 2011). In addition, periodontal micro‐organisms might penetrate into the probing may reveal the presence of calculus tubules, resulting in pulp inflammation and/ on the root surface. Pulp sensitivity tests are or necrosis (Adriaens et al. 1988). generally negative when the endodontium is To differentiate between endodontic‐ involved, whereas the radiographic evalua- periodontal lesions with primary periodontal tion does not prove the primary origin of the and endodontic origin, anamnesis and lesion. clinical examination have to be exhaustively Once the endodontic therapy is properly per- performed (see Figure 4.8). A history of formed (European Society of Endodontology 70 Chapter 4
Figure 4.8 Degree III furcation involvement on 4.6 (LR6) with progressive deepening of the defect and secondary pulp necrosis after 14 years. Root canal therapy led to resolution of the endodontic component of the defect. Besides scaling and root planing and oral hygiene instructions, no further periodontal treatment was performed.
2006; Shenoy and Shenoy 2010), clinical success basically depends on the outcome of the Box 4.5 True combined lesions.
periodontal therapy and the patient’s ability to ●● Tooth history: caries, cracks, extensive comply with potential long‐term maintenance. restoration, crown or bridge abutment, As previously mentioned, multi‐rooted teeth incongruous root canal treatment, dental might have a better prognosis than single‐ trauma, probing pocket depth deepen- rooted teeth, since root resection represents an ing, bleeding on probing. alternative for tooth survival. ●● Root surface: rough on probing because of subgingival plaque and calculus. True Combined Lesion ●● Pocket conformation: wide and conical A true combined lesion (Box 4.5 and pocket. Table 4.6) means that the endodontic and ●● Sensitivity pulp test response: negative. periodontal infections simultaneously exist ●● Radiographic signs: communicating or as independent, separated, or merging non‐communicating extensive apical, lat- lesions. When the periodontal pocket deep- eral, and/or inter‐radicular radiolucencies. ens up to the periapical lesion, the endodon- ●● Treatment: root canal treatment, oral hygiene tic and periodontal components of the defect instructions (OHI), and root debridement. are unidentifiable. Symptoms are similar to The Endodontist’s View 71
Table 4.6 True periodontal‐endodontic combined lesions.
Diagnostic Elements Findings Clinical Management
Presence of caries/restorations/cracks + Anamnesis Clinical examination Subgingival calculus + Periodontal probing History of trauma +/− Radiographic examination Sensitivity tests Abscess +* Splinting of mobile teeth (if needed) Not isolated, wide deep pocket/furcation + Oral hygiene instructions and § Bleeding on probing + non‐surgical periodontal therapy Endodontic treatment Thermal test − Periodontal re‐evaluation after a Electric test − few months Surgical periodontal therapy (if Lateral/apical/inter‐radicular radiolucency + needed) Mobility + Palpation test + Percussion test + * It depends on whether the phase is acute or chronic. § Deep Root Debridement Should Be Avoided Before Determining The Endodontic Component Of The Defect (see Section 4.5.3)
Differential Diagnosis Vertical root fracture Favourable Endodontic Congruous endodontic treatment Prognostic Factors No symptoms Partial probing depth reduction within 30 days Fistular track closure within 30 days Mobility reduction Partial radiolucency improvement within 6 months
Source: Adapted from AIE – Collana di Monografie Piccin Nuova Libraria S.p.A 2014. those previously mentioned for the com- multi‐rooted teeth, since root resection might bined lesions with primary endodontic or be a treatment option if not all the roots are periodontal origin. The radiographic evalua- severely involved and tooth anatomy is indica- tion shows extensive osseous radiolucencies, tive for this procedure (Zehnder et al. 2002; communicating or not, similar to those of Rotstein and Simon 2004; Sunitha et al. 2008). vertically fractured teeth. Indeed, pulp space invasion through vertical root fracture might 4.5.2 Diagnosis of Endodontic‐ also be considered as a true combined lesion. periodontal Disease Prior to endodontic therapy, mobile teeth should be splinted and carefully debrided. Diagnosis of endodontic‐periodontal lesions Once the root canal treatment is properly per- can be easily performed when the patient has formed (European Society of Endodontology been monitored over time. Similar clinical 2006), the endodontic component of the and radiographic findings might make the defect is expected to heal within a couple of differential diagnosis somewhat challenging. months (Shenoy and Shenoy 2010; see To avoid any misinterpretation, comprehen- Figure 4.9). Tooth prognosis would entirely sive information can be obtained through depend on both the periodontal pocket depth detailed anamnesis and clinical examination, and the related periodontal therapy. Uncertain and by the use of specific tests aimed to assess prognosis concerns more single‐rooted that the vitality of the pulp. Primary endodontic 72 Chapter 4
Figure 4.9 Class 3 inter‐radicular defect and concomitant decay of the furcation roof on 4.7 (LR7). The caries progression led to pulp necrosis. Tunnelling spontaneously occurred after non‐surgical periodontal treatment. One‐year follow‐up after root canal therapy.
lesions generally originate from infected and 4.5.2.3 Percussion non‐vital pulp, whereas vital teeth are more This test indicates the presence of periradic- characteristic of primary periodontal disease ular inflammation without revealing the (Rotstein and Simon 2004; Bergenholtz and status of the pulp. An abnormal positive Hasselgreen 2008; Sunitha et al. 2008; Parolia response shows inflammation of the perio- et al. 2013). dontal ligament, but it does not indicate whether the origin is endodontic or perio- 4.5.2.1 Clinical Examination dontal. The test should be compared to Pulpal and periodontal diseases might have control teeth. many clinical signs in common, such as gin- gival swelling, pus discharge, probing, tooth 4.5.2.4 Bite Test mobility, and tenderness to percussion. Teeth This test does not disclose the condition of have to be evaluated for caries, incongruous the pulp. However, it might be positive in under‐ or over‐contoured restorations, loss vital teeth affected by cracked tooth syn- of marginal seal, erosions, abrasions, cracks, drome (Cameron 1964) and in non‐vital and fractures. All these situations are more teeth with periradicular inflammation. related to endodontic disease. 4.5.2.5 Mobility 4.5.2.2 Palpation This clinical sign does not prove whether the Palpation is performed by applying firm dig- origin of the lesion is primarily periodontal ital pressure in correspondence with the or endodontic. It might be speculated that its root and the apex, with the index finger primary cause is periodontitis. In fact, tooth pressing the mucosa against the underlying mobility depends on the amount and inflam- cortical bone. A positive response might mation of the residual supporting tissues. indicate an active periradicular inflamma- The greater the bone loss, the higher the tory process. However, this test does not mobility. However, periradicular oedema or indicate whether the origin is endodontic or trauma, with or without tooth fracture, can periodontal. The test should be compared to also lead to similar mobility (Biancu et al. control teeth. 1995; Séguier et al. 2000). The Endodontist’s View 73
4.5.2.6 Fistula Tracking under‐contoured restorations, pulp caps, Endodontic and periodontal diseases can periradicular radiolucencies, periodontal lead to the formation of a fistulous sinus ligament widening, calculus, alveolar bone track. Following a minor resistance path, loss, and root fractures, this examination inflammatory exudate drains off into the oral alone does not indicate whether the radiolu- mucosa through the attached buccal gingiva cency has an endodontic, periodontal, or any or the vestibule. The track is generally more additional origin. It is important to consider representative of the endodontic infection that some other pathologies, such as cysts rather than the periodontal disease, which and neoplasia, can resemble periodontal or often drains through the periodontal pocket endodontic lesions in radiographic without any fistulous sinus track formation. appearance. Fistula tracking is performed by inserting a Occlusal trauma may also lead to radio- semirigid radiopaque material, commonly a graphic radiolucencies on the lateral, apical, gutta‐percha cone, into the sinus track until or inter‐radicular aspect of the root. In resistance is met (see Figure 4.10). A radio- periodontally involved teeth suffering from graph is taken to identify the course of the occlusal trauma, the amount of deminerali- sinus tract and, therefore, the tooth involved. zation is not quantitatively reflected in the probing pocket depth, which is less deep 4.5.2.7 Cracked Tooth Testing than could be guessed radiographically. Cracked teeth (Cameron 1964) or vertical Occlusal adjustment might be necessary and root fractures can be diagnosed through the must always precede any endodontic or observation of incomplete or complete periodontal therapy. Demineralization cracks by transillumination. The fibre‐optic resolves within a few months when the light source is directly placed on the cleaned occlusal interferences and the mobility are tooth. Cracks can be appreciated with a mag- eliminated by grinding and splinting, respec- nification source by evaluating the disrup- tively [75,81,96,97] (Bergenholtz and tion of the light transmission (Liewehr 2001; Hasselgreen 2008; Carnevale et al. 2008; Liewehr et al. 2010). Unlike a vertical root Lindhe et al. 2008; Kerns and Glickman 2011; fracture with a ‘tear‐shaped’ radiographic see Figures 4.11 and 4.12). radiolucency, cracked teeth do not generally show any pathognomonic radiographic signs. 4.5.2.9 Pocket Probing To assess whether the origin of the lesion is 4.5.2.8 Radiographs endodontic or periodontal, probing can be Despite the benefits of radiographs, consist- crucial in the diagnosis (Harrington and ing in the detection of caries, over‐ or Steiner 2002). Defects are evaluated for (a) (b)
Figure 4.10 Fistulous sinus track between 1.6 (UR6) and 1.7 (UR7) (a). Fistula tracking revealed the origin of the endodontic infection on 1.7 (b). 74 Chapter 4
(a) (b)
Figure 4.11 Radiographic radiolucency on 3.6 (LL6) affected by secondary occlusal trauma without furcation involvement (a). Six‐month follow‐up after root debridement and occlusal adjustment (b). Source: AIE—Collana di Monografie Piccin Nuova Libraria S.p.A 2014, p. 139.
Figure 4.12 Degree II furcation defect (lingual) on 3.6 (LL6) affected by secondary occlusal trauma. Being the possible result of jiggling movements, the apical radiolucency present on the mesial root disappeared after the occlusal adjustment. Twenty‐year follow‐up after non‐surgical periodontal therapy and oral hygiene instructions. Source: AIE—Collana di Monografie Piccin Nuova Libraria S.p.A 2014, p. 140.
extent, severity, and shape by means of a of the defect without any further concomi- calibrated periodontal probe. The presence tant causes, such as vertical root fracture or of plaque and calculus, detected by sounding periodontal involvement. On the contrary, a the root surface with the tip of the probe, persisting sinus track might imply periodon- explains the periodontal involvement, tal involvement or unsolved endodontic although this may not be necessarily easy to infection (Harrington and Steiner 2002; detect. Primary periodontal lesions are fre- Walton and Torabinejad 2002; Rotstein and quently characterized by wide calculus‐ Simon 2004). induced defects in patients with further periodontal pockets, whereas primary endo- 4.5.2.10 Pulp Vitality Tests dontic lesions typically show narrow solitary Pulp vitality tests are very important to eval- calculus‐free defects. Inter‐radicular involve- uate whether the lesion has an endodontic or ment without further signs of periodontal periodontal origin (Walton and Torabinejad disease might indicate the endodontic origin 2002). The sensitivity rather than the vitality of the lesion. of the pulp is assessed through sensory nerve Periodontal probing can be considered as a stimulation. Two different stimuli, electric prognostic indicator in the short term. In and/or thermal (cold or hot), can be applied, fact, early fistulous sinus track resolution and complaints and painful sensations are after root canal therapy (Shenoy and Shenoy recorded. Figure 4.13 summarizes the diag- 2010) might confirm the endodontic origin nostic tests for pulp health assessment, and The Endodontist’s View 75
Figure 4.13 Diagnostic tests for pulp health assessment. Source: AIE—Collana di Monografie Piccin Nuova Libraria S.p.A 2014, pp. 266–268, 271.
Box 4.6 considers how sensitivity tests might negatives can be wrongly recorded (Abou‐ be misinterpreted. Rass 1982; Mejàre et al. 2012; Levin 2013). A Vital teeth react to cold and hot stimuli by lack of response is often associated with pulp exhibiting short‐lasting sharp pain or mild necrosis (Rowe and Pitt Ford 1990; Peters heat sensation, respectively. Intense and et al. 1994). long‐lasting painful reactions might indicate Vital teeth react to an electric test by exhib- irreversible pulp changes. In molars, tissue iting tingling, slight discomfort, or a burning degeneration might be limited to part of the sensation. Scored values per se do not mean pulp only (see Figure 4.14) and the reliability the presence or absence of pathology, since of the tests might be questioned, as false no general threshold for pulpal disease has been established so far. As a general rule, the Box 4.6 Clinical situations where pulp higher the scored values, the higher the prob- response to sensitivity tests might be ability of irreversible pulpal alterations. To misinterpreted. better assess the response, healthy teeth should be taken as controls. By comparing the ●● Teeth with calcified root canals. values obtained at different follow‐up stages, ●● Multi‐rooted teeth with partially affected pulp. more clinical information is provided for the diagnosis. However, false negatives and posi- ●● Teeth with partial‐ or full‐coverage restorations. tives might make clinical evaluation some- what challenging (Rotstein and Simon 2004; ●● Traumatized teeth. Gopikrishna et al. 2007; Chen and Abbott ●● Endodontically treated teeth with untreated canals. 2009; Jafarzadeh and Abbott 2010; Mejàre et al. 2012; Alghaithy and Qualtrough 2017). 76 Chapter 4
Figure 4.14 Pulp necrosis limited to the distal root on 4.6 (LR6) and result after root canal therapy.
While a lack of response can be associated pulp blood flow through laser doppler flow- with pulp necrosis, exaggerated or misleading metry or similar procedures. Many investiga- responses following cold or electric tests can tions have been conducted to validate the be the result of pulpitis, patient anxiety, efficacy of these tests. However, their clinical dentinal hypersensitivity, trauma, or enamel‐ applicability is still questioned (Gopikrishna to‐dentine cracks (Abou‐Rass 1982; Eli 1993; et al. 2007; Mejàre et al. 2012; Alghaithy and Peters et al. 1994; Bastos et al. 2014). Cold and Qualtrough 2017). hot stimuli can respectively mitigate or exacer- bate the symptoms in partially necrotic teeth. 4.5.2.11 Cavity Test Vital teeth with a history of deep caries, By drilling the cavity without anaesthetic, the periodontitis, bruxism, or trauma may not pulp status can be objectively evaluated respond to thermal or electrical stimuli through patient‐referred symptoms. The so‐ because of the reparative changes in the pulp called cavity test can be performed when all tissues (Bastos et al. 2014). Partial‐ or full‐ the aforementioned tests have failed to give coverage restorations can also act as a barrier comprehensive information about the vitality to thermal and, to a lesser degree, electrical of the pulp. Positive and negative responses stimuli, preventing the pulp from being indicate vital and necrotic pulp, respectively. properly evaluated (Rowe and Pitt Ford 1990; If no symptoms are reported by extending Peters et al. 1994; Myers 1998; Petersson the cavity towards the pulp chamber, partial et al. 1999). or complete pulp necrosis is confirmed and The vitality rather than the sensitivity of the endodontic treatment can be started the pulp can be assessed by measuring the (Kerns and Glickman 2011). The Endodontist’s View 77
4.5.2.12 Selective Anaesthesia Test Despite the similar clinical and radio- To determine the origin of pain, teeth might graphic findings, the presence of plaque and be selectively anaesthetized by carefully calculus is crucial for the diagnosis and prog- injecting the anaesthetic through the perio- nosis of combined or true endodontic‐ dontal ligament. Periodontal intraligament periodontal lesions. From a treatment injection is limited to a single tooth without viewpoint, the calculus, if present, might be involving the adjacent teeth. The test is use- useful to detect the limit between the perio- ful to identify the origin of pulpitis‐related dontal (rough surfaces due to calculus) and radiating pain (D’Souza et al. 1987; Rotstein endodontic component of the defect (smooth and Simon 2004). surfaces without calculus). When this differ- ential diagnosis is not possible, deep and 4.5.3 Management of heavy debridement should be avoided before Endodontic‐periodontal Disease root canal therapy, since healthy cementum might be wrongly removed, and a second re‐ To properly manage endodontic‐periodontal evaluation of the site should be made two to pathology (Box 4.7; Berner and Graber 2008), three months after the endodontic treatment prognosis and treatment decision‐making (Zehnder 2001; Parolia et al. 2013; Paul and should be based on scrupulous diagnosis. Hutter 1997). This time is required for the The pulp should be assessed for sensitivity, initial bone remineralization, thus the extent whereas bone defects should be assessed for of the periodontal component can be more severity, extension, and shape. precisely assessed. Primary endodontic disease is character- Tooth maintainability should be deeply ized by necrotic pulp and narrower calculus‐ questioned once the extent of the defect is free defect, thus the prognosis would mainly seen to depend more on periodontal than depend on the outcome of root canal therapy. endodontic disease. The prognosis depends Once calculus‐related pockets are excluded on periodontal disease severity, overall treat- and root canal treatment is properly per- ment execution, and patient response, formed, the diagnosis of primary endodontic motivation, and compliance. Cases of true lesions is confirmed by the disappearance of combined disease might have more a guarded symptoms, physiological values on soft tissue prognosis than the combined endodontic‐ probing, and bony remineralization on recall periodontal lesions (Paul and Hutter 1997; radiographs. Rotstein and Simon 2004; Bergenholtz and Primary periodontal lesions show vital Hasselgreen 2008; Kerns and Glickman 2011; pulp and a wide calculus‐associated pocket. Schmidt et al. 2014). In this case, the prognosis depends on peri- odontal disease severity, treatment execu- 4.5.4 Endodontic‐periodontal Disease tion, and patient response, motivation, and in Endodontically Treated Teeth compliance. Sensitivity tests cannot be used for diagnostic purposes in endodontically treated teeth. Improper root canal treatment (see Figure 4.15) Box 4.7 Proper management of or iatrogenic injuries (see Figure 4.16), such as endodontic‐periodontal pathology. stripping or perforation, should be radio-
●● Collect all the information referred to by graphically detected to determine whether the the patient (i.e. previous trauma, pulp origin of the lesion is endodontic, particularly capping). if there are no signs of periodontal disease. The ●● Perform all the tests mentioned. diagnostic dilemma can only be solved through ●● Match and interprete the data collected. proper endodontic retreatment. By controlling the infection, clinical and radiographic healing 78 Chapter 4
Figure 4.15 True combined lesion on 3.6 (LL6) with an incongruous root canal therapy. The endodontic infection led to the apical resorption of the distal root. Despite the inter‐radicular radiolucency, furcation probing was negative. A periodontal defect was present on the distal aspect of the tooth. Two‐year follow‐up after non‐surgical periodontal therapy, oral hygiene instructions, and root canal retreatment.
Figure 4.16 Inter‐radicular defect on 3.6 (LL6) due to stripping of the mesial root and results after rizectomy.
can be expected within two to three months 4.6 Relationship Between after the retreatment (European Society of Pulp and Periodontal Endodontology 2006; Shenoy and Shenoy Furcation Therapies 2010). If resolution does not occur, periodontal disease, vertical root fracture, or persisting 4.6.1 Non‐surgical Periodontal Therapy endodontic infection can be individually con- sidered as possible causes of the disease The previous chapter discussed how, since (Rotstein and Simon 2004). bacteria are the primary aetiological factor in The Endodontist’s View 79 periodontal disease, periodontal furcation Besides the patient’s pain perception and therapy aims to subgingivally remove plaque threshold, eating habits, such as consumption and calculus from the contaminated root of citrus fruit, fruit juice, yogurt, and wine, surfaces (Wennström et al. 2005; Tomasi and can promote the onset of root dentine hyper- Wennström 2009). Despite the benefits for sensitivity. Acid nourishment can act as periodontal health (Löe et al. 1965), mechan- conditioners for mineralized tissues, prevent- ical instrumentation might have some side ing the tubules from occluding (Bergenholtz effects on root integrity and, therefore, on and Ricucci 2008; Addy et al. 1987). the endodontium. Following root cementum A wide number of treatment options seem and superficial dentine removal, bacteria can to be effective in the management of dentinal more easily penetrate into the tubules and hypersensitivity. Chemical or physical agents induce a localized inflammatory response on are professionally or domestically applied, to the pulp (Adriaens et al. 1988; Bergenholtz either desensitize the nerve or cover the and Ricucci 2008). Nevertheless, some exposed dentinal tubules (Gillam and authors have reported that cementum and Orchardson 2006). Sometimes, for stressed dentine removal do not appear to have con- patients with poor eating habits and a low sequences for pulp health (Bergenholtz and pain threshold, dentinal hypersensitivity can Lindhe 1978), even when the exposed root is persist for months or years after mechanical in contact with plaque (Nilvéus and Selvig instrumentation, and root canal treatment 1983; Hattler and Listgarten 1984). In fact, might be required to improve their daily oral the incidence of pulp lesions was seen to be hygiene and the related quality of life (Bartold similar between scaling and root planing– 2006; Gillam and Orchardson 2006). treated and untreated teeth (Bergenholtz and Lindhe 1978). 4.6.2 Regenerative Furcation Among the instrumentation‐related side Therapy effects, root dentine hypersensitivity is widely reported as a complaint by patients. Chapters 6 and 7 will cover the regenerative In fact, half of cases usually report sensitivity options for periodontal furcation involve- after subgingival scaling and root planning ment (FI). Despite the effort to establish (von Troil et al. 2002). Painful symptoms, whether a negative effect of guided tissue which affect the upper premolars and first regeneration (GTR) on the pulp exists, clear molars more than the rest of the teeth evidence is still lacking (Chen et al. 1997). (Bartold 2006), are normally evoked by evap- According to Cortellini and Tonetti (2001), orative, tactile, thermal, or osmotic stimuli, GTR of deep intrabony defects extended to and can prevent the patient from undertak- the apical third of the root does not nega- ing daily oral hygiene procedures. In accord- tively influence the vitality of the tooth. This ance with the most accredited hydrodynamic is particularly evident when the neuro‐vas- theory, fluid shift across the exposed tubules cular bundle is not damaged by debridement. can be responsible for the painful sensation Clinical attachment level (CAL) gain follow- (Pashley et al. 1996). ing GTR appears to be quite similar between Generally, root dentine hypersensitivity vital and endodontically treated teeth. In disappears within a couple of weeks after fact, the healing process does not seem to be subgingival debridement because of the nat- influenced by root canal therapy successfully ural occlusion of the tubules. Mineral crystal performed prior to the regeneration deposition on the tubular lumen inactivates (Cortellini and Tonetti 2001). the hydrodynamic mechanism for dentinal As reported by other authors (Lasho et al. pain and limits the potential for an inward 1983; Polson et al. 1984; Gkranias et al. 2012; diffusion of bacterial elements towards the Garg et al. 2015), conditioners, such as citric pulp (Yoshiyama et al. 1989; 1990). acid and ethylenediaminetetraacetic acid 80 Chapter 4
(EDTA), are effective in smear layer, endo- tooth is vital or the previous endodontic toxins, and anaerobic bacteria removal. Root treatment is incongruous (see Figures 4.17 conditioning improves the attractiveness of and 4.18). Rubber dam is required for optimal the surface as a substrate to which cells/ working conditions (Ahmad 2009; Lin et al. blood components can adhere (Boyko et al. 2014). During cleaning and shaping, root 1980), therefore the exposed collagen fibres integrity has to be preserved as much as pos- can act as a matrix for a new connective tissue sible by minimally removing the dentine attachment to cementum (Pitaru and Melcher along the canals. To avoid resection‐related 1987). Conversely, smear layer dissolution gutta‐percha exposure, the canal space has to can threaten pulp health. By removing this be filled 2–3 mm apical to the furcation protective barrier, dentine permeability (Marin et al. 1989). Prior to the resective increases and the pulp might be more likely to therapy, resin composites can be used to be injured (Ryan et al. 1984; McInnes‐Ledoux adhesively build up the abutment. Endodontic et al. 1985). As observed by Cotton and Siegel posts or screws might be necessary whenever (1977), citric acid application on freshly cut the retention for the build‐up material is dentine may have a detrimental toxic effect poor. When the endodontic and restorative on human pulp. However, several studies do protocols are properly followed, retention‐ not endorse this finding (Nilvéus and Selvig related complications such as build‐up 1983; Lambrianidis et al. 1988). debonding or breaking are generally avoided Without evidence‐based operating proto- (Carnevale et al. 2008). cols, the recommendations in Box 4.8 should Occasionally, the FI might be preoperatively be followed. or intraoperatively underestimated and its resolution might not be obtained by barrelling 4.6.3 Resective Therapy only (Jameson and Malone 1982). The exposed root canal entrances have to be carefully As discussed by Rotundo and Fonzar in sealed after the resective therapy, since the Chapter 8, endodontic treatment is manda- incidence of pulp failures increases over time tory before resective therapy whenever the (Smukler and Tagger 1976). In particular, 41%,
Box 4.8 Recommendations for regenerative furcation therapy.
●● For deep periodontal defects, with or without furcation involvement, on impairment‐free vital teeth, regenerative therapy may be performed without endodontic pre‐treatment, since pulp vitality is likely to be preserved. ●● For up‐to‐the‐apex periodontal defects, scaling and root planing (SRP) procedures might dam- age the neuro‐vascular bundle of the tooth. Since pulp necrosis might occur during periodon- tal healing, according to some authors root canal treatment could be preventively performed to avoid any interference with the regeneration process (Cortellini and Tonetti 2001). ●● For deep periodontal defects on asymptomatic congruously root‐filled teeth with periapical radiolucency, root canal retreatment should be delayed, since a periapical lesion might require up to five years for comprehensive radiographic healing (Molven et al. 2002; Zitzmann et al. 2009; Abbott 2011). ●● For deep periodontal defects on symptomatic incongruously root‐filled teeth with periapical radiolucency, root canal retreatment is mandatory before proceeding with guided tissue regeneration therapy. ●● For deep periodontal defects on symptom‐free incongruously root‐filled teeth without peria- pical translucency, no evidence‐based endodontic protocol has been defined so far, thus root canal retreatment may be performed or not, depending on restorative purposes. The Endodontist’s View 81
Figure 4.17 Pulp exposure after resective therapy on vital 4.6 (LR6). Root canal treatment was performed one week later.
Figure 4.18 Degree II furcation defect (mesial and distal) on 2.6 (UL6). Minimally invasive access to the endodontic space was obtained after isolation with rubber dam. Canals were conservatively shaped and filled with gutta‐percha apical to the furcation floor. Resin composite was used to fill the root canal entrances and to build up the cavity access. The rizotomy (root separation) of the mesio-buccal and palatal roots and the rizectomy (root amputation) of the disto-buccal root were performed after endodontic treatment. All the root canals were endodontically treated, since there was no pre‐operative certainty of the extraction of the distal root.
62%, and 87% of resected teeth show pulp before the resective therapy, or at least necrosis after six months, one year, and five within two weeks afterwards (Smukler and years, respectively (Filipowicz et al. 1984). Tagger 1976). Because of the poor short‐term endodontic The operating recommendations in prognosis, vital teeth should be devitalized Box 4.9 should be followed. 82 Chapter 4
Box 4.9 Recommendations for resective therapy.
●● Cleaning and shaping should be conservatively performed, and residual dentine thickness should be preserved as much as possible to avoid root weakening. ●● For canal filling, gutta‐percha should be extended 2–3 mm apical to the furcation. ●● For the build‐up, resin composite should be used to adhesively restore the abutment. ●● Endodontic posts or screws should be placed only in low‐retention teeth. ●● Vital resected teeth should be endodontically treated within two weeks after the resective therapy.
Summary of Evidence
●● Endodontium and periodontium influ- ●● Pulp sensitivity tests and periodontal ence each other during health, function, probing are essential for the differential and disease. diagnosis of endodontic and periodontal ●● The histological pulp changes induced by diseases. periodontal disease can be reparative or ●● When combined endodontic and perio- degenerative. Pulp necrosis generally dontal lesions merge, root canal therapy occurs when the apical neuro‐vascular should be carried out a few months before bundle is involved. any further surgical periodontal treat- ●● Accessory canals in the furcation ment, in order to evaluate the part of the region are frequent and might repre- defect originating from the endodontic sent a comm unication pathway between disease. endodontic and periodontal patholo- ●● The vitality of the pulp seems to hinder gies through the induction of inflam- bacteria migration from the periodontal matory responses. pocket to the endodontium. ●● Primary endodontic lesions might resem- ●● Except for root resective therapy, non‐ ble a furcation class III periodontal defect, surgical, surgical, and regenerative perio- when the fistulous sinus tract drains dontal therapies for furcation lesions do through the periodontal ligament in the not benefit from any preventive root canal inter‐radicular space of multi‐rooted teeth. treatment.
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Chapter 5
Why do We Really Care About Furcations? Long‐term Tooth Loss Data Luigi Nibali
Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK
5.1 Introduction which results in gingival bleeding, discomfort, and eventually tooth mobility and exfoliation. Chapter 1 highlighted how the anatomy of This is also potentially associated with onset multi‐rooted teeth favours microbial accu- of systemic diseases like diabetes mellitus, mulation, leading to periodontal breakdown rheumatoid arthritis, and cardiovascular dis- inside the root separation area. Furthermore, ease (EFP 2014). Therefore, the ‘effects’ or we have now learned (see Chapter 3) that end‐points of periodontitis could be meas- plaque removal inside the furcation area is a ured as tooth loss, decreased patient quality of rather daunting and difficult task, both for life (QOL), and perhaps systemic effects of the the clinician and for patients themselves. It is periodontal inflammatory reaction. It is logi- therefore natural to assume that teeth cal to assume that these would be the out- affected by furcation involvement (FI), being comes measured by any study assessing the more exposed to the microbial challenge, will impact of periodontitis. However, reality tells develop periodontal progression more rap- us that, since periodontitis is a chronic disease idly and will have a higher risk of tooth loss. that usually occurs over a long time span, most This chapter reviews the evidence for this periodontal studies focus on other, shorter‐ and aims to provide long‐term data on tooth term measures of disease as main outcomes, loss in teeth with FI. This answers the ques- such as probing pocket depth (PPD), clinical tion ‘Why do really we care about furca- attachment levels (CAL), and bleeding on tions?’ and perhaps provides the rationale for probing (BOP). This is done with the under- the whole book, justifying the interest in standing that these are surrogate markers of furcations as a therapeutic challenge for peri- the really relevant outcomes just described. odontists, general dentists, and hygienists. Recent systematic reviews on furcations followed this approach and focused on short‐ term outcomes after regenerative surgery 5.2 Measures of Disease (Graziani et al. 2015; Reddy et al. 2015; see Progression Chapters 6 and 7). This clearly represents a limitation as, although an association exists The reader of this book will be well aware that between these clinical parameters and dis ease periodontitis causes inflammatory resorption progression and tooth loss (Claffey and of the attachment apparatus of the tooth, Egelberg 1995; Chambrone et al. 2010), it is a
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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far from ideal approach. On the other end, the cases deemed to have reached stability will outcome ‘tooth loss’ is severely influenced by enter a phase named ‘maintenance care’ or the treating clinician, and by their treatment ‘supportive periodontal therapy’ (SPT) philosophy and inclination to be more or less directly or after the provision of surgical ther- conservative. With this in mind, in the view of apy, depending on the case (see Figure 5.1). this author studies on FI should ideally meas- Provision of regular SPT, consisting of oral ure ‘tooth loss’, QOL measures, and measures hygiene reinforcement and motivation, peri- of systemic burden of periodontitis as out- odontal charting, and supra‐ and subgingival comes. In reality, what emerges from the peri- debridement, is associated with a reduced risk odontal literature is that only the outcome of tooth loss (Lee et al. 2015). Long‐term lon- ‘tooth loss’ has been assessed by a large gitudinal studies in unspecified periodontitis enough number of studies to allow for making cohorts or chronic periodontitis in SPT conclusions on how it can be influenced by FI. reported tooth loss of approximately 0.10 (Hirschfeld and Wasserman 1978), 0.13 (McGuire and Nunn 1996), 0.15 (Eickholz 5.3 Tooth Loss et al. 2008), 0.18 (McFall 1982), and up to 0.30 teeth per patient per year (Tsami et al. 2009). Although natural tooth exfoliation can still A systematic review of studies including peri- occur in the general population, it is assumed odontal maintenance care following compre- that ‘tooth loss’ usually occurs as tooth extrac- hensive periodontal treatment showed that in tion performed by a dentist, at least in indus- the studies included, 3919 teeth from a total of trialized countries. Severe periodontitis is 41 404 were lost during the maintenance estimated to be the sixth most prevalent period. From 36 to 88.5% of patients did not chronic disease in humans (Kassebaum et al. experience tooth loss during the follow‐up 2014) and it is considered one of the main period in the different studies. The percent- causes of tooth loss (Hull et al. 1997; Al‐ ages of tooth loss due to periodontal reasons Shammari et al. 2005; Akhter et al. 2008). varied from 1.5 to 9.8%. Patient‐related fac- Periodontal treatment classically consists of tors (i.e. age and smoking) and tooth‐related oral hygiene instructions, supra‐ and subgin- factors (tooth type and location, and the initial gival tooth debridement (with or without tooth prognosis) were associated with tooth adjunctive therapy such as antimicrobials), loss (Chambrone et al. 2010). In a more recent followed by a re‐evaluation. At this stage, systematic review, Trombelli and co‐workers
Periodontal visit
Periodontitis Health
Cause-related Supportive therapy periodontal therapy (Maintenance)
Re-evaluation
Corrective Re-evaluation (surgical) therapy
Figure 5.1 The different steps of periodontal therapy. Long-term Tooth Loss Data 93 observed a weighted mean yearly tooth loss treatment if any they received during the rate during SPT of 0.15 and 0.09 teeth/patient/ follow‐up period. year for follow‐up of 5 years and 12–14 years, Similarly, data were recently published on a respectively (Trombelli et al. 2015). Another total of 3267 molars of 1897 subjects partici- systematic review in aggressive periodontitis pating in the 11‐year follow‐up of the Study (AgP) cases, including 16 longitudinal studies, of Health in Pomerania (SHIP; Nibali et al. revealed that the average tooth loss for all AgP 2017). All subjects had half‐mouth periodon- cases was 0.09 teeth/patient/year (95% confi- tal examinations, including FI measurements dence interval [CI] = 0.06–0.16), therefore in with a straight probe in one upper and one line with chronic periodontitis (CP) studies lower molar at baseline. Only 28% of subjects (Nibali et al. 2013). reported having had some form of unspeci- But what is the relative contribution of FI fied ‘gum treatment’ throughout the course to the tooth loss outcome? The following of the observational period. In total, 375 sub- paragraphs will review the evidence from the jects (19.8%) lost molars during the follow‐ periodontal literature for tooth loss in molars up period. Respectively 5.6%, 12.7%, 34.0%, with FI. and 55.6% of molars without FI, degree I FI, degree II FI, and degree III FI were lost. As well as initial PPD and CAL and diagnosis of periodontitis (p < 0.001), FI was associated 5.4 Tooth Loss for Untreated with molar loss in the 11‐year follow‐up. The Furcation‐involved Teeth calculated incidence rate ratios (IRR) for molar loss were 1.73 (95% CI = 1.34–2.23, Although it seems almost obvious from what p < 0.001) for degree I FI and 3.88 (95% has been discussed so far that molars with FI CI = 2.94–5.11, p < 0.001) for degree II–III, have a greater risk of being extracted com- compared with without FI at baseline. These pared with molars with no FI, very few stud- results were confirmed in subanalysis of the ies have systematically assessed this question 72% of subjects who had no periodontal and the magnitude of such a risk, especially treatment during the course of the study in untreated populations. Bjorn and Hjort (who could more genuinely be considered (1982) published the results of a longitudinal ‘untreated’; Nibali et al. 2017). study on a sample of 221 staff members of a Swedish industrial company, originally examined in 1965 and then re‐examined in 1978. These subjects were not receiving a 5.5 Tooth Loss for Treated specific treatment protocol. Radiographic Furcation‐involved Teeth mandibular molar inter‐radicular bone destruction was used for furcation diagnosis, Fu and Wang summarized in Table 3.1 some in the absence of clinical data. Only 1.1–2.7% longitudinal studies reporting tooth loss by of the molars had bone loss affecting more FI by research groups in the USA and Europe. than 50% of the distance vertex to apex, and The classic study by Hirschfeld and bone loss in furcation increased from 18 to Wasserman (1978) was perhaps the first large 32% in the 13‐year follow‐up period. During published study assessing long‐term tooth this time, 9% of furcated molars were lost, prognosis in patients with periodontitis. but only 2.5% were estimated to have been Following up 600 patients during SPT for at lost due to progressive FI. Although these least 15 years retrospectively (average percentages are relatively low, we should 22 years), the authors observed that 300 highlight that this was a general population patients had lost no teeth from periodontal (not specifically subjects selected for hav- disease, 199 had lost 1–3 teeth, 76 had lost ing periodontitis) and it is not clear what 4–9 teeth, and 25 had lost 10–23 teeth. These 94 Chapter 5
figures helped identify three different groups five decades from the 1970s to the 2010s, and of patients based on progression pattern: the interventions of these studies (divided ‘well‐maintained’ (the great majority), ‘down- into active and supportive periodontal ther- hill’, and ‘extreme downhill’. Of 1464 teeth apy). Five of the included papers focused on which originally had FI, 460 were lost after specific treatment for a specific group of the average 22 years follow‐up, 240 of them furcation‐involved teeth (Haney et al. 1997; by one‐sixth of the patients who deteriorated Yukna and Yukna 1997; Eickholz and the most. Hausmann 2002; Little et al. 1995; A systematic review on long‐term tooth Zafiropoulos et al. 2009), while fourteen loss related to FI revealed that the survival papers assessed long‐term tooth loss in rate of molars treated non‐surgically was cohorts of periodontitis patients during more than 90% after 5–9 years, with different maintenance care and were suitable for breakdowns according to treatment proto- meta‐analysis. SPT protocols (when speci- cols and varying degrees of disease severity fied) generally included periodic (3‐ to 6‐ to (Huynh‐Ba et al. 2009). Although no meta‐ 12‐monthly) periodontal clinical measure- analysis could be produced, the authors con- ments, oral hygiene instructions, and subgin- cluded that initial FI (degree I) could be gival debridement and a range of different successfully managed by non‐surgical periodontal surgeries if considered neces- mechanical debridement, and that vertical sary. The risk of bias analyses performed root fractures and endodontic failures were using the Newcastle Ottawa scale showed the most frequent complications observed that study quality scores ranged from a total following resective procedures of molars of 3 to a total of 5 (out of a maximum total of with FI. 9 stars). The asymmetrical results of funnel A more recent systematic review tried to plots of meta‐analysis of relative risk for answer the focused question: ‘What is the tooth loss based on follow‐up periods risk of tooth loss in teeth with furcation revealed potential publication bias (see involvement and which factors affect the Nibali et al. 2016). outcome?’ (Nibali et al. 2016). Longitudinal Data on tooth loss by furcation diagnosis human studies in patients with CP present- was obtained, when possible with a break- ing data on furcation diagnosis and tooth loss down on first, second, and third molars. were considered eligible. In order to be Although studies focusing only on AgP had included, studies had to have ‘secure’ furca- been excluded, some of the included studies tion diagnosis (clinical with Nabers probe or incorporated a small subset of AgP cases equivalent), treatment of FI provided, a fol- (Dannewitz et al. 2006; Pretzl et al. 2008; low‐up of at least three years, and had to Salvi et al. 2014; Graetz et al. 2015) and only report tooth loss data by furcation diagnosis. in one of these papers was it possible to The literature search was conducted at Ovid obtain separate data on CP from the authors Medline, Embase, LILACS, and Cochrane (Dannewitz et al. 2006). Only data on tooth Library and complemented by a hand search. loss following initial therapy (during mainte- Studies were selected in two‐stage screening nance care) were analysed. carried out by two independent reviewers. Following an initial screening of 1207 arti- 5.5.1 Tooth Loss for FI vs No FI cles, full‐text review resulted in 21 articles which met the defined inclusion criteria. Grouping studies reporting data on tooth loss Table 5.1 reports the characteristics of the for molars with and without FI, a total of 8143 sample included in the reviewed studies, molars without FI and a total of 5772 molars which had been carried out in the USA with FI were included. Tooth survival ranged (n = 11), Germany (n = 6), Sweden (n = 2), from 94 to 100% after 4–7.5 years in regenera- Switzerland (n = 1), and Italy (n = 1) across tion studies (Haney et al. 1997; Yukna and Table 5.1 Summary of study procedures for all included studies.
Follow‐up years Supportive periodontal therapy Author/ Year Sample no. (range) Inclusion/disease classification Active periodontal therapy (APT) (SPT)
Lindhe and 75 5 ≥50% loss of periodontal support and OHI, SRP, restorative therapy if needed, 3–6 monthly OHI and Nyman 1975 optimal oral hygiene periodontal surgery in PPDs > 4 mm prophylaxis by hygienist, yearly (gingivectomy, Widman flaps, bone periodontal examinations and recontouring, furcation plasty, tunnelling, radiographs root resection as indicated) Hirschfeld and 600 22 (15–53) ‘Early’: PPD of 4 mm or less, with Subgingival scaling with or without Deep scaling + ‘problem areas’ Wasserman 1978 gingival inflammation and subgingival surgery (additional surgical procedure or retreated when necessary, calculus; ‘intermediate’: PPD of non‐surgical procedure performed occlusion 4–7 mm; ‘advanced’: PPD > 7 mm, depending on tooth diagnosis) checked and adjusted as furcation involvement indicated, OHI McFall 1982 100 19 (15–29) ‘Early’: PPD ≤ 4 mm (n = 11); Supragingival and subgingival scaling, Generally every 3–4 to 6 months ‘intermediate’: PPD 4–7 mm (n = 53); polishing, OHI, occlusal adjustment and (including curettage, muco‐ ‘advanced’ PPD > 7 mm (n = 36) biteguards if needed, gingival curettage, periosteal flaps, osseous surgery, gingivectomy, gingivoplasty, ostectomy, root resection if needed) osteoplasty Goldman et al. 211 22.2 (15–34) CP Oral physiotherapy, supragingival and 3–6‐month recalls (selective 1986 subgingival scaling, OHI grinding and coronal reshaping, adjunct restorative treatment if needed) Wood et al. 1989 63 13.6 (10–34) Patients with moderate periodontitis OHI, non‐surgical (SRP, curettage, Not reported treated and maintained by SRP for 10 occlusal adjustment) and surgical years or longer treatment (gingivectomy, flap surgery, flap curettage, osseous contouring, osseous grafting, root amputation) Kuhrau et al. 1990 59 5.8 (4–8) Patients with periodontitis with Surgical therapy (modified Widman flap, ‘Regular’ furcation‐involved teeth treated root resection, tunnelling) surgically Wang et al. 1994 24 8Patients with CP who had completed SRP followed by one of three procedures: 3‐month recall interval for an 8‐year clinical trial and had no pocket elimination maintenance prophylaxis and more than 2 first or second molars surgery, modified Widman flap surgery, or yearly examinations missing at baseline gingival curettage
(Continued)
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Follow‐up years Supportive periodontal therapy Author/ Year Sample no. (range) Inclusion/disease classification Active periodontal therapy (APT) (SPT)
Little et al. 1995 18 4.6 Patient with periodontal disease with Surgical therapy consisting of osseous 3‐monthly following surgery to deep class Il or III molar furcation resectioning and/or recontouring to the control plaque and potential invasion adjacent mesial tooth and tunnelling bacterial pathogens McGuire and 100 10 Chronic generalized moderate to SRP, OHI, removal of fremitus, surgery if 2‐ or 3‐month intervals (majority Nunn 1996 severe adult periodontitis indicated (osseous surgery, open SRP, under a 3‐month interval) – SRP, rarely bone grafts) polishing, minor occlusal adjustments Haney et al. 1997 13 4–5 CP Coronally advanced flap procedures and 6‐monthly for 5 years citric acid root treatment with or without adjunctive implantation of freeze‐dried, demineralized, allogeneic bone Yukna and Yukna 13 6.7 (6–7.5) Grade II molar furcation Regenerative surgery with bone grafts and Weekly, then monthly deplaquing 1997 defects, with adjacent bone crest coronally advanced flaps until surgical re‐entry at 6–12 height > 75% of the root length and months, then 3‐month recalls coronal to the furcation bone level McLeod et al. 114 12.5 (5–29) Moderate to advanced Non‐surgical therapy (OHI, SRP, occlusal 6‐monthly 1998 periodontitis with 4–7 mm or greater adjustment, AL occasional use of systemic AB) followed by surgical treatment (pocket reduction, pocket elimination, occasional regeneration) Eickholz and 95 Advanced periodontal disease Guided tissue regeneration 3‐monthly for the first 2 years Hausmann 2002 (OHI and professional tooth cleaning), then 3–6‐monthly according to individual risk Checchi et al. 92 6.7 (3–12) Chronic adult periodontitis who OHI, SRP, re‐evaluation, and periodontal 3–4‐monthly hygienist 2002 completed APT and have been on a surgery appointment recall recall SPT schedule
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Yukna 1997; Eickholz and Hausmann 2002), (Kuhrau et al. 1990; McLeod et al. 1998; Haney 89% after 5.8 years in a tunnelling study (Little et al. 1997; Yukna and Yukna 1997; Dannewitz et al. 1995), 79% after a minimum of 4 years in et al. 2006). a root resection study (Zafiropoulos et al. In studies reporting data for only first and 2009), and 43–100% after 5–53 years for stud- second molars (Hirschfeld and Wasserman ies including combined therapies (Hirschfeld 1978; McFall 1982; Goldman et al. 1986; and Wasserman 1978; McFall 1982; Goldman Wood et al. 1989; Dannewitz et al. 2006; et al. 1986; Wood et al. 1989; Kuhrau et al. Pretzl et al. 2008; Johansson et al. 2013; 1990; Wang et al. 1994; McGuire and Nunn Miller et al. 2014; Graetz et al. 2015), the 1996; Checchi et al. 2002; Dannewitz et al. following relative risks (RR) of tooth loss 2006; Pretzl et al. 2008; Johansson et al. 2013; were detected (see Figure 5.2): Miller et al. 2014; Salvi et al. 2014; Graetz et al. 2015). Among teeth reported in these studies, ●● RR = 2.90 (95% CI = 2.01–4.18) for molars the average tooth loss/patient/year was 0.01 with FI vs no FI (p < 0.0001; various lengths and 0.02 for molars without and with FI, of follow‐up). respectively. Periodontal progression, endo- ●● RR = 1.46 (95% CI = 0.99–2.15, p = 0.06) for dontic complications, caries, and fractures molars with FI vs no FI (p < 0.0001; 5–10 were reported as main causes of tooth loss years follow‐up).
With FI No FI Risk Ratio Risk Ratio Study or Subgroup Events Total Events Total Weight IV. Random, 95% Cl Year IV. Random, 95% Cl 5–10 years Dannewitz et al. 2006 24023 1115 6.9% 2.13 [0.83, 5.45] 2006 Pretzl et al. 2008 39051 30930 11.0% 1.35 [0.88, 2.06] 2008 Subtotal (95% Cl) 630 420 17.9% 1.67 [1.14, 2.43] Total events 74 35 Heterogeneity: Tau2 = 0.00; Chi2 = 0.75, df = 1 (P = 0.39); I2 = 0% Test for overall effect: Z = 1.90 (P = 0.06)
10–15 years Wood et al. 1989 35 151 27 215 10.7% 1.86 [1.17, 2.91] 1989 Johansson et al. 2013 30 94 37 267 11.1% 2.18 [1.44, 3.31] 2013 Miller et al. 2014 127 419 50 397 11.9% 2.41 [1.79, 3.24] 2014 Subtotal (95% Cl) 664 879 33.7% 2.21 [1.79, 2.74] Total events 192 116 Heterogeneity: Tau2 = 0.00; Chi2 = 0.92, df = 2 (P = 0.63); I2 = 0% Test for overall effect: Z = 7.30 (P < 0.0001) >15 years Hirchfeld & Wasserman 1978 384 1285 124 2250 12.5% 5.42 [4.48, 6.56] 1978 McFall 1982 82 147 25 492 11.1% 10.98 [7.30, 16.51] 1982 Goldman et al. 1986 235 562 110 835 12.4% 3.17 [2.60, 3.88] 1986 Graetz et al. 2015 315 1183 118 1022 12.4% 2.31 [1.90, 2.80] 2015 Subtotal (95% Cl) 3177 4599 38.4% 4.46 [2.62, 7.62] Total events 192 116 Heterogeneity: Tau2 = 0.28; Chi2 = 67.73, df = 3 (P = 0.00001); I2 = 96% Test for overall effect: Z = 5.49 (P < 0.0001) Total (95% Cl) 4471 5898 100.0% 2.90 [2.01, 4.18] Total events 1282 528 Heterogeneity: Tau2 = 0.27; Chi2 = 104.40, df = 8 (P < 0.00001); I2 = 92% Test for overall effect: Z = 5.72 (P < 0.0001) 0.01 0.1 110 100 Favors FI Favors No FI
Figure 5.2 Forest plot presenting relative risk (RR) of tooth loss based on follow‐up periods (excluding third molars). Meta‐analysis for the comparison of tooth loss among selected studies presented an overall odds ratio of 2.90 (95% confidence interval [CI] = 2.01–4.18, p < 0.0001). For studies with a follow‐up period of 5–10 years, 10–15 years, and > 15 years, the RR of tooth loss between teeth with and without furcation involvement was 1.46 (95% CI = 0.99–2.15, p = 0.06), 2.21 (95% CI = 1.79–2.74, p < 0.0001), and 4.46 (95% CI = 2.62–7.62, p < 0.0001), respectively. Source: Nibali et al. (2016). Long-term Tooth Loss Data 99
●● RR = 2.21 (95% CI = 1.79–2.74, p < 0.0001) 5.5.3 Tooth Loss by Vertical for molars with FI vs no FI (p < 0.0001; Furcation Component 10–15 years follow‐up). The previous discussion points to the fact that ●● RR = 4.46 (95% CI = 2.62–7.62, p < 0.0001) the great majority of long‐term follow‐up stud- for molars with FI vs no FI (p < 0.0001; > 15 ies of molars with FI have focused on the hori- years follow‐up). zontal component, as measured by the Hamp Only the comparison for studies over more classification (Hamp et al. 1975). Chapter 2 than 15 years had a high degree of heteroge- also introduced the concept of ‘vertical’ FI and neity (p value for chi‐square test < 0.0001 and its relative subclassification into A, B, and C I2 test = 96%), hence it needs to be interpreted (Tarnow and Fletcher 1984), which could be cautiously. When third molars were included, associated with the measure of horizontal only small changes to the summary estimate involvement. A recent paper hypothesized that for risk of tooth loss by FI were detected (see different levels of vertical FI may have a bear- Nibali et al. 2016 for details). ing on the risk of tooth loss of horizontal degree II FI (Tonetti et al. 2017). The authors 5.5.2 Tooth loss by Different retrospectively assessed 200 molars followed Furcation Degree up for 10 years of supportive therapy after con- servative periodontal surgery with limited An important question with clinical relevance osseous surgery. Vertical furcation subclassifi- is whether the degree of FI affects the risk of cation was established according to a modifi- tooth loss. We previously (Section 5.4) dis- cation of the classification proposed by Tarnow cussed an increased risk of tooth loss by and Fletcher (1984) using bone loss observed increased degree of FI in a largely untreated in a periapical radiograph and clinical probing population participating in the SHIP in depths/CAL. A gradually higher incidence of Pomerania (Nibali et al. 2017). When studies tooth loss was observed for degree II FI with included in Nibali et al.’s (2016) systematic bone loss up to the apical third, middle third, review of treated patients reporting tooth loss or coronal third of the root (respectively 77%, by degree of FI were considered (McGuire and 33%, and 9% tooth loss at 10 years). The Nunn 1996; Dannewitz et al. 2006; Johansson authors advocated that the vertical component et al. 2013; Salvi et al. 2014, Graetz et al. 2015), might be an important predictor of tooth loss 8%, 18%, and 30% of the total of teeth with fur- in molars with degree II horizontal FI. They cation degrees I, II, and III, respectively, were also suggested that vertical involvement of the lost in the follow‐up period (0.01, 0.02, and 0.03 apical third is often associated with the teeth/patient/year). Meta‐analysis for tooth presence of an intrabony defect within the fur- loss among the included studies (see Figure 5.3) cation defect. Treating such intrabony defects presented a relative risk of tooth loss of: may reduce the level of vertical FI, thus poten- tially reducing the future risk of molar loss ●● RR = 1.67 (95% CI = 1.14–2.43, p = 0.008) (Tonetti et al. 2017). for FI degree II vs I. ●● RR = 1.83 (95% CI = 1.37–2.45, p < 0.0001) for FI degree III vs II. ●● RR = 3.13 (95% CI = 2.30–4.24, p < 0.0001) 5.6 Conclusions on Risk of for FI degree III vs I. Tooth Loss by Furcation The comparisons presented a low to moder- Involvement ate degree of heterogeneity among the selected studies (p value for chi‐square Based on the review presented here (Nibali test = 0.04, 0.20, and 0.26, and I2 test = 61%, et al. 2016), FI approximately doubles the risk 33%,and 25%, for degree II vs I, III vs II, and of tooth loss for molars in supportive perio- III vs I comparisons, respectively). dontal therapy for up to 10–15 years. In 100 Chapter 5
Larger degree Lesser degree Risk Ratio Risk Ratio Study or Subgroup Events Total Events Total Weight IV. Random, 95% Cl Year IV. Random, 95% Cl II vs. I McGuire & Nunn 1996 27 153 14 178 6.1% 2.24 [1.22, 4.12] 1996 Dannewitz et al. 2006 3 98 9 95 2.4% 0.32 [0.09, 1.16] 2006 Johansson et al. 2013 10 25 18 67 6.0% 1.49 [0.80, 2.77] 2013 Salvi et al. 2014 28 118 36 376 7.7% 2.48 [1.58, 3.88] 2014 Graetz et al. 2015 108 357 121 638 10.2% 1.60 [1.27, 2.00] 2015 Subtotal (95% Cl) 751 1354 32.3% 1.67 [1.14, 2.43] Total events 176 198 Heterogeneity: Tau2 = 0.10; Chi2 = 10.50, df = 4 (P = 0.03); I2 = 62% Test for overall effect: Z = 2.66 (P = 0.008) III vs. II McGuire & Nunn 1996 19 64 27 153 7.1% 1.68 [1.01, 2.80] 1996 Dannewitz et al. 2006 11 47 3 98 2.5% 7.65 [2.24, 26.11] 2006 Johansson et al. 2013 2 2 10 25 5.4% 2.06 [1.04, 4.11] 2013 Salvi et al. 2014 30 69 28 118 8.0% 1.83 [1.20, 2.79] 2014 Graetz et al. 2015 86 188 108 357 10.2% 1.51 [1.27, 1.89] 2015 Subtotal (95% Cl) 370 751 33.3% 1.83 [1.37, 2.45] Total events 148 176 Heterogeneity: Tau2 = 0.05; Chi2 = 7.21, df = 4 (P = 0.12); I2 = 45% Test for overall effect: Z = 4.05 (P < 0.0001) III vs. I McGuire & Nunn 1996 19 64 14 178 5.9% 3.77 [2.01, 7.08] 1996 Dannewitz et al. 2006 11 47 9 95 4.5% 2.47 [1.10, 5.55] 2006 Johansson et al. 2013 2 2 18 67 5.8% 3.06 [1.62, 5.80] 2013 Salvi et al. 2014 30 69 36 376 8.1% 4.54 [3.01, 6.85] 2014 Graetz et al. 2015 86 188 212 357 10.2% 2.41[1.93, 3.02] 2015 Subtotal (95% Cl) 370 1354 34.5% 3.13 [2.30, 4.24] Total events 148 198 Heterogeneity: Tau2 = 0.06; Chi2 = 8.01, df = 4 (P = 0.09); I2 = 50% Test for overall effect: Z = 7.32 (P < 0.0001)
0.01 0.1 1 10 100 Favors larger degree Favors lesser degree
Figure 5.3 Forest plot presenting relative risk (RR) of tooth loss based on degrees of furcation involvement (excluding third molars). Meta‐analysis for the comparison of tooth loss among selected studies presented an RR of 1.67 (95% confidence interval [CI] = 1.14–2.43, p = 0.008), 1.83 (95% CI = 1.37–2.45, p < 0.0001), and 3.13 (95% CI = 2.30–4.24, p < 0.0001) when comparing degree II to I, degree III to II, and degree III to I furcation involvement, respectively. Source: Nibali et al. (2016).
particular, first and second molars with FI had and perhaps higher risk of tooth loss could be an RR of tooth loss of 1.46 (p = 0.06) up to 10 attributed to molars with furcation not under- years and of 2.21 from 10 to 15 years going regular periodontal treatment (Nibali (p < 0.0001), compared with molars with no FI et al. 2017). Furthermore, there is enough evi- (RR 1.69 and 2.06, respectively, including third dence that the degree of FI (Hamp et al. 1975) molars). Studies up to 15 years of follow‐up is significantly associated with risk of tooth had consistent results and reported similar loss during supportive periodontal therapy, relative risk for tooth loss. This may be attrib- increasing from furcation degree I to II to III utable to the similar designs of these studies, (Nibali et al. 2016, 2017). The vertical furca- consisting of initial periodontal therapy, surgi- tion subclassification and potential intrabony cal therapy when needed (including access defects associated with one or multiple roots flaps, osseous resective surgery, root resec- within the furcation may also affect the long‐ tion, tunnelling, or occasionally regenerative term tooth loss risk (Tonetti et al. 2017). surgery), and then supportive periodontal Based on the available evidence, it is therapy (at regular intervals for most studies, worth mentioning that it is not possible to generally every 3, 4, 6, or up to 12 months). discriminate the relative contribution of FI A three to four times higher risk of tooth loss and PPD on molar loss. In other words, we was observed for studies with longer follow‐ cannot be certain that the higher risk of ups (>15 years, up to 53 years), although data tooth loss in molars with FI is due to them relative to this outcome have to be interpreted having FI rather than to them having a deep cautiously due to high heterogeneity. A similar pocket. The relative contribution of FI to Long-term Tooth Loss Data 101
(a) (b) (c)
(d) (e) (f)
Figure 5.4 (a, b) Clinical photographs of 55‐year‐old male patient affected by chronic periodontitis; (c) periapical radiographs of upper right molars showing triple degree III furcation involvement on UR6 and 7; (d, e) clinical photographs taken 10 years after tunnelling surgery; (f) Periapical photographs at 10‐year follow‐up. molar loss could be tested by assessing risk most molars affected by FI respond well to of tooth loss prospectively in molars with periodontal treatment, judging by the fact similar pocket depth differing only by FI (for that even in the presence of degree III FI, example, a 6 mm vertical PPD in a buccal only 30% of molars were lost with up to surface of a lower molar with no FI vs a 6 mm 15 years of follow‐up (see Figure 5.4). vertical PPD of a lower molar with degree II The risk of tooth loss (for FI vs non‐FI molars) FI). However, we are not aware of any studies is in the region of 1.5–2.2 up to 15 years in testing this hypothesis. An indirect compar- maintenance. Such risk seems to increase ison of the risk of tooth loss attributable only sharply after the 15‐year time point, although to residual PPD is difficult, as limited data study heterogeneity does not allow clear con- are available and merely on single‐rooted clusions on this. Similarly, an increased risk of teeth, since most studies present short‐term tooth loss by FI exists for cases not undergoing disease progression data only (Badersten periodontal maintenance. Among the relevant et al. 1984) or tooth loss data for all teeth long‐term outcomes introduced in Section 5.2, combined (Matuliene et al. 2008). we are not aware of any studies specifically In conclusion, in patients undergoing com- assessing the effect of FI on the systemic inflam- prehensive periodontal treatment (cause‐ matory burden, while patient‐reported out- related, surgical therapy if needed, and SPT), comes are covered in Chapter 13.
Summary of Evidence
●● Periodontal treatment and maintenance ●● Degree of horizontal FI affects risk of care lead to low tooth loss rates of molars tooth loss (increasing from degree I to II with furcation involvement (FI). to III). ●● The tooth loss of molars with FI is approx- ●● Degree of vertical FI may also affect the imately double that of molars without FI risk of tooth loss (increasing from subclas- up to 15 years of follow‐up. sification A to B to C). 102 Chapter 5
References
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survival of molars with class II furcation furcation involvement and mobility on involvement during supportive periodontal future clinical periodontal attachment loss. care. Journal of Clinical Periodontology 44, Journal of Periodontology 65, 25–29. 1140–1144. Wood, W.R., Greco, G.W., and McFall, W.T., Jr Trombelli, L., Franceschetti, G., and Farina, R. (1989). Tooth loss in patients with moderate (2015). Effect of professional mechanical periodontitis after treatment and long‐term plaque removal performed on a long‐term, maintenance care. Journal of Periodontology routine basis in the secondary prevention of 60, 516–520. periodontitis: A systematic review. Journal Yukna, R.A., and Yukna, C.N. (1997). Six‐year of Clinical Periodontology 42 (Suppl. 16), clinical evaluation of HTR synthetic bone S221–S236. grafts in human grade II molar furcations. Tsami, A., Pepelassi, E., Kodovazenitis, G., and Journal of Periodontal Research 32, Komboli, M. (2009). Parameters affecting 627–633. tooth loss during periodontal maintenance in Zafiropoulos, G.G., Hoffmann, O., Kasaj, A. a Greek population. Journal of the American et al. (2009). Mandibular molar root Dental Association 140, 1100–1107. resection versus implant therapy: A Wang, H.L., Burgett, F.G., Shyr, Y., and retrospective nonrandomized study. Journal Ramfjord, S. (1994). The influence of molar of Oral Implantology 35, 52–62. 105
Chapter 6
Regenerative Therapy of Furcation Involvements in Preclinical Models: What is Feasible? Nikolaos Donos1, Iro Palaska1, Elena Calciolari1, Yoshinori Shirakata2, and Anton Sculean3
1 Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK 2 Department of Periodontology, Kagoshima, University Graduate School of Medical and Dental Sciences, Kagoshima, Japan 3 Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland
6.1 Introduction 6.2 Available Preclinical Models In everyday clinical practice, the presence of furcation involvement constitutes a sig Different animal species have been used nificant challenge (de Santana et al. 1999; to evaluate the regeneration of furcation Avila‐Ortiz et al. 2015). Regeneration of the defects, with non‐human primates, dogs, furcation defect with restitution ad integrum rabbits, and pigs being the most commonly is a highly desirable outcome in these cases. employed (Struillou et al. 2010; Kantarci This chapter and the next will review the et al. 2015). Variations between species current evidence on pre‐clinical and clinical include anatomy, dimensions of teeth and human studies on the potential to regenerate alveolar process, gingival biotype, local phys furcation defects. iological environment, animal behaviour, The regeneration of furcation involve and healing rate (Caton et al. 1994). ments following the use of various bio Small animals (especially mice and rats) logical materials, extracellular matrix have generated substantial data on the patho proteins, growth factors, and cell therapy is a genetic mechanisms of systemic inflamma complex biological process involving various tion and their correlation with periodontal tissue components, including epithelium, disease in transgenic and knockout animal connective tissue, cementum, and alveolar models (Graves et al. 2008). The major draw bone (Ivanovic et al. 2014). Historically, back of small animals is the limited similarity animal models have been used as proof‐of‐ of their dentition to the human dentition, principle models and for providing first‐ which limits the possibility of translating the level in vivo evidence in potential translation results to the clinical situation. Conversely, of different regenerative materials to the the dental anatomy of large animals clinical setting. (mainly non‐human primates and dogs) may
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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resemble better the human dento‐alveolar dogs present, to a certain extent, some architecture. In these animals, it has been similarity to those of humans. However, dogs suggested that it is feasible to study wound lack lateral jaw movements and premolar healing/regeneration in periodontal defects occlusal contacts (Kantarci et al. 2015). In of clinically relevant size and configuration dogs, the severity of periodontal disease (Selvig 1994). increases with age and can result in tooth loss (Berglundh et al. 1991). In regenerative peri 6.2.1 Non‐human Primates odontal medicine, the dog model has been used for the histological demonstration of Non‐human primates have naturally occur guided tissue regeneration (GTR) in various ring dental plaque, calculus, oral microbial defect types, such as furcations, supracrestal, pathogens, and periodontal disease, although and infrabony defects (Caffesse et al. 1990). In this occurs late in life and the lesions tend addition, the dog model has been employed to be asymmetrical (Schou et al. 1993; Oz in studies which have led to our current and Puleo 2011). Therefore, if osseous lesions understanding of the limitations of regener are investigated, they are usually experimen ative approaches, including membrane‐ tally induced. Similar dental anatomy and associated properties (Araujo et al. 1998). periodontal wound healing (Caton and Kowalski 1976), suitability of furcation sites 6.2.3 Miniature Pig Model (Giannobile et al. 1994), and experimentally induced defects that do not spontaneously The miniature pig model has emerged as an regenerate indicated that mature, adult, alternative to the dog model. Varieties of Macaca mulatta and Macaca fascicularis miniature pig have been extensively used in species could be used as models for evaluat biomedical research (Polejaeva et al. 2000). ing periodontal regenerative procedures These animals have oral and maxillofacial (Schou et al. 1993). However, it should be structures similar to those of humans in emphasized that their use is controversial, as terms of anatomy, physiology, and disease this model shares some structural and func development (Wang et al. 2007). Natural tional features with humans, thus raising sig gingivitis can be observed at 6 months of age. nificant ethical concerns. Besides the ethical The pattern of disease progression follows issues related to the close phylogenetic rela the same stages as that in humans: gingival tionship with humans, primate research also swelling, plaque accumulation, calculus requires expensive facilities, with dedicated formation, and bleeding on probing (Lang and trained personnel and environmental et al. 1998). Histologically, these clinical enrichment. features are accompanied by inflammatory cell infiltration and vasodilatation. Starting 6.2.2 Dog Model at 16 months of age, miniature pigs may develop advanced periodontitis, with pocket Dogs are among the most widely used exper depths up to 5 mm and alveolar bone resorp imental animals for studying naturally occur tion (Kantarci et al. 2015). ring gingivitis and periodontitis, wound healing, and tissue regeneration (Wikesjö et al. 1994). The Beagle dog (Canis lupus 6.3 Defect Types familiaris) is commonly used because of its size and its cooperative nature, but several Four types of experimentally induced furca studies have also used mongrel dogs tion defects have been used for testing the (Struillou et al. 2010). The characteristics of effects of different therapeutic modalities in periodontal tissues and the size of teeth in pre‐clinical studies. These include defects Regenerative Therapy in Animal Models 107 resulting from naturally occurring periodon of bias when studying the effect of different titis and three types of experimentally surgical techniques and biomaterials on produced defects: the acute defect, the tissue regeneration (Caton et al. 1994; chronic defect, and the combined acute/ Mardas et al. 2012). chronic defect. 6.3.2.2 The Chronic Defect Model 6.3.1 Naturally Occurring These defects are created by placing ortho Periodontitis Defects dontic elastics or ligatures around the cir cumference of teeth, or slightly apical to Historically, periodontal defects caused by the gingival margin. The elastics/ligatures natural periodontal disease have been gradually migrate apically, as plaque‐induced considered as a necessity in the study of peri inflammation destroys the periodontal liga odontal regeneration (Haney et al. 1995). ment and supporting bone in 3–6 months These defects occur late in the animal’s life (Caton and Kowalski 1976). Then, the root and the lesions are usually asymmetrical, surfaces are carefully scaled and planed and a as they result from a gradual and variable notch is placed on the roots, at the base of destruction of the periodontium, and include the defect, as a reference for the histological deposition of calculus and endotoxins on analysis. The advantage of this model is that the root surface (Haney et al. 1995). In addi spontaneous healing is not observed, but the tion, they feature compromised mucogingi disadvantages include the considerable time val dimensions, which is a confounding needed for the creation of the defects and factor when these models are used to study the asymmetrical nature of the defects. the biological potential of regeneration under In addition, conventional root debridement optimized conditions of wound healing produces root surface conditions similar to (Wikesjö et al. 1994). Taking into account the those of surgically induced (acute) defects. aforementioned limitations, the rationale Taking into account these limitations, the rel for using these types of defects to study evance for using this type of defect to study periodontal wound healing/regeneration periodontal wound healing/regeneration appears to be limited (Caton et al. 1994). appears to be limited (Caton et al. 1994).
6.3.2.3 The Acute/Chronic 6.3.2 Experimentally Defect Model Induced Defects The majority of the available pre‐clinical 6.3.2.1 The Acute Defect Model studies use this model to study wound In this model, mucoperiosteal flaps are healing/periodontal regeneration in class II elevated and the bone, the periodontal liga or III furcation defects. This defect is devel ment, and cementum are surgically removed oped by surgically removing alveolar bone, to create the defect type of the desired shape periodontal ligament, and cementum in the and dimension. Reference notches are usu experimental site. Prior to flap closure, the ally created by a round bur on the roots, at defect is placed into a chronically inflamed the level of the reduced alveolar bone. These state to reduce spontaneous regeneration by notches start on the buccal aspect of the root placing a foreign body, such as metal strips, and extend into the furcation area, and they orthodontic wires and bands, impression are used as a reference point for the histo material, or gutta‐percha for 1–3 months logical analysis. The major drawback of the (Caton et al. 1994). At surgical re‐entry, the acute defect model is that approximately foreign bodies are removed, and the lesions 50–70% of spontaneous regeneration can be are debrided from granulation tissue, plaque expected, thus creating an important source biofilm, and calculus. After the root surface 108 Chapter 6
is scaled, the tested biomaterial/active prin scaled and root planed. Following removal of ciple can eventually be delivered into the granulation tissue and complete root instru defect (Araújo and Lindhe 1997; Takayama mentation, reference notches were placed in et al. 2001; Donos et al. 2003b). The advan the roots at the level of the alveolar bone tages of this model are that defects are pro crest, using a number 1/2 round bur. These duced rapidly, they do not heal spontaneously, notches were positioned on the buccal and bilateral symmetrical periodontal tissue aspects of the roots and extended interproxi loss can be predictably induced. mally and into the furcation areas, as deep as the involvement of the class II furcation 6.3.3 The Critical Size Defect permits. After the root surface is scaled, Concept in Furcation Studies the tested biomaterial/active principle can be delivered into the defect. A critical size defect (CSD) is defined as ‘the smallest size intra‐osseous wound in 6.3.3.2 Furcation Degree III CSD a particular bone and species that will not The first attempts to create defects that heal spontaneously during the lifetime of would not heal spontaneously were made by the animal’ (Schmitz and Hollinger 1986). the team of Ellegaard et al. (1974), who Even if a certain biological variability exists induced through‐and‐through bifurcation between different animal models, it is of the defects in posterior teeth of Rhesus monkeys outmost importance that the experimental by passing a round bur through surgically bone defect created is of a critical size for denuded bifurcations. The size of the open the animal model used, thus avoiding ings was approximately 2 mm in diameter. the occurrence of spontaneous periodontal To avoid spontaneous healing, a steel wire regeneration and allowing testing of the of periodontal dressing was placed in the true regenerative potential of the biomateri defects for four weeks. This study has shown als and surgical techniques investigated. that following surgical removal of the inter‐ However, because most pre‐clinical studies radicular septum and the promotion of have an evaluation time limit, Gosain et al. plaque retention in the monkey’s posterior (2000) state that the CSD in animal research teeth, bifurcation defects may develop into refers to the size of a defect that will not heal lesions, which after six weeks of healing over the duration of the study. display features similar to those of inter‐ radicular pockets in humans. Six weeks post‐ 6.3.3.1 Furcation Degree II CSD operatively the height of the bone in the In order to test the regenerative potential of lesions produced was essentially maintained different regenerative treatments in class II at the level determined at the time of surgery. furcation defects, the majority of studies The lesions were characterized by chroni have used surgically created CSDs measuring cally inflamed connective tissue covered 5 mm in height (from the roof of the bifurca with epithelium of varying thickness, and tion) and 2 mm in depth (Lekovic and Kenney they showed no tendency for spontaneous 1993; Hürzeler 1997; Deliberador et al. 2006). healing. After intrasulcular incisions were made from Based on this concept, Klinge et al. (1981), the mesial side of the involved teeth (mainly by using two different animal models (dog premolars) to the distal side of the molars, a model and non‐human primate model), mucoperiosteal flap was elevated to expose examined the influence of different defect both buccal and lingual alveolar bone plates. sizes and different flap management The defects were then created by using techniques on the healing potential after carbide round burs under abundant saline reconstructive surgery using citric acid irrigation. The interproximal bone remained conditioning. Chronic through‐and‐through intact. Then, the surfaces were carefully defects of different sizes were created. Regenerative Therapy in Animal Models 109
Specifically, bone was surgically removed furcation defects: (i) a small, 2 × 2 mm key‐ from the furcation area and around the cir hole furcation defect, where the removal of cumference of the tooth, including the proxi the supporting bone and root cementum was mal bone (horizontal defect). Three different confined to the furcation area, thus leaving levels of bone reduction were studied (2 mm, intact the interdental alveolar bone; (ii) a 3.5 mm, and 5 mm high). In addition, two large key‐hole defect about 3 mm in the different positions of the flap were studied apico‐coronal direction and 4 mm in the (coronally positioned flap and replaced flap). mesio‐distal direction; and (iii) a large It was demonstrated that new attachment ‘horizontal’ defect about 5 mm in the apico‐ occurred for teeth treated with coronally coronal direction and about 4 mm in the positioned flaps regardless of the defect size. mesio‐distal direction, where the removal of This implied that variations in the dimension bone and root cementum was performed of the defects played a secondary role in the within the furcation area and extended at the healing potential, and that the adequate post‐ buccal/lingual and interproximal surfaces. It operative flap coverage of the furcation was was observed that small key‐hole, degree III the critical step for the successful healing of furcation defects healed following GTR through‐and‐through defects. treatment with complete new attachment. In a subsequent study by Klinge et al. At control sites, only minor amounts of new (1985a), it was shown that healing was attachment formation occurred. In larger accomplished in even larger defects (~9 mm) defects, it was observed that GTR therapy when a coronal flap placement was used. It is failed to generate new attachment to a degree possible that the magnitude of coronal flap where the furcation defects became closed. It positioning is of limited importance, pro was also observed clinically that at such sites, vided a certain amount of coverage of the extensive flap recession occurred following furcation is accomplished. It was also noticed suture removal. The study revealed that the that one important reason for the failure at size of the furcation defect and the degree of larger defects was found to be recession of bone loss adjacent to the defect were deter the flap, which resulted in early exposure of mining factors for the outcome of this kind of the furcation site (Klinge et al. 1985a). To treatment. Thus, if the furcation defect was counteract such soft tissue recession, the associated with circumferential bone loss, or authors developed a technique which if the defect was more than 3 mm in the involved the utilization of ‘crown attached’ apico‐coronal direction, complete new sutures and reported that, provided flap attachment failed to occur. Thus, while small recession was prevented, new attachment key‐hole defects – that is, small vertical occurred at both large and small defects defects – healed, large key‐hole defects and (Klinge et al. 1985a). Similar results were horizontal defects were consistently associ obtained by Lindhe et al. (1995), who showed ated with flap recession and failure. Taking that comparatively large furcation defects into consideration the CSD concept (smallest (‘key‐hole’ defects with cross‐section dimen bone defect created), the key‐hole defect was sions of > 11 mm2) could be successfully optimal for testing the regenerative potential regenerated by GTR therapy provided that of different materials, and the approach the soft‐tissue flaps covering the membranes based on this study was adopted in clinical are prevented from receding apical of the studies as well. furcation fornix during healing, and that The most widely used model in regenera the clot in the furcation defect remains tive studies remains the critical size supra‐ non‐infected. alveolar periodontal defect model, which was The potential for new attachment forma developed in beagle dogs by Wikesjö and his tion after GTR was examined by Pontoriero team (Wikesjö et al. 1999). Supra‐alveolar et al. (1992) in three differently shaped critical size periodontal defects are produced 110 Chapter 6
by the resection of the buccal and lingual/ Sander and Karring 1995; Sanz et al. 2015). palatal bone of premolar teeth. Osseous A variety of biocompatible barriers, non‐ resection can be restricted to the interdental absorbable (Caffesse at al. 1990, 1994; area, which measures approximately 4–5 mm Danesh‐Meyer et al. 1997; Bogle et al. 1997; (height) and 3 mm (width; Araújo et al. 1998), Lekovic et al. 1998; Macedo et al. 2006) or or extended to create a horizontal circumfer bioabsorbable (Cirelli et al. 1997; Hürzeler ential defect up to 5–6 mm below the fornix et al. 1997; de Andrade et al. 2007; Wang of furcation (Giannobile et al. 1998; Wikesjö et al. 2014) has been used for the regenera et al. 2003a, b). In this model, innate regen tion of class II furcation defects. From a eration of alveolar bone and cementum does clinical and histological point of view, similar not exceed 25% of the defect height over a results can be achieved in GTR, whether bio three‐week healing interval following wound absorbable (such as collagen‐based) or non‐ closure or primary intention healing. absorbable (such as polytetrafluoroethylene, Extending the healing interval to eight weeks ePTFE) membranes are applied (Murphy and does not result in additional regeneration Gunsolley 2003). However, the bioabsorba (Wikesjö et al. 1994, 2003a, b; Koo et al. ble membranes do not require a second 2004). This defect is a valuable model to test surgery for their retrieval, thus reducing the regenerative potential of candidate the patient’s discomfort and morbidity. treatments on class III furcation defects, The studies applying non‐resorbable and as it allows evaluation of the regenerative resorbable membranes in critical size (5 mm potential of experimental treatments under in height × 2 mm in depth), surgically created optimal conditions and in a biologically furcation II defects showed a mean percent controlled environment. By applying this age of bone fill and new cementum forma model, different studies have evaluated tion ranging between 60 and 80% (Caffesse at root‐conditioning protocols, bone grafts al. 1990, 1994; Cirelli et al. 1997; Danesh‐ and bone substitutes, biological substances, Meyer et al. 1997; Bogle et al. 1997; Hürzeler and different barrier membranes (GTR) as et al. 1997; Lekovic et al. 1998; Macedo et al. stand‐alone protocols or in combination 2006; de Andrade et al. 2007; Wang et al. (Sanz et al. 2015). 2014). The results of these studies are presented in detail in Table 6.1.
6.4 Regeneration 6.4.2 Bone Grafts and GTR Treatments of Class II Furcation Defects The placement of bone grafts or alloplastic materials in furcation defects in association 6.4.1 Guided Tissue Regeneration with flap surgery or GTR has been exten sively evaluated in animal experiments. The potential to regenerate furcation defects The biological rationale behind the use of in a predictable manner emerged with the grafts is the assumption that the material development of the concept of GTR more may contain bone‐forming cells (osteogene than 30 years ago (Karring and Warrer 1992; sis) or serve as a scaffold for bone formation Karring et al. 1993). The use of a barrier (osteoconduction), or that the matrix may membrane prevents both gingival epithelial contain bone‐inductive substances (osteoin cells and connective tissue cells from repop duction), which could stimulate both the ulating the root surface during healing, and regrowth of bone and the formation of new allows repopulation only by cells from the attachment (Karring and Cortellini 1999). periodontal ligament or the alveolar bone Limited studies in naturally occurring marrow, thus inducing the formation of new defects showed that bone grafts combined cementum and connective tissue attachment with different barrier membranes did (Nyman et al. 1980; Karring et al. 1980, 1993; not enhance the regeneration process of Regenerative Therapy in Animal Models 111
Table 6.1 Guided tissue regeneration (GTR) in class II furcation defects.
Healing time Study Model Tooth Type of membrane (months) Histomorphometric results
NATURALLY OCCURING PERIODONTITIS Bogle Dog Mandibular Control: Open‐flap 6 Cementum formation (%) et al. 1997 premolars debridement Control: 71 Experimental group: Test: 17* Bioabsorbable Bone filling (%) polylactic acid–based Control: 74 membrane Test: 14* ACUTE DEFECT MODEL Caffesse Dog Mandibular Control: PTFE non‐ 6 Notch to new et al. 1994 premolars resorbable membrane cementum (mm) Test 1: Bioabsorbable Control: 4.42 ± 1.40 type I barrier Test 1: 4.42 ± 1.08 Test 2: Bioabsorbable Test 2: 5.80 ± 0.68 type II barrier Notch to bone crest (mm) Control: 2.72 ± 1.43 Test 1: 2.95 ± 1.24 Test 2: 4.55 ± 1.05 Danesh‐ Sheep Mandibular Control: Open‐flap 2 Alveolar bone height (%) Meyer premolars debridement Control: 61.5 ± 7.13 et al. 1997 Test 1: PTFE non‐ Test 1: 78.4 ± 6.89* resorbable membrane Test 2: 71.7 ± 6.73 Test 2: PTFE non‐ Cementum height (%) resorbable soft‐tissue Control: 93.0 ± 4.34 patch Test 1: 98.5 ± 1.01* Test 2: 98.4 ± 1.03* ACUTE/CHRONIC DEFECT MODEL Cirelli Mongrel Mandibular Control: Open‐flap 3 Cementum formation (%) et al. 1997 dogs premolars debridement Control: 59.34 Test: GTR with Test: 92.35* anionic collagen Bone filling (%) membrane Control: 48.58 Test: 56.33 2 Macedo Dog Mandibular Control: PTFE non‐ 3 New tissue (mm ) et al. 2006 bicuspids resorbable (Gore‐Tex+) Control: 12.45 ± 3.54 removed at 2 weeks Test: 14.32 ± 4.01 Test: PTFE non‐ + Bone height (mm) resorbable (Gore‐Tex ) Control: 3.56 ± 1.21 removed at 4 weeks Test: 4.03 ± 0.94 2 de Andrade Dog Mandibular Control: Bioabsorbable 3 New tissue (mm ) et al. 2007 premolars membrane Control: 8.01 ± 2.69 (polyglycolic acid) Test: 7.21 ± 1.33 Test: Acellular dermal Bone height (mm) matrix Control: 2.56 ± 0.84 Test: 2.86 ± 0.32 (Continued ) 112 Chapter 6
Table 6.1 (Continued)
Healing time Study Model Tooth Type of membrane (months) Histomorphometric results
Wang Dog Mandibular Control: Open‐flap 2 Micro‐CT scanning et al. 2014 premolars debridement New alveolar bone 2 Test 1: Open‐flap surface (mm ) debridement + LIPUS Control: 82.84 ± 16.67 Test 2: Resorbable Test 1: 98.44 ± 18.57 bovine collagen Test 2: 132.11 ± 22.76* membrane (BioGide†) Test 3: 150 ± 21.20* Test 3: Resorbable bovine collagen membrane (BioGide†) + LIPUS Hürzeler Monkey Mandibular Control: Open‐flap 5 Cementum et al. 1997 molars debridement deposition (mm) Test: Synthetic Initial defect size: 5.05 ± 0.45 resorbable membrane Control: 0.83 ± 0.19 Resolute‡ (glycolide/ Test: 2.88 ± 0.63* lactic copolymer) Bone formation (mm) Initial defect size: 2.81 ± 0.65 Control: 1.14 ± 0.35 Test: 2.78 ± 0.53* CHRONIC DEFECT MODEL 2 Caffesse Dog Mandibular Control: Open‐flap 3 Furcation fill (mm ) et al. 1990 premolars, debridement Control: Ep + CT + B = 1.94 molars Test: PTFE non‐ Experimental: Ep + CT+ resorbable membrane B = 3.38 (Gore‐Tex+) (no statistical analysis) Lekovic Dog Mandibular Control: Open‐flap 6 Notch to new et al. 1998 premolars, debridement cementum (mm) molars Test 1: PTFE non‐ Control: 0.24 ± 0.007 resorbable membrane Test 1: 1.96 ± 0.031* Test 2: Silicone rubber Test 2: 2.16 ± 0.011* barrier material Test 3: 2.18 ± 0.015* Test 3: Polycarbonate Test 4: 2.04 ± 0.037* filter with pore size of Notch to bone crest (mm) 0.45 barrier material Control: 0.32 ± 0.017 Test 4: Test 1: 1.18 ± 0.019* Polycarpolactone Test 2: 1.44 ± 0.014* barrier material Test 3: 1.32 ± 0.015* Test 4: 1.2 ± 0.010*
*Statistically significant difference from control; +Gore‐Tex, W.L. Gore and Assoc., Flagstaff, AZ, USA; †Biogide, Geistlich Biomaterials, Wolhusen, Switzerland; ‡Resolute, W.L. Gore and Assoc., Flagstaff, AZ, USA. CT = computed tomography; LIPUS = low‐intensity pulsed ultrasound; PTFE = polytetrafluoroethylene. Regenerative Therapy in Animal Models 113
furcation class II defects (Caffesse et al. analysis showed significantly more buccal‐ 1993; Lekovic and Kenney 1993). Likewise, palatal defect fill in furcation defects treated in critical size acute defects in the dog with PTG (96.8%) compared to the DBBM model, Deliberador et al. (2006) compared (62%) and control groups (72.2%, p < 0.05; the results of autogenous bone (AB) alone Wohlfart et al. 2012). It should be noted that and in combination with a calcium sulphate in this study, degree II furcation defects paste as a barrier to an empty defect (con larger than what was typically used were sur trol). At three months, most specimens gically created (buccal bone was removed to failed to show complete bone fill of the fur half of the root width) and this might have cation. New bone formation was moderate affected their regenerative potential. and restricted between the notch areas to the mid portion of the defect. The amount 6.4.3 Enamel Matrix Proteins of periodontal regeneration in the three groups was approximately 50% of the root Biomimetic substances have been tested in length, without differences between the experimental studies to assess their regener groups. Areas of ankyloses were also pre ative capability in furcation lesions. This sent in some sections, but no active root group of proteins, which play a key role in resorption was observed. More recently, root formation during odontogenesis, have Struillou et al. (2011) investigated the demonstrated in both in vitro and in vivo regenerative capacity of injectable biphasic studies a capacity to attract and increase the calcium phosphate (BCP) in combination migration and proliferation of undifferenti with injectable polymer (Si‐HPMC) in crit ated mesenchymal cells, which then form ical size (5 mm high, 3 mm deep), acute sur acellular cementum, periodontal ligament, gically created defects in premolar furcation and alveolar bone (Zetterström et al. 1997; of beagle dogs. Three months after treat Amin et al. 2012, 2013, 2014, 2016). ment, a bone in‐growth of 23% ± 10% Remarkably, not only did regenerative tech and 35.5% ± 13.9% was observed in the niques using enamel matrix derivatives show empty and biomaterial‐filled defects, enhanced hard‐tissue formation, they also respectively. Although a tendency for higher reported increased gingival tissue thickness bone in‐growth was observed in the defects using the beagle dog model (Al Hezaimi et al. filled with the biomaterial, this difference 2012). As class II furcation defects are non‐ did not reach statistical significance. containing defects, it has been suggested that Deproteinized bovine bone mineral the use of biological substances may be clini (DBBM) is an extensively used bone substi cally applied in combination with different tute with documented reconstructive poten bone graft materials, although this combina tial (Baldini et al. 2011). In a mini‐pig animal tion therapy has not yet been experimentally model, the potential of porous titanium evaluated to provide histological outcomes granules (PTGs) and DBBM in the recon (Sculean et al. 2007; Trombelli and Farina structive treatment of surgically created 2008). In an experimental study in mongrel acute buccal degree II furcation defects was dogs, the use of enamel matrix derivative tested. Six weeks after treatment, the histo (EMD) alone was associated with better logical analysis showed significantly regenerative outcomes in comparison to its increased vertical bone formation in both the combined use with ePTFE membranes in PTG (62.5%) and control (empty; 64.3%) critical size acute/chronic surgically created groups compared to the DBBM‐treated buccal class II furcation defects. Following defects (41.9%, p < 0.01), which, on the con eight weeks of healing, the EMD group trary, had a reduced regenerative response. resulted in 67% new bone formation and 94% The micro‐computed tomography (CT) new cementum. The combined approach 114 Chapter 6
resulted in compromised healing due to periodontal defects in dogs, which were then membrane exposure (28% new bone, 80% expanded in culture and transplanted into new cementum; Regazzini et al. 2004). critical size surgically created class II furca tion defects in the same animals. At 42 days 6.4.4 Growth Factors post‐surgery, a trend towards better bone formation (control 32.9% vs test 51.2%) and Growth factors form a class of natural less cementum formation (control 71.7% vs polypeptides that act as biological mediators test 75.5%) in the test group was reported, regulating cell proliferation, chemotaxis, but no statistical analysis was performed in differentiation, and synthesis. These factors the study (Dogan et al. 2002). also play a major role during tissue regenera The successful use of PDL cells to regener tion, by binding to specific receptors on the ate class II furcation defects was documented cell surface. Growth and differentiation fac by Suaid and co‐workers in a dog model. PDL tor technologies have been evaluated for cells obtained from extracted teeth were cul their potential to enhance periodontal wound tured in vitro and phenotypically character healing/regeneration in healthy and systemi ized with regard to their biological properties. cally compromised conditions (Stavropoulos Acute CSDs were then surgically created and and Wikesjö 2012; Bizenjima et al. 2015). treated with either GTR (control group) or Such biologically active substances, used GTR associated to a cell‐seeded collagen either alone or in combination with GTR, sponge (test group). Three months after treat have also been tested for their efficacy in ment, the histomorphometric analysis showed improving regeneration outcomes in critical that the cell‐treated group presented a supe size furcation lesions. In particular, fibroblast rior length of new cementum (8.08 ± 1.08 mm growth factor (FGF; Murakami et al. 1999, vs 6.00 ± 1.5), a greater extension of periodon 2003; Takayama et al. 2001), bone morpho tal regeneration (7.28 ± 1.00 mm vs 3.94 ± 1.20, genetic proteins (BMPs; Ripamonti et al. p < 0.05), a lower formation of connective tis 1996, 2001), transforming growth factor‐β sue/epithelium (0.60 ± 0.99 mm vs 2.15 ± 1.92, (TGF‐β; Teares et al. 2008, 2012), insulin p < 0.05), a larger area of new bone growth factor (IGF‐1), and platelet‐derived (9.02 ± 2.30 mm2 vs 7.01 ± 0.61, p < 0.05), and a growth factor (PDGF; Soares et al. 2005) are smaller area of connective tissue/epithelium the most studied. The results of the applica (4.22 ± 0.95 mm2 vs 5.90 ± 1.67, p > 0.05), com tion of growth factors in class II furcation pared with the control group (Suaid et al. defects are presented in Table 6.2. 2011). More recently, Chantarawaratit et al. (2014) employed primary human PDL cells 6.4.5 Cell Therapy treated with acemannan, a polysaccharide extracted from aloe vera gel, for the regenera The most common cells applied for regener tion of critical size acute class II furcation ation are mesenchymal stem cells (MSCs), as defects in mongrel dogs. It was observed that these pluripotent cells can differentiate into a acemannan significantly increased the per significant number of cell types, including centage of new bone formation at 30 and osteoblasts, fibroblasts, and cementoblasts 60 days post‐operatively, as well as the percent (Risbud and Shapiro 2005). MSCs have been age of new cementum formation at 60 days isolated from periodontal ligament (PDL; post‐operatively (Chantarawaratit et al. 2013). Seo et al. 2004; Trubiani et al. 2005) and it Simsek et al. (2012) compared the effec was demonstrated that, when they are cul tiveness of MSCs with platelet‐rich plasma tured in contact with native PDL cells, MSCs (PRP) as a scaffold to PRP alone, autogenous acquire the characteristics of PDL cells, cortical bone (ACB) graft alone, and the making them suitable for periodontal regen combination of ACB with PRP in the eration purposes (Kramer et al. 2004). Dogan treatment of acute/chronic class II furcation and co‐workers retrieved cells from regenerated defects versus open flap debridement Regenerative Therapy in Animal Models 115
Table 6.2 Growth factors in class II furcation defects.
Healing time Histomorhometric Study Model Tooth Type of membrane (months) results
ACUTE/CHRONIC DEFECT MODEL Murakami Dog Mandibular Test 1: Gelatinous carrier 1.5 New bone formation et al. 1999 premolars, (fibrin gel) alone rate (%) molars Test 2: b‐FGF + carrier Test 1: 42.8 ± 10.7 Test 2: 79.6 ± 16.8* New cementum formation rate (%) Test 1: 34.3 ± 14.5 Test 2: 75.8 ± 22.7* Murakami Non‐human Mandibular Test 1: Carrier alone 2 New bone formation et al. 1999 primates molars Test 2: b‐FGF + carrier rate (%) Test 1: 54.3 ± 8.0 Test 2: 71.3 ± 13.5* New cementum formation rate (%) Test 1: 38.9 ± 9.2 Test 2: 71.2. ± 15.2* Murakami Dog Mandibular Control: Gelatinous carrier 1.5 New bone formation et al. 2003 molars (fibrin gel) alone rate (%) Test 1: 0.1% b‐ Test 1: 35.4 ± 8.9 FGF + gelatinous carrier Test 2: 83.6 ± 14.3* New cementum formation rate (%) Test 1: 37.2 ± 15.1 Test 2: 97.7 ± 7.5* Takayama Non‐human Maxillary, Control: Open‐flap 2 New bone formation et al. 2001 primates mandibular debridement rate (%) molars Test 1: Gelatinous carrier Control: 44.7 ± 6.2 Test 2: 0.1% FGF‐2 Test 1: 54.3 ± 8.0 Test 3: 0.4% FGF‐2 Test 2: 58.0 ± 21.9 Test 3: 71.3 ± 13.5* New cementum formation rate (%) Control: 46.7 ± 12.1 Test 1: 38.9 ± 9.2 Test 2: 79.1 ± 23.9* Test 3: 72.2 ± 14.4* Keles et al. Dog Mandibular Control: Open‐flap 3 New cementum (%) 2009 premolars debridement Control: 45.60 ± 11.92 Test 1: Platelet pellet Test 1: 83.99 ± 7.70* Test 2: Platelet Test 2: 81.63 ± 8.17* pellet + resorbable New bone (%) membrane of polylactic acid + Control: 42.44 ± 6.07 (Atrisorb ) Test 1: 62.64 ± 7.89 Test 2: 61.06 ± 7.90
(Continued ) 116 Chapter 6
Table 6.2 (Continued)
Healing time Histomorhometric Study Model Tooth Type of membrane (months) results
Suaid Dog Mandibular Control: Synthetic 3 New bone (mm) et al. 2010 premolars resorbable membrane Control:4.33 ± 0.62 Resolute† (glycolide/lactic Test: 5.01 ± 0.63 copolymer) + bioactive glass ‡ New cementum (mm) (Perioglas ) Control: 9.20 ± 3.21 Test: Synthetic resorbable Test: 12.45 ± 1.73* membrane Resolute (glycolide/lactic copolymer) + bioactive glass (Perioglas) + PRP Teares Baboon Mandibular Control: Carrier alone: 2 New cementum (mm) et al. 2008 molars Basement membrane matrix Control: 3.7 ± 0.7 (Matrigel¶) Test 1: 3.5 ± 0.6 Test 1: TGF‐β3 with carrier Test 2: 6.1 ± 0.4* Test 2: TGF‐β3 with carrier New bone (mm): and minced muscle tissue Control: 2.3 ± 0.4 Test 1: 2.8 ± 0.8 Test 2: 4.7 ± 0.3* Teares Baboon Mandibular Test 1: Matrigel containing 2 New cementum (mm): et al. 2012 molars 25 µg of recombinant hOP‐1 Test 1: 6.18 ± 0.33* Test 2: Matrigel containing Test 2: 3.65 ± 0.88 75 µg TGF‐β3 Test 3: 5.45 ± 0.89* Test 3: Matrigel with 25 µg Test 4: 2.69 ± 1.06 hOP‐1 and 25 µg TGF‐β3 New bone (mm): (20:1 ratio) Test 1: 5.93 ± 0.92 Test 4: Matrigel with 25 µg Test 2: 5.67 ± 1.17 hOP‐1 and 1.25 µg TGF‐β3 Test 3: 7.07 ± 0.57* (20:1 ratio) plus morcellated Test 4: 4.73 ± 1.08 autogenous muscle ACUTE DEFECT MODEL Ripamonti Baboon Mandibular Control: Carrier 2 No bone formation et al. 1996 molars Test 1: Carrier + 0.1 µg/ml was detected hOP‐1 New cementum Test 2: Carrier + 0.5 µg/ml formation (distal hOP‐1 root) Control: 2.6 ± 0.2 Test 1: 6.2 ± 0.5* Test 2: 6.7 ± 0.3*
Ripamonti Baboon Mandibular Test 1: BMP2 (100 µg/ml) 2 New bone formation et al. 2001 molars Test 2: hOP‐1 (100 µg/ml) Test 1: 4.2 ± 0.2 Test 3: hOP‐1 + BMP2 Test 2: 3.7 ± 0.4 (100 µg/ml) Test 3: 3.1 ± 0.2 New cementum formation (distal root) Test 1: 3.7 ± 0.4 Test 2: 5.7 ± 0.3* Test 3: 3.6 ± 0.2 Regenerative Therapy in Animal Models 117
Table 6.2 (Continued)
Healing time Histomorhometric Study Model Tooth Type of membrane (months) results
Soares Dog Mandibular Control: No graft 45 days New cementum et al. 2005 molars Test: Reparative tissue of Control: 2.49 ± 0.82 extraction socket enhanced Test: 2.48 ± 0.47 with PDGF‐BB + IGF New bone Control: 2.73 ± 0.42 Test: 2.49 ± 0.71
*Statistically significant difference from control; +Atrisorb, Atrix Laboratories, Fort Collins, CO, USA; †Perioglas, US Biomaterials, Alachua, FL, USA; ‡Resolute, W.L. Gore and Assoc., Flagstaff, AZ, USA; ¶ Matrigel™, BD Biosciences, San Jose, CA, USA; b‐FGF = basic fibroblast growth factor; BMP2 = bone morphogenetic protein‐2; hOP‐1 = human osteogenic protein‐1; IGF = insulin growth factor; PDGF = platelet‐derived growth factor; PRP = platelet‐rich plasma; TGF = transforming growth factor.
(control) in the dog model. At eight weeks, The results of the different studies are cementum formation was significantly presented in Table 6.3. GTR resulted in higher in the ACB, combination of ACB/PRP, significantly more gain of connective tissue and combination of MSCs/PRP groups com attachment and regrowth of alveolar pared to the control group (p < 0.05). It was bone than control therapy, where no mem concluded that periodontal regeneration brane was used. Complete closure of class III with complete filling of class II furcation furcation defects with the formation of peri defects can be obtained with the use of GTR, odontal ligament and regrowth of the bone PPR, MSCs, and their combinations. Finally, was achieved. It was shown that the size of it was shown that a collagen matrix overlaid the defect and the shape of the surrounding with embryonic stem cells (ES) is able to bone determined the outcome of regenera improve the regeneration of class II furcation tion, as already mentioned. The treatment defects (4 mm wide, 5 mm deep) in mini‐pigs failures were consistently associated with (Yang et al. 2013). recession of the covering flaps and exposure of the defect. In addition, the results also demonstrated that bioabsorbable mem 6.5 Regeneration branes provided a barrier that was equally Treatments of Class III effective to that of non‐bioabsorbable mem Furcation Defects branes (Lindhe et al. 1995; Araújo et al. 1998).
6.5.1 Guided Tissue Regeneration 6.5.2 Bone Grafts
Starting from the late 1980s, the effects of The first attempts to treat class III furcation placing non‐bioresorbable or bioabsorbable defects with the use of bone grafts (fresh membranes on degree III furcation CSD autogenous hip marrow grafts, autogenous defects (3 mm wide and 4 mm high) as cancellous bone grafts) were made by compared with those in control sites was Ellegaard et al. (1974, 1975) in the monkey evaluated in dogs (Niederman et al. 1989; model and Nilvéus et al. (1978) in the dog Pontoriero et al. 1992; White et al. 1994; model. Although a higher frequency of furca Lindhe et al. 1995; Araújo et al. 1997, 1998). tion closure occurred with the use of the 118 Chapter 6
Table 6.3 Guided tissue regeneration (GTR) in class III furcation defects.
Healing time Histomorhometric Study Model Tooth Type of membrane (months) results
ACUTE DEFECT MODEL White et al. Dog Mandibular Control: Open‐flap 3 Distance from notch 1994 premolars debridement to coronal extent of Test: PTFE non‐resorbable bone (mm) membrane Control: ‐0.21 ± 7.27 Test: 1.50 ± 4.31 ACUTE/CHRONIC DEFECT MODEL 2 Pontoriero Dog Mandibular Control: No membrane 4 Surface area (mm ) et al. 1992 premolars Test: PTFE non‐ Small key‐hole resorbable membrane defect (Gore‐Tex+) Control: 4.8 ± 1.3 ●● Small key‐hole defect Test: 4.1 ± 1.4 (2 × 2 mm) Large key‐hole ●● Large key‐hole defect defect: (3 × 4 mm) Control: 13.6 ± 1 ●● Furcation defect part of Test: 12.8 ± 2.8 circumferential loss of attachment Furcation defect part of circumferential loss Control: 22.3 ± 2.8 Test: 20.9 ± 2.4 Lindhe et al. Dog Mandibular Study 1: 5 Study 1 1995 premolars Control: No membrane Amount of new Test: PTFE non‐resorbable cementum membrane Control: 43% (±12) Study 2: Test: 74% (±11)* Control: PTFE non‐ Height of new resorbable membrane bone (mm) Test: Synthetic resorbable Control: 0.7 ± 0.6 membrane made of Test: 1.7 ± 0.5 glycolide/lactic copolymer (Resolute†) Study 2 Amount of new cementum Control: 82% (±13) Test: 86% (±11) Height of new bone (mm) Control: 2.8 ± 1.4 Test: 3.1 ± 1.1 Araújo et al. Dog Mandibular Synthetic resorbable 5 Mineralized 1997 premolars membrane made of bone (%) glycolide/lactic copolymer 36 (±12.6) (Resolute) PDL (%) 20 (±11.1) Regenerative Therapy in Animal Models 119
Table 6.3 (Continued)
Healing time Histomorhometric Study Model Tooth Type of membrane (months) results
Araújo et al. Dog Mandibular Test 1: Synthetic resorbable 6 Mineralized bone (%) 1998 premolars membrane made of Test 1: 35 (±3) glycolide/lactic copolymer Test 2: 12 (±7)* (Resolute) PDL (%) Test 2: Absorbable Test 1: 19 (±4)* membrane made of ‡ Test 2: 6 (±2) polylactic acid (Guidor ) Araújo et al. Dog Mandibular Synthetic resorbable 6 Bone tissue (%) 1999 premolars membrane made of 78 (±4.8) glycolide/lactic copolymer (Resolute) CHRONIC DEFECT MODEL Gonçalves Dog Mandibular Control: Synthetic 4 New cementum (mm) et al. 2006 premolars resorbable membrane Control: 3.59 ± 1.67 made of glycolide/lactic Test: 6.20 ± 2.26 mm* copolymer New bone (mm) (Resolute) + removal of Control: 1.86 ± 1.76 cementum (scaling and Test: 4.62 ± 3.01 mm* root planing) Test: Synthetic resorbable membrane made of glycolide/lactic copolymer (Resolute) + preservation of cementum (polishing)
*Statistically significant difference from control; +Gore‐Tex, W.L. Gore and Assoc., Flagstaff, AZ, USA; †Resolute, W.L. Gore and Assoc., Flagstaff, AZ, USA; ‡Guidor, Sunstar Americas Inc., Schaumburg, IL, USA; PDL = periodontal ligament; PTFE = polytetrafluoroethylene. grafts, ankyloses and root resorption were in new bone formation and new cementum documented as well. By using acute/chronic in acute surgically created lesions (defect surgically created class III defects (larger height was 4 mm) after eight weeks of than CSD) in dogs, Roriz et al. (2006) studied treatment, but total closure of the furcation the regenerative potential of bovine‐derived was not achieved (Saito et al. 2012). bone matrix with or without ePTFE mem brane. Twelve weeks after treatment, it was 6.5.3 Enamel Matrix Proteins concluded that both treatments had similar results and were not able to result in closure The first study evaluating the effect of EMD of class III furcation defects. It should be in combination with GTR versus GTR alone noted that in this study, the size of the defect in class III furcation defects was performed (more than 4 mm in height) may have con by Araújo and Lindhe (1997) in surgically tributed to the lack of complete fill of the fur created acute/chronic lesions in the dog cation in both groups. Another pre‐clinical model. At four months, the central portion of study using the dog model showed that both control and test furcation defects (4 mm implantation of beta tricalcium phosphate high, 3 mm wide) was closed and the relative (β‐TCP) with a tunnel pipe structure resulted amounts of mineralized bone, bone marrow, 120 Chapter 6
and periodontal ligament were similar in A new liquid carrier for EMD, Osteogain both groups. (Institut Straumann AG, Basel, Switzerland), In a subsequent study, Donos et al. (2003b) specifically designed for mixing with differ evaluated the healing of mandibular degree ent biomaterials, has also been for the first III furcation treated with GTR, EMD, or a time tested in the regeneration of acute/ combination in monkeys. The dimensions of chronic class III furcation defects in mon the furcation defects were approximately keys (Shirakata et al. 2017). The dimensions 4 mm wide and 3 mm high, corresponding to of the exposed furcation defects were 5 mm the CSD. The alveolar bone on the buccal wide and 5 mm high (Figure 6.2). When com and lingual aspect of the mesial and distal paring the histological outcome of defects root of each molar was also removed, creat treated with open‐flap debridement (OFD; ing a ‘horizontal’ pattern of bone loss. control), OFD and a collagen sponge satu However, the height of alveolar bone on the rated with EMD (OFD/EMD), and OFD and mesial and distal interproximal aspect of a collagen sponge saturated with Osteogain each experimental tooth was maintained. At (OFD/Osteogain), higher amounts of con five months of healing, similar results in nective tissue were observed in both test terms of quality of the regenerated periodon groups. Furthermore, the OFD/Osteogain tal tissues were reported in the sites treated group showed higher new attachment with GTR alone or in combination with formation, cementum, and new bone area. EMD. Remarkably, the application of EMD None of the treatments achieved complete alone resulted in unpredictable amounts of regeneration; that is, class III furcation regenerated periodontal tissues and defect persisted after treatment (Figure 6.3). closure by newly formed bone (Figure 6.1). The same group also showed that only when 6.5.4 Growth Factors GTR or GTR associated with EMD was applied was it possible to obtain complete These biologically active substances, used defect regeneration (up to the fornix; Donos either alone or in combination with GTR, et al. 2003b; Gkranias et al. 2012). Moreover, have been tested for their efficacy in improv they demonstrated different histological fea ing regenerative outcomes in class III furca tures in relation to the different treatment tion lesions. Rossa et al. (2000) combined the modalities. The sites treated according to the use of b‐FGF with GTR for the treatment of GTR principle showed a predominance of acute/chronic surgically created defects in cellular cementum with extrinsic fibres or dogs. The defects had a vertical height of mixed fibres, while in the sites that were 5 mm and a horizontal width of 7 mm. The treated with EMD or a combination of GTR proximal bone crest was not removed, result and EMD, the cementum was characterized ing in an angular‐type defect rather than a apically as acellular and with extrinsic fibres horizontal one. The study showed improve and coronally as mixed with stratified fibres. ments in histological outcomes, such as In a recent investigation in dogs, the com newly formed cementum, and lower extent bined use of EMD with a synthetic bone graft of epithelial migration when b‐FGF was asso (Emdogain Plus, Institut Straumann AG, ciated with GTR in comparison to GTR Basel, Switzerland) was compared to coro alone. However, differences between experi nally repositioned flap for the treatment of mental and control groups did not reach sta surgically created acute class III furcation in tistical significance (this might be due to the dogs. After two months of healing, in the large size of the created defects) and full clo experimental group, a significant amount of sure of the furcation was not achieved in any new attachment and bone formation was of the specimens. Conversely, the combina observed in the majority of the specimens tion of b‐FGF with β‐TCP was shown to (Mardas et al. 2012). enhance connective tissue attachment and to Regenerative Therapy in Animal Models 121
(a) (b)
(c) (d)
Figure 6.1 Overview photomicrographs of all class III furcation defects in different groups. (a) Furcation treated with ethylenediaminetetraacetic acid (EDTA). Regeneration was observed only at the level of the notch, with connective tissue and granulation tissue plus epithelium covering the rest of the space. (b) Furcation treated with enamel matrix derivative (EMD). The furcation was partially closed and a layer of new cementum with inserting fibres identified coronal to the notch. Regenerated bone filled most of the furcation area. (c) Guided tissue regeneration (GTR)‐treated furcation where the membrane remained covered. The entire circumference of the defect is covered with a layer of new cementum. Regenerated alveolar bone fills the furcation defect completely. (d) Furcation treated with GTR + EMD. The furcation was closed and new cementum can be seen on most of the circumference of the defect. The defect was filled with new bone up to the fornix. induce higher bone formation (up to the and resulted in ankyloses and root resorption fornix) compared to b‐FGF alone in class III (Wikesjö et al. 1999, 2003a; Takahashi et al. furcation acute smaller defects (4 mm high) 2005). The use of PDGF in combination with created in dogs (Saito et al. 2013). GTR has been successfully tested by Park By using the supra‐alveolar, critical size et al. (1995) in acute/chronic supra‐alveolar, model, the effect of recombinant human critical size surgically created defects in bea bone morphogenetic protein (rhBMP2) was gle dogs. They reported almost complete clo tested and substantial regeneration of alveo sure of the lesions without the occurrence of lar bone and cementum was demonstrated resorption or ankyloses. Using the supra‐ (Wikesjö et al. 1994). However, treatment alveolar, critical size model, different con with rhBMP2 did not appear to induce a centrations of osteogenic protein‐1 (OP‐1) functionally oriented periodontal ligament, were evaluated in acute lesions in the dog. (a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 6.2 Clinical appearance of the mandibular buccal aspect of Macaca fascicularis. (a) Induction of chronic inflammation. After fabrication of class III furcation defects, impression materials were placed to encourage growth of oral microflora along the exposed root surfaces. (b) Prior to reconstructive surgery. (c) Immediately after flap reflection. Note the excessive granulation tissue in the chronic defects. (d) Defects were exposed and debrided again at the time of reconstructive surgery. (e) Osteogain/absorbable collagen sponge (ACS) construct before surgical implantation. (f) Left (second molar): ACS alone; right (first molar): placement of Osteogain/ACS. (g) Flaps coronally repositioned and sutured. (h) 16 weeks after reconstructive surgery.
Chapter No.: 1 Title Name:
(d) (e) (f)
(g) (h) (i)
(j) (k) (l)
Figure 6.3 Overview photomicrographs of all class III furcation defects in different groups (Azan‐Mallory staining). (a) OFD (open‐flap debridement) group overview (scale bar: 1 mm). (b) Higher magnification of framed area (left) in (a) (scale bar: 200 µm). (c) Higher magnification of framed area (right) in (a) (scale bar: 200 µm). (d) Absorbable collagen sponge (ACS) group overview (scale bar: 1 mm). (e) Higher magnification of framed area (left) in (d) (scale bar: 200 µm). (f) Higher magnification of framed area (right) in (d) (scale bar: 200 µm). (g) Emdogain/ACS group overview (scale bar: 1 mm). (h) Higher magnification of apical framed area (left) in (g) (scale bar: 200 µm). (i) Higher magnification of framed area (right) in (g) (scale bar: 200 µm). (j) Osteogain/ACS group overview (scale bar: 1 mm). Arrowhead: notch (apical extent of root planing). (k) Higher magnification of framed area (left) in (j) (scale bar: 200 µm). (l) Higher magnification of framed area (right) in (j) (scale bar: 200 µm). JE = junctional epithelium, NB = new bone; NC = new cementum; PDL = periodontal ligament.
Chapter No.: 1 Title Name:
At a dose of 7.5 µg/ml of OP‐1 in a collagen however necessary for microscopic and his carrier 3.9 ± 1.7 mm and 6.1 ± 3.4 mm2 of lin tological analyses that define the biological ear bone height and bone area were achieved. impact of the regenerative methods and These outcomes were significantly improved materials applied (Kantarci et al. 2015). in comparison to the outcomes achieved in Therefore, it has been suggested that animal the defects treated with surgery only or with studies are still an important step for estab carrier only (Giannobile et al. 1998). lishing cause‐and‐effect relationships and for the initial evaluation of principles in the 6.5.5 Cell Therapy development of new regenerative devices and advanced therapeutics. Only limited studies have investigated the Regenerative therapy of advanced furca use of cell therapy in the treatment of class III tion involvement (classes II and III) has been furcation defects. Autogenous periosteal extensively studied in pre‐clinical models, cells combined with the application of β‐TCP but the question remains whether this pre‐ have shown improved periodontal tissue clinical evidence is enough to support the regeneration in acute/chronic surgically cre clinical use of the different techniques and ated defects compared to β‐TCP‐treated and materials investigated in regenerative perio empty defects in a dog model. The furcation dontal therapy. The clinical challenge in fur defects were approximately 3 mm wide and cation involvement is the destruction of the 4 mm high (Jiang et al. 2010). More recently, horizontal component, but also the com Nagahara et al. (2015), using the same defect bined need for vertical periodontal regenera size, also confirmed that applying a β‐TCP tion within the same area. There is extensive scaffold to bone marrow mesenchymal stem evidence that, independent of the defect type cells helps enhance new bone formation in and animal model adopted, regenerative class III furcation defects exposed to inflam periodontal surgery using a combination of mation in beagle dogs. barrier membranes and grafting materials Using the supra‐alveolar, critical size may result in periodontal regeneration to a model, autologous periodontal ligament cells varying extent (Sculean et al. 2008). GTR is were isolated from extracted teeth, cultured more predictable in class II furcation than in and phenotypically characterized, and even class III furcation defects. Some studies tually applied on a collagen sponge carrier reported failures in the closure of the furca alone or in combination with GTR in surgi tion, often associated with recession of the cally created acute/chronic defects in the covering tissue flaps, which subsequently beagle dog model (Murano et al. 2006; Suaid resulted in exposure of the membrane. These et al. 2012). After three months of healing, results suggested that regenerative outcomes both groups resulted in additional new in the treatment of furcation defects are only cementum and new periodontal ligament possible if the healing environment under production, together with a larger area of the membrane is well protected by the flaps new bone formation. during healing, and the barrier membranes are not exposed and hence contaminated by the oral micro‐environment (Klinge et al. 6.6 Discussion 1981, 1985a, b; Lindhe et al. 1995). Superior histological outcomes, predominantly bone It is well accepted that there is no single repair, following the use of a combination of animal model that represents all aspects of grafting materials and barrier membranes, periodontal human disease, tissue architec compared with grafting materials alone or ture, and the healing and ageing processes. membranes alone, were only found in non‐ However, human studies cannot always be contained periodontal defects (class III coupled with tissue harvesting, which is furcation defects). However, in contained Regenerative Therapy in Animal Models 125 defects, such as class II furcation lesions, no functions of mesenchymal stem cells have additional advantage of a combined treat received increasing attention as a regenera ment was suggested overall. This implies tive mechanism (Nagata et al. 2017). The that the principal mechanism by which a possibility of enhancing the regeneration graft material supports regeneration may of furcation defects with the help of trans not be its osteoconductivity, but rather its planted conditioned medium obtained from space provision capacity, a question which cultured periodontal stem cells is certainly warrants further investigation (Polimeni an interesting and stimulating area for future at al. 2004). research. Biological and biomimetic substances, such as EMD, have also been tested in exper 6.6.1 Limitations of Pre‐clinical imental studies to assess their regenerative Studies capability in furcation lesions. As class III furcation defects are non‐contained defects, It is important to recognize the limitations of the use of biologics is associated with impor animal studies, as answers obtained from tant limitations. Owing to their liquid/gel‐ experiments performed under standardized like consistency, any space‐making effect is conditions are specific to the questions in fact prevented, and therefore the regenera posed, and do not necessarily translate into tive potential of such materials may be lim the clinical setting (Donos et al. 2003a). In ited in furcation defects. Remarkably, in addition, ‘biological variability’ is still a con some studies, the use of EMD in combina cern and is often resorted to as an explana tion with GTR in class III furcation defects tion for divergent experimental results. This resulted in some periodontal regeneration. variability may be due to the erratic behav However, there should always be caution in iour of genetic, biochemical, physiological, extrapolating results from experimental or immunological host factors, or to the studies in animals to the clinical scenario, microbial flora associated with the individual where it has been shown that the same treat animal. The lack of genetically defined stocks ment principles may not apply in class III within dogs and primates (the animals mainly clinical cases (Donos et al. 2003a, 2004). used in this field of research), together with Growth and differentiation factor technol the ethical concerns, may represent an ogies have also been evaluated for their important limiting factor in our attempts to potential to enhance periodontal wound reduce the effect of biological variability. healing/regeneration in furcation lesions As mentioned previously, regenerative (Stavropoulos and Wikesjö 2012). Such bio therapies require a histological demonstra logically active substances, used either alone tion of the actual outcome of periodontal or in combination with GTR, seem to be regeneration by measuring the tooth‐ promising in enhancing the regenerative out supporting tissues (i.e. cementum, periodon comes in class II and III furcation defects, tal ligament, and alveolar bone) over a but further pre‐clinical and clinical research previously diseased root surface (Sanz et al. is needed to adequately evaluate the efficacy 2015). The heterogeneity of the available of these novel treatments in periodontal studies in terms of species, study design, wound healing/regeneration. Cell‐based observation period, and materials makes therapies have also received considerable them difficult to compare. The evaluation of attention in regenerative medicine, but their the results may also be impaired by the diffi experimental evaluation in the treatment of culty in standardizing the defect morphology periodontal furcation lesions is still at a very and the extent of bone loss (horizontal and early stage of development. non‐horizontal), as well as by the different In recent years, due to the low rate of cell nature of the defects (naturally occurring vs survival after cell implantation, the paracrine ligature induced, or acute vs chronic). 126 Chapter 6
The different anatomy and dimensions of most commonly employed (Crigger et al. teeth and alveolar processes in the available 1978). The true value of the histological anal experimental animal models may reduce the ysis of mesial‐distal sections in class II and III clinical value of the outcomes. For example, furcation has been questioned by Selvig experimental procedures performed in nar (1994). This plane might impair interpreta row and shallow two‐rooted canine mandib tion, since it is very difficult to determine at ular and maxillary premolar furcation defects which point in the buccal‐lingual direction with short trunks might translate poorly to the section was obtained. When the section clinical furcation defects in humans, espe is obtained at the most proximal point from cially when considering the large three‐ the intact attachment apparatus (e.g. from rooted maxillary molars. the lingual wall of the buccal furcation Another important factor affecting the defect), analysis might provide a false idea of outcome of pre‐clinical studies is the concept a greater regenerative response than a sec of the CSD. It was shown that degree III fur tion obtained at a more distant point from cation involvements with a cross‐section the remaining periodontium, simply because dimension larger than 4 mm are more diffi of a smaller distance from precursor cells in cult to regenerate than smaller ones the first case. According to Bogle et al. (1997), (Pontoriero et al. 1989, 1992). On the other for a more precise histomorphometric evalu hand, complete healing was reported in ation of the whole regenerative process of larger degree III furcation involvements furcation lesions, buccal‐lingual histological when the membrane was kept completely sections must be obtained, because they covered by the flap during healing (Lindhe allow for an analysis of the healing response et al. 1995; Araújo et al. 1997, 1998; Araújo from the lingual limits of the defect to the and Lindhe 1997). These results indicate that buccal cemento‐enamel junction. defect morphology might be less important Another difficulty when trying to compare than post‐surgical flap dehiscence and con pre‐clinical studies is the different ways of sequent exposure of the membrane. The calculating the results. In some studies the complete closure of degree III furcation is attachment gain is measured in millimetres, unpredictable and depends on the size of the while in others it is calculated as a percentage entrance of the defect (Pontoriero et al. 1989, of the original defect height. The use of per 1992), the height of the defect, and the com centages compensates for differences in size plete flap coverage of the membrane during between different experimental teeth and the healing period (Lindhe et al. 1995). Key‐ defects, but tends to mask the fact that a hole furcation defects without concomitant large percentage change may reflect a very horizontal bone reduction seemed to provide small change in real units of measurement better post‐operative support to the flaps (Selvig 1994). and prevent recession. In addition, taking Furthermore, it is still unclear what is the into consideration that the healing process in necessary minimum observation period to dogs is more rapid compared to humans ensure that the observed result is, in fact, the (Cardarapoli et al. 2003; Mardas et al. 2012), endpoint of the healing process. The obser the development of new, more challenging vation period in most pre‐clinical studies CSDs (width, height) should be considered to varies from a couple of weeks up to three or evaluate the regenerative potential of differ six months. If the aim is to record the maxi ent materials. mum extent of repair, including cementum The lack of standardization in terms of and bone regeneration, a longer observation sample orientation for histological evalua period should be recorded. Cementum does tion and quantitative assessment is another not form on root‐planed surfaces in the dog potential source of bias. In the early studies, before approximately three weeks after sur the mesial‐distal section plane was the one gery. At six weeks, considerable amounts of Regenerative Therapy in Animal Models 127 new cementum may have formed. Connective animal experiment has not been done pre tissue attachment may be well established at viously. Also, the minimum possible num its final level six months after surgery, but the ber of animals required should be used to final picture of mature cementum and bone yield meaningful data and not maximum formation may not be expressed until a precision. later stage. It has been reported that regen ●● Refinement: A multitude of refinements of erated tissues continue their formation and/ technique that would reduce animal harm or remodelling even after three months of are ready for immediate application in bio wound healing, and that this process medical research. can continue for up to six months (Araújo Since 1986, the European Union (EU) has et al. 1997). had specific legislation covering the use of animals for scientific purposes. 6.6.2 Ethical Codes for Animal The Council for International Organiz Experimentation ations of Medical Sciences (COIMS) is an international non‐governmental representa There is increasing concern in society and tive of many branches of medicine and cog the medical profession regarding animal wel nate disciplines, which has laid down the fare, with significant controversy surround guiding principles to provide a conceptual ing the use of animals in research and testing ethical framework acceptable to both the (Biller‐Andorno et al. 2015). It has been sug international biomedical community and gested that animal experiments can be sanc animal welfare groups. COIMS set the fol tioned if there is no alternative means of lowing international guiding principles achieving the same scientific or educational (Howard‐Jones 1985): objective, and if the benefits to society out ●● The use of animals for scientific purposes weigh the costs in terms of animal harm is innately undesirable. (Rusche 2003). Harming animals is highly ●● Another method should be used whenever undesirable and experiments can only be jus possible. tified if the social good derived from this type ●● The use of animals in the present state of of use actively outweighs the negative aspect knowledge is unavoidable. of harming a sensitive creature (Kolar 2006). ●● Scientists should have a moral obligation Whenever possible, alternative methods in designing the plan for the minimal num should be sought. The three Rs (3Rs) princi ber of animals to be employed. ple, which should be applied as a guide when conducting animal research, includes The guiding principles are the product of replacement, reduction, and refinement: consultation with a large and representative sample of the biomedical community, ●● Replacement: Using an experimental sub including experts from the World Health ject that is phylogenetically lower or using Organization (WHO) and representatives of non‐animal systems. A few promising animal welfare groups. alternative methods put forward recently are in vitro techniques; tissue culture methods; use of lower organisms including microbes, tissues from slaughter, and 6.7 Conclusions autopsy embryos; and non‐animal systems such as computers or mathematical Furcation involvement poses one of the most modelling. difficult challenges in periodontal therapy. ●● Reduction: Before proposing to conduct Based on the available data, if one considers animal experimentation, efforts should closure of the furcation defect as the main be made to ascertain that the proposed endpoint of therapy, then the results of 128 Chapter 6
regeneration have to be regarded as satisfy studies, the effectiveness and relevance for ing and predictable only for class II furcation clinical practice may be questioned. In the involvements. Conversely, class III furcation future, new regenerative treatment modali defects are still considered a great challenge ties and the development of more challeng in terms of periodontal regeneration and, ing CSDs in pre‐clinical studies are clearly although the efficacy of different treatments needed to improve the predictability of com has been demonstrated in some pre‐clinical plete resolution of class III furcation defects.
Summary of Evidence
●● Animal studies, despite their limitations, of different treatments has been demon are an important step for establishing strated in some pre‐clinical studies. cause‐and‐effect relationships and for the ●● The concept of the critical size defect (CSD) initial evaluation of principles in the is an important factor affecting the outcome development of new regenerative devices in pre‐clinical studies, and new, more chal and advanced therapeutics. lenging CSDs (in width and height) should ●● Independent of the defect type and animal be developed to evaluate the regenerative model adopted, regenerative periodontal potential of different materials in furcation surgery using a combination of barrier involvement. This is in particular consider membranes and grafting materials may ation of the higher regeneration ability of result in periodontal regeneration to a animals in comparisons to humans. variable extent in furcation involvements. ●● Growth and differentiation factor tech ●● The results of regeneration have to be nologies and cell‐based therapies have regarded as satisfying and predictable also received considerable attention in only for class II furcation involvements, as regenerative medicine, but their experi class III furcation defects are still consid mental evaluation in the treatment of per ered a great challenge in terms of perio iodontal furcation lesions is still at a very dontal regeneration, although the efficacy early stage of development.
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cementogenesis by recombinant human Schmitz, J.P., and Hollinger, J.O. (1986). The osteogenic protein‐1 (hop‐1/bmp‐7) in the critical size defect as an experimental model baboon (Papio ursinus). Archive of Oral for craniomandibulofacial nonunions. Biology 41, 121–126. Clinical Orthopaedics and Related Research Risbud, M.V., and Shapiro, I.M. (2005). The 205, 299–308. effect of brain‐derived neurotrophic factor Schou, S., Holmstrup, P., and Kornman, K.S. on periodontal furcation defects: Stem cells (1993). Non‐human primates used in studies in craniofacial and dental tissue engineering. of periodontal disease pathogenesis: A Orthodontic and Craniofacial Research 8, 54. review of the literature. Journal of Roriz, V.M., Souza, S.L., Taba, M., Jr, et al. Periodontology 64, 497–508. (2006). Treatment of Class III furcation Sculean, A., Nikolidakis, D., and Schwarz, F. defects with expanded (2008). Regeneration of periodontal tissues: polytetrafluoroethylene membrane Combinations of barrier membranes and associated or not with anorganic bone grafting materials – biological foundation matrix/synthetic cell‐binding peptide: A and preclinical evidence: A systematic histologic and histomorphometric study in review. Journal of Clinical Periodontology dogs. Journal of Periodontology 77, 490–497. 35, 106–116. Rossa, C., Marcantonio, E., Jr, Cirelli, J.A. et al. Sculean, A., Windisch, P., Döri, F. et al. (2007). (2000). Regeneration of Class III furcation Emdogain in regenerative periodontal defects with basic fibroblast growth factor therapy: A review of the literature. Fogorvosi (b‐FGF) associated with GTR: A descriptive Szemle 100, 220–232. and histometric study in dogs. Journal of Selvig, K.A. (1994). Discussion: Animal models Periodontology 71, 775–784. in reconstructive therapy. Journal of Rusche, B. (2003). The 3Rs and animal welfare: Periodontology 65, 1169–1172. Conflict or the way forward? ALTEX 20, Seo, B.M., Miura, M., Gronthos, S. et al. 63–76. (2004). Investigation of multipotent Saito, A., Saito, E., Kuboki, Y. et al. (2013). postnatal stem cells from human Periodontal regeneration following periodontal ligament. Lancet 10–16, application of basic fibroblast growth 149–155. factor‐2 in combination with beta tricalcium Shirakata, Y., Miron, R.J., Nakamura, T. et al. phosphate in class III furcation defects in (2017). Effects of EMD liquid (Osteogain) dogs. Dental Materials Journal 232, on periodontal healing in class III furcation 256–262. defects in monkeys. Journal of Clinical Saito, E., Saito, A., Kuboki, Y. et al. (2012). Periodontology 44, 298–307. Periodontal repair following implantation of Simsek, S.B., Keles, G.C., Baris, S., and beta‐tricalcium phosphate with different Cetinkaya, B.O. (2012). Comparison of pore structures in Class III furcation defects mesenchymal stem cells and autogenous in dogs. Dental Materials Journal 31, cortical bone graft in the treatment of class 681–688. II furcation defects in dogs. Clinical Oral Sander, L., and Karring, T. (1995). New Investigation 16, 251–258. attachment and bone formation in Soares, F.P., Hayashi, F., Yorioka, C.W. et al. periodontal defects following treatment of (2005). Repair of Class II furcation defects submerged roots with guided tissue after a reparative tissue graft obtained from regeneration. Journal of Clinical extraction sockets treated with growth Periodontology 22, 295–299. factors: A histologic and histometric study Sanz, M., Jepsen, K., Eickholz, P., and Jepsen, in dogs. Journal of Periodontology 76, S. (2015). Clinical concepts for regenerative 1681–1689. therapy in furcations. Periodontology 2000 Stavropoulos, A., and Wikesjö, U.M. (2012). 68, 308–332. Growth and differentiation factors for 134 Chapter 6
periodontal regeneration: A review on Teares, J.A., Ramoshebi, L.N., and Ripamonti, factors with clinical testing. Journal of U. (2008). Periodontal tissue regeneration by Periodontal Research 47, 545–553. recombinant human transforming growth Struillou, X., Boutigny, H., Badran, Z. et al. factor‐beta 3 in Papio ursinus. Journal of (2011). Treatment of periodontal defects in Periodontal Research 43, 1–8. dogs using an injectable composite Trombelli, L., and Farina, R (2008). Clinical hydrogel/biphasic calcium phosphate. outcomes with bioactive agents alone or in Journal of Material Sciences Materials in combination with grafting or guided tissue Medicine 22, 1707–1717. regeneration. Journal of Clinical Struillou, X., Boutigny, H., Soueidan, A., and Periodontology 35, 117–135. Layrolle, P. (2010). Experimental animal Trubiani, O., Di Primio, R., Traini, T. et al. models in periodontology: A review. Open (2005). Morphological and cytofluorimetric Dental Journal 4, 37–47. analysis of adult mesenchymal stem cells Suaid, F.A., Macedo, G.O., Novaes, A.B. et al. expanded ex vivo from periodontal (2010). The bone formation capabilities of ligament. International Journal of the anorganic bone matrix‐synthetic cell‐ Immunopathology and Pharmacology 18, binding peptide 15 grafts in an animal 213–221. periodontal model: A histologic and Wang, S., Liu, Y., Fang, D., and Shi, S. (2007). histomorphometric study in dogs. Journal of The miniature pig: A useful large animal Periodontology 81, 594–603. model for dental and orofacial research. Suaid, F.F., Ribeiro, F.V., Gomes, T.R. et al. Oral Disease 13, 530–537. (2012). Autologous periodontal ligament Wang, Y., Chai, Z., Zhang, Y. et al. (2014). cells in the treatment of Class III furcation Influence of low‐intensity pulsed ultrasound defects: A study in dogs. Journal of Clinical on osteogenic tissue regeneration in a Periodontology 39, 377–384. periodontal injury model: X‐ray image Suaid, F.F., Ribeiro, F.V., Rodrigues, T.L. et al. alterations assessed by micro‐computed (2011). Autologous periodontal ligament tomography. Ultrasonics 54, 1581–1584. cells in the treatment of class II furcation White, C., Jr., Hancock, E.B., Garetto, L.P., and defects: A study in dogs. Journal of Clinical Kafrawy, A.A. (1994). A histomorphometric Periodontology 38, 491–498. study on the healing of class III furcations Takahashi, D., Odajima, T., Morita, M. et al. utilizing bone labelling in beagle dogs. (2005). Formation and resolution of Journal of Periodontology 65, 84–92. ankylosis under application of recombinant Wikesjö, U.M., Guglielmoni, P., Promsudthi, A. human bone morphogenetic protein‐2 et al. (1999). Periodontal repair in dogs: (rhBMP‐2) to class III furcation defects in Effect of rhBMP‐2 concentration on cats. Journal of Periodontal Research 40, regeneration of alveolar bone and 299–305. periodontal attachment. Journal of Clinical Takayama, S., Murakami, S., Shimabukuro, Y. Periodontology 26, 392–400. et al. (2001). Periodontal regeneration by Wikesjö, U.M., Kean, C.J., and Zimmerman, FGF‐2 (bFGF) in primate models. Journal of G.J. (1994). Periodontal repair in dogs: Dental Research 80, 2075–2079. Supraalveolar defect models for evaluation Teares, J.A., Petit, J.C., and Ripamonti, U. of safety and efficacy of periodontal (2012). Synergistic induction of periodontal reconstructive therapy. Journal of tissue regeneration by binary application of Periodontology 65, 1151–1157. human osteogenic protein‐1 and human Wikesjö, U.M., Lim, W.H., Thomson, R.C. transforming growth factor‐β3 in Class II et al. (2003a). Periodontal repair in dogs: furcation defects of Papio ursinus. Journal of Evaluation of a bioabsorbable space‐ Periodontal Research 47, 336–344. providing macroporous membrane with Regenerative Therapy in Animal Models 135
recombinant human bone morphogenetic porous titanium granules or deproteinized protein‐2. Journal of Periodontology 74, bovine bone. Journal of Periodontology 83, 635–647. 211–221. Wikesjö, U.M., Xiropaidis, A.V., Thomson, Yang, J.R., Hsu, C.W., Liao, S.C. et al. (2013). R.C. et al. (2003b). Periodontal repair in Transplantation of embryonic stem cells dogs: Space‐providing ePTFE devices improves the regeneration of periodontal increase rhBMP‐2/ACS‐induced bone furcation defects in a porcine model. Journal formation. Journal of Clinical Periodontology of Clinical Periodontology 40, 364–371. 30, 715–725. Zetterström, O., Andersson, C., Eriksson, L. Wohlfahrt, J.C., Aass, A.M., Rønold, H.J. et al. et al. (1997). Clinical safety of enamel matrix (2012). Microcomputed tomographic and derivative (EMDOGAIN) in the treatment histologic analysis of animal experimental of periodontal defects. Journal of Clinical degree II furcation defects treated with Periodontology 24, 697–704. 137
Chapter 7
Regenerative Therapy of Furcations in Human Clinical Studies: What has been Achieved So Far? Søren Jepsen and Karin Jepsen
Department of Periodontology, Operative and Preventive Dentistry, University of Bonn, Germany
7.1 Introduction tooth‐supporting tissues, including cemen- tum, periodontal ligament, and alveolar bone, Different strategies are available to address over a previously diseased root surface. Even the problem of furcation involvement (FI). though such outcomes have been demon- One option is the elimination of the furcation strated in well‐controlled experimental animal defect. This can be achieved by removal of the studies for a variety of treatment modalities involved root(s) using resective approaches (see Chapter 6), information derived from (see Chapter 8). Alternatively, periodontal tis- human histology is scarce. Four histological sues that have been destroyed by periodonti- studies investigated human degree II furcation tis can be regenerated, thereby decreasing the defects (Harris 2002; Stoller et al. 2001; Camelo lesion. Regenerative periodontal therapy of et al. 2003; Nevins et al. 2003), one studied furcation defects has proven successful in degree III defects (Mellonig et al. 2009), while many experimental pre‐clinical studies (see one presented data from degree II and III fur- Chapter 6). cation defects (Gottlow et al. 1986). This chapter reviews the evidence for the effectiveness of regenerative therapy for the 7.2.1.1 Degree II Furcation Defects treatment of furcation defects in different Regarding degree II defects, all five studies clinical scenarios, in order to address the reported partial regeneration of the perio- question: ‘What has been achieved so far?’ dontal tissues. Two studies applied deminer- alized freeze‐dried bone allograft (DFDBA) 7.2 Outcome Measures combined with recombinant human platelet‐ for Regenerative Therapy derived growth factor‐BB (rhPDGF‐BB) and in Furcation Defects reported formation of bone, cementum, and periodontal ligament coronally to the notch (Camelo et al. 2003; Nevins et al. 2003). Two A variety of outcome measures can be other studies used barrier membranes considered to assess the effectiveness of (guided tissue regeneration, GTR) and regenerative furcation therapies. described formation of cementum, perio- 7.2.1 Human Histology dontal ligament, and bone (Gottlow et al. 1986; Stoller et al. 2001). Harris (2002) used Evidence for periodontal regeneration requires a combination (DFDBA + polyhydroxyal- the histological demonstration of restored kanoate [PHA] + tetracycline + resorbable
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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membrane) and observed partial defect GTR studies to report the reduction in hori- closure with new bone, cementum, and con- zontal probing during re‐entry, and also the nective tissue attachment coronal or limited frequency (predictability) of complete furca- to the notch area. tion closure (Jepsen et al. 2002). As an alternative to open probing bone 7.2.1.2 Degree III Furcation Defects level assessments during a re‐entry proce- The two studies evaluating degree III furcation dure, probing bone measurements were pro- defects reported only partial regeneration. posed and evaluated (Suh et al. 2002). In Gottlow et al. (1986), using barrier membranes some clinical trials, horizontal probing bone (GTR), demonstrated 2.8 mm new cementum level was assessed after only six months, and with inserting collagen fibres in a 7 mm furca- it may be speculated that this is too early for tion defect. Mellonig et al. (2009), using a com- a final evaluation of bone fill in furcation bined technique (rhPDGF + beta‐tricalcium defects. Patient‐reported outcomes follow- phosphate [β‐TCP] + collagen membrane) ing regenerative furcation surgery may reported partial closure in three out of the four include postoperative pain, the rate of com- defects. The histomorphometric data revealed plications, perceived benefit, and change in new cementum ranging from 0.0 to 5.5 mm, quality of life (see Chapter 13). while the length of new bone and new collagen fibres ranged from 0.0 to 2.0 mm. 7.3 Clinical Scenarios 7.2.2 Clinical Outcomes Most of the currently available clinical stud- From a clinical point of view, complete elimi- ies to date have been devoted to mandibular nation of the inter‐radicular defect appears to molars with buccal/lingual degree II furca- be the most important outcome. Decreasing tion defects and maxillary molars with buc- furcation degree is associated with a cal/interproximal degree II furcation defects. decreased long‐term tooth loss risk (see More limited information is available on Chapter 5). Thus, the main outcome variables mandibular degree III furcation defects and for studies evaluating the efficacy of regener- maxillary degree III furcation defects, ative techniques in furcations are change of whereas there is a paucity of data on regen- furcation status (conversion into class I or erative treatment in degree I furcations and complete closure) and horizontal hard‐tissue in maxillary premolars (Avila‐Ortiz et al. fill. As histological evidence for successful 2015; Reddy et al. 2015). furcation regeneration is not a practical out- The efficacy of various regenerative come variable for controlled clinical trials, approaches in furcation defects has been changes in direct bone measurements (hori- evaluated by several systematic reviews with zontal probing bone level, at surgery and or without meta‐analyses (Jepsen et al. 2002; during re‐entry) serve as primary outcome Murphy and Gunsolley 2003; Reynolds et al. variables for evaluating clinical success, while 2003; Kinaia et al. 2011; Chen et al. 2013; clinical attachment level gain (horizontal/ Avila‐Ortiz et al. 2015) and has also been vertical probing attachment level), probing addressed in a recent comprehensive narra- depth reduction (horizontal/vertical), and tive review (Sanz et al. 2015), which served as radiographic assessments may serve as sec- a basis for this chapter. ondary outcomes (Machtei 1997). Bone fill during a re‐entry procedure is the only com- 7.3.1 Degree II Furcation Defects ponent of a regenerated periodontium that can be accurately assessed clinically. In fact, it 7.3.1.1 Barrier Membranes (GTR) was stated at a European consensus confer- After clinical case series (Becker et al. 1988) ence that it would be desirable for all future had demonstrated promising results for GTR Regenerative Therapy in Human Clinical Studies 139 therapy in furcation defects using expanded Horwitz et al. 2004). However, other authors PTFE barriers (Gore‐Tex Periodontal have found deep baseline pockets to be asso- Membrane, W.L. Gore and Assoc., Flagstaff, ciated with significant reductions in the AZ, USA), several randomized controlled number of complete furcation closures clinical trials compared GTR therapy with (Bowers et al. 2003). This discrepancy may open‐flap debridement (OFD, representing be a result of differences in bone morphol- standard control treatment) in human degree ogy. Wide furcations respond less favourably II furcation defects. Several studies observed and in deep degree II furcations (≥5 mm) more favourable horizontal probing attach- complete closure is less likely (Bowers et al. ment level gain and horizontal probing bone 2003). If the fornix of the furcation is located level gain after GTR than after OFD in degree apically to the interproximal alveolar crest II furcation defects of mandibular molars (key‐hole defect), more horizontal attach- (Pontoriero et al. 1988; Lekovic et al. 1989, ment gain may be expected than in teeth 1991; Mellonig et al. 1994; Wang et al. 1994; with a furcation fornix located coronally of Mombelli et al. 1996; Prathibha et al. 2002; the interproximal bone level. If there is bone Cury et al. 2003; Bremm et al. 2004; see also coronal of the furcation fornix adjacent to Table 7.1), of maxillary molars (Metzler et al. the tooth, coverage and stabilization of the 1991; Mellonig et al. 1994; Pontoriero and membrane may be achieved by a coronal Lindhe 1995a; Avera et al. 1998; see also positioning of the flap. Under such condi- Table 7.2), and of maxillary and mandibular tions, the surface of the periodontal ligament molars (Flanary et al. 1991; Paul et al. 1992; to provide cells to colonize the blood clot Twohey et al. 1992; Caton et al. 1994; Yukna within the defect is larger than in a tooth and Yukna 1996; see also Table 7.3). Whereas where the fornix is located coronal of the some authors observed more favourable alveolar crest (Bowers et al. 2003; Horwitz results six months after GTR therapy in et al. 2004). maxillary degree II furcations only in buccal When comparing the use of non‐resorbable sites (Pontoriero and Lindhe 1995a), others and biodegradable barrier membranes in the reported statistically better horizontal prob- treatment of mandibular degree II furcation ing bone level gain also in mesiopalatal defects, similar horizontal defect fill has degree II furcations nine months following been reported (Blumenthal 1993; Bouchard GTR (Avera et al. 1998). et al. 1993; Christgau et al. 1995; Hugoson A systematic review with meta‐analyses et al. 1995; Yukna and Yukna 1996; assessed the efficacy of membrane therapy in Caffesse et al. 1997; Eickholz et al. 1997, the treatment of periodontal furcation 1998; Garrett et al. 1997; Scott et al. 1997; defects measured against standard surgical Dos Anjos et al. 1998; Pruthi et al. 2002; see periodontal treatment (i.e. OFD; Jepsen et al. also Table 7.4). Only a few studies have com- 2002), and confirmed the superiority of GTR pared the clinical efficacy of different bioab- over OFD in class II furcation defects; sorbable barrier membranes for treatment however, the results also showed significant of Class II furcations; none found one bioab- heterogeneity, indicating high variability. sorbable material to be superior to another These results were subsequently also con- (Vernino et al. 1999; Eickholz et al. 2000). firmed by other systematic reviews (Murphy and Gunsolley 2003; Kinaia et al. 2011). This 7.3.1.2 Combination Therapy (GTR variability may be explained by prognostic and Bone Grafts) factors (e.g. smoking, peri‐surgical antibiot- The combination of a barrier membrane ics, or defect morphology; Bowers et al. 2003; with a filler material may enhance the hori- Horwitz et al. 2004). Deep pockets at base- zontal fill of molars with degree II FI as line facilitate more favourable results after shown in a systematic review with meta‐ regenerative therapy (Machtei et al. 1994; analysis (Chen et al. 2013). Out of four studies 6 months 6 months 6 months 9 months Observation period Expanded polytetrafluoroethylene Expanded polytetrafluoroethylene Expanded polytetrafluoroethylene Expanded polytetrafluoroethylene Barrier material a a a a a a 10 10 8 8 n
1.0* 8 1.1* 0.4 0.2 Gain (mm) 0.9* 17
Table 7.1 Comparison of clinical results after open‐flap debridement and guided tissue regeneration in degree II furcation defects of mandibular molars.
Open‐flap Guided tissue debridement regeneration Barrier Guided tissue regeneration baseline (mm) 3.2 3.5 3.4 Study baseline Gain baseline Gain material/ Observation Authors type Parameter (mm) (mm) n (mm) (mm) n filler period 10 10 n 8 8 Lekovic et al. 1989 RCTHo rizontal probing 12 Expanded 6 months bone level polytetrafluoroethylene Buccal No data ‐0.14 No data 0.18 12 a Lekovic et al. 1991 RCTHo rizontal probing 15 Connective tissue graft 6 months 0.3 8 4.9 0.3 0.2 0.2 Gain (mm) 0.3 17 3.7 bone level including periosteum Buccal 4.2 ‐0.2 4.2 1.6 * 15a Mellonig et al. RCTHorizontal probing 7.6 1.0 11 8.4 4.5 * 11a Expanded 6 months 1994 bone level polytetrafluoroethylene Wang et al. 1994 RCTHorizontal probing 5.58 1.08 12 6.00 2.04 * 12a BioMend®b 12 months bone level Prathibha et al. RCTHorizontal probing 4.7 0.64 10 4.79 2.38 * 10a TefGen®c 6 months 2002 bone level 4.5 3.2 3.4 3.2 No data ‐0.69 No data 1.19* 3.7 Open‐flap debridement baseline (mm) Comparison of open‐flap debridement with guided tissue regeneration in combination with fillers Houser et al. 2001 RCTHorizontal probing 6.2 0.9 13 5.7 3.0 * 18 BioGide®d bone level and BioOss®
Tsao et al. 2006 RCTHorizontal probing 4.7 0.2 94.3 1.1 * 9 Puros® e 6 months bone level 4.4 1.1 * 9 BioMend and Puros
*St atistically significant difference between open‐flap debridement and guided tissue regeneration; a split‐mouth design; Horizontal probing bone level Horizontal probing bone level Buccal Mesiolingual Distolingual Horizontal probing bone level Mesiolingual Horizontal probing bone level and Buccal interproximal b bovine type 1 collagen; c polytetrafluoroethylene; d deproteinized bovine bone mineral/porcine collagen; emineralized solvent‐dehydrated bone allograft; RCT = randomized controlled trial. RCT RCT RCT RCT Study Study type Parameter Comparison of clinical results after open‐flap debridement and guided tissue regeneration in degree II furcation defects of maxillary II furcation molars. in degree after open‐flap debridement and guided tissue regeneration of clinical results Comparison Mellonig et al. 1994 Mellonig Pontoriero and Pontoriero Lindhe 1995a et al. 1998 Avera Authors Metzler et al. 1991 Table 7.2 *Statistically significant between difference open‐flap and guided debridement tissue regeneration;
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Table 7.1 Comparison of clinical results after open‐flap debridement and guided tissue regeneration in degree II furcation defects of mandibular molars.
Open‐flap Guided tissue debridement regeneration Barrier Study baseline Gain baseline Gain material/ Observation Authors type Parameter (mm) (mm) n (mm) (mm) n filler period Table 7.2 Comparison of clinical results after open‐flap debridement and guided tissue regeneration in degree II furcation defects of maxillary molars.
Lekovic et al. 1989 RCTHo rizontal probing 12 Expanded 6 months bone level polytetrafluoroethylene Open‐flap Guided tissue Buccal No data ‐0.14 No data 0.18 12 a debridement regeneration Study baseline Gain baseline Gain Barrier Observation Lekovic et al. 1991 RCTHo rizontal probing 15 Connective tissue graft 6 months Authors type Parameter (mm) (mm) n (mm) (mm) n material period bone level including periosteum a Buccal 4.2 ‐0.2 4.2 1.6 * 15 a a Metzler et al. 1991 RCT Horizontal probing 3.7 0.3 17 3.7 0.9 * 17 Expanded 6 months Mellonig et al. RCTHorizontal probing 7.6 1.0 11 8.4 4.5 * 11 Expanded 6 months bone level polytetrafluoroethylene 1994 bone level polytetrafluoroethylene Buccal and Wang et al. 1994 RCTHorizontal probing 5.58 1.08 12 6.00 2.04 * 12a BioMend®b 12 months interproximal bone level Mellonig et al. 1994 RCTHorizontal probing 4.5 0.3 8 4.9 1.0 * 8a Expanded 6 months Prathibha et al. RCTHorizontal probing 4.7 0.64 10 4.79 2.38 * 10a TefGen®c 6 months bone level polytetrafluoroethylene 2002 bone level Pontoriero and RCT Horizontal probing 10 10a Expanded 6 months Lindhe 1995a bone level polytetrafluoroethylene Comparison of open‐flap debridement with guided tissue regeneration in combination with fillers a Buccal 3.2 0.3 10 3.2 1.1 * 10 d Houser et al. 2001 RCTHorizontal probing 6.2 0.9 13 5.7 3.0 * 18 BioGide® Mesiolingual 3.4 0.2 8 3.5 0.4 8 a bone level and BioOss® Distolingual 3.2 0.2 8 3.4 0.2 8 a Avera et al. 1998 RCT Horizontal probing Expanded 9 months Tsao et al. 2006 RCTHorizontal probing 4.7 0.2 94.3 1.1 * 9 Puros® e 6 months bone level polytetrafluoroethylene bone level 4.4 1.1 * 9 BioMend Mesiolingual No data ‐0.69 No data 1.19 * and Puros *St atistically significant difference between open‐flap debridement and guided tissue regeneration; a *St atistically significant difference between open‐flap debridement and guided tissue regeneration; split‐mouth design; a split‐mouth design; RCT = randomized controlled trial. b bovine type 1 collagen; c polytetrafluoroethylene; d deproteinized bovine bone mineral/porcine collagen; emineralized solvent‐dehydrated bone allograft; RCT = randomized controlled trial.
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Open‐flap Guided tissue debridement regeneration 0.8 19 3.3 1.1 27 5.0 0.3 0 7 4.71 Gain (mm) Study baseline Gain baseline Gain Barrier Authors type Parameter (mm) (mm) n (mm) (mm) n material Observation period
Flanary et al. 1991 RCTHorizontal probing 2.9 0.8 19 3.3 1.5 * 19a Biobrane® b 6 months bone level Paul et al. 1992 (132) RCTHorizontal probing 3.86 074.71 0.86 * 7 a Collistar® b 6 months bone level a 2.9 5.3 2.6 3.86 Open‐flap debridement baseline (mm) Twohey et al. 1992 RCT Horizontal probing 8 8 Biobrane 6 months bone level Buccal 2.6 0.3 3.3 1.4 * Yukna and Yukna RCTHorizontal probing 5.3 1.1 27 5.0 2.0 * 27 a BioMend® c 6–12 months 1996 bone level (mean = 11.1 months)
*St atistically significant difference between open‐flap debridement and guided tissue regeneration; a split‐mouth design; b poly‐dimethyl‐siloxane mechanically bonded to a fine‐knit, flexible nylon fabric; c bovine type 1 collagen; RCT = randomized controlled trial. Horizontal probing bone level Horizontal probing bone level Horizontal probing bone level Buccal Horizontal probing bone level Study Study type Parameter RCT RCT RCT RCT Comparison of clinical results after open‐flap debridement and guided tissue regeneration in degree II furcation defects of maxillary II furcation and mandibular in degree after open‐flap debridement and guided tissue regeneration of clinical results Comparison Flanary et al. 1991 Authors Yukna and Yukna and Yukna Yukna 1996 Twohey et al. 1992 Twohey Paul et al. 1992 (132) Paul split‐mouth design;split‐mouth *Statistically significant between difference open‐flap and guided debridement tissue regeneration; a Table 7.3 molars.
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on mandibular molars, two showed statisti- Mandibular Molars cally significantly more horizontal bone fill In a case series study with 36 months of fol- following the combination therapy (Wallace low‐up on 10 patients with 8 buccal and 8 et al. 1994; Luepke et al. 1997; Simonpietri lingual degree II FI, the use of EMD was eval- et al. 2000; Maragos et al. 2002; see also uated (Donos et al. 2003a). The follow‐up Table 7.5). periods were 6, 12, and 36 months. At the buccal furcation defects, the horizontal prob- 7.3.1.3 Long‐term Results ing attachment level measurements were Long‐term data following GTR therapy in reduced from 4.0 mm at baseline to 2.6 mm furcation defects are sparse (Figueira et al. at 6 months, demonstrating a mean horizon- 2014). Using GTR, horizontal probing attach- tal probing attachment level change of ment level gains from 0.75 to 4.1 mm and 1.4 mm. However, at 12 and 36 months the horizontal probing bone level gains from change was reduced to 0.8 mm and 0.6 mm, 0.2 to 4.5 mm may be achieved, and degree II respectively, and, as such, the horizontal furcation defects may be closed or converted probing attachment level changes were not to degree I. Molars with degree I FI have a adequate to transform the degree II FI to better long‐term prognosis than molars with degree I. At the lingual sites, the horizontal degree II defects (McGuire and Nunn 1996), probing attachment level changes were mini- whereas a gradual increase in the risk of tooth mal. In all cases, following the 12‐month loss was observed for molars with degree II healing period the furcation defects remained and III FI (Nibali et al. 2016). To date there are as degree II. This study was performed in a only limited data on the long‐term results small number of mandibular molars, and it (≥4 years) after GTR therapy in degree II fur- did not have a control group in which either cations. Significant gains in horizontal attach- OFD or another established regenerative ment (2.59 mm) were obtained one year post procedure, such as GTR, was performed. surgery for GTR‐treated sites. These changes When investigating the adjunctive use of were maintained over four years with a slight EMD with OFD in 10 patients with 20 degree decline at the end of year 3 (Machtei et al. II furcation defects on contralateral molars 1996). Mean horizontal probing attachment by re‐entry after 6 months, a significantly level gains after the use of non‐resorbable and enhanced horizontal bone gain (2 mm in the biodegradable barriers could be maintained EMD vs 0.8 mm in the OFD group) of the for five years (Eickholz et al. 2001). A 10‐year bony defects was found in EMD‐treated follow‐up of 18 teeth in 9 patients revealed furcations (Chitsazi et al. 2007). Complete further stability of horizontal probing attach- furcation closure was reported in 1 of the ment level gains between 12 and 120 months. 10 defects treated with EMD. However, a re‐ However, two molars were lost in one patient, entry at 6 months post‐operatively may be and another molar lost more than 2 mm of too early to evaluate bone fill of a furcation horizontal probing attachment level (Eickholz lesion. et al. 2006). A multi‐centre randomized controlled clinical trial compared EMD with GTR in 7.3.1.4 Enamel Matrix Derivative (EMD) the treatment of degree II buccal furcation Only a limited number of clinical studies defects in mandibular molars (Jepsen et al. have evaluated enamel matrix derivative 2004). In this study, the investigators treated (Emdogain, Straumann, Basel, Switzerland) 45 patients with a total of 90 similar degree for the treatment of FI, either alone or in II furcation defects on contralateral molars, combination with another regenerative either with EMD or with a bioresorbable therapy (for review Donos et al. 2010; Koop membrane. The clinical measurements et al. 2012; Miron et al. 2014, 2016), and no performed at baseline, 8 months, and meta‐analyses have been performed. 14 months following surgery included Table 7.5 Comparison of clinical results after guided tissue regeneration using a barrier membrane alone and in combination with osseous grafts in degree II furcation defects of mandibular molars (all randomized controlled trials).
Guided tissue Guided tissue regeneration regeneration barrier barrier material material + osseous alone graft (baseline) Gain baseline Gain Osseous graft Observation Authors Defect type Parameter (mm) (mm) n (mm) (mm) n material period
Wallace et al. Mandibular Horizontal Expanded 710Decalcified 12 months 1994 molars probing bone polytetrafluoroethylene freeze‐dried bone level allograftb Buccal 6.0 2.3 6.5 2.4 Luepke et al. 1997 Mandibular Horizontal Guidor®c 1.80 14 5.90 2.1 14a Decalcified 6 months molars probing bone 6.03 freeze‐dried bone level allograftb Simonpietri‐C Mandibular Horizontal Gengiflex®d 2.47 15 5.53 3.27 * 15a Bon‐Apatite®e 6 months et al. 2000 molars probing bone 5.0 level
Maragos et al. Mandibular Horizontal CaSO4 0.9 11 3.5 1.2 11 CaSO4 / 12 months 2002 molars probing bone 3.8 3.7 2.2 14 doxycycline level CaSO4 / decalcified freeze‐dried bone allograftb
*St atistically significant difference between guided tissue regeneration and guided tissue regeneration + osseous grafts; a split‐mouth design; b decalcified freeze‐dried bone allograft; c synthetic biodegradable polymer; d cellulose; e anorganic bovine bone.
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gingival margin levels, pocket probing From the same sample of patients, it was depth, bleeding on probing, vertical attach- also observed that the best clinical outcome ment levels, vertical bone sounding from a in buccal degree II furcation defects follow- stent at five buccal sites per tooth, and hori- ing treatment with EMD was in male patients zontal bone sounding at the furcation area. over 54 years of age who were non‐smokers Similar defect measurements were per- (Hoffmann et al. 2006), which is in agree- formed during a re‐entry procedure on all ment with observations in previous studies defects at 14 months post surgery. Change with GTR (Machtei et al. 1994). However, of horizontal furcation depth (comparing these results need to be interpreted with cau- intrasurgical baseline and re‐entry meas- tion, because the number of patients in each urements) served as the primary outcome subgroup (age, gender, smoking habit, etc.) variable. The results indicated that both was relatively low. Furthermore, in this study regenerative procedures produced clinical patient selection was of paramount clinical improvement. More specifically, EMD dem- importance, because all selected teeth pre- onstrated a mean reduction of horizontal sented with proximal levels at or above the probing bone level of 2.6 mm, whereas the fornix of the furcation and there was always a GTR‐treated sites showed a horizontal zone of keratinized tissue of at least 2 mm probing bone level reduction of 1.9 mm present, for covering the furcation following (Table 7.6). Complete furcation closure was the application of EMD. Similar results, with achieved in 8 of the 45 furcation defects regard to the treatment with EMD in man- treated with EMD and in 3 of the 45 defects dibular degree II FI, were reported in another treated with GTR. Partial closure (resulting randomized controlled trial with re‐entry in a change from degree II to degree I) was after 12 months (Barros et al. 2005). In the same (27 of 45) in both groups. No 10 patients with 20 paired furcation defects, change in furcation status was observed in 9 GTR therapy using an expanded PTFE mem- of 45 and in 11 of 45 defects, respectively, brane led to a mean horizontal defect fill of and deterioration was observed in one of 45 3.3 mm, whereas EMD application resulted EMD‐treated sites and in four of 45 GTR‐ in a mean horizontal defect fill of 2.2 mm, treated sites. Furthermore, less post‐opera- with no significant difference between the tive pain and swelling was reported modalities (Table 7.6). following the use of EMD, which could be explained by the antibacterial (Sculean et al. Maxillary Molars 2001) or anti‐inflammatory potential that A randomized controlled trial with a split‐ EMD might possess (Myhre et al. 2006; mouth design in 15 patients with one pair of Nokhbehsaim et al. 2012). The study con- contralateral degree II proximal FI compared cluded that the use of EMD not only has a the use of EMD with OFD in conjunction similar effect to GTR in transforming degree with conditioning of the root surfaces with II buccal furcation defects to degree I in a ethylenediaminetetraacetic acid (EDTA) gel predictable manner, but it may also achieve (Casarin et al. 2008). At 6 months, a mean complete closure of the furcation defects to horizontal bone gain was 1.0 mm for the con- a greater extent than GTR. Furthermore, for trol group and 1.1 mm for the test group. furcation defects at mid‐buccal sites, the However, there was a statistically significant EMD‐treated sites presented less gingival difference in the number of remaining degree recession than the GTR‐treated sites (Meyle II FI, in favour of EMD. Of 15 proximal et al. 2004). This could be attributed to the degree II furcations, 2 were completely fact that no measurable bone resorption closed and 9 were converted into degree I, 6 occurred in the EMD‐treated sites, whereas months following EMD application. In con- slight bone resorption occurred in the GTR‐ trast, following OFD, only 5 furcations were treated sites. converted into degree I, with the other Regenerative Therapy in Human Clinical Studies 147
Table 7.6 Comparison of clinical results after guided tissue regeneration or enamel matrix derivative (Emdogain) application in degree II furcation defects of mandibular molars.
Guided tissue regeneration EMD Barrier Study baseline Gain baseline Gain material/ Observation Authors type Parameter (mm) (mm) n (mm) (mm) n filler period
Jepsen et al. RCT Horizontal No data 1.9 45 No data 2.6* 45a Resolut®b 14 months 2004 probing bone level Buccal Barros et al. RCT Horizontal No data 3.3 15 No data 2.2 15a Expanded 6 months 2005 probing polytetrafluoro- bone level ethylene
*Statistically significant difference between guided tissue regeneration and enamel matrix derivative; asplit‐mouth design; bsynthetic biodegradable polymer; RCT = randomized controlled trial.
10 defects remaining degree II. Of the and a resorbable membrane (GTR; Jaiswal 15 patients, 12 were followed up for 24 months and Deo 2013). Using a parallel design, (Casarin et al. 2010) and at this time point 30 buccal or lingual mandibular degree II the test group presented with 5 remaining furcations in 30 patients received either degree II furcations versus 10 degree II furca- EMD + DFDBA + GTR, DFDBA + GTR, or tions in the control group (p < 0.05). Overall, OFD. After 12 months, mean reductions in the treatment response of proximal furca- horizontal probing depths were 2.1 mm for tions in maxillary molars to EMD application the EMD + DFDBA + GTR group and 1.5 mm was not as favourable as that of mandibular for the DFDBA + GTR group (p > 0.05). The furcations. The authors attributed this to number of degree II furcations that were more difficult access and higher plaque closed or converted to class I was greater for retention during follow up. EMD + DFDBA + GTR. A recently published parallel group rand- 7.3.1.5 Combination Therapy (EMD omized controlled trial with 40 patients and Bone Grafts) compared EMD, beta‐tricalcium phosphate Only a few clinical studies have evaluated the coated hydroxyapatite (ß‐TCP/HA), and combination of EMD with bone grafts or EMD + ß‐TCP/HA in buccal mandibular bone substitutes in furcation defects (Miron degree II furcation defects (Queiroz et al. et al. 2014). 2016). After 12 months, the mean horizontal clinical attachment level gain was 2.7 mm for Mandibular Molars EMD, 2.6 mm for β‐TCP/HA, and 2.9 mm In a case series of 11 patients, each contribut- for EMD + β‐TCP/HA, with no significant ing one buccal mandibular degree II furcation differences among the groups. After defect, a combination therapy of EMD and 12 months, 13 of 13 furcations in the EMD autologous bone grafts was evaluated (Aimetti group, 10 of 14 furcations in the β‐TCP/HA et al. 2007). After two years, complete clinical group, and 12 of 14 furcations in the β‐TCP/ closure was achieved in four sites and all resid- HA + EMD group improved their diagnoses ual defects were reduced to degree I. to degree I. However, complete furcation A comparative study tested the effective- closure was not detectable during the ness of EMD in combination with DFDBA study period. 148 Chapter 7
Maxillary Molars application of PRP, all furcation defects A randomized controlled trial evaluated the retained their degree II status. combination of EMD + ß‐TCP/HA com- Another randomized controlled trial of pared with ß‐TCP/HA alone in 30 patients nine months’ duration evaluated in a split‐ with 30 proximal class II furcation defects in mouth design the use of autologous PRF in maxillary molars (Peres et al. 2013). Mean the treatment of mandibular degree II furca- horizontal bone level gains after 6 months tion defects in comparison with OFD, in 18 were 1.7 mm for both treatment modalities. patients with 36 furcations (Sharma and The EMD + ß‐TCP/HA group showed 7 Pradeep 2011). Complete clinical closure was closed furcations and 7 converted to degree achieved in 12 of 18 test defects, whereas I, versus 4 closed furcations and 10 con- another 5 were reduced to degree I. Change verted to degree I in the ß‐TCP/HA group in horizontal clinical attachment level (p > 0.05). amounted to 2.7 mm following PRF versus At present, no long‐term data (>3 years) are 1.9 mm following OFD (p < 0.05). available for the effects of EMD application in A randomized controlled trial compared the regenerative therapy of furcation defects. PRP, PRF, and OFD in the treatment of 72 mandibular degree II furcations in 42 patients 7.3.1.6 Platelet Concentrates after nine months (Bajaj et al. 2013). In this Growth and differentiation factor technolo- study, both forms of autologous platelet con- gies have been evaluated for their potential centrates led to significantly better outcomes to enhance periodontal wound healing/ in all clinical and radiographic parameters regeneration (Stavropoulos and Wikesjö compared with the OFD control, with no dif- 2012). Autologous platelet concentrates, ferences between PRP and PRF. Horizontal such as platelet‐rich plasma (PRP) and plate- clinical attachment gain amounted to let‐rich fibrin (PRF), are a source for growth 2.75 mm (PRF) and 2.5 mm (PRP). factors that can be applied to the periodontal It should be noted that all these studies are wound (Dohan Ehrenfest et al. 2009; Del from the same centre. More recently the Fabbro et al. 2011). Very recently, systematic authors have published modified PRF proto- reviews with meta‐analyses have evaluated cols using the addition of synthetic statins the regenerative potential of these approaches and hydroxyapatite (HA) bone grafts (Pradeep for furcation defects (Troiano et al. 2016; et al. 2016), or the addition of alendronate gel Castro et al. 2017). While three original stud- (Kanoriya et al. 2017), thereby further ies were included in one systematic review enhancing the outcomes of PRF therapy. (Troiano et al. 2016), the other included only Finally, another group of authors (Siddiqui two of them (Castro et al. 2017). These stud- et al. 2016) evaluated in a six‐month study the ies are presented in more detail in what efficacy of PRF compared to ß‐TCP and to follows. OFD alone in the treatment of degree II man- dibular furcation defects. Horizontal probing Mandibular Molars bone level changes amounted to 2.1 mm, In a randomized clinical trial of six months’ 2.2 mm, and 1.0 mm, respectively. duration using a split‐mouth design (Pradeep et al. 2009), the effectiveness of autologous 7.3.2 Degree III Furcation Defects PRP was compared with OFD in the treat- ment of 20 patients with a total of 40 man- 7.3.2.1 Barrier Membranes (GTR) dibular degree II furcation defects. Although Only two randomized controlled clinical there was significantly more horizontal clini- trials have compared OFD and GTR in cal attachment level gain (2.5 mm vs 0.8 mm) molars with degree III FI (Pontoriero et al. and radiographic bone fill following the 1989; Pontoriero and Lindhe 1995b). Regenerative Therapy in Human Clinical Studies 149
Mandibular Molars treatment modalities. At 6 and 12 months, The earlier study reported therapy in man- partial closure of the degree III involvements dibular molars (Pontoriero et al. 1989). After had occurred in 6 of the 14 treated furca- assessing FI clinically, only 1 of 42 furcations tions. The remaining teeth still presented was scored as ‘through‐and‐through’ (degree through‐and‐through furcation defects. III). After flap elevation, but before debride- Within the limits of this case series, and tak- ment, all 42 furcations were scored as degree ing into account the small number of patients III. Six months after treatment, furcation and furcations included in each treatment involvement was assessed clinically (i.e. with- group, it was concluded that the use of EMD out elevation of a flap). In the GTR group, 3 alone or in combination with GTR did not molars remained as degree III, whereas in the result in predictable regeneration of degree OFD group, 11 remained as degree III, indi- III mandibular defects. cating better results with GTR.
Maxillary Molars 7.4 Furcation Regeneration: OFD and GTR were also compared in the Step‐by‐step Procedure treatment of maxillary interproximal degree III furcation defects (Pontoriero and Lindhe The suggested treatment sequence is as 1995b). Baseline and six‐month examinations follows: were performed by re‐entry after flap eleva- tion. Neither OFD nor GTR led to even partial 1) Patient selection. Systemic factors that closure of the 22 degree III furcations. limit the success of periodontal surgery, These results are supported by other clini- such as uncontrolled diabetes and immu- cal trials, which also demonstrated very low nocompromised status, must be consid- frequency and predictability of closure in ered. Poor patient compliance, inadequate degree III furcation defects after GTR ther- oral hygiene, and smoking are the most apy: no complete and 3 partial closures of 10 frequent patient factors limiting the selec- degree III furcations, 12 and 24 months tion of this procedure. Treatment options following GTR (Eickholz et al. 1998); and 6 and alternatives must be presented to the partial closures of 10 degree III furcations, 24 patient and the potential problems and months after GTR (Eickholz and Hausmann). the additional costs should be discussed. Complete closure of degree III furcations Regenerative furcation surgery should be (as evaluated during re‐entry) was never part of a comprehensive treatment plan reported (Jepsen et al. 2002). aiming at complete periodontal and func- tional rehabilitation. 7.3.2.2 Enamel Matrix Derivative 2) Tooth selection. Adequate access to the One case series study evaluated the treat- surgical site and also for future mainte- ment of degree III mandibular furcation nance is extremely important. Molars defects by the use of EMD alone or in combi- with degree II furcations (mandibular and nation with a bioresorbable membrane buccal maxillary FI) are the best candi- (Donos et al. 2004). Nine patients with a dates to be considered for a regenerative total of 14 degree III mandibular furcation procedure. Based on the available evi- defects were assigned to one of three groups: dence, interproximal maxillary degree II EMD in four defects; GTR in three defects; furcation defects are significantly less and EMD + GTR in seven defects. None of suited, most likely due to limited access. the treatments resulted predictably in com- Degree III mandibular and maxillary plete healing of the defects, and there was furcations have shown various treatment no obvious difference between the various responses and in general there are no 150 Chapter 7
significant differences in treatment out- entrance and to promote wound and clot comes comparing regenerative therapy stabilization. In order to facilitate com- with conventional surgery. Defect and site plete coverage of the barrier, the perios- characteristics have been identified that teum can be cut to allow for a coronal have impacts on the outcomes of regen- advancement of the flap. The flap is erative furcation surgery (Reddy et al. secured in a coronal position by a sling 2015). For example, a thicker biotype and suture and interrupted sutures over the the absence of soft‐tissue recession can vertical releasing incisions (Figure 7.2), or positively influence healing following interdental sutures in the case of a laterally GTR procedures. More favourable out- extended flap (Figure 7.1). The patient is comes can be expected in sites in which instructed to abstain from mechanical the remaining interproximal bone height plaque removal in the surgical area for a is coronal to the entrance of the furcation period of up to four weeks. During this defect, compared to those in which the time, chlorhexidine rinses or topical gel bone is at or apical to the furcation application are used. The patient returns entrance (Figure 7.1). Interdental root for monitoring of healing after one and proximity may impair proper defect two weeks, when sutures are removed. debridement. Presence of a root canal fill- Interdental hygiene and mechanical ing is not a contraindication to furcation plaque removal are started again after four regeneration per se, provided there are no weeks, and the personalized maintenance signs of apical pathology. recall programme will be determined. 3) Regenerative periodontal surgery. The goal is to obtain sufficient access to the defect for meticulous debridement and applica- 7.5 Furcation Regeneration: tion of the regenerative device. In the case How to Take the Next Step? of isolated defects, vertical releasing incisions may be used (Figure 7.2). It emerges clearly from this chapter that the Alternatively, the flap can be extended lat- main challenge for regenerating furcation erally (Figure 7.1). Keratinized tissues defects is presented by improving the pre- should be preserved by intrasulcular inci- dictability in degree II FI (in particular maxil- sion and the elevation of a full‐thickness lary interproximal furcations) and even more mucoperiostal flap. Granulation tissue by achieving regeneration in degree III furca- will be removed and the exposed root tion defects (maxillary or mandibular). surfaces carefully cleaned by hand instru- However, the previous chapter produced ments, power‐driven scalers (optionally clinical and histological evidence for regen- with diamond‐coated tips), or rotary eration of degree III furcations in animal instruments. Root anomalies such as models, including complete closure with the enamel projections/pearls should be formation of periodontal ligament and removed. If EMD is part of the regenera- regrowth of the bone with GTR (Lindhe et al. tive strategy, it is usually applied following 1995; Araújo et al. 1998) or GTR associated two minutes of root conditioning with with EMD (Donos et al. 2003a, 2003b; EDTA and rinsing with sterile saline. Gkranias et al. 2012) in animal models. So Subsequently a bone graft/substitute can how can we take the decisive step towards be used to fill the furcation defect. predictable furcation regeneration based on Alternatively, a GTR barrier membrane pre‐clinical studies? can be applied, with or without an addi- Complete flap coverage of the membrane tional defect filler (Figures 7.1 and 7.2). during healing seems to be crucial, probably The barrier membrane is secured by a more than defect morphology (Lindhe et al. resorbable sling suture to cover the furcation 1995; Araújo et al. 1997, 1998; Araújo and Regenerative Therapy in Human Clinical Studies 151
(a) (b) (c) (d) (e)
(f) (g) (h) (i)
(j) (k) (l)
(m) (n) (o) (p) (q)
Figure 7.1 (a) Periodontal measurements at baseline, tooth no. 36 (LL6). Probing depth mesial and distal: 2 mm, furcation degree II buccally, horizontal probing: 4 mm, recession 3 mm. (b) Radiograph of tooth no.36 with visible furcation defect, adjacent bone level at forcation fornix. (c) Flap elevation: intrasulcular incision/ horizonal release, mucoperiostal flap, papillae de‐epithelialized, periosteal split in the vestibule. Root surface debridement. (d) Horizontal probing bone level: 4 mm. (e, f) Placement of a bioresorbable matrix barrier (Guidor™ MSL‐configuration, Sunstar Americas, Inc., Schaumburg, IL, USA) to facilitate guided tissue regeneration. Fixation of the barrier with integrated sling sutures. (g, h) Coronally advanced flap secured with sling and interrupted sutures. (i) One day after periodontal regenerative surgery. (j) Clinical view 3 weeks after surgery with matrix exposure. (k, l) Exposed matrix partially removed. (m, n) 5 weeks after surgery. (o, p) 12 months after surgery. Horizontal and vertical probing depths: 2 mm, recession 3 mm. (q) Radiograph taken 12 months after surgery. Almost complete radiographic bone fill in furcation area.
Lindhe, 1998). Unfortunately, the different encountered in humans. Therefore, more anatomy and dimensions of teeth and alveo- progress in techniques and materials is lar processes in the experimental animal needed in order to predictably achieve in models reduce their external validity to humans the same results observed in animal human cases. Furthermore, experimentally models, before implementing regenerative induced furcation defects in animal models surgery as the treatment of choice for every may not reproduce the chronic lesions deep furcation defect. 152 Chapter 7
(a) (b) (c) (d)
(e) (f) (g) (h)
(i) (j) (k)
(l) (m) (n)
Figure 7.2 (a, b) Periodontal measurements at baseline, tooth no. 46 (LR6). Probing depth mesial and distal: 3 mm, furcation degree II. Situation 2 months after an acute abscess and mobility grade 2 treated with debridement of the accessible root surfaces and local antimicrobials. (c) Radiograph of tooth no. 46 with visible furcation defect, proximal bone loss to the level of the furcation, and a very short distal root. (d) Horizontal probing bone level: 7 mm, crown margin reduced and polished. (e, f) Debrided root surfaces. Flap design: intrasulcular incision/ vertical release mesial, mucoperiostal flap, papilla mesial de‐epithelialized, periosteal split in the vestibule. The distal papilla was left intact, but mobilized and slightly elevated by a tunnelling procedure. (g) Placement of a bioresorbable matrix barrier (Guidor™ MSL‐configuration, Sunstar Americas, Inc., Schaumburg, IL, USA) after application of a xenogeneic bone mineral into the furcation defect (Bio‐oss collagen™, Geistlich Biomaterials, Wollhusen, Switzerland) to facilitate guided tissue regeneration. (h) Coronally advanced minimally rotated flap secured with sling and interrupted sutures. (i) Clinical view one day after periodontal regenerative surgery. (j, k) Clinical view 2 weeks after surgery. (l) Clinical view 3 months after surgery. (m) 9 months, vertical and horizontal probing depths: 2 mm. (n) 9 months, radiographic fill of the furcation defect.
Summary of Evidence
●● Various regenerative approaches have ●● Complete furcation closure in degree II FI shown to be effective in the treatment of is not a predictable outcome degree II furcation involvement (FI) com- ●● Degree III FI cannot be improved predict- pared with access flap surgery. ably by regenerative therapy. Regenerative Therapy in Human Clinical Studies 153
References
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Chapter 8
Furcation Therapy: Resective Approach and Restorative Options Roberto Rotundo1 and Alberto Fonzar 2
1 Periodontology Unit, UCL Eastman Dental Institute, London, UK 2 Private practice, Udine, Italy
8.1 Anatomical Considerations (Huynh‐Ba G et al. 2009). From an anatomi- for Treatment Planning cal point of view, the poorer pro gnosis of furcation‐involved teeth may be due to the Furcation defects present the greatest chal- fact that the persistence of a defect within the lenges to the success of periodontal therapy, inter‐radicular space creates an anatomical as a reduced efficacy of periodontal therapy environment that interferes with professional and higher risk of tooth loss have been con- and domiciliary oral hygiene. Numerous sistently observed in multi‐rooted teeth with morphological factors may explain the aetiol- furcation involvement, regardless of the ogy, the more severe disease progression, and treatment modality employed. Regenerative the less favourable response to periodontal therapy might be considered the ideal treat- treatment of furcation‐involved molars (De ment for furcations. However, indications for Sanctis and Murphey 2000). These factors regenerative periodontal therapy (discussed (extensively covered in Chapter 1) are: in Chapter 7) are still very limited. Maxillary ●● Furcation access diameter. molars with degree II interproximal furca- ●● Root irregularities and roughness. tions, as well as all degree III furcation‐ ●● Anatomical complexity of the root complex. involved molars, are generally not suitable ●● Cervical enamel projections. for regenerative therapy. Therefore, diff erent ●● Enamel pearls. treatment strategies (such as resective) have ●● Accessory pulp canals. to be employed to eliminate or manage fur- cation defects. The survival of molars with furcation 8.2 Pre‐surgical Diagnosis involvement in longitudinal studies following different treatment procedures was discussed 8.2.1 Pre‐surgical Clinical Diagnosis in Chapter 5. It is interesting to notice how a systematic review observed that the most fre- An accurate and precise pre‐surgical diagno- quent complications occurring during the sis is essential in order to approach correctly follow‐up period were caries in the furcation patients affected by periodontal disease area after tunnelling procedures, and root complicated by the invasion of molar furca- fractures after root‐resective procedures tion areas. Before planning the definitive
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
treatment plan, clinicians should carefully fundamental to combine the clinical and radi- evaluate the following: ological data in order to perform an accurate diagnosis of multi‐rooted affected teeth. ●● Patient’s periodontal and caries risk profile. As discussed in Chapter 2, cone‐beam ●● Horizontal (Hamp et al. 1975) and vertical computed tomography (CBCT) may improve (Tarnow and Fletcher 1984) amount of per- diagnostic accuracy and optimize treatment iodontal tissue loss in the inter‐radicular planning in periodontal defects, particularly areas. in maxillary molars with furcation involve- ●● Anatomy and morphology of the root ment. However, the higher irradiation doses complex: the length of the root trunk, the and cost–benefit ratio should be carefully degree of separation, and the divergence analysed before using CBCT for periodontal between the roots, as well as their shape lesions (including tooth furcation; Walter and length. et al. 2016). The radiographic analysis should ●● Amount of residual attachment and prob- allow the clinician to evaluate the following: ing pocket depth (PPD) of each single root. ●● Access for oral hygiene procedures. ●● Horizontal and vertical amount of hard ●● Endodontic prognosis of each single root tissue loss in inter‐radicular areas. (endodontically treated teeth). ●● Length of root trunk. ●● Need for endodontic treatment (endodon- ●● Length, divergence, and shape of roots. tically untreated teeth). ●● Presence/absence of fusion between roots. ●● Need for restorative treatment and restor- ●● Amount of residual support. ative deficiencies (i.e. insufficient residual ●● Endodontic diagnosis and prognosis. healthy tooth structure). ●● Presence of post and core build‐up restoration. ●● Single tooth or multiple molars with furca- ●● Presence of caries in furcation‐involved tion involvement. molars. This information should be obtained by We should also remember that radiolucency carefully combining the data acquired from in the inter‐radicular area does not always both clinical and radiological analysis. indicate the presence of a furcation involve- ment. Trauma from occlusion (occlusal 8.2.2 Pre‐surgical Radiological interferences, bruxism, clenching) with the Diagnosis consequent increased tooth mobility may produce vascular changes along the whole It has been observed that clinical examination periodontal space, involving also the inter‐ alone detected furcation involvement in only radicular area, which leads to periodontal 3% of maxillary and 9% of mandibular molars. ligament space remodelling and bone demin- The combination of radiographic and clinical eralization (Svanberg and Lindhe 1973; examinations improved detection to 65% in Polson et al. 1976a, b). In such a case the maxillary molars, but only 23% in mandibular radiolucency is not confirmed by the clinical molars (Ross and Thompson 1978). Parallel examination (probing fails to detect an periapical and/or vertical bite‐wing radio- involvement of the furcation) and the defect graphs should always be taken after the clinical usually disappears some weeks following the examination in order to confirm the informa- elimination of the occlusal overload. tion obtained through the periodontal probing (Horwitz et al. 2004). It is important to know that the bone density (especially in mandibular 8.3 Treatment of Furcation molars) and the superimposition of the palatal Defects root (maxillary molars) could partially hide the root complex, and so make it difficult or The objectives of periodontal therapy in impossible to confirm the defect previously multi‐rooted teeth with furcation involve- detected by probing. Therefore, it appears ment are no different from the objective of Resective Approach and Restorative Options 163 single‐rooted teeth therapy: arresting disease ●● Strategic value of the tooth. progression and maintaining the teeth in ●● Root complex anatomy and morphology. health and function with proper aesthetics. ●● Periodontal condition of adjacent teeth. These goals can be met first by eliminating ●● Need for prosthetic rehabilitation. the microbial plaque from the surfaces of the ●● Need for endodontic treatment. root complex, and then by establishing an ●● Bone volume/quality. anatomy that facilitates proper self‐performed ●● Financial considerations for the patient. plaque removal. Treatment options for molars with furca- tion involvement could be divided into three 8.4 Resective Procedures and different modalities: Restorative Approaches ●● Conservative procedures: subgingival debridement, access‐flap surgeries, tunnel 8.4.1 Indications preparation. The main aim of these proce- Resective techniques have been developed dures is to remove the residual bacterial especially for deep class II and class III furca- infection and improve self‐performed tion‐involved molars to overcome these ana- plaque control. tomical limitations by physically removing ●● Regenerative procedures (already discussed both the dental (the roof of the involved fur- in Chapters 6 and 7): guided tissue regen- cation) and osseous (pocket elimination) eration, induced periodontal regeneration, structures that make up the defect. bone grafting. The goal of these proce- Several definitions for resective proce- dures is not only the removal of the resid- dures have been proposed by different ual infection, but also the elimination of authors and therefore there is no uniformity the furcation defect through reconstruc- in the terms used in the literature. According tion of the lost inter‐radicular periodontal to Carnevale et al. (1995), the terms are tissues. defined as follows: ●● Resective procedures: root separation, root resection, root amputation. The objective of these procedures is to eliminate the 8.4.1.1 Root Separation inter‐radicular lesion by completely remov- This indicates the sectioning of the multi‐ ing both the dental and osseous structures rooted tooth with the maintenance of all the that make up the defect. The tooth and roots (Figure 8.1). This procedure can be root complex morphology is deeply used for treating the following clinical changed by this therapeutic modality, in situations: order to open the furcation completely and ●● Deep class II and class III furcated molars. create an area conducive to performing ●● Root‐trunk fracture or decay. easier and better plaque removal. ●● Perforation of the middle of the furcation The choice of the appropriate treatment trunk. modality for a given clinical situation Root separation is usually indicated in the depends on a wide variety of factors that following clinical situations: should be carefully evaluated before initiat- ●● ing treatment: Mandibular molars for separating the mesial from the distal root (premolarization). ●● Degree of furcation involvement. ●● Maxillary molars for separating the mesial ●● Patient expectations. root from the undivided distal and palatal ●● Patient compliance. roots. ●● Patient susceptibility to periodontal disease. ●● Maxillary molars for dividing the palatal ●● Patient susceptibility to caries. root from the undivided mesial and distal ●● Amount of residual attachment. roots. The separation of the three roots of a 164 Chapter 8
(a) (b) (c)
(d) (e) (f)
Figure 8.1 Root separation (rizotomy: sectioning of the multi‐rooted tooth with the maintenance of all the roots) of a mandibular first molar affected by degree III furcation involvement (a–d), followed by an apical positioned flap (e) and final restoration (f), allowing self‐performed oral hygiene.
maxillary molar should be considered quite ●● Root or root trunk fracture or perforation. exceptional, because the presence of all the ●● Untreatable apical endodontic lesion roots would make the passage of plaque affecting one root. removal devices too difficult or impossible. ●● Severe root decay or resorption. ●● Severe recession or dehiscence affecting one root. 8.4.1.2 Root Resection This indicates the sectioning of the multi‐ When considering root resection for treating rooted tooth and the removal of one or two molars with furcation involvement, the clini- roots and the associated portion of the crown. cian has to choose between different Even if in the literature this term is often used alternatives. regardless of how the crown is treated, it is opportune to distinguish it from the term Mandibular Molars ‘root amputation’, which refers to the removal These have only one furcation and therefore of one root without removal of the overhang- there are just two possibilities (Figure 8.2): ing portion of the crown. Root amputation ●● Resection of the mesial root. can usually be indicated in the maxillary ●● Resection of the distal root. molars for removing the distal root, thus avoiding the need to restore the tooth with a Assuming that the two roots do not pre sent crown in a conservative treatment plan. significant differences in terms of periodontal, The root resection procedure can be used endodontic, and restorative prognosis, the fol- for treating the following clinical situations: lowing morphological characteristics should be considered before deciding which root has ●● Deep class II and class III furcated molars to be extracted (Majzooub and Kon 1992): with severe root proximity or a long root trunk. ●● The mesial root usually presents a greater ●● Severe bone loss affecting one or more root surface, but also quite often a deep roots of molars with and without furcation concavity, making it difficult first to prop- involvement. erly prepare and restore it, and for the Resective Approach and Restorative Options 165
Figure 8.2 Root resection (rizectomy) of the mesio‐buccal root of an upper maxillary molar, without separation of the other two roots, performed due to the severe loss of bone support caused by an endodontic‐ periodontal lesion. Degree III furcation involvement on the mesial and buccal furcations was present, with no distal furcation involvement. This procedure was carried out after appropriate endodontic therapy. Three months after the root resection, an apically positioned flap was performed and a provisional prosthetic crown was positioned. Three months later, a final metal‐ceramic crown was cemented, with a good long‐term (five years) clinical result (last image).
patient to keep clean with standard plaque‐ the distal root less prone to root fracture; control procedures. It is important to easier to treat endodontically, to prepare, stress the risk of producing a fenestration and to restore; and finally for the patient to in the distal surface of the root, during keep clean through self‐performed plaque both the tooth preparation and the endo- removal. dontic treatment/retreatment of the two Maxillary Molars narrow and superficial root canals. These have three furcations and therefore ●● The distal is a comparatively large root, several root resection possibilities (Figure 8.3): with usually one wide root canal and an oval convex cross‐section with a greater ●● Resection of the mesio‐buccal root with- bulk of dentine. These characteristics make out separating the other two roots. This 166 Chapter 8
Figure 8.3 Root separation of all three roots of a maxillary upper second molar and extraction (rizectomy) of the disto‐buccal root.
procedure can be performed in case of when the palatal root is affected by a deep involvement of the buccal and/or mesial infrabony defect or an endodontic or furcation (in such a case root separation is restorative untreatable problem. also possible), and when the mesio‐buccal When all three furcations of a maxillary root is affected by a deep infrabony defect molar are involved, following root separation or an untreatable endodontic or restorative one or two roots can be extracted. In such problem. After the mesio‐buccal root clinical situations, if two roots are maintain- removal, the residual root trunk shows a able (a careful evaluation of periodontal, flat or convex mesial surface that facilitates endodontic, and prosthetic prognosis is an both prosthetic procedures and self‐ essential prerequisite), the following options performed plaque control. are possible (Figure 8.4): ●● Resection of the disto‐buccal root without separating the other two roots. This proce- ●● Root separation of all three roots and dure can be performed in case of involve- extraction of the disto‐buccal one. The ment of the buccal and/or distal furcation, disto‐buccal root is statistically the most and when the disto‐buccal root is affected frequently extracted (Rosenberg 1978; by a deep infrabony defect or by an untreat- Ross and Thompson 1978), because it is able endodontic or restorative problem. usually the shortest with a long root trunk Following the extraction of the disto‐buccal and therefore has a smaller amount of bone root, the residual root trunk often exhibits support. The anatomy and morphology of a deep distal concavity, which should be the root trunk usually make access between flattened during tooth preparation in order the divided mesial and palatal roots easy to improve the quality of the prosthetic for the patient’s self‐performed oral restoration and the patient’s self‐performed hygiene. plaque removal. ●● Root separation of all three furcations and ●● Resection of the palatal root without sepa- extraction of the mesio‐buccal root. This rating the other two roots. This procedure option is less frequent than the previous can be performed in case of involvement of one, because often the disto‐buccal root is the mesial and/or distal furcation (in such too thin, and also because proper self‐ a case root separation is also possible), or performed plaque removal in the distal Resective Approach and Restorative Options 167
Figure 8.4 Root separation in a mandibular first molar affected by degree III furcation involvement associated with periodontal‐endodontic pathology on the distal root. Distal root resection (rizectomy) was carried out, maintaining the mesial root in situ. A prosthetic metal‐ceramic crown was carried out after the three‐month healing period.
furcation is nearly impossible if distally teeth were still present, 2 teeth were lost the neighbouring molar is present. because of periodontal complications, and 1 ●● Root separation of all three furcations and because of root perforation, meaning a extraction of the palatal root. This option survival rate of 85%. Hamp et al. (1975) is less frequent too because of the anatomy reported a survival rate of 100% after 5 years of the palatal root (large root surfaces and in 87 molars treated by means of root resec- an oval convex cross‐section with thick tion and/or separation. The authors attrib- dentine), but also because the thickness of uted their success to the elimination of the palatal bone makes this root particu- plaque‐retentive areas in the furcations, larly stable and firm. When the clinician meticulous patient oral hygiene, and regular has to choose between the mesial and the maintenance care. palatal root, they should consider that the Langer et al. (1981) reported a survival rate mesial root has a root surface area that is of 62% in a 10‐year retrospective evaluation equal to or even larger than the palatal one, of 100 molars (50 maxillary and 50 mandibu- but it presents two or even three narrow lar) treated with resection. The main causes root canals instead of the sole and wide of tooth loss were root fracture in 18 teeth canal of the palatal root. (47.4%), periodontal complications in 10 teeth (26.3%), endodontic failures in 7 teeth 8.4.2 Scientific Evidence (18.4%), and cement washouts leading to car- ies in 3 teeth (7.9%). It is interesting to point Ten studies (only one prospective) reporting out that the ratio of maxillary to mandibular the results of root resection with at least five‐ failures was approximately 2:1 and only year follow‐up were found in the literature 15.8% of the tooth loss occurred within the (see Table 8.1). The survival rates reported in first five years after surgery, whereas these studies range from about 60 to 100% the vast majority – that is, 55.3% of the after a mean observation period of 5–10 years. losses – occurred between the fifth and sev- Bergenholtz (1972) retrospectively enth years of function. The remaining losses reported the results of 45 teeth treated with took place between the eighth and tenth root resection up to 11 years before. Out of years of observation. Buhler (1988) presented the 20 teeth with a 5–10‐year follow‐up, 17 a 10‐year follow‐up of 28 root‐resected 100% 89.4% 92.9% 100% 62% 67.9% Group II 98.4% Group 5 years: 83% 10 years: 68% 5 years: 98.9% 10 years: 93.1% Survival 80% root fracture Not reported 47.4% root fracture 26.3% periodontal 18.4% endodontic 7.9% wash‐out/caries 33.3% endodontic 22.2% perio‐endo 22.2% periodontal 11.1% root fracture 111% wash‐out/canes 33.3% caries 33.3% root fracture 33.3% PPD > 5mm (group II) 81.3% periodontal 25% perio‐endo 28.1 endodontic 33.3% endodontic 25% root caries 25% periodontal 16.7 root fracture 66.6% periodontal 33.3% root perforation 85% Complications
Table 8.1 Clinical studies on the treatment of furcation‐involved molars with root separation/resection.
Number Author Year Study design of teeth Follow‐up (mean) Complications Survival
Bergenholtz 1972 Retrospective 45 5–10 years 66.6% periodontal 33.3% root perforation 85% Hamp et al. 1975 Retrospective 87 5 years 100% Langer et al. 1981 Retrospective 100 10 years 47.4% root fracture 26.3% periodontal 62% 18.4% endodontic 7.9% wash‐out/caries Buhler 1988 Retrospective 28 10 years 33.3% endodontic 22.2% perio‐endo 22.2% 67.9% periodontal 11.1% root fracture 111% Group II 185 teeth:7–11Group years wash‐out/canes Carnevale et al. 1991 Retrospective 488 Group I 303 teeth: 3–6 years 33.3% caries 33.3% root fracture 33.3% PPD Group II 98.4% Group II 185 teeth:7–11 years > 5mm (group II) Blomlof et al. 1997 Retrospective 78 5–10 years 81.3% periodontal 25% perio‐endo 28.1 5 years: 83% 10 endodontic years: 68% Carnevale et al. 1998 Prospective 175 10years 33.3% endodontic 25% root caries 25% 5 years: 98.9%
Number of teeth (mean) Follow‐up periodontal 16.7 root fracture 10 years: 93.1% Hou et al. 1999 Retrospective 52 6.7 (5–13 years) 100% Svardstrom &. 2000 Retrospective 47 9.5 (8–12 years) 80% root fracture 89.4% Wennstrom Dannewitz et al. 2006 Retrospective 19 ~9 (~5–12 years) Not reported 92.9%
PPD = probing pocket depth. 2000 Retrospective 47 9.5 (8–12 years) 1988 Retrospective 28 10 years Year design Study Clinical studies on the treatment of furcation‐involved molars with root separation/resection. molars with root of furcation‐involved Clinical studies on the treatment Svardstrom &. Svardstrom Wennstrom Dannewitz et al. 2006 Retrospective 19 ~9 (~5–12 years) Langer et al.Buhler 1981 RetrospectiveCarnevale et al. 100 1991 Retrospective 10 years 488 I 303 teeth: Group 3–6 years Blomlof et al.Carnevale et al. 1997 1998 Retrospective et al.Hou Prospective 78 175 1999 Retrospective 5–10 years 52 10years 6.7 (5–13 years) Author Bergenholtz et al.Hamp 1972 1975 Retrospective Retrospective 45 87 5–10 years 5 years Table 8.1
Chapter No.: 1 Title Name:
molars, mainly used as bridge abutments. observation period of about 9 years, 8 resected The calculated survival rate was 67.9% and teeth were lost, yielding a survival rate of the reasons for tooth loss were as follows: 57.9%. The complications – that is, the reason endodontic failures 33.3%, combined perio- for the tooth loss – were not reported. dontal and endodontic lesions 22.2%, perio- It is fitting to consider that a true com- dontal reasons 22.2%, root fracture 11.1%, parison among these studies is almost and loss of retention leading to secondary impossible: different pre‐therapeutic condi- caries 11.1%. Curiously similar to the find- tions of the involved molars, no uniformity ings of Langer and co‐workers, no tooth loss in the terminology used, different reasons could be observed during the first four years for performing these procedures (periodon- following therapy. tal? endodontic? root fracture? caries?), Carnevale et al. (1991) published a retro- different techniques used in each step of spective analysis of 488 molars after tooth both root separation and resections (endo- resection and/or separation and prosthetic dontic treatment, tooth build‐up, prepara- reconstruction. The follow‐up period was tion, provisional and definitive crown
Table 8.1 Clinical studies on the treatment of furcation‐involved molars with root separation/resection. 3–6 years for 303 teeth (62%) and 7–11 years morphology), different recall intervals, and for 175 teeth (38%). Considering only the smoking habits (Mullally and Linden 1996) Number Author Year Study design of teeth Follow‐up (mean) Complications Survival group with the longer follow‐up, 3 teeth were make drawing indisputable conclusions lost (1 for caries, 1 for root fracture, and 1 for about the efficacy of this therapeutic modal- Bergenholtz 1972 Retrospective 45 5–10 years 66.6% periodontal 33.3% root perforation 85% PPD > 5 mm), yielding a survival rate of 98.4%. ity an impossible task. In spite of that, it Hamp et al. 1975 Retrospective 87 5 years 100% Langer et al. 1981 Retrospective 100 10 years 47.4% root fracture 26.3% periodontal 62% In contrast to Langer et al. (1981) and Bühler must be pointed out that with the exception 18.4% endodontic 7.9% wash‐out/caries (1998), most failures occurred early (3–6‐year of three studies, the average survival rate of Buhler 1988 Retrospective 28 10 years 33.3% endodontic 22.2% perio‐endo 22.2% 67.9% periodontal 11.1% root fracture 111% group) rather than later (7–11‐year group). the molars treated with root separation/ wash‐out/canes The authors attributed the high success rate resection was very high (close to 90%) and Carnevale et al. 1991 Retrospective 488 Group I 303 teeth: 3–6 years 33.3% caries 33.3% root fracture 33.3% PPD Group II 98.4% Group II 185 teeth:7–11 years > 5mm (group II) to an optimal hygiene regimen and frequent comparable to that of implants inserted in Blomlof et al. 1997 Retrospective 78 5–10 years 81.3% periodontal 25% perio‐endo 28.1 5 years: 83% 10 maintenance recall. A more recent 10‐year the posterior areas of the mouth, and that endodontic years: 68% follow‐up prospective investigation by the reasons for tooth extraction were mainly Carnevale et al. 1998 Prospective 175 10years 33.3% endodontic 25% root caries 25% 5 years: 98.9% periodontal 16.7 root fracture 10 years: 93.1% Carnevale et al. (1998) reported the success related to endodontic complications and Hou et al. 1999 Retrospective 52 6.7 (5–13 years) 100% rate of root‐resective therapy in 175 molars root fractures, and not to periodontal Svardstrom &. 2000 Retrospective 47 9.5 (8–12 years) 80% root fracture 89.4% Wennstrom used as abutments for single‐unit crowns or disease recurrence. Dannewitz et al. 2006 Retrospective 19 ~9 (~5–12 years) Not reported 92.9% fixed dental prostheses to be 98.9% after PPD = probing pocket depth. 5 years and 93% at the end of the study. Only 12 of 175 teeth (7%) were extracted, 4 for 8.4.3 Contraindications endodontic reasons, 3 for root caries, 3 for Root‐separation/resection procedures pre sent periodontal reasons, and 2 for root fracture. some important anatomical and technical Hou et al. (1999) reported a survival rate of contraindications: 100% of 52 root‐separated molars in a case series including 25 patients followed up for a ●● Poor compliance with oral hygiene. mean observation period of 6.7 years (range ●● Patients with high caries susceptibility. 5–13 years). Svardström and Wennström ●● Patients with severe parafunctional habits. (2000) reported a survival rate of 89.4% of 47 ●● Inadequate residual attachment on the molars 8–12 years following root‐resective remaining roots. procedures (mean observation period ●● Serious discrepancies in adjacent inter- 9.5 years). Five teeth (10.6%) had to be proximal bone level. extracted during the follow‐up period and ●● Unfavourable anatomical factors (long root root fracture was the main reason for extrac- trunk, short divergence between roots, tion (80.0%). Dannewitz et al. (2006) per- fused roots, presence of inter‐radicular formed 19 root resections while treating 305 septa). furcation‐involved molars. Following a mean ●● Retained roots endodontically untreatable. 170 Chapter 8
●● Excessive endodontic instrumentation of contraindications for a root‐separation/resec- retained roots. tion procedure. Particular caution should be ●● Severe root decay/resorption. used when the multi‐rooted teeth are intact, because this is an invasive procedure involving We should also bear in mind that these are a considerable biological cost that must always sensitive techniques that require a careful be carefully evaluated. interdisciplinary approach, a widespread knowledge of prosthodontics, endodontics, and periodontology, and an accurate evalua- 8.4.4.3 Endodontic Treatment tion of the cost–benefit ratio with respect to Since root and/or build‐up fractures have the treatment alternatives. The need for often been reported as one of the most endodontic treatment, prosthetic rehabilita- frequent reasons for the failure of a root‐ tion, and periodontal surgery actually makes separation/resection procedure, correct this therapeutic modality a demanding treat- endodontic treatments must preserve as ment, in terms of both economic cost and much tooth structure as possible at both cor- biological tissue loss. onal (access opening should be kept as small as possible) and radicular levels (conserva- 8.4.4 Step‐by‐step Procedure tive instrumentation). Excessive instrumen- tation of radicular canals and/or immoderate Considering that root separation/resection is pressure during gutta‐percha condensation an interdisciplinary procedure and that most should be avoided. of the failures reported in the literature are Although a vital root resection is possible basically generated by reasons other than without any initial post‐surgical discomfort new periodontal breakdown, first careful for the patient (Smukler and Tagger 1976), patient selection and then precise sequenc- when the tooth to be treated is vital or the ing and correct execution of each phase of root filling is suboptimal, endodontic treat- the therapeutic protocol are crucial to the ment/retreatment should be always the first long‐term success of the procedure. The sug- procedure performed. The reasons for a gested therapeutic sequence is as follows. preliminary root canal treatment are:
●● 8.4.4.1 Patient Selection Easier rubber dam isolation and easier access for the endodontist. This is the first, fundamental step of the ●● Evaluation of tooth/root endodontic sequence, because not all patients are equally prognosis before separation/resection suitable for root separation/resection. Poor procedure. patient compliance, high caries susceptibil- ●● Crown build‐up before separation/resec- ity, and limited financial resources are the tion procedure. most frequent factors limiting the use of this procedure. Treatment options must be If from a clinical and radiological point of presented to the patient and the potential view it is not possible to identify the root(s) problems should be discussed. Root separa- to be resected with certainty, each root has to tion/resection should be considered as part be endodontically treated/retreated. In order of an overall treatment plan aiming at to avoid useless treatments and costs, when complete periodontal, functional, and the clinical periodontal evaluation of the aesthetic rehabilitation. tooth is deeply doubtful, endodontic treat- ment can be exceptionally postponed until 8.4.4.2 Tooth Selection after the root separation/resection. In these As already mentioned, long root trunk, short cases, root canal treatment should be per- divergences between the roots, fused roots, formed within two weeks (Smukler and and presence of inter‐radicular septa represent Tagger 1976). Resective Approach and Restorative Options 171
8.4.4.4 Crown Build‐up ●● Possibility of reducing tooth mobility After completion of the endodontic therapy, before surgery by splinting the roots with the crown of the molar, the pulp chamber, the provisional restoration. and almost 2–3 mm of the canals apical to ●● If the root trunk is short and infrabony the furcation entrance are prepared, etched, defects are not present, periodontal sur- and filled with light or chemically cured gery can often be avoided. composite by using a dentine adhesive to Root separation or resection can otherwise improve the retention of the material. This be performed following the same technique step is of the outmost importance, because during the periodontal surgical phase, if the replacement of the missing coronal and there is a diagnostic problem or difficult radicular tooth structure should provide to access (Carnevale et al. 1990). the abutments a complete marginal seal and Before starting with tooth preparation/ proper retention and resistance for the sub- resection, it is of the utmost importance to sequent full‐coverage restoration. carefully probe each root and especially the 8.4.4.5 Root separation/resection During furcation area in order to identify three‐ Preliminary Prosthetic Preparation dimensionally the position of furcation entrances, the anatomy of the root trunk, and Root separation/resection may be per- the potential presence of infrabony defects formed as part of the initial tooth prepara- affecting one or more roots (Zappa et al. tion for the prosthetic rehabilitation 1993). Considering the reduced diameter (‘prosthetic preparation’), when a prefabri- and thickness of the roots, the preparation cated shell provisional restoration is relined must be as conservative as possible. For this and temporarily cemented. Performing root reason, tooth structure saving a knife‐edge separation/resection prior to and not dur- finishing line should be preferred. Usually ing periodontal surgery (Carnevale et al. local anaesthesia is not necessary during the 1981, 1997) presents several important root‐separation phase and therefore should clinical advantages: not be used, because the patient’s feeling of ●● Accurate evaluation of the periodontal pain can help the clinician to avoid moving condition of the molar and thus the possi- the bur too deeply in the tissue and therefore bility to change the treatment plan at an reducing the risk of damaging the preserved early stage. In molars with furcation inter‐radicular attachment. involvement, it is often impossible to pre- In order to get access to the subgingival cisely assess the inter‐radicular attachment root surfaces with the precise root axis and loss before root separation, and therefore to limit soft‐tissue damage, a small‐diameter no conclusive clinical decision about the flame‐shape diamond bur can be used, and prognosis of the tooth can be made prior the buccal and lingual enamel prominence to this procedure. should be eliminated first. The access to each ●● Earlier elimination/reduction of the inter‐ involved furcation (buccal and lingual in radicular periodontal infection and earlier mandibular molars; buccal, mesial, and distal extraction of hopeless roots. This can in the maxillary) should be initially ‘marked’ enhance the healing of the infrabony with vertical grooves that can be used as ref- lesions that might be present in the inter‐ erence points during the root‐separation/ radicular area at the extraction site, and resection procedure. In every passage the therefore generate an osseous morphology flame‐shape diamond bur has to be moved more favourable for being corrected at the first forwards into the furcation and then time of resective bone surgery. backwards, working in both interproximal ●● Creating access for plaque removal in an line angles of each root in order to widen the otherwise inaccessible area. space previously created between the roots. 172 Chapter 8
Once the furcation has been separated, the specific commercially available reinforcing whole roof of the involved furcation must be fibres or, in the case of long‐span bridges or eliminated and an adequate space for plaque‐ in patients with parafunctional habits, removal devices should be created between replaced after an impression with a custom‐ the roots. made metal‐reinforced temporary restoration. It is important to remember that the distal aspect of the molar mesial root (especially 8.4.4.7 Periodontal Surgery the mandibular one) often presents a deep The objectives of this phase of the root‐sepa- concavity. In order to avoid weakening the ration/resection procedure are the following: mesial root or creating a root fenestration, ●● To eliminate possible angular bone defects the desired distance within the distal root around the maintained roots and recreate should be created by preparing the mesial a positive bone architecture in order to aspect of the distal root rather than the distal obtain an environment favourable to good of the mesial one. The mesial and distal sur- hygiene and easy dental care. Bone resec- faces of mesial and distal mandibular roots tion may also be performed to reduce the and the buccal and palatal surface of respec- bucco‐lingual dimension of the alveolar tively mesio‐buccal and palatal roots must be process in the extraction sites. Soft‐ and parallel to each other (if both the roots are hard‐tissue management and post‐surgical maintained) and to the neighbouring abut- care are the same as used for pocket elimi- ments to ensure a proper insertion axis of the nation with resective osseous surgery. prosthetic rehabilitation, while the inter- ●● To facilitate both soft adaptation and dom- proximal surfaces can be divergent in order iciliary plaque removal by modifying the to widen the space between the roots. root contour through intrasurgical prepa- In order to be sure that the whole roof of the ration of prosthetic abutments. involved furcation has been eliminated, a curved periodontal probe (Nabers probe) Following flap elevation, the maintained should be moved in the apico‐coronal direction roots and the other non‐vital abutments are to detect the potential presence of furcation newly prepared with the purpose of remov- lips or ledges. With the aim of facilitating provi- ing the residual plaque and calculus, improving sional relining and domiciliary plaque removal the space between the roots, eliminating any in the exposed root surfaces, at the end of tooth residual undercuts, and reducing the natural preparation/resection, the root surfaces should anatomical concavities present on the root be made smooth and even by using fine and surfaces. As proposed by Di Febo (1985), extra‐fine diamond burs, and the line angles of concavities can be reduced by preparing a the abutment should be rounded. chamfer on only the portions of the roots that are convex, without touching the con- 8.4.4.6 Provisional Restoration cave portions, which thereby present a knife‐ At the end of tooth separation/resection, a edge finishing line (‘combined preparation’). prefabricated shell provisional restoration is The intra‐operative preparation does not relined and temporarily cemented. In order always extend to the alveolar crest. On the not to disturb both soft and hard interproxi- contrary, the operator should prepare the mal tissue healing, it is important to shorten tooth to the level of connective tissue attach- at about the gingival level and to precisely ment and avoid, wherever possible, injuring refine the margins of the relined provisional intact fibres and removing healthy cemen- restoration. The excess of temporary cement tum. Following intra‐surgical abutment must be carefully removed and the preparation and before suturing, the tempo- patient should be taught to clean the new rary restoration must be relined with a interproximal spaces properly with appro- self‐curing acrylic resin and the margins priate plaque‐removal devices. The provi- trimmed 3 mm short of the alveolar crest so sional restoration can be strengthened with as not to disturb the healing process. Resective Approach and Restorative Options 173
Throughout the tissue maturation period, oral hygiene as much as possible, and the patients are maintained on a plaque‐control patient should be taught to use self‐per- programme that includes professional tooth formed plaque‐removal devices correctly. At cleaning and oral hygiene instruction once a the completion of therapy, patients are then month. In order to reduce the risk of cement enrolled in a personalized maintenance recall washout during these recall appointments, programme that generally includes three‐ the provisional restoration should be monthly appointments. removed and re‐cemented and, where neces- sary, new interdental plaque‐removal devices are recommended (Walter et al. 2011). 8.5 Conclusions
8.4.4.8 Final Prosthesis The long‐term prognosis of teeth with Once the healing period is complete and furcation involvement treated with conven- before the impression for the definitive tional therapy demonstrates a higher fre- prosthesis, the endodontic, periodontal, and quency of tooth loss than non‐furcated provisional prosthetic treatments have to be molars. The reduced success rate may be due clinically and radiographically re‐evaluated. to the fact that the persistence of a defect If the treatments could achieve successful within the inter‐radicular space creates an outcomes, the abutments can be refined and anatomical environment that interferes with polished and the final impression can be oral hygiene efforts. In fact, partial gain of taken, with or without extra‐thin retraction clinical attachment levels within the defect, cords. The design and construction of the although statistically or clinically significant, metal framework in combination with a good may not effectively improve the outcome dur- crown fitting and sitting play a fundamental ing the maintenance phase of therapy. It is role in the long‐term success of fixed bridges important to point out that comparative stud- using root‐separated or root‐resected abut- ies between the different procedures are lack- ments (Carnevale et al. 1991; Newell 1991). ing, and therefore in treatment decisions for The strength and stability of the metal frame- furcation‐involved molars there is no scien- work should compensate for the structural tific evidence that a given treatment modality weakness of the abutments, and for the high is superior to the others. Patient‐related fac- tooth mobility often present in severely tors such age and health conditions, compli- involved periodontal cases (Wang et al. ance, susceptibility to caries, strategic value of 1994). For the same mechanical reasons, the tooth in relation to the overall treatment occlusion should be designed and set to min- plan, functional and aesthetic demands, and, imize occlusal lateral forces. Interproximal last but not least, financial resources should spaces should be created in order to facilitate guide clinicians in their choice of treatment.
Summary of Evidence
An accurate and precise diagnosis is essen- ●● Endodontic treatment and tooth tial in order to correctly approach affected restoration. molar furcation areas. In particular, clini- ●● Root separation/resection. cians must initially evaluate all the patient‐ ●● Provisional restoration. and tooth/site‐related factors that are able ●● Periodontal surgery. to determine indications and contraindica- ●● Final prosthesis. tions for the treatment of the defects. Afterwards, this step‐by‐step approach should be followed: 174 Chapter 8
References
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Newell, D.H. (1991). The role of the dog: A methodological study. Odontologisk prosthodontist in restoring root‐resected Revy 24, 269–282. molars: A study of 70 molar root Svardstrom, G., and Wennstrom, J.L. (2000). resections. Journal of Prosthetic Dentistry Periodontal treatment decisions for molars: 65, 7–15. An analysis of influencing factors and Polson, A.M., Meitner, S.W., and Zander, H.A. long‐term outcome. Journal of (1976a). Trauma and progression of Periodontology 71, 579–585. marginal periodontitis in squirrel monkeys. Tarnow, D., and Fletcher, P. (1984). IV Reversibility of bone loss due to trauma Classification of the vertical component of alone and trauma superimposed upon furcation involvement. Journal of periodontitis. Journal of Periodontal Periodontology 55, 283–284. Research 11, 290–298. Walter. C., Schmidt, J.C., Dula, K., and Polson, A.M., Meitner, S.W., and Zander, H.A. Sculean, A. (2016). Cone beam computed (1976b). Trauma and progression of tomography (CBCT) for diagnosis and marginal periodontitis in squirrel monkeys. treatment planning in periodontology: III Adaption of interproximal alveolar bone A systematic review. Quintessence to repetitive injury. Journal of Periodontal International 47, 25–37. Research 11, 279–289. Walter, C., Weiger, R., and Zitzmann, N.U. Rosenberg, M.M. (1978). Management of (2011). Periodontal surgery in furcation‐ osseous defects. In: Clinical Dentistry, vol. 3 involved maxillary molars revisited: An (ed. J.W. Clark), 103. Philadelphia, PA: introduction of guidelines for Harper & Row. comprehensive treatment. Clinical Oral Ross, I.F., and Thompson, R.H., Jr (1978). A Investigations 15, 9–20. long term study of root retention in the Wang, H.L., Burgett, F.G., Shyr, Y., and treatment of maxillary molars with furcation Ramfjord, S. (1994). The influence of molar involvement. Journal of Periodontology 49, furcation involvement and mobility on 238–244. future clinical periodontal attachment loss. Smukler, H., and Tagger, M. (1976). Vital root Journal of Periodontology 65, 25–29. amputation: A clinical and histologic study. Zappa, U., Grosso, L., Simona, C. et al. (1993). Journal of Periodontology 47, 324–330. Clinical furcation diagnosis and Svanberg, G., and Lindhe, J. (1973). interradicular bone defects. Journal of Experimental tooth hypermobility in the Periodontology 64, 219–227. 177
Chapter 9
Furcation Tunnelling Stefan G. Rüdiger
Department of Periodontology, Public Dental Service/Malmö University, Malmö, Sweden
9.1 Introduction advanced inter‐radicular bone loss (furcation involvement of at least deep grade II or grade Furcation involvement has been shown to be III ‘through and through’; Hamp et al. 1975) associated with tooth loss during supportive when accessibility to the furcation area for periodontal therapy (Graetz et al. 2015; plaque removal is difficult. This is particu- Dannewitz et al. 2016; see also Chapter 5). larly the case if a deep lingual (at lower Characterized by ridges and concavities molars) or mesio‐palatal (at upper molars) (Svärdström and Wennström 1988), the furca- furcation involvement is present. If there is tion area is – for patients and dental profes- no bone loss at the lingual furcation (at lower sionals alike – particularly difficult to clean. molars) or the mesio‐buccal furcation High plaque and consequently high bleeding entrance (at upper molars), and at the same scores are generally associated with break- time a buccal furcation involvement grade II down of periodontal tissues during mainte- not exceeding half the buccal‐lingual width nance (Lang et al. 1990; Eickholz et al. 2008). of the molar, there might be a possibility of Creating an inter‐radicular space accessible the patient accessing the furcation entrance for brushing between the roots at deeply with an interdental brush and thus create involved furcation sites – a procedure referred healthy conditions. The converse condition – to as ‘furcation tunnelling’ – will allow for reg- that is, no bone loss at the buccal furcation ular plaque removal from the furcation area entrance and a lingual involvement grade (Figure 9.1), thus reducing the bacterial chal- II – would speak in favour of a tunnel proce- lenge to the periodontal tissues and possibly dure to ensure lingual healing, as cleaning of the risk of disease recurrence at these sites. In a lingual furcation entrance is difficult to this chapter, case selection, treatment proce- manage for the patient. dure, and the scientific background of the A prerequisite for the tunnelling procedure long‐term prognosis of molars undergoing is sufficient residual bone support at all roots. tunnel preparation will be discussed. As a rule of thumb, the alveolar bone support should be of equal amounts at all roots, and at least cover one‐third of the root length. 9.2 Indication Bone loss should mainly be horizontal. Otherwise, root resection may be considered The furcation tunnelling procedure should instead (see Chapter 8). be considered at stable (no more than mobil- The accessibility of the buccal furcation ity grade I) furcation‐involved molars with entrance should already at an early stage be
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
(a) (b)
(c)
Figure 9.1 Example of a well‐functioning tunnel at a maintenance visit. The tunnel has been in function for seven years. Healthy periodontal tissues are noted around the two roots from the buccal (a) and lingual (b) aspects. On the intraoral radiograph (c), the inter‐radicular alveolar bone is dense, which can be taken as a sign of stable conditions.
judged clinically and radiographically. The Assessing the upper molars is more length of the root trunk and the diameter of difficult, as the palatal root is often superim- the furcation entrance are variables to con- posed on the furcation area on radiographs. sider. Reasonably, the length of the root An eccentrically taken (especially distal trunk should not exceed 4 mm and the diam- eccentric) radiograph might help to project eter of the furcation entrance should be at the furcation area in a mesio‐buccal direc- least 0.5 mm. Otherwise, it will be difficult tion. In comparison to lower molars, upper for the patient to find the furcation entrance molars more often have a longer root trunk and insert the interdental brush into the fur- and a narrower divergence angle between cation. Considering anatomical measure- the two buccal roots. A further anatomical ments, first mandibular molars would be the complication in the upper jaw is the fact that most suitable candidates for the tunnelling three roots create three furcation entrances. procedure, considering root trunk dimen- If an interdental brush is inserted into the sions and the divergence angle of the roots buccal furcation entrance, the tooth anat- (Chiu et al. 1991; Hou and Tsai 1997; omy would usually guide the brush to the Paolantonio et al. 1998; Kerns et al. 1999). In mesio‐palatal furcation entrance (Figure 9.2). addition, the angle of the furcation area itself Thus the distal furcation entrance, which is should be looked at. A narrow furcation roof usually located in the middle of the distal would impede brushing. approximal surface, would not be cleaned Furcation Tunnelling 179
Graetz et al. 2015; Dannewitz et al. 2016) in periodontitis patients underwent this treatment. Though deep grade II furcation involvements are often given as an indica- tion for the tunnelling procedure in text- books, in an actual retrospective cohort of maintenance patients in a specialist unit, the tunnelling procedure was considered only for molars with initial furcation involvement grade III (Dannewitz et al. 2016).
Figure 9.2 Root anatomy guides the interdental brush from the buccal to the mesio‐palatal furcation entrance. When an interdental brush is inserted into 9.3 Patient Selection the buccal furcation entrance, root anatomy will usually lead the brush to the mesial furcation Before introducing the tunnelling procedure entrance. as a possible treatment option, the patient’s ability and attitude to brushing between roots should be assessed. If a surgical tunnel (see Section 9.6). Provided that proper case preparation has been performed and the selection is carried out, the decision on tun- patient is not able or willing to brush it, the nelling procedure can be taken intraopera- purpose of the treatment will be defied and tively. This bears the advantage of a more compliance could be further affected. Further accurate furcation measurement, as calculus on, it is advisable not to introduce inter‐ and in particular granulation tissue can radicular cleaning as the first oral hygiene obstruct the path for the furcation probe, instruction procedure, but instead to con- thus underestimating the degree of furcation centrate on getting to know the patient by involvement. their ability at ordinary interdental brushing. Another factor to consider when planning As soon as the standard of oral hygiene is for a tunnelling procedure is if prosthetic acceptable, brushing of a furcation entrance treatment will be necessary in the area. A can be introduced as a preparatory step to a tunnelling procedure might help avoid pros- furcation preparation. thetic treatment and thereby preserve an intact dental arch. If prosthetic treatment is inevitable, the prognosis of a furcation‐tun- nelled molar should be weighed thoroughly 9.4 The Tunnelling Procedure: against the prognosis of the entire prosthetic Surgical Steps construction, considering a possible loss of the furcation‐tunnelled tooth. It can be If an interdental brush can be inserted easily noted that in one study 33 out of 156 tun- into the buccal furcation entrance and with nelled teeth were given a prognosis suffi- only minor resistance pass through the entire cient to serve as an abutment for fixed furcation area, it may be worth trying to create bridges (Helldén et al. 1989). Given the fact the furcation non‐surgically. This can be an that specific anatomical prerequisites and advisable strategy if otherwise there is no indi- the patient’s full cooperation are required cation for periodontal surgery. If the gingiva for a successful tunnelling procedure, this over the lingual furcation entrance obstructs type of treatment is performed only occa- the interdental brush from passing through an sionally. In follow‐up studies of periodontal otherwise entirely accessible through‐and‐ patients in specialist surroundings, 1–5% of through furcation, lingual gingivectomy may molars (Hamp et al. 1975; Kuhrau et al. 1990; be performed (Figure 9.3). 180 Chapter 9
to ensure accessibility for the interdental brush, a round bur or Waerhaug diamond can be used. The bur should preferably first be inserted from the furcation entrance that is more involved. As soon as the operator has an idea of the direction, further osteoplasty is performed stepwise from both furcation entrances. The furcation entrances should be free of any bone ridges, which have to be removed, thus ensuring full accessibility to the furcation (Figure 9.5). Figure 9.3 Tunnel preparation by gingivectomy. The ideal distance from the fornix to the If the interdental brush – coming from the buccal bone crest to allow for interfurcation clean- furcation entrance – cannot pass a through‐and‐ through furcation involvement at the lingual aspect ing should be around 5–6 mm, which is the due to soft‐tissue obstruction, gingivectomy at the diameter of a size 7 interdental brush (3 mm) lingual aspect will create accessibility through the plus 2–3 mm needed for the dento‐gingival whole furcation. junction, and to allow for possible rebound of gingival tissues inside the furcation. However, no specific studies have investigated this In most cases, periodontal flap surgery aspect. The advantage of the Waerhaug dia- should be performed to ensure good post‐ mond is that its torpedo‐like form allows the operative access through the whole furca- bur to find its way through the furcation, tion area. After local anaesthesia and whereas such tactility is not achieved with a elevation of a full‐thickness flap, granulation round bur. Oscillating techniques (e.g. piezo- tissue is removed to judge the bone level in electric instruments) can also be applied for the furcation involvement. Before flap gentle ostectomy/osteoplasty, particularly design, careful attention should be paid to in the inner furcation area. After scaling the amount of buccal ketarinized gingiva and root planing, the flaps are reposi- present. In cases of large amounts of kerati- tioned by sutures, ensuring bone coverage. nized gingiva, a scalloped incision can be Interproximal single interrupted or vertical performed by the furcation entrance, fol- mattress sutures may be used. Sutures lowed by the removal of the secondary flap anchoring the flap to the periosteum need to after intrasulcular incisions, to expose the be performed in case of an apically reposi- furcation area. Otherwise, in cases with a tioned flap. At lower molars, a suture can be limited amount of keratinized gingiva, intra- placed through the furcation. In the upper sulcular incisions with no paramarginal jaw, root anatomy makes the furcation more incisions are preferred, in order to preserve difficult to access for interdental cleaning, the keratinized tissues and facilitate tissue and exposure of the furcation entrances by handling. In this case, a full split‐thickness trimming the periodontal flap can be advisa- flap can be executed, if possible associated ble (Figure 9.6). Periodontal dressing can be with lateral buccal relieving incisions, to applied to avoid granulation tissue growing then apically reposition the flap by peri- in the furcation area. Thus, the furcation tun- osteal suturing (Friedman 1962) to expose nel will be void of granulation tissue and the furcation area. These two different already accessible to an interdental brush at options are illustrated in Figure 9.4. suture removal. It is important to remember A straight periodontal probe, or alterna- that the periodontal dressing should only be tively a sterile interdental brush (e.g. size yel- placed into the furcation entrance and not low 0.7; TePe, Malmö, Sweden) can be used through the whole furcation area, as it can be to test accessibility. If bone must be removed painful for the patient when the dressing is (a) (b)
(c) (d)
Figure 9.4 Different approaches for tunnelling surgery needed according to the amount of keratinized gingiva (KG). In a case of an adequate amount of KG (a), scalloped incisions can be performed to expose the furcation area for self‐performed cleaning (b). In a case of a reduced amount of KG (c), an apically repositioned flap is performed in order to preserve the KG while still exposing the furcation area for self‐performed cleaning (d).
(a) (b)
(c) (d)
Figure 9.5 Osteoplasty during tunnel operation and suturing through the furcation. A furcation entrance can be obstructed by soft tissue (a) and bone ridges (b). A positive bone architecture has to be created by intrasurgical osteoplasty (see arrows) to secure easy insertion of the interdental brush through the furcation. Good soft‐tissue adaptation can be achieved in the furcation entrances by placing a suture through the furcation (c), ensuring good healing (d).
Chapter No.: 1 Title Name:
(a) (b)
Figure 9.6 At upper molars, root anatomy does often not form a straight pathway from the buccal to the mesial furcation entrance (in contrast to the furcation at lower molars). In such a case, it is more advisable to open the furcation by trimming the flaps, to leave the furcation entrances to heal openly (a), and not to place sutures, which after healing ensures good accessibility for the patient (b).
removed from the inner part of the furcation. may not be epithelial coverage of the intraop- In such cases, brushing in the furcation might eratively exposed bone, which will be the even not be possible at suture removal due to cause of tenderness on touching. The focus tenderness in the inner part of the furcation. for the first post‐operative oral hygiene To a greater extent than ordinary flap sur- instruction should be on the correct horizon- gery, periodontal surgery for tunnel prepara- tal insertion of the interdental brush into the tion involves a certain ambivalence between furcation entrance. The direct instruction to leaving the surgical area to heal by secondary the patient should be to ‘insert the brush as intention and the general intention of perio- far as possible’. Ideally, the patient should be dontists to achieve primary healing (which seen for post‐operative follow‐up four and means that areas, such as the furcation eight weeks after surgery. At four weeks, it entrance, that it is crucial to clean at an early should be tested whether the brush can be stage should be covered by tissue). Post‐opera- inserted over the middle of the furcation area, tive follow‐up of the latter needs to concentrate possibly to the lingual furcation entrance. An on training the patient to find the furcation interdental brush should preferably be used in entrance, whereas in the case of secondary its original straight shape, but if necessary it healing the patient has to be encouraged to can be bent to prevent the brush getting stuck dare to brush the furcation area despite post‐ in the lingual gingival tissues, which tend to operative tenderness. This dilemma can only grow in a coronal direction during the healing be solved for each patient individually. As process. The patient should be instructed to already pointed out, the patient’s attitude feel the tip of the brush on the inside to ensure towards oral hygiene has to be known to the that it has been inserted the whole way therapist before the treatment decision for a through (Figure 9.7). If tissue regrowth is too tunnelling procedure should be taken. extensive, an additional gingivectomy can be advisable. Good oral hygiene can be revealed anatomically by good adaptation of the gin- 9.5 Postoperative Follow‐Up and giva in the furcation entrances (Figure 9.8). Oral Hygiene in the Furcation From a psychological point of view, it is important that all personnel involved should At suture removal 7–10 days after the surgery, truly believe in the concept of the tunnelling the tissues in the furcation area are often still procedure. Otherwise, the patient will not too tender to allow for through‐and‐through learn to brush the furcation tunnel. Especially brushing. At this time point in healing, there for a referral clinic, this aspect is important, as Furcation Tunnelling 183
brush the furcation tunnel, 80% used an interdental brush, and 27% an interspace brush in addition to a common toothbrush (see also Chapter 13).
9.6 Types of Teeth
For lower molars, the brushing procedure is straightforward. There is one way in and one way out, and usually the interdental brush can Figure 9.7 Meticulous oral hygiene instruction. It is easily be inserted through the whole furcation. necessary to thoroughly explain to the patient the The trifurcation of upper molars makes mat- technique of brushing a furcation tunnel. One crucial piece of information is to point out that the ters more complicated. In most cases, the root interdental brush has to be inserted through the anatomy guides an interdental brush from the whole furcation tunnel. The patient should feel the buccal furcation entrance to the mesial furca- tip of the brush with the tongue. tion entrance, which is in most cases located in the mesio‐palatal line angle. Often the path- way through the furcation does not allow a straight brush to be inserted. Thus, the patient must be instructed to bend the brush to get it through the whole furcation. Alternatively, the patient can be instructed to insert the brush from the lingual aspect. The distal furcation entrance of upper molars is located in the middle of the approx- imal space. The distal furcation entrance is not accessible for brushing as long as the neighbouring distal tooth is in place. It can Figure 9.8 Gingival topography reveals the patient’s be argued that ordinary interdental brushing capability to brush the tunnel. Excellent oral hygiene would result in some cleaning of the furca- after furcation tunnelling is often revealed by the tion entrance, since the bristles would open inter‐radicular gingiva showing the path of the as the interdental brush is moved through interdental brush through the tunnel furcation. Good the interdental space. This might be an expla- adaption of the gingiva to the root surface is seen. nation for why upper molars with a function- ing tunnel from the buccal to the mesial keeping patients with a furcation tunnel for a furcation entrance can be kept over a pro- prolonged maintenance phase can be consid- longed period of time, despite the fact that ered to ensure a good long‐time prognosis. the distal furcation entrance might not In some cases it may be necessary to always be accessible for direct brushing. instruct the patient to brush the furcation When the neighbouring posterior tooth is from the palatal or lingual aspect to get the missing and the patient’s dexterity is well best brushing result. This technique requires developed, a functioning double tunnel may extensive training exercises with the patient. be created (Figure 9.9). Double tunnels are In one study, patients were asked about not often mentioned in the literature. Helldén their experience and brushing habits as far as et al. (1989) reported double tunnels per- the furcation tunnel was concerned (Helldén formed on 33 maxillary molars; however, et al. 1989). The majority (92%) did not expe- they did not specify the treatment outcome rience discomfort in relation to the furcation for this type of tunnelling. Two contralateral tunnel; 70% of patients said it was easy to double tunnels had in a case report been 184 Chapter 9
(a) (b)
Figure 9.9 In rare cases, double tunnels can be created. In this case, the distal furcation entrance was reached through the buccal entrance (a). The patient had learned to access both the mesial and the distal entrance through the buccal entrance (b).
proven to remain in stable condition over a for brushing (Joseph et al. 1996; see period of two years of maintenance therapy also Chapter 1). Thus, the position of the (Rüdiger 2001). maxillary first premolar in the dental arch Furcation tunnels in second molars are and its root anatomy do not favour the pos- more difficult to reach for the patient in both sibility of using furcation tunnel proce- the upper and lower jaws. Firstly, traction of dures in first upper premolars. During the corner of the mouth in combination with 15 years of clinical work at a referral clinic the more posterior positioning of second for periodontology, the author has only molars impedes correct positioning of the once come across the opportunity to intro- interdental brush into the furcation entrance. duce the brushing procedure in a through‐ Secondly, the diverging angle of the roots and‐through furcation involvement in an (buccal roots for the upper jaw) of second is upper first premolar. The second premolar smaller than that of first molars, and the root was missing and the first premolar was trunk is usually longer of second than of third rotated to such a degree that the insertion molars (Kerns et al. 1999). of an interdental brush through the furca- In the literature, one case of a furcation tion was possible. The bone loss had tunnel of a first upper premolar is men- reached the apical third of the roots tioned. However, no details were given on (Figure 9.10). Initially an improvement was how this furcation tunnelling worked in noted, but when the patient came back for terms of oral hygiene, and if this tunnelled a three‐month follow‐up, the bone loss to premolar was among the tunnelled teeth the apices was noted and the tooth had to that had to be extracted (Hamp et al. 1975). be extracted. As both furcation entrances of first upper premolars are situated in the approximal spaces, the furcation entrances are difficult 9.7 Pulp Reaction to reach if the tooth is not rotated and no neighbouring teeth are missing. Further The tunnelling procedure exposes consider- on, the majority of maxillary first premo- able root surface areas. A pulp reaction lars (63%) have fused roots, and of those might be expected, as accessory root canals having furcated roots only 10% had are frequently found in the furcation area of the bifurcation in the cervical third of the multi‐rooted teeth (Lowman et al. 1973; root lengths; that is, possibly accessible Vertucci and Williams 1974; Niemann et al. Furcation Tunnelling 185
caries in the furcation ranges from 4.4 to 57.1% (see Table 9.1). Considering that root caries after periodontal treatment in general has been reported to occur with a preva- lence of 82–90% after 10 years of mainte- nance therapy (Ravald and Hamp 1981; Reiker et al. 1999), caries at furcation‐tun- nelled teeth is not to be seen as an unusual finding. Caries in the furcation tunnel is often difficult to detect clinically and – when clinically manifest – is beyond restorative dentistry’s therapeutic range, thus extrac- Figure 9.10 Upper left first premolar with mesial tion may become inevitable (Figures 9.11 bone loss reaching the apical third of the root was and 9.12). chosen for furcation tunnelling. Clinically, at the mesial aspect over the furcation entrance, there was a pronounced swelling corresponding to the radio‐ 9.9 Maintenance Phase juxtaradicular translucency. Though good compliance with interdental brushing was achieved, the progression of periodontitis could not be A crucial point during the maintenance arrested. The tooth lost stability only a few months phase is the time when the patient is dis- later and had to be extracted. charged from the periodontal practice. The introduction and instruction of the refer- ring clinic are indicative of continuous good prognosis of the furcation‐tunnelled tooth. 1993; Zuza et al. 2006). However, only a A general recommendation is periodontal minority (10%) of the accessory canals in supportive therapy every third month. the furcation are real communications Reminding the patient of the furcation tun- connecting the pulpal chamber with the nel is an important psychological aspect for periodontium; the majority are blind canals this type of patient. It has been shown that with an opening to either side and ending in tunnelled molars can be kept over several the dentine (Zuza et al. 2006). Further on, years of supportive periodontal therapy (see pulpal necrosis only occurs when the main Table 9.1). Caries was given as a main rea- apical foramina are involved, even if a pul- son for tooth loss during maintenance. pal inflammation can be seen at accessory There are indications of a prognostic canals (Langeland et al. 1974). These ana- breaking point at 10 years of maintenance, tomical and histological findings corrobo- when the percentage of tooth loss notably rate clinical observation that endodontic increases (Dannewitz et al. 2006, 2016). In complications were not reported as a major several studies (see Table 9.1), fluoride complication after furcation tunnelling prophylaxis is recommended to prevent the (see Table 9.1). development of caries lesions in the furca- tion tunnel. In two studies (Topoll and Lange 1987; Eickholz et al. 1991), patients 9.8 Caries after Furcation not complying with this recommendation Tunnelling were over‐represented among patients los- ing the tunnelled tooth. Large studies Molars subjected to furcation tunnelling are needed to draw conclusions and pro- were reported to be at risk for root caries in vide guidelines on long‐term survival of the furcation area. The prevalence of root tunnelled molars. Reason for Reason for extraction Caries – 6/10 teeth because of caries; other reasons not specified Extracted tunnelled re‐examined teeth/all (%) tunnelled teeth 3/7 = 42.9% No extractions reported 10/149 = 6.7%
Table 9.1 Summary of follow‐up studies of multi‐rooted teeth subjected to furcation tunnel preparation. Supportive periodontal (SPT);therapy flouride application 3–6 months 3–4 months; 14 patients withcomplied fluorideof recommendation prophylaxis (gel application) 3–6 months; all patients advisedwere use to fluoride dentrifrice, also directly in rinse and to with tunnel, the 0.025% fluoride solution Follow‐up Supportive periodontal Extracted tunnelled Sample years (mean Types of tunnelled therapy (SPT); flouride teeth/all re‐examined Reason for Author/Year n ± SD/range) Type of study No. of teeth teeth application tunnelled teeth (%) extraction
Hamp et al. 100 5Prospective follow‐up of 310 multi‐rooted 6 lower first 3–6 months 3/7 = 42.9% Caries 1975 multi‐rooted teeth teeth, 7 (2.3%) of molars, 1 upper which tunnelled first premolar Topoll and 28 1–8; mean Retrospective follow‐up 34 tunnelled molars 32 lower molars, 3–4 months; 14 patients No extractions – Lange 1987 3.4 of tunnelled molars 2 upper molars complied with reported after resection of recommendation of fluoride Types of tunnelled Types teeth 6 lower first molars, 1 upper first premolar 2 upper molars after resection of palatalthe root 52 lower molars, 91 upper molars, had 33 of which tunnels ‘double’ the palatal root prophylaxis (gel application) Helldén 107 0.8–8.9; Retrospective follow‐up 156 tunnelled 52 lower molars, 3–6 months; all patients 10/149 = 6.7% 6/10 teeth because et al. 1989 mean 3.1 of tunnelled molars; molars 91 upper molars, were advised to use fluoride of caries; other 102/107 of patients 33 of which had dentrifrice, also directly in reasons not and 149/156 of ‘double’ tunnels the tunnel, and to rinse with specified tunnelled molars were 0.025% fluoride solution reexamined Kuhrau 59 4–8; mean Retrospective follow‐ 275 molars, 14 14 lower molars Regular SPT; intervals not 2/14 = 14.3% Caries et al. 1990 5.8 up of molars (5.1%) of which specified under SPT tunnelled No. of teeth No. 310 multi‐rooted teeth, 7 (2.3%) of tunnelled which 34 tunnelled molars 32 lower molars, 156 tunnelled molars Eickholz 56 1–5; mean Retrospective follow‐up 76 tunnelled lower 76 lower molars 3 months; 39 patients 5/68 = 7.4% Not specified et al. 1991 2.0 of tunnelled lower molars complied with molars under SPT; recommendation to brush a 49/56 of patients and concentrated fluoride gel 68/76 of tunnelled into the tunnel molars were reexamined Little et al. 18 5.8 ± 0.83 Prospective follow‐up of 18 tunnelled molars 13 lower, 5 upper 3 months; 2/18 = 11.1% Caries 1995 tunnelled molars molars Prospective of follow‐up multi‐rooted teeth Retrospective follow‐up of tunnelled molars Retrospective follow‐up of tunnelled molars; 102/107 of patients and 149/156 of tunnelled molars were reexamined Follow‐up Follow‐up (mean years ± SD/range) of study Type 3.4 mean 3.1 28 1–8; mean 100 5 107 0.8–8.9; Sample n Summary of follow‐up studies of multi‐rooted teeth subjected to furcation tunnel preparation. subjected teeth to furcation Summary studies of multi‐rooted of follow‐up Author/Year et al. Hamp 1975 Topoll and Topoll Lange 1987 Helldén et al. 1989 Table 9.1
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(c) (d)
(a) (b)
(c) (d)
Figures 9.11 and 9.12 Development of caries in furcation tunnels. In these two cases, caries developed within the furcation area – before caries developed (a) and (c); with the established lesions (b) and (d). Caries development was associated with inadequate oral hygiene during supportive periodontal therapy. The lesions may be easily missed by mere clinical examination. Radiographs should therefore be taken during supportive periodontal therapy to detect caries development at an early stage.
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Summary of Evidence
●● The tunnelling procedure is a treatment ●● After periodontal treatment, the majority method applicable in approximately of tunnelled molars can successfully be 1–5% of all molar teeth in patients kept in maintenance care over many years. referred for the treatment of periodontal The prognosis declines after a decade. disease. ●● Caries is the most frequent complication ●● The best candidates for the tunnelling leading to loss of tunnelled molars during procedure are lower first molars. maintenance.
References
Chiu, B.M., Zee, K.Y., Corbet, E.F., and Friedman, N. (1962). Mucogingival surgery: Holmgren, C.J. (1991). Periodontal The apically repositioned flap. Journal of implications of furcation entrance Periodontolology 33, 328–340. dimensions in Chinese first permanent Graetz, C., Schützhold, S., Plaumann, A. et al. molars. Journal of Periodontology 62, (2015). Prognostic factors for the loss of molars: 308–311. An 18‐years retrospective cohort study. Dannewitz, B., Krieger, J.K., Hüsing, J., and Journal of Clinical Periodontolology 42, Eickholz, P. (2006). Loss of molars in 943–950. periodontally treated patients: A Hamp, S.‐E., Nyman, S., and Lindhe, J. (1975). retrospective analysis five years or more Periodontal treatment of multirooted teeth: after active periodontal treatment. Journal Results after 5 years. Journal of Clinical of Clinical Periodontolology 33, 53–61. Periodontology 2, 126–135. Dannewitz, B., Zeidler, A., Hüsing, J. et al. Helldén, L.B., Elliot, A., Steffensen, B., and (2016). Loss of molars in periodontally Steffensen, J.E.M. (1989). Prognosis of treated patients: Results 10 years and more tunnel preparations in treatment of class III after active periodontal therapy. Journal of furcations: A follow‐up study. Journal of Clinical Periodontolology 43, 53–62. Periodontology 60, 182–187. Eickholz, P., Kaltschmitt, J., Berbig, J. et al. Hou, G.L., and Tsai, C.C. (1997). Types and (2008). Tooth loss after active periodontal dimensions of root trunk correlating with therapy. 1: Patient‐related factors for risk, diagnosis of molar furcation involvements. prognosis, and quality of outcome. Journal Journal of Clinical Periodontology 24, of Clinical Periodontolology 43, 165–174. 129–135. Eickholz, P., Topoll, H.H., Hucke, H.P., and Joseph, I., Varma, B.R., and Bhat, K.M. (1996). Lange, D.E. (1991). Postoperative Befunde Clinical significance of furcation anatomy of nach Tunnelierung furkationsbeteiligter the maxillary first premolar: A biometric Unterkiefermolaren (Grad III) [Postsurgical study on extracted teeth. Journal of findings after tunnel preparation in Periodontology 67, 386–389. mandibular molars with class III furcation Kaltschmitt, J., Radek, M., Dannewitz, B., and involvement]. Deutsche Zahnärztliche Eickholz, P. (2006). Success of tunnel Zeitschrift 45, 356–357. preparations in molars with class III Feres, M., Araujo, M.W., Figueiredo, L.C., and furcation involvement. Journal of Clinical Oppermann, R.V. (2006). Clinical evaluation Periodontology 33 (7), 116. of tunnelled molars: A retrospective study. Kerns, D.G., Greenwell, H., Wittwer, J.W. et al. Journal of the International Academy of (1999). Root trunk dimensions of 5 different Periodontology 8, 96–103. tooth types. International Journal of 190 Chapter 9
Periodontics and Restorative Dentistry 19, Ravald, N., and Hamp, S.‐E. (1981). Prediction 83–91. of root surface caries in patients treated for Kuhrau, N., Kocher, T., and Plagmann, H.C. advanced periodontal disease. Journal of (1990). Parodontalbehandlung Clinical Periodontology 8, 400–414. furkationsbefallener Zähne: Mit oder ohne Reiker, J., van der Velden, U., Barendregt, D.S., Radektomie? [Periodontal treatment of and Loos, B.G. (1999). A cross‐sectional furcally involved teeth: With or without root study into the prevalence of root caries resection?]. Deutsche Zahnärztliche in periodontal maintenance patients. Zeitschrift 45, 455–457. Journal of Clinical Periodontology 26, Lang, N.P., Adler, R., Joss, A., and Nyman, S. 26–32. (1990). Absence of bleeding on probing: An Rüdiger, S.G. (2001). Mandibular and indicator of periodontal stability. Journal of maxillary furcation tunnel preparations: Clinical Periodontology 17, 714–721. Literature review and a case report. Journal Langeland, K., Rodrigues, H., and Dowden, W. of Clinical Periodontology 28, 1–8. (1974). Periodontal disease, bacteria, and Svärdström, G., and Wennström, J.L. (1988). pulpal histopathology. Oral Surgery, Oral Furcation topography of the maxillary and Medicine, Oral Pathology 37, 257–270. the mandibular first molars. Journal of Little, L.A., Beck, F.M., Bagci, B., and Horton, Clinical Periodontology 15, 271–275. J.E. (1995). Lack of furcal bone loss Topoll, H.H., and Lange, D.E. (1987). Die following the tunnelling procedure. Journal Tunnelierung mehrwurzliger Zähne: of Clinical Periodontology 22, 637–641. Ergebnisse 8 Jahre post operationem. Lowman, J.V., Burke R.S., and Pelleu G.B. [Tunnel preparation of multirooted (1973). Patent accessory canals: Incidence in teeth: Results 8 years after surgery]. molar furcation region. Oral Surgery, Oral Deutsche Zahnärztliche Zeitschrift 42, Medicine, Oral Pathology 36, 580–584. 445–449. Niemann, R.W., Dickinson, G.L., Jackson, C.R. Vertucci, F.J., and Williams, R.G. (1974). et al. (1993). Dye ingress in molars: Furcation canals in the human mandibular Furcation to chamber floor. Journal of first molar. Oral Surgery, Oral Medicine, Endodontics 19, 293–296. Oral Pathology 38, 308–314. Paolantonio, M., di Placido, G., Scarano, A., Zuza, E.P., Toledo, B.E., Hetem, S. et al. (2006). and Piattelli, A. (1998). Molar root furcation: Prevalence of different types of accessory Morphometric and morphologic analysis. canals in the furcation area of third molars. International Journal of Periodontics and Journal of Clinical Periodontology 77, Restorative Dentistry 18, 489–501. 1755–1761. 191
Chapter 10
Innovative and Adjunctive Furcation Therapy: Evidence of Success and Future Perspective Luigi Nibali and Elena Calciolari
Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK
10.1 Introduction endoscopy was proposed nearly 20 years ago (Ozawa et al. 1999). The periodontal endo- This book’s journey has taken the reader scope has been specifically designed to explore through the anatomy of molars with furcation and visualize periodontal pockets in patients involvement (FI) and the challenges facing the with periodontitis. The advantage of this clinician engaging in periodontal treatment of instrument is the subgingival visualization of such molars. Recent technological advances the root surface at high magnification (24× to have led to the birth of several techniques and 48×; Kwan 2005). When combined with the devices which can help in the treatment of use of micro ultrasonic instruments, endo- molars with FI. The aim of this chapter is to scopic debridement can be accomplished in a review what has changed in the treatment of more accurate, conservative, and minimally furcation‐involved teeth in recent years, to invasive way (Geisinger et al. 2007), thus present the evidence for the efficacy of these potentially reducing the need for surgical new therapeutic modalities, and to predict intervention. Molars with FI, due to their dif- possible future treatment avenues. A major ficult access for debridement, may represent improvement in periodontal non‐surgical optimal candidates for this technology. treatment, including the treatment of furcation However, when comparing 35 pairs of multi‐ defects, has been achieved with the introduc- rooted teeth that received either endoscopy‐ tion of mini‐curettes and slim‐line ultrasonic aided scaling and root planing (SRP) or inserts, which have been covered in Chapter 3. traditional SRP, Michaud and co‐workers Other treatments, which we could consider (2007) did not find a significant difference in ‘alternative’ to the ‘traditional’ treatments calculus deposit removal between the two described so far, are described in what follows. groups, as assessed on digital images taken with a stereomicroscope. The same conclu- sions were reported by a more recent rand- 10.2 Periodontal Endoscope omized split‐mouth study, where one quadrant underwent traditional SRP and another quad- In an attempt to overcome the limitations of rant underwent SRP with the help of the peri- traditional closed‐root instrumentation and odontal endoscope (Blue et al. 2013). to give the clinician the possibility of visu- Nevertheless, a significant decrease in perio- ally debriding root surfaces, periodontal dontal outcomes of inflammation (namely
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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bleeding on probing, BOP, and gingival index, The current evidence supporting the GI) was observed in the endoscopy‐aided SRP adjunctive use of dental lasers (mainly the group compared to the SRP group. diode or the Nd:YAG) is of poor quality and Although endoscopy may be an attractive insufficient to warrant their use in the treat- option, especially for sites that have not ment of chronic or aggressive periodontitis responded to traditional non‐surgical treat- or in periodontal maintenance therapy (Cobb ment and for patients where surgery is con- 2016). In fact, since the 2011 statement from traindicated, the use of the periodontal the American Academy of Periodontology endoscope may be difficult in narrow furca- that the use of dental lasers as monotherapy tions, or in curved roots, root proximity, and or in addition to non‐surgical periodontal in the presence of overhanging restorations, instrumentation did not provide any tangible as that may hinder the access for the endo- advantage in terms of subgingival debride- scope and the instruments (Kwan 2005). ment, reduction of subgingival bacterial Furthermore, we should not forget that, apart levels, and root debridement (American from the high cost, the use of endoscopic Academy of Periodontology 2011), very little instrumentation can be difficult to master, it has changed. Recent meta‐analyses have requires dedicated training, and it is associ- claimed short‐term (six months) benefits of ated with a steep learning curve. the use of the Nd:YAG or diode lasers in con- junction with non‐surgical periodontal ther- apy in terms of probing pocket depth (PPD) 10.3 Laser Therapy and BOP reductions compared with mechan- ical debridement alone (Roncati and Gariffo In the past two decades, the use of lasers in 2014; Sgolastra et al. 2014). However, they the treatment of periodontal disease has also highlighted the poor quality of the attracted increasing interest. The word ‘laser’ available studies and the need for long‐term, is an acronym for ‘light amplification by well‐designed, parallel, independent rand- stimulated emission of radiation’ and it omized controlled trials (RCTs) with suffi- broadly refers to any device that emits light, cient statistical power and appropriate laser is spatially coherent, and is collimated. Lasers settings in order to be able to draw more can be classified according to their active robust conclusions. medium (gas lasers and solid lasers), tissue Besides the limited scientific evidence, applicability (hard‐tissue and soft‐tissue current limitations on the use of lasers to lasers), range of wavelength, and risk associ- treat molars with FI include the often high ated with their application (Verma et al. cost of the devices (which makes it difficult 2012). Dental laser wavelengths are typically to justify their use to the patient), the need located within the near, mid, and far infrared for additional education/training of the prac- portions of the electromagnetic spectrum titioner (this includes education on the dif- (EMS; Lomke, 2009). ferent properties associated with the different In periodontal therapy, different lasers wavelengths, as well as some fundamentals have been proposed for removal of pocket of physics), and the need to implement safety epithelium (Borrajo et al. 2004; Saglam et al. measures. In addition, and probably most 2014; Ustun et al. 2014), removal of subgingi- importantly, there is a lack of evidence on the val calculus deposits (Eberhard et al. 2003; best setting to use for each different laser in Schwarz et al., 2003; Lopes et al. 2010), terms of wavelength, energy density, power reduction of bacterial load (Moritz et al. output, frequency/duration of irradiation, 1998; Yaneva et al. 2014), root surface decon- distance between the cells, and the laser tamination (Barone et al. 2002), and enhance- spot/probe. ment of periodontal regeneration (Dogan To the best of our knowledge, there is only et al. 2016; Taniguchi et al. 2016). a limited number of studies that have Innovative and Adjunctive Furcation Therapy 193
specifically considered laser treatment in also in furcation‐involved molars. Another molars with FI, and the results are in line application of phototherapy in periodontol- with those reported for other periodontally ogy is antimicrobial photodynamic therapy, involved teeth. In a double‐blind RCT, de which combines LLLT and a photosensitizer Andrade et al. (2008) compared clinical and with the aim of destroying pathogens in the microbiological parameters of 17 patients pocket with reactive oxygen species, and this with class II furcation lesions treated either will be discussed in more detail in the next with SRP, or with SRP followed by pulsed section. Nd:YAG laser treatment. The results showed that the adjunctive laser promoted a signifi- cant higher reduction in the total bacteria 10.4 Photodynamic Therapy colony‐forming units (CFU) immediately after the treatment, but after six weeks no The rationale behind photodynamic therapy significant differences were detected between (PDT) comes from the need to obtain anti- the two groups. Furthermore, no significant microbial effects without the risk of causing differences in terms of periodontal clinical the onset of microbial resistance. With PDT, parameters between baseline and six weeks bacteria are sensitized using a dye (photo- after treatment were found between the two sensitizer) coming into contact with their groups. In a more recent split‐mouth study, membrane, and are then destroyed following an erbium, chromium: yttrium‐scandium‐ irradiation with light of the correct energy gallium‐garnet (Er,Cr:YSGG) laser was used and wavelength. More specifically, a laser in association with SRP in molars with degree light is used to activate the dye molecules to II or III furcation involvement (Ge et al. reach a high energy triplet state, which reacts 2017). A significantly higher reduction of with oxygen to create singlet oxygen, which PPD and BOP was observed at six and twelve in turn destroys the bacterial membrane. weeks in the laser‐treated group compared Toluidine blue (TBO) and methylene blue to the control group (SRP only). The visual (MB) are used as dyes, due to their ideal analogue scale (VAS) pain score was also sig- properties of low toxicity, cationic charge for nificantly lower when the laser was applied. attachment to Gram‐ membranes, red light An attractive additional laser‐based treat- absorption, rapid transition from ‘singlet’ to ment modality is the so‐called phototherapy, ‘triplet’ state, long maintenance of ‘triplet’ photomodulation, or low‐level laser therapy state, and high production of photoproduct (LLLT), which employs lasers at a low dose (Atieh 2010; Soukos and Goodson 2011; with the aims of alleviating pain or inflam- Gursoy et al. 2013). mation, inducing immunomodulation, and Although the original concept of PDT is promoting wound healing and tissue regen- already over 100 years old, only in recent eration (Anders et al. 2015). Recent evidence years has it reached clinical applications in suggests that LLLT is able to enhance osteo- various fields of medicine, including oncol- blastic proliferation and differentiation ogy, dermatology, and dentistry (Konopka (Amid et al. 2014), increase gene expression and Goslinski 2007). Its characteristics make of collagen and vascular endothelial growth PDT potentially suitable for the treatment of factor in fibroblastic cells (Martignago et al. periodontitis, either in the non‐surgical or 2015), promote the production of nucleic surgical phase, with the aim of boosting the acid (Saperia et al. 1986), and increase mito- antimicrobial effects of mechanical plaque chondrial respiratory chain and adenosine removal without the risk of causing micro- triphosphate (ATP) synthesis (Agrawal et al. bial resistance (Andrade et al. 2013; Sgolastra 2014). Future studies are needed to explore et al. 2013a, b; Souza et al. 2016). Studies the potential benefits of adding LLLT to, for have shown that photo‐inactivation of path- instance, periodontal regenerative treatment, ogenic bacteria harvested from periodontal 194 Chapter 10
pockets is possible in vitro by using TBO and Owing to the difficult access for mechan- a 635 nm laser activation (Qin et al. 2008). ical debridement, furcation defects repre- Despite some promising animal models and sent an ideal scenario where PDT could be clinical studies, a systematic review and helpful during initial therapy, surgical ther- meta‐analysis of seven RCTs using PDT as an apy, or maintenance in order to reduce adjunct or alternative to subgingival debride- bacterial load and promote healing. An ment showed no significant clinical benefits, advantage of PDT includes the possibility with reduction in some bacteria in some to apply it topically into a periodontal studies (Porphyromonas gingivalis) but not pocket, thus avoiding overdose and reduc- in others, and no consistent adverse events ing the probability of side effects and reported (Sgolastra et al. 2013a). The same microflora disturbance in other sites of the group performed a new systematic review oral cavity (which are instead associated that included both RCTs and parallel‐design with systemic antimicrobials; Wainwright studies (Sgolastra et al. 2013b). After remov- 1998; Hamblin and Hasan 2004). Figure 10.1 ing outlier studies, the meta‐analysis indi- shows a case of furcation involvement cated a significant positive effect in terms of treated with PDT. PPD reduction (0.19, 95% confidence inter- De Almeida and co‐workers (2008) histo- val [CI] 0.007–0.31, p = 0.002) and CAL gain metrically assessed the influence of PDT on (0.37, 95% CI 0.26–0.47, p < 0.0001) at three bone loss in furcation areas of rats with experi- months. However, the clinical significance of mentally induced periodontitis. The PDT these data is limited and no differences were group demonstrated less bone loss compared observed at six months. Remarkably, sub- to the control group, the group treated only group analysis revealed that studies adopting with topical MB, and the group treated only a time of application of 60 seconds showed a with LLLT at 7 days (1.986 ± 0.417 mm2). At 15 higher and significant PPD reduction and days, the PDT (1.641 ± 0.115 mm2) and MB CAL gain. groups (1.991 ± 0.294 mm2) demonstrated
(a) (b)
Figure 10.1 Upper left first molar (UL6) of patient with chronic periodontitis, affected by degree II FI and treated with photodynamic therapy, following non‐surgical furcation debridement with ultrasonic devices. (a) Application of dye (methylene blue) inside the furcation area; (b) activation of the dye by photodynamic therapy light. Innovative and Adjunctive Furcation Therapy 195 less bone loss compared to the control 10.5 Air‐polishing Devices (4.062 ± 0.416 mm2) and LLLT (2.641 ± 0.849 mm2) groups. Since in periodontally compromised teeth To the best of our knowledge, only a few root surfaces are subjected to continuous RCTs have evaluated PDT specifically in abrasive instrumentation during lifelong per- molars with FI. A double‐blind RCT evalu- iodontal maintenance therapy, debridement ated PDT for the treatment of class II furca- techniques that are at the same time effective tions in patients with chronic periodontitis and minimally invasive should be aimed at. (Luchesi et al. 2013); 21 patients who under- Keeping this in mind, air‐polishing devices went SRP with the adjunct of the photosen- might represent a valid alternative to sitizer only (control) and 16 patients who mechanical instrumentation. Air‐abrasive underwent SRP followed by PDT (test) technology has been applied in the dental completed the six‐month follow‐up. While field for more than 60 years (reviewed by PDT was able to reduce gingival crevicular Petersilka 2011). The idea is to use an abra- fluid (GCF) levels of inflammatory media- sive powder that is introduced into a stream tors and the concentration of P. gingivalis of compressed air to clean and polish the and Tannerella forsythia at six months, no tooth surface by removing the deposits significant differences in terms of CAL and attached to it or by smoothing their texture. PPD were detected between the two groups This abrasive process depends on the prop- at either three or six months. Nevertheless, erties of the particles applied (shape, geo- when interpreting these results we need to metrical form, hardness) and on the pressure consider that the study lacked a true nega- of the air and water used (Petersilka 2011). tive control group, as the presence of the Sodium bicarbonate–based air polishing photosensitizer dye may have optimized the has been successfully applied for supragingi- results of the control group. Moreover, this val plaque and stain removal since the 1980s study used a single PDT application as an (Berkstein et al. 1987; Barnes et al. 1990). adjunct to SRP, while it is plausible that However, the use of sodium bicarbonate on repeated PDT applications would have cement and dentine is not advisable, as sig- resulted in more positive outcomes (Lulic nificant tissue removal may occur (Atkinson et al. 2009). In a split‐mouth RCT, Andrade et al. 1984; Horning et al. 1987; Petersilka et al. (2013) collected data on 14 patients et al. 2003a). Furthermore, this type of air‐ with bilateral lower molars with class III polishing device may cause reversible soft‐ furcation lesions scheduled for extraction. tissue irritation and damage, such as In the control side traditional SRP was per- epithelial erosions with exposure of the formed, while in the test side SRP was fol- underlying connective tissue (Hunter et al. lowed by a session of PDT. At 45 days post 1989; Kontturi‐Narhi et al. 1989; Kozlovsky initial therapy, the class III furcation lesions et al. 2005). To overcome these limitations were surgically accessed, and flap surgery and minimize the hard‐ and soft‐tissue with SRP and flap surgery with SRP + PDT trauma, glycine powder air‐polishing devices was performed in the control and test group, have been introduced. Several clinical trials respectively. At 21 days post surgery, the have evaluated the efficacy of this air‐polish- newly formed granulation tissue was col- ing system for subgingival biofilm removal lected, and real‐time polymerase chain with positive results, but no study distin- reaction (PCR) showed a significant up‐ guished between single‐ and multi‐rooted regulation of the TIMP‐, 2/MMP‐2, and teeth. In a randomized split‐mouth con- OPG/RANKL mRNA ratios in the test trolled study in patients receiving supportive group, thus suggesting a role for PDT in periodontal therapy, the use of glycine positively modulating extracellular matrix powder was more effective in reducing the and bone remodelling. number of CFU in comparison to hand 196 Chapter 10
instrumentation with curettes in pockets of directly in the site could lead to a further 3–5 mm (Petersilka et al. 2003b, c). Another reduction in microbial load and a better heal- split‐mouth controlled study did not find ing of the lesion. Local antimicrobials could significant differences at a microbiological be used as topical applications, for sustained level between SRP and subgingival air polish- release (drug delivered in effective concen- ing; however, the use of glycine‐based air trations for less than 24 hours) or controlled polishing was perceived as less painful/ delivery (drug delivered in effective concen- uncomfortable by the patients and less time trations for more than 24 hours), within consuming by the operator (Moene et al. different delivery systems (Herrera et al. 2010). While only shallow pockets (up to 2012; Jepsen and Jepsen 2016). The use of 5 mm) were included in these studies, a more antiseptics (including chlorhexidine, sodium recent study from Flemmig and co‐workers hypochlorite, and povidone‐iodine) and anti- (2012) considered pockets from 4 to 9 mm. biotics (including tetracyclines and metroni- Their results showed that glycine air polish is dazole) has been reported in the periodontal more effective in removing the subgingival literature and several agents are available on biofilm, and may induce a beneficial shift of the market. Systematic reviews show that the oral microbiota (lower total viable bacte- when local antibiotics are used as adjuncts rial count) compared to traditional SRP. to subgingival debridement, short‐term In conclusion, air‐polishing devices might improvement in clinical parameters meas- represent a valid alternative to mechanical ured as PPD reductions and CAL gain can be instrumentation, for both periodontal treat- achieved (Hanes and Purvis 2003; Bonito ment and periodontal maintenance therapy. et al. 2005; Matesanz‐Perez et al. 2013). No The use of glycine powder air polishing studies with long‐term data on periodontal seems well tolerated by the patient and no stability or tooth loss are available. severe adverse events have been reported. As repeatedly observed before, difficulty in However, a few cases of air emphysema (all accessing the furcation area for debridement successfully healed) have been reported and the potentially high microbial load inside (Finlayson and Stevens 1988; Fruhauf et al. the furcation lesions make FI potentially 2005) and the patient needs to be informed amenable to the adjunctive use of local anti- about this rare complication. New air‐polishing microbials. However, what is the evidence for powders, such as erythritol‐based powders the role of local antimicrobials specifically (Hagi et al. 2013, 2015), are now under inves- for the healing and maintenance of FI molars? tigations and future randomized trials will Tonetti and co‐workers (1998) included 127 have to confirm their efficacy. Further studies patients with class II mandibular furcation on molars with FI are advisable to test the with BOP in SPT in a randomized multi‐ efficacy of this technique specifically for centre controlled trial. All subjects received multi‐rooted teeth. SRP and oral hygiene instructions, while tests also had tetracycline fibres applied inside the furcation defects. Subjects were 10.6 Local Antimicrobials followed up to six months, when periodontal clinical measurements were taken for the last Given the microbial aetiology of periodonti- time before the end of the study. The authors tis, antimicrobial adjuncts to mechanical observed that, despite increased reductions debridement could be considered a valid in BOP and PPD in the test group at three treatment option for periodontal treatment. months (compared to controls), no differ- Bearing in mind that mechanical subgingival ences between groups were observed at six biofilm disruption with ultrasonic inserts months. Consistent results were observed in and curettes is essential for the healing of a separate study on 32 patients with chronic periodontal pockets (Badersten et al. 1984), periodontitis, who received initial pocket/ the additional use of antimicrobial agents root debridement by ultrasonic instrumentation, Innovative and Adjunctive Furcation Therapy 197 followed by random assignment to further forms, thanks to their effect on the subgingi- treatment by ultrasonic instrumentation val microbiota. Baer and Socransky (1979) with or without adjunctive local application followed up patients with ‘periodontosis’ of an 8.8% doxycycline gel in residual defects (what we would now classify as aggressive (Tomasi and Wennstrom 2011). Clinical periodontitis, AgP), treated with oral hygiene examinations were repeated three and nine instructions, non‐surgical, and surgical months after retreatment. The retreatment approaches associated with adjunctive sys- including the local antibiotic resulted in temic antibiotics, and concluded that antibiot- ‘closure’ of 50% of degree I furcation sites, ics such as te tracyclines and penicillin could compared to 29% for sites treated with be a helpful adjunct to patient management, mechanical debridement only (p > 0.05), and including full‐thickness flaps and curettage. in a reduction in depth of degree II furcation Later, metronidazole was introduced in peri- sites of 17% in the test and 11% in the control odontal therapy for its effect on Aggregatibacter group (p > 0.05). No differences for the out- actinomyecetemcomitans (then known as come variable ‘furcation improvement’ were Actinobacillus actinomycetemcomitans; Saxen detected between the two groups, suggesting and Asikainen 1993). Interest in the use of that improvement in molar FI after non‐sur- adjunctive systemic antibiotics increased with gical periodontal therapy was not enhanced the evidence from laboratory studies, showing by adjunctive locally applied doxycycline that the rate of metronidazole uptake by (Tomasi and Wennstrom 2011). A. actinomyecetemcomitans bacterial cells The use of povidone‐iodine as an adjunct to simultaneously incubated with amoxicillin SRP in the treatment of class II furcations has was higher than the uptake in cells incubated been investigated in two RCTs, but only lim- with metronidazole alone (Pavicic et al. 1995). ited (Ribeiro Edel et al. 2010) or no additional Hence, several papers were published suggest- clinical benefits (Del Peloso Ribeiro et al. ing improved clinical outcomes (PPD 2006) resulted from the use of this antiseptic. reductions and CAL gains) when the amoxi- In a randomized parallel‐arm controlled cillin–metronidazole ‘cocktail’ was used as an study, the clinical efficacy of subgingival adjunct to SRP (van Winkelhoff et al. 1992; ultrasonic instrumentation irrigated with Winkel et al. 2001). While several randomized essential oils (EOs) was compared with chlo- placebo‐controlled trials on the adjunctive use rhexidine (CHX) or distilled water (control) of amoxicillin and metronidazole flourished, in 45 patients with class II FI (Yilmaz and several other antibiotics or combinations of Bayindir 2012). When comparing the test them were introduced as adjuncts to perio- groups (EOs and CHX) to the control group, dontal therapy, for both chronic and aggres- no significant differences in the improvement sive periodontitis. of periodontal clinical parameters were Most original papers and systematic reported at one and three months after treat- reviews only report short‐term data (e.g. six ment, with the exception of BOP, which was months or twelve months), making it diff icult significantly reduced in the EOs group com- to understand possible long‐term benefits. pared to the CHX and control groups at both Systematic reviews tend to agree that sys- one and three months. Figure 10.2 shows a temic antibiotics used as adjuncts to SRP case of a maxillary molar furcation lesion provide clinical improvements (PPD reduc- treated with local antibiotics. tions, CAL gain) compared with SRP alone or SRP and placebo. These clinical improve- ments range from 0.3 to 0.5 additional PPD 10.7 Systemic Antimicrobials reductions and 0.2 to 0.4 mm additional CAL gain (as full‐mouth average), and seem to be Systemic antibiotics have been proposed since more pronounced in AgP cases (Herrera the 1970s as adjuncts for the treatment of et al. 2002, 2012; Sgolastra et al. 2012a, b; periodontitis, initially mainly for early‐onset Buset et al. 2015). Studies venturing into 198 Chapter 10
(a) (b)
(c)
(e)
(d)
Figure 10.2 Application of local antibiotic after non‐surgical debridement in degree II mesial furcation lesion of a maxillary second molar, associated with mesial intrabony defect (10 mm probing pocket depth) and extensive presence of subgingival deposits. (a) Periapical radiograph; (b) clinical photograph; (c) antibiotic application from the mesio‐buccal aspect of the pocket associated with the furcation defect; (d) antibiotic overflowing from the pocket; (e) radiographic re‐evaluation six months after treatment, showing bone fill with reduction in the intrabony defect depth (now 6 mm probing pocket depth and degree I furcation involvement).
longer‐term follow‐ups show conflicting hydrochloride (HCl) four times a day for evidence. A study on 506 patients with mod- three weeks adjunctive to SRP found that erate to severe periodontitis observed reduc- short‐term benefits seemed to disappear tions in attachment loss favouring the test with time (Ramberg et al. 2001). A recent group (adjunctive amoxicillin and metroni- systematic review highlighted that the clini- dazole) for up to 27 months of follow‐up cal benefits of adjunctive systemic antibiotics (Harks et al. 2015). A prospective study with seem to diminish over time, from the three‐ 13‐year follow‐up using 250 mg tetracycline month follow‐up to the one‐year follow‐up Innovative and Adjunctive Furcation Therapy 199
(Keestra et al. 2015). Hence, doubts persist Probiotics are defined as ‘living microor- about the long‐term effect of antibiotics used ganisms which, when administered in ade- as adjunctive therapy. quate amounts, confer a health benefit for Furthermore, adverse events and risk of the host’ (FAO/WHO 2001). The most com- developing antibiotic resistance should be an mon probiotics belong to two main genera, important concern when deciding whether Lactobacillus and Bifidobacterium. The to use adjunctive antibiotic therapy. suggested mechanisms of action of probiot- Generally, deep pockets seem to benefit ics in the oral cavity include a modulation of more from an adjunctive antibiotic regime, the host immune‐inflammatory response, a as the antibiotic could be of more help in direct inhibition of periodontopathogenic sites where the effectiveness of mechanical bacteria via the production of antimicrobial debridement is more limited (Guerrero et al. substances (such as lactic acid, hydrogen per- 2005). For the same reasons, it can be sup- oxide, and bacteriocin‐like substances), and posed that teeth affected by FI could benefit an indirect effect originating from competi- from adjunctive systemic antibiotics. tive exclusion systems, so that by competing However, no study seems to have specifically for the same niches and nutrients, ‘good’ bac- tested this hypothesis. To the best of our teria can reduce the chances of pathogens knowledge, only a subanalysis of data from a replicating and adhering to tooth surfaces large clinical trial has tried to answer the (Laleman and Teughels 2015). However, question of whether systemic amoxicillin and three systematic reviews have been recently metronidazole adjunctively to mechanical published to evaluate the overall efficacy of debridement might significantly improve probiotic therapy in the treatment of perio- periodontal clinical parameters at molar and dontally compromised teeth. Matsubara and premolar furcation sites (Eickholz et al. co‐workers (2016) included 12 RCTs 2016). Although PPD reduction and CAL (both split mouth and parallel designed) and gain at furcation sites were noticeably concluded that the use of oral probiotics improved after antibiotic therapy compared alone or associated with SRP is well tolerated with placebo, no difference in the change of (no adverse effects reported) and is associ- furcation degrees between the treatments ated with an overall tendency for improved could be detected. clinical parameters and reduced levels of periodontal pathogens. Martin‐Cabezas and co‐workers (2016) included only RCTs com- 10.8 Probiotics paring SRP alone (or associated with pla- cebo) to SRP associated with assumption of When considering the pathogenesis of peri- Lactobacillus reuteri in the quality assess- odontitis, it is well accepted that this disease ment. Meta‐analysis showed a statistically requires the presence of a susceptible host significant CAL gain (‐0.42 mm, p = 0.002) together with the presence of pathogenic and BOP reduction (‐14.66, p = 0.003) for bacteria (Socransky and Haffajee 1992). SRP associated with the probiotic treatment Periodontitis is thought to be the result of a versus SRP alone in the short term. dysbiotic process, characterized by a shift in Furthermore, when stratifying for pocket the composition of the normal subgingival depth, the use of probiotics was significantly biofilm towards a more pathogenic one beneficial in moderate (‐0.18, p = 0.001) and (Hajishengallis and Lamont 2012). Therefore, deep (‐0.67, p < 0.001) pockets. Finally, there has been growing interest in the possi- Gruner and co‐workers (2016) included bility of using probiotics with the aim of RCTs broadly evaluating the efficacy of shifting the oral microbiota equilibrium back any form of probiotic therapy for the to a condition of oral health. management of caries and periodontitis. 200 Chapter 10
The meta‐analysis reported that probiotics with traditional surgical techniques. significantly reduced BOP (standardized Remarkably, recent RCTs show that, when a mean difference, SMD: ‐1.15; 95% CI good stabilization of the blood clot in the ‐1.68/‐0.62), PPD (SMD: ‐0.86, 95% CI surgical area is achieved, the use of grafting ‐1.55/‐0.17), and gingival index (SMD: ‐0.86; materials may not add any additional bene- 95% CI ‐1.52/‐0.20), but did not affect plaque fits in intrabony defects (Trombelli et al. index or CAL. Unfortunately, specific studies 2010; Cortellini and Tonetti 2011; Ribeiro investigating this treatment modality in fur- et al. 2011; Mishra et al. 2013). The same cation lesions are missing. principles of reduction of surgical flap, Although clinical data look promising, the minimizing trauma, and stimulating the for- heterogeneity of the available studies in mation of a stable blood clot could be imple- terms of population included (experimental mented for surgical approaches to furcations. gingivitis patients, healthy patients, patients However, these techniques are explicitly not with chronic periodontitis, patients with indicated for furcation lesions (Cortellini and aggressive periodontitis), parameters evalu- Tonetti 2007), and there seems to be a lack of ated (microbiological parameters in plaque specific innovative surgical techniques for or saliva, plaque index, PPD, CAL, etc.), pro- the treatment of furcation‐involved molars. tocol adopted (probiotics as monotherapy vs probiotics after SRP), and probiotics employed do not allow robust conclusions to 10.10 Furcation ‘Filling’ be drawn. Further research is needed to dem- onstrate the efficacy of certain probiotic Some researchers have attempted closure of strains in oral health, as well as their desired the furcation lesion with the use of restora- concentration and vehicle. tive materials (e.g. ionomeric cement or cal- cium hydroxiapatite cement). This defies the principles of periodontal regeneration and of 10.9 Surgical Innovations maintenance of reduced microbial load in the furcation region discussed in this book. Periodontal surgical techniques have gradu- Not surprisingly, such therapy has encoun- ally striven to become less and less invasive, tered failure, with worsening in periodontal in order to reduce morbidity and patient clinical measurements and high risk of tooth discomfort. The development of minimally loss (Anderegg and Metzler 2000; Fowler and invasive surgical periodontal techniques Breault 2001; Rupprecht et al. 2001). This includes the use of microsurgical instru- stresses once more the importance of allow- ments and magnification, and it is based on ing plaque removal, either self‐performed or the principle of preserving as much of the professional or both, inside the furcation soft tissue as possible (Harrel 1999). Incisions, lesion when regeneration of the furcation flap elevation, and suturing techniques have lesion is not feasible. been modified by a series of papilla‐preser- vation techniques (Takei et al. 1985; Cortellini et al. 1995, 1999) and, more recently, by mini- Conclusion mally invasive surgical therapy (Cortellini and Tonetti 2007, 2009; Trombelli et al. Researchers and clinicians are striving to 2009), moving from double flaps to single identify more efficient ways for the successful flaps. These techniques are aimed mainly at treatment of periodontitis, and specifically the treatment of intrabony defects, and have of molars with furcation involvement. been shown to yield favourable clinical Keeping in mind the uncontested impor- results with reduced tissue trauma compared tance of oral hygiene instructions and Innovative and Adjunctive Furcation Therapy 201
subgingival debridement, new technologies and probiotics have been tested as adjuncts could soon provide a helping hand for the for the treatment and long‐term mainte- treatment of complex cases. Tools to improve nance of furcation lesions. Sadly, the evi- the efficacy of intrafurcation biofilm removal, dence for their efficacy in the clinical to reduce the treatment time, and to improve outcomes of furcation treatment is still lack- the patient’s perceived comfort, such as peri- ing, despite some initial promising results. odontal endoscope, lasers and air‐powder Future well‐designed studies are warranted devices, or antimicrobial agents (local or to shed light on the additional benefits asso- systemic antibiotics, photodynamic therapy) ciated with these new treatment modalities.
Summary of Evidence
●● The treatment of molars with furcation with the potential of being used for the involvement desperately needs new meth- treatment of specific furcation cases. ods to improve clinical efficacy, patient ●● Clinical efficacy, costs, and learning comfort, and long‐term outcomes. curves for these potential adjuncts still ●● Antimicrobial adjuncts (local antibiotics, need to be systematically assessed before photodynamic therapy) and probiotics they can potentially be routinely imple- and technology for improved biofilm mented in the treatment of molars with removal (periodontal endoscope, lasers, furcation involvement. and air‐powder devices) are being tested,
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Chapter 11
Furcation: Why Bother? Treat the Tooth or Extract and Place an Implant? Nikos Mardas1 and Stephen Barter 2
1 Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK 2 Private practice, Eastbourne, UK
11.1 Implants vs Periodontal tooth with a furcation defect (Zitzmann et al. Multi‐rooted Teeth: What is 2011; Donos et al. 2012). the Clinical Problem? The difficulty in assessing the prognosis of teeth with bone loss beyond the root furca- tion following periodontal treatment and the Previous chapters have unequivocally shown increased popularity of dental implants have that in periodontal patients, the posterior shifted the decision from treating these teeth maxilla and mandible are often those areas towards replacing them with implants. In that are the worst affected in terms of severity other words, why bother with treating diffi- of periodontal disease and ultimately tooth cult‐to‐treat molars with FI, when we could loss (Hirschfeld and Wasserman 1978; McFall, extract them and replace them with implants? 1982; McGuire and Nunn 1996), and that fur- The concept of extracting teeth with FI with cation defects are a well‐established local risk questionable prognosis and substituting factor for both attachment and tooth loss. them with dental implants is mainly based on The predictability of either regenerative the following clinical assumptions: (Avila‐Ortiz 2015) or resective (Langer et al. 1981; Carnevale et al. 1991; Blomlöf et al. ●● The lower predictability of furcation treat- 1997) surgical management of teeth with fur- ment in relation to the high morbidity, cation involvement (FI) is variable, and is time, and cost of such treatments, which dependent on a number of local (related to usually involve complex periodontal sur- furcation anatomy) and systemic factors. gery, endodontic and restorative compo- Besides the therapeutic advances in the man- nents, and the need for lengthy supportive agement of furcation defects, periodontal periodontal therapy. treatment success rates are higher in single‐ ●● The higher long‐term survival rates of rooted teeth (Wang et al. 1994), making it implant‐supported restorations (Moraschini easier to predict their prognosis in compari- et al. 2015), which, besides their higher cost, son to multi‐rooted teeth (McGuire 1991). can make them a better restorative solution Therefore, patient‐related factors, treat- in terms of cost versus benefit (Brägger et al. ment cost, and the dentist’s clinical experi- 2005; Bouchard et al. 2009). ence and training often influence the decision ●● The potentially superior functional and on whether to treat or extract a multi‐rooted aesthetic outcomes of implant‐supported
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
restorations over the surgical management implants or bridgework (Pretzl et al. 2009; of teeth with FI, which may result in Fardal et al. 2013). This is of course related to increased tooth mobility, root hypersensi- the additional consideration of the higher tivity, and gingival recession. rate of technical complications associated ●● An early, ‘strategic’ extraction will prevent with implant‐borne prostheses (Brägger further bone loss and thereby facilitate et al., 2005; Albrektsson et al. 2012). This will implant treatment that may otherwise be be discussed in more detail in Chapter 12. difficult considering the anatomical limita- Finally, we cannot base our decision on tions that are usually present in the poste- patient preferences or aesthetic outcomes, rior maxilla and mandible (Kao 2008). since studies comparing aesthetic or patient‐ based outcomes following periodontal treat- All these assumptions could be strongly ment for retention of teeth with FI or dental debated in the light of clinical evidence. implants do not exist (Lang et al. 2012). Although reported implant survival rates are Based on this evidence, we could claim that high, they may not surpass the longevity of dental implants are not a substitute for furca- periodontally compromised teeth (Donos tion‐involved teeth, but rather a solution for et al. 2012), especially in the posterior max- restoring a lost molar when the treatment to illa, where a variety of local factors (quality maintain teeth has failed or is not indicated. and quantity of bone, proximity to anatomi- Therefore, different considerations should be cal structures, and need for grafting) may involved in the decision‐making process for result in reduced implant survival rates each clinical approach, and it cannot simply (Drago 1992; Becker et al. 1999; Graziani be about ‘keeping bone for an implant’ by et al. 2004, Pjetursson et al. 2008). When removing the tooth early. These considera- implants are placed in patients with a history tions include the following: of periodontal disease, they are associated with a higher incidence of biological compli- ●● The strategic role of the furcation‐involved cations (peri‐implantitis), characterized by a tooth in the overall restorative treatment similar pathogenesis and systemic risk plan. factors (e.g. smoking, diabetes) to periodon- ●● The predictability of the periodontal furca- tal disease. tion treatment following an estimation of: Consequently, implants in ‘periodontal –– Local factors such as the extent of FI, patients’ present lower success and probably the residual attachment levels, presence lower survival rates than implants placed in of caries, endodontic complications, periodontally healthy patients (Donos et al and restorative problems. 2012; Sousa et al. 2016a). Severe forms of –– Systemic factors such as smoking, dia- periodontal disease, which commonly result betes, or specific medication that may in posterior teeth with advanced furcation influence the longevity of periodontal defects, are associated with higher rates of teeth (but potentially also of implants). implant loss (Sousa et al. 2016a) and –– The patient’s compliance in maintaining increased peri‐implant bone loss around a high level of oral hygiene and in follow- implants placed to substitute teeth with FI ing an intensive supportive periodontal (Hardt et al. 2002). In the only comparative therapy programme. study available to date, Fugazzotto (2001) ●● The predictability of an implant‐supported reported similar success rates of implants restoration following an estimation of: (97%) and root‐resected molars (96.8%) after –– Residual bone quantity in relation to 0–13 years of function. Furthermore, more anatomical limitations and the com- recent cost‐effectiveness studies have shown plexity of any bone augmentation pro- that the cost of periodontal therapy is rela- cedures necessary to overcome these tively lower than the cost and maintenance of limitations. Furcation: Why Bother? 211
–– Systemic factors that may influence the It is often assumed that the posterior max- longevity of implants or compromise illa has ‘poor’ bone quality, based on thinner the results of bone augmentation. cortical plates and a less dense trabecular –– Patient compliance and their ability to structure, with increasing adipose content undergo the necessary surgical and towards the maxillary tuberosity region restorative procedures. giving a lower bone ‘density’. Some authors ●● Patient’s expectations in terms of aesthetics, suggest that implant placement in type 4 function, duration, and type of treatment. bone is associated with an increased failure ●● A detailed cost–benefit analysis that rate (Goiato et al. 2014). However, higher should be presented to the patient and rates of implant failure have also been include initial and maintenance therapies, reported in dense mandibular bone (van as well as the cost for the management of Steenberghe et al. 2003). complications for each clinical approach. Bone density in the posterior mandible can also be variable. When alveolar ridge width When the decision to extract a tooth with FI reduces following tooth loss, the cortical is taken, the clinical issues with placing an plates may become closer together, leaving a implant are largely centred on whether suf- smaller trabecular space between them. ficient residual alveolar bone remains for Conversely, a medullary compartment with the placement of an implant of adequate sparse trabeculation may be found, even in the length without the need for bone augmenta- presence of thick cortical plates, and achiev- tion. There are different anatomical consid- ing primary implant stability may be difficult. erations in each arch and conditions may The lower vascularity of bone with a have significant variance, even between dif- smaller trabecular compartment may result ferent sites in the same patient. These are in decreased oxygen tension in the bone and described later in the chapter, as are the a reduction in vital osteocytes, with a conse- subquestions regarding what constitutes quent effect on bone healing and osseo‐inte- ‘sufficient’ alveolar bone height and implant gration (van Steenberghe et al. 2003). length. However, there are publications that show little variation in implant survival rates in ‘poor’‐ or ‘good’‐quality bone, particularly if 11.2 Anatomical Considerations the implants have a micro‐roughened surface for implant Placement in the (Stanford 2010). Posterior Maxilla and Mandible It is possible that a significant confounding factor is the operator, in that it may be more 11.2.1 Bone ‘Quality’ difficult to achieve adequate primary implant stability in soft bone. On the contrary, oste- Leckholm and Zarb (1985) classified the otomy preparation may be more challenging concept of bone ‘quality’ into four subtypes in dense bone, and without careful tech- depending on the ratio of cortical to cancel- nique, sharp drills, and adequate cooling, the lous bone, and since then other classifica- bone may be overheated, causing local necro- tions of bone quality have been proposed. sis and rapid loss of initial mechanical However, bone quality is not only deter- implant stability, before the biological stabil- mined by the density of the cortical and ity achieved by new bone formation cancellous components. It is characterized has reached a sufficient state (Bashutski by a combination of factors, such as the et al. 2009). degree of vascularity and cellular vitality, the Excessive insertion torque of an implant quality of the collagen content and mineral placed in dense bone may also cause ‘com- crystal size, plus accumulated microscopic pression necrosis’ (Chrcanovic and Custódio damage and rate of bone turnover. 2009), with damage to the microvascular 212 Chapter 11
system and trabecular structure beyond the different sites in the same individual, and will physiological capacity of bone repair. Similar affect the possibility of implant placement mechanisms have been described in ortho- with or without bone augmentation. When a paedic surgery (Winwood et al. 2006). molar tooth with periodontal disease‐related Similar criticism has been applied to the bone loss to or beyond the root furcations is use of osteotomes in the posterior maxilla to extracted, a greater degree of pre‐extraction ‘improve’ bone density by condensation alveolar bone loss will have occurred, result- rather than drilling in soft bone (Blanco et al. ing in an even bigger osseous defect 2008). Compressing bone in this way does (Figure 11.1). not increase bone density, but may lead to a Alveolar ridge preservation is a treatment need for increased bone remodelling due to concept that could potentially reduce the trabecular damage that cannot be fully real- post‐extraction ridge dimensional changes ized due to microvascular damage. (MacBeth et al. 2017), decrease the clinical In conclusion, besides bone quality there need for additional ridge augmentation dur- are considerable site‐ and patient‐specific ing implant placement, and consequently variables that, together with operator experi- facilitate implant placement (Mardas et al. ence and skill, can have a significant impact 2015). These potential advantages, however, on the outcome of implant placement. may not directly apply to the molar regions, and the clinician should base their decision 11.2.2 Bone Loss and Implant on the accurate diagnosis of all local and Positioning patient‐related factors (i.e. tooth location, reason for extraction, treatment duration, It is an accepted fact that resorption and healing time, cost–benefit, and patient remodelling of the alveolar process takes expectations and preferences). place following the extraction of a tooth. The Post‐extraction alveolar resorption occurs relative volumes of alveolar and basal bone in an apico‐lingual direction, moving the loss will be subject to variation between crest of the ridge medially and reducing the different individuals and even between available vertical height of bone (Cawood
(a) (b)
Figure 11.1 (a) Left maxillary first molar affected by endodontic‐periodontal pathology. (b) Computed tomography (CT) scan taken after extraction, showing reduction of vertical height, as well as root residuals. Furcation: Why Bother? 213 and Howell 1988). The former may lead to a and orthodontic treatment with premolar tendency to place the implant too medially in extractions may result in mesial movement the bony ridge; the latter may create a of molar teeth, making the region more vis- tendency to place the implant at a deeper ible. While it may not be possible to avoid a vertical position than adjacent teeth in longer implant crown than adjacent teeth, bounded saddles, or complicate implant ‘filling’ the buccal corridor with the correct placement due to the proximity of important crown contour may be of aesthetic and anatomical structures. functional importance. It is no longer acceptable merely to place Bone loss renders certain anatomical struc- the implant into the available bone volume tures more superficial and this may create and attempt to restore this ‘as well as possi- problems for implant placement. In the max- ble’ once the implant is integrated. According illary molar regions, the main issue is the to the principle of ‘restoration‐driven implant degree of pneumatization of the maxillary placement’, the implant should be installed in antra; in the mandible, the position of the the correct position for the intended restora- inferior alveolar nerve and submandibular tion. Therefore, whatever the intended fossa are the relevant considerations. In clini- restorative outcome is, the optimal implant cal practice these anatomical limitations are position should be planned at the outset. usually managed with bone‐augmentation Furthermore, the ongoing maintenance of procedures or reduced‐length implants. peri‐implant tissue health should be an essential part of the pre‐operative planning, especially in patients who are clearly suscep- 11.3 Implant Placement in the tible to periodontal disease and therefore at a greater risk of biological complications. The Mandibular Molar Region pre‐operative implant restorative plan should be based on the following factors: Loss of vertical height of bone in the poste- rior mandible may occur following extrac- ●● The restoration being in the appropriate tion of mandibular multi‐rooted teeth. As position for a balanced occlusion. this process occurs, the residual crest of bone ●● The possibility of placing the implant such becomes closer to the mandibular canal. that it emerges through attached mucosa. Depending on individual site anatomy, this ●● The avoidance of lateral overhangs of the can commonly render the inferior alveolar restoration such as ridge‐lap, either of the nerve so superficial that implant placement implant‐supported crown or caused by can be difficult, or inadvisable. pink‐coloured gingivae imitating exten- Damage to the inferior alveolar nerve in sions of veneering material. These create the mandibular canal may occur by compres- stagnation areas, and may impede effective sion, penetration, or transection of the canal, oral hygiene by the patient and access for with either surgical drills or the implant peri‐implant probing for the clinician. itself. As the nerve exits the canal, there is ●● The avoidance of a significant vertical dif- also a risk of iatrogenic damage during flap ference between the bone crest of an adja- preparation, elevation, or retraction. cent tooth and the implant/abutment Careful pre‐surgical investigation is essen- interface, which may otherwise result in a tial, taking into consideration that there is a deep soft‐tissue pseudo‐pocket around the considerable degree of variation in the course implant, again creating a stagnation area. of the inferior alveolar nerve, including bifid ●● Even in the posterior region, aesthetics may canals, multiple canals, and multiple mental still be an issue. Maxillary molar‐to‐molar foramina (Carter and Keen 1971; Naitoh smiles are common, particularly in females, et al. 2009). 214 Chapter 11
Damage to the inferior alveolar nerve can The options available to the clinician for take many forms, with all but the most minor implant placement in resorbed mandibular carrying a significant risk of irreversible neu- molar sites are: ropathy (Seddon 1942). Consequent altered ●● Horizontal augmentation (where vertical sensation, often accompanied by neuropathic height is not an issue). pain, can cause a lifelong reduction in quality ●● Vertical augmentation. of life and significant psychological difficul- ●● Use of shorter implants. ties (Lam et al. 2003). It is important to realize that nerve dam- The technique of inferior alveolar nerve lat- age can occur even without actual penetra- eralization will not be discussed, as this is tion of the canal, via a compression injury neither a technique that is commonly used (neurapraxia) being compounded by due to a significant complication rate, nor for inflammatory oedema within the canal, or which there is a large body of clinical and bleeding that, as a consequence of the neu- scientific documentation. rotoxicity of haemoglobin, causes further Vertical bone‐augmentation techniques neural damage (Regan and Rogers 2003). have been described for many years, includ- Prompt and appropriate action must be ing onlay grafting and distraction osteogen- taken in the event of actual or suspected esis. However, the ability of these techniques damage; early intervention can reduce to predictably regenerate the desired vertical the risk of lifetime impact (Renton and bone volume is limited, both by anatomical Yilmaz 2012). and biological demands as well as the due to In cases of multiple tooth loss and extended practical difficulties often encountered by edentulous spaces, more advanced vertical the operator (Rocchietta et al. 2008). bone loss will also render the submandibular It is difficult to determine the efficacy of space more superficial. Within this space are different techniques due to the usual factors: branches of blood vessels, which, if damaged few studies, wide variation in techniques and by inadvertent perforation of the lingual materials, and a lack of appropriate measure- mandibular cortex, can cause significant ments, even in such basic matters as pre‐ and haemorrhage. In rare cases the airway may post‐augmentation bone levels (Keestra et al. be compromised to a life‐threatening degree 2016). (Niamtu 2001; Dubois et al. 2010). A similar criticism can be applied to lateral Accurate pre‐surgical clinical and radio- bone augmentation (Esposito et al. 2009). logical investigation is therefore para- Consequently, it is valid considering the mount, and an adequate safety margin must alternative of short or reduced‐diameter be maintained between the osteotomy implants. preparation and important anatomical features. 11.4 Bone Augmentation 11.3.1 Bone Augmentation for Implant Placement in the for Implant Placement in the Maxillary Molar Region Mandibular Molar Region The options available to the clinician for When there is inadequate vertical height of implant placement in resorbed maxillary bone over the inferior dental canal for the molar sites are: safe placement of dental implants, short‐arch or non‐implant‐supported restoration is ●● Horizontal augmentation (where vertical undoubtedly the most predictable option, height is not an issue). and should always be considered rather than ●● Subantral augmentation via a lateral risking iatrogenic nerve damage. antrostomy (classic ‘sinus lift’). Furcation: Why Bother? 215
●● Subantral augmentation via implant oste- (Timmenga et al. 2003). The general princi- otomy (variously called ‘osteotome tech- ple is that access to the antrum is created via nique’, ‘sinus tap’, and other monikers). an osseous window and the Schneiderian ●● Use of shorter implants. membrane is elevated intact, creating a subantral space into which a biocompatible 11.4.1 Horizontal Bone Augmentation scaffold can be inserted to conduct new bone growth, providing an adequate bed for The concept of horizontal (lateral) bone aug- implant placement. As with any surgical pro- mentation is well documented (Donos et al. cedure there is the potential for complica- 2008; Chappuis et al. 2017), with predictable tions; consequently, any surgeon performing outcomes provided that the basic tenets of the procedure should be properly trained guided bone regeneration are observed: and experienced, and able to deal with intra‐ and post‐operative complications. ●● Space maintenance and form shaping. The main complication leading to chronic ●● Blood clot stabilization. rhino‐sinus symptoms is the perforation of ●● Effective compartmentalization of the the Schneiderian membrane, with the poten- graft (prevention of soft‐tissue invasion). tial escape of graft materials into the sinus. ●● Adequate vascular and cell supply. Loss of graft compartmentalization may For the first and second requirements to be result in an inflammatory reaction, the loss satisfied, the graft material and the mem- of patency of the ostium (van den Bergh et al. brane have to possess sufficient rigidity to 2000; Wiltfang et al. 2000; Doud Galli et al. preserve the form of the graft and eliminate 2001), a compromised mucociliary transport micro‐motion. This could be achieved in system, and ultimately a potential need for three‐walled defects that can adequately graft removal with endoscopic sinus surgery. contain a particulate graft, or when a block of The reported incidence of membrane perfo- augmentation material or a semirigid and ration is from 10% to over 50% of cases reinforced membrane is used in cases of (Timmenga et al. 1997; Block et al. 1998; non‐space‐containing defects. Schwartz‐Arad et al. 2004; Pikos 2008; It is widely recognized that barrier mem- Pjetursson et al. 2008). There are many brane function is an essential component in authors who suggest that, up to a certain size, the achievement of a predictable outcome, repair of the ruptured sinus lining with a col- particularly when using particulate grafts. lagen membrane is possible (Becker et al. Any free graft has to have an adequate cell 2008); others question the efficacy of this and vascular supply to be viable. This is technique (Aimetti et al. 2001). largely derived from adequate adjacent Even without membrane perforation, there healthy bone. One therefore has to exercise is a certain incidence of post‐operative caution when considering the simultaneous chronic sinusitis in patients predisposed to placement of an implant, which has the rhino‐sinus disease (Timmenga et al. 1997). potential to form a barrier between the host An accurate medical history with relevant bone and the graft material, depending on questions is therefore important in patient defect morphology. assessment. There is evidence that certain osteocon- 11.4.2 Sinus Lift ductive bone grafts, like deproteinized bovine bone mineral, can provide a bone‐ The sinus lift technique was first described formation outcome as reliable as autogenous using a lateral antrostomy in 1980 by Boyne bone, which removes the need for a donor and James, and has since proved to be a safe site and simplifies the overall procedure con- and predictable procedure, with no lasting siderably (Handschel et al. 2009; Kim et al. effect on maxillary sinus health and function 2009). It seems that covering the antrostomy 216 Chapter 11
with a barrier membrane after graft place- situations of significant residual alveolar ment tends to result in a better implant prog- ridge height (rAH). When a perforation of nosis (Jensen and Terheyden 2009), perhaps the Schneiderian membrane was suspected, because to achieve the optimal restorative the implant was placed without any bone position, the implant tends to be placed as grafts to reduce the risk of sinusitis presented buccally as possible and the use of mem- by graft particles escaping into the sinus; branes appears to have a significant impact something that did not influence the implant‐ on the amount of soft‐tissue invasion into the related outcomes. lateral aspect of the graft (Choi et al. 2009). A significant determinant of implant suc- However, subantral augmentation does not cess using the osteotome technique is the replace the alveolar bone; it provides a differ- height of the rAH (Toffler 2004). As rAH ent volume of bone to facilitate implant decreases, the need for greater graft height placement. Depending on the degree of increases. This means a greater degree of lateral bone loss, implants placed into this membrane elevation, which may result in an bone bed may not be closely related to the increased rate of Schneiderian membrane positions of the missing teeth. Some clini- perforation (Nkenke et al. 2002; Velloso cians suggest that for implant placement to 2006). However, with this ‘blind’ approach it be appropriate for a fixed reconstruction, is not possible to reliably detect membrane lateral augmentation will also be required perforations (Ferrigno et al. 2006; Ardekian (Chiapasco and Zaniboni 2009). Lateral bone et al. 2006). Other risks associated with the grafting in such a situation will not always be osteotome technique include benign parox- practical, particularly if there are adjacent ysmal positional vertigo (Iida et al. 2000; teeth with bone loss: reconstruction of any Kaplan et al. 2003; Di Girolamo et al. 2005; vertical component of bone loss will be tech- Chiarella et al. 2008; Kim et al. 2010) and loss nically difficult and unpredictable. of the implant into the sinus where simulta- Implant survival rates are variously quoted neous implant placement is attempted as being equal to (61.7–100%, average 91.8%; (Galindo et al. 2005; Chiapasco et al. 2009), Wallace and Froum 2003) or slightly more var- or even several years after implant placement iable (73–100% for non‐ augmented sinuses, (Udea and Kaneda 1992; Iida et al. 2000). 36–100% for augmented sinuses on a patient Even if a reasonable degree of augmentation basis; 75–100% for both non‐augmented and material can be inserted via the implant oste- augmented sites on an implant basis; Graziani otomy without membrane perforation, bone et al. 2004) than those reported in the unaug- growth is known to be incremental from the mented posterior maxilla, suggesting that bony walls, since the vascular and osteoblastic variables such as implant type and operator cell supply derives primarily from there (Jensen experience are important factors. et al. 1998). It has been shown that there is sig- nificant remodelling of grafts placed using the 11.4.3 Osteotome‐mediated osteotome technique, and that actual bone Sinus Floor Elevation gain is limited to small amounts of additional bone on the walls of the implant, with little This technique was first described by bone at the apex after 12 months (Brägger et al. Summers (1998) and has since seen several 2004; Leblebicioglu et al. 2005). Furthermore, iterations of modifications, in a desire to occlusal load in the posterior maxilla is pri- simplify the process of subantral augmenta- marily borne by the cortical plates and dissi- tion. The basic theory is that the floor of pated to the palatal bone and zygomatic the antrum is elevated blindly, via the process (Gross and Nissan 2001; Gross et al. implant osteotomy, without perforating the 2001; Yacoub et al. 2002). The degree of bone Schneiderian membrane. Most of the reports contact on the implant is of course determined detailing this technique were performed in by available rAH, and also by the amount of Furcation: Why Bother? 217 graft; however, if that graft is not in contact Besides the technique’s extensive use, the with the walls of the sinus, contribution to ‘evidence’ supporting the osteotome‐mediated load‐bearing capacity is insignificant (Tepper sinus floor elevation has a significant degree et al. 2002). The quality of regenerated bone is of heterogeneity and drawing meaningful also important in reducing the stress in the conclusions is difficult (Tan et al. 2008). native bone, which could otherwise lead to Similar outcomes in terms of implant sur- crestal bone resorption (Fanascu et al. 2003). vival can be achieved with short implants, This has raised questions of whether there is and some authors have suggested that there a critical height of bone at which there is an may not be any harm in placing an implant advantage of the osteotome technique over the that penetrates the antral floor (Brånemark lateral window approach in terms of implant et al. 1984; Pierreisnard et al. 2003). survival. In a meta‐regression analysis of the Given the increased morbidity and overall two approaches, it was noted that there was a treatment time scale associated with the lat- correlation between bone height and implant eral window approach to sinus floor augmen- survival, with an rAH of 4 mm, in the lateral tation, and the doubt surrounding the value window approach. There was no correlation of the osteotome technique, it is highly rele- with the osteotome approach, but the rAH and vant to question the need for such additional implant survival rate were highly variable in surgery if it can be avoided. An example of the included studies, with many different tech- osteotome‐mediated sinus elevation and niques being used (Chao et al. 2010). implant placement is provided in Figure 11.2.
(a) (b)
(c)
Figure 11.2 (a) Left maxillary first molar affected by root fracture. (b) Implant placement was carried out three months after extraction, with the use of osteotome‐mediated sinus elevation associated with bone grafts. (c) An implant‐supported crown was placed three months later. 218 Chapter 11
11.5 Short Implants ultra‐short implants the available data are limited. One study showed that 6 mm long Dental implants with an infrabony length implants had an average survival rate of of ≤ 8 mm have been defined as short 93.7% following an observation period of at (Renouard and Nisand 2006), although least one year after placement (Srinivasan ‘ultra‐short’ implants are considered to be et al. 2014). those with lengths ≤ 6 mm (Deporter 2013). Short implants could be considered as a Short implants have been suggested as an valid treatment alternative to sinus floor aug- alternative to bone augmentation procedures mentation for the restoration of maxillary in the maxillary and mandibular posterior molars, provided that the residual height of segments, where the residual post‐extraction the alveolar ridge is ≥ 5 mm. The 16–18‐month bone volume is limited by anatomical struc- survival rate for short implants was similar to tures (maxillary sinus, mandibular canal), that of long implants placed in augmented but there is sufficient alveolar ridge width to sinuses (99% vs 99.5%; Thoma et al. 2015). The allow the use of standard implant diameters complication rate was significantly higher in of ≥ 3.75 mm. Short implants offer a less inva- patients receiving sinus aug mentation. sive treatment approach for patients who are Membrane perforation (Figure 11.3) was not able to undergo more complex bone‐ the most common complication, although augmentation procedures, thereby minimiz- this did not seem to compromise implant ing complication rates, morbidity, cost, and survival. duration of treatment (Nisand and Renouard Short implants may also be considered as 2014; Thoma et al. 2015). On the other hand, an alternative to simultaneous or staged ver- short implants will usually present a higher tical bone augmentation in the posterior crown‐to‐implant ratio, especially in cases mandible when the residual height of the with increased interarch distance that may alveolar ridge is ≥ 5 mm. Felice et al. (2014) lead to unfavourable loading conditions and reported similar survival rates but fewer more technical complications (Quaranta complications and peri‐implant crestal bone et al. 2014). It remains uncertain whether a loss with 6.6 mm short implants placed in high crown‐to‐implant ratio may lead to posterior maxilla in comparison to vertical excessive crestal bone loss and implant fail- augmentation after five years of loading. A ure (Garaicoa‐Pazmino et al. 2014). Various recent systematic review based on only four modifications in implant design, surface randomized controlled trials, mainly by the technology, and different implant insertion same group, concluded that similar survival methods have been suggested to address rates (95.1% vs 96.2%) and maintenance of these issues (Deporter 2013). Finally, the crestal bone level should be expected after clinical implications of peri‐implantitis on both procedures in the short term (Nisand implant prognosis may be more pronounced et al. 2015). The complication rate was again in the case of shorter implants compared to higher with vertical augmentation, where longer implants. temporary nerve paraesthesia was observed Systematic reviews present comparable in 56% of cases, in contrast to only 17% when mid‐term survival rates between short and short implants were used. Graft fracture, longer implants with moderate rough sur- inability to place long implants, and soft‐ faces (Annibali et al. 2012; Atieh et al. 2012). tissue dehiscence were other observed Most of the reported failures were predomi- complications. nantly early, with superior survival rates in Besides the encouraging short‐term results the mandible. However, short implants with in terms of survival rates, long‐term data on a reduced diameter (<3.75 mm) may have short implants as an alternative to sinus or higher failure rates (up to 10%) after 3–5 vertical bone augmentation are still lacking, years in function (das Neves et al. 2006). For and it remains unclear to what extent the Furcation: Why Bother? 219
Figure 11.3 Sinus membrane perforation occurred during lateral window sinus elevation approach and repaired with the use of a resorbable membrane. type of prosthetic restoration (single or The disease affects both soft and hard tissues splinted crowns, cantilevers) may influence around osseo‐integrated implants, leading to bone levels or implant survival. For this rea- bone loss and the formation of a peri‐implant son, it has been recommended that short pocket (Zitzmann and Berglundh 2008). The implants should be used only if bone quality prevalence of peri‐implantitis was reported is favourable, and that immediate loading to be of the order of 10% of implants and 20% and non‐working side occlusal interferences of patients (circa 5–10‐year follow‐up after are avoided. implant placement; Mombelli et al. 2012), and from 1 to 47% (estimated weighted mean [EWM] 22%, 95% confidence interval [CI] 11.6 Implant Biological 14–30%; Derks and Tomasi 2015). However, Complications the prevalence of peri‐implantitis was 39.3% at a patient level in patients with a history of Several longitudinal studies report implant periodontitis (Marrone et al. 2013), and survival rates ranging from 92.8 to 97.1% lower survival and success rates were over a period up to 10 years (Albrektsson and observed in these patients when compared to Donos 2012; Srinivasan et al. 2014), support- periodontally healthy individuals (Sousa ing the use of dental implants as a valid treat- et al. 2016). In addition, the severity and type ment option for the replacement of missing of periodontal disease appear to exert a nega- teeth. However, implant failures remain a tive effect on the rate of biological complica- possibility. Failures can be divided into bio- tions with dental implants (Mengel et al. logical (early or primary, and late or second- 2007; Gatti et al. 2008; De Boever et al. 2009; ary), mechanical, technical, iatrogenic, and Levin et al. 2011; Roccuzzo et al. 2014). those related to inadequate patient adapta- Other risk indicators strongly associated tion (Heitz‐Mayfield et al. 2014). with peri‐implantitis are smoking, excess The biological complications (and specifi- cement, poor oral hygiene, and lack of sup- cally peri‐implantitis) are usually the most portive periodontal therapy (Renvert and difficult to manage. Peri‐implantitis is a site‐ Quirynen 2015), whereas there is limited and patient‐specific, chronic infection that is evidence regarding the association between initiated by polymicrobial dysbiotic biofilms diabetes, alcohol consumption, and peri‐ (Edmiston et al. 2015; Hajishengallis 2015). implant diseases, with conflicting and limited 220 Chapter 11
evidence for the association with peri‐ the initial severity of disease, and defect mor- implant diseases and absence of keratinized phology may influence the outcome of non‐ mucosa, genetic traits, implant surface char- surgical and surgical therapies (Schwarz et al. acteristics, time of loading, and the position 2006, 2010; Sousa et al. 2016). Although there of the implant within the arch (Heitz‐ is evidence that some non‐surgical methods Mayfield 2008; Dereka et al. 2012; Renvert for implant surface decontamination may be and Polyzois 2015). effective at reducing the bacterial load, non‐ The therapy of peri‐implantitis is mainly surgical treatment is insufficient to treat peri‐ directed at the disruption and removal of the implantitis and does not lead to satisfactory biofilm, the resolution of inflammation, and clinical outcomes (Renvert et al. 2008, 2009). ultimately the arrest of disease progression A meta‐analysis of treatment outcomes has (Heitz‐Mayfield and Mombelli 2014). identified the main surgical procedures that Suggested therapies are based on well‐estab- are predominantly performed: access‐flap lished clinical protocols used for the treat- debridement; surgical resection; regeneration ment of periodontitis, including various with bone grafts; and guided tissue regenera- combinations of mechanical and non‐ tion (Chan et al. 2014). In the latter case, the mechanical debridement methods with or outcomes of regenerative therapy are reported without surgical access, and the use of adjunc- to vary the most. For this reason, several tive therapies such as antibiotics, antiseptics, clinicians often suggest implant explantation and laser treatments (Lindhe and Meyle 2008). as the only predictable approach for managing While the elimination of the bacterial patho- advanced peri‐implantitis, and advocate that gens and their remnants is vital for clinically prevention is the most effective way to man- stable outcomes, implant surface topography, age biological complications around implants.
Summary of Evidence
●● Dental implants are not an alternative to plexity, cost, and sometimes the treatment periodontal treatment of furcation‐ time and risk of complications. involved teeth, but rather a restorative ●● Short implants could be an alternative to solution when any other treatment to extensive vertical bone‐augmentation pro- maintain them in the dentition has failed cedures; however, their use has not been or is not indicated. adequately evaluated in the long term. ●● Loss or extraction of furcation‐involved ●● Biological complications and especially teeth usually results in extensive bone loss peri‐implantitis are quite common in that may complicate implant placement: patients with a history of periodontal in the maxilla due to sinus pneumatiza- disease. This risk should be extensively tion and in the mandible due to the posi- presented and discussed with the patient tion of the inferior alveolar nerve and before the extraction of teeth with furca- submandibular fossa. In clinical practice tion involvement and their replacement these anatomical limitations are usually with dental implants, acknowledging at managed with extensive bone augmenta- the same time the limitations of current tion procedures that increase the com- peri‐implantitis treatment modalities.
References
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Chapter 12
Is it Worth it? Health Economics of Furcation Involvement Falk Schwendicke1 and Christian Graetz 2
1 Department of Operative and Preventive Dentistry, Charité‐Universitätsmedizin Berlin, Berlin, Germany 2 Clinic for Conservative Dentistry and Periodontology, Christian‐Albrechts‐University, Kiel, Germany
12.1 Health Economic since they might determine the utilization Relevance of Furcation of services, with those who cannot afford Involvement treatment avoiding it, increasing existing health disparities (Zhong 2010). A growing number of patients keep the In general, systematic periodontal treat- majority of their teeth throughout their life, ment seems to allow long‐term retention of with even multi‐rooted teeth being retained. most periodontally compromised teeth In Germany, for example, around one‐third (Hatch et al. 2001; Loesche et al. 2002; Fardal of adults aged 65 years or older retain all et al. 2004; Chambrone and Chambrone their first or second molars (Jordan and 2006; Eickholz et al. 2008; Graetz et al. Micheelis 2016). This high number of 2017a,b, 2011, 2013, 2015; Johansson et al. retained teeth generates periodontal treat- 2013; Salvi et al. 2014). In many cases, such ment needs (Jordan and Micheelis 2016; retention of teeth in subjects with periodon- Holtfreter et al. 2010; Kassebaum et al. 2014). titis seems affordable, with costs for support- On the other hand, those who loose teeth are ive periodontal therapy (SPT) being limited more likely to have them replaced nowadays (Pretzl et al. 2009; Fardal and Grytten 2013; than in the past, mainly because the demand Schwendicke et al. 2016b). for replacements is growing while replace- In contrast, for multi‐rooted teeth with ment via implant‐supported crowns is widely furcation involvement (FI) – that is, mainly available (Micheelis and Schiffer 2006; compromised molars – long‐term retention Roos‐Jansaker et al. 2006). might be more difficult to achieve, with Both tooth retention and replacement survival times being possibly correlated with generate costs, which are relevant not only the degree of FI (Checchi et al. 2002; König for patients (when they bear them on their et al. 2002; Dannewitz et al. 2006a; Johansson own) but also for public or private insurers et al. 2013; Graetz et al. 2015), as discussed in (who need to weigh incurring costs against Chapter 5. As a result, more complex and the resulting health benefit and the demand expensive treatments and more frequent SPT from patients for such costly procedures; visits are often needed for retaining such that is, their justifiability in both the public teeth, which might have an impact on the and private domain). Treatment costs are costs of tooth retention (Pretzl et al., 2009; also relevant from an equity perspective, Lee et al. 2012; Schwendicke et al. 2014).
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
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Given the growing demand for retaining or such strict separation is done for health replacing molars and the wide availability of economic studies. both options in most developed dental set- ●● Cost‐utility analyses measure costs against tings, costs come into focus. In rationalized the resulting utility, like quality‐ or disabil- healthcare settings, where funding is limited ity‐adjusted life years. They involve the and competition for it between sectors is subjective value placed by someone (usu- high, it is important to quantify both the ally patients) on a certain health state. One costs of a disease and the cost‐effectiveness needs to elicit these utilities, which is not of different treatment options. For molars always easy and has not been widely done with FI, this means estimating the annual so far with regard to tooth values. (What is retention costs, and comparing them with the utility of a filled tooth against a sound the alternative costs for tooth replacement one? What that of a periodontally impaired via implant‐supported crowns, or fixed or but asymptomatic molar against a non‐ removal dental prostheses. Such cost estima- compromised molar?) tion should best account not only for perio- ●● Cost–benefit analyses transform effective- dontal but also endodontic, restorative, and ness or utility – that is, the health out- prosthetic treatments. Moreover, the func- come – into a monetary value. They tionality (or other kind of utility) of retained theoretically allow comparison of effort versus replaced or even missing furcation‐ and outcome on the same scale, but their involved molars needs to be known to weigh methodology is not fully accepted and has it against the expected costs. Last, the evalu- only very sparsely been applied in dentistry ation of costs and utilities (or any other so far. kind of health benefit) should be performed in time horizons relevant to payers and con- All these types of analyses can be performed sumers; that is, long term. in one of two ways. The first involves the (re‐)use of primary data, for example from cohort or controlled studies. For example, 12.2 Health Economic cohort studies allow estimation of the exact Analyses costs incurred for staff (via recording staff hours and factorizing them with the costs per hour for different staff) or materials (fac- Health economic analyses are typically torizing unit price and used units). This defined according to the evaluated outcome micro‐costing allows very detailed and real- (Vernazza et al. 2012): istic cost estimation. In addition, these stud- ●● Cost‐of‐disease studies investigate the ies can estimate the effectiveness of the required treatment efforts for managing or performed treatments (how long a tooth was resolving a disease or its symptoms. Such retained etc.). Randomized controlled trials costs are usually termed direct costs. Cost‐ also often collect cost data, allowing com- of‐disease studies further measure indirect parison of different treatment strategies (like costs (e.g. those for getting to the doc tor or scaling and root planing versus open‐flap dentist) and opportunity costs (e.g. those for debridement). not being able to work during this time). The second way also involves re‐use of ●● Cost‐effectiveness studies measure costs data, although not in the original framework against the effectiveness of a treatment. of a clinical study, but rather in a mathemati- Effectiveness usually means a clinical out- cal model. Modelling studies construct a come (survival time of a tooth, retention hypothetical path of a tooth or patients (‘the time of a restoration), as determined in a model’) reflecting the clinical (natural) path- real‐life setting or in rather artificial way. Teeth or patients can translate from one (randomized controlled) settings. Note to another health status (e.g. molar with FI that while the latter is termed ‘efficacy’, no without furcation caries → molar with FI Health Economics of Furcation Involvement 231 with furcation caries), with the chance of treatments, including subgingival debride- such translation depending on transition ment (Graetz et al. 2015). The therapeutic probabilities. For each translation, a treat- strategy for these molars was aimed at ment is assumed (e.g. application of fluoride improving access to furcations, allowing varnish to arrest a lesion, or restoration), regular individual and professional oral generating costs. Many of these models are hygiene in these areas (Figure 12.1). analysed via Monte Carlo micro‐simulations, Conservative scaling and root planing which allow parameter uncertainty to be (SRP) had been performed for molars with introduced. This is done via simulating a probing pocket depths (PPDs) < 5 mm with- number of patients (e.g. 1000), with transi- out bleeding on probing, and open‐flap tion probabilities (or other uncertain param- surgery including furcation debridement if eters) being randomly sampled from a certain PPD ≥ 5 mm plus bleeding or PPD ≥ 6 mm range of the parameter. The sampling of this regardless of bleeding was present (Kocher population is then simulated again for a and Plagmann 1999). Root‐resection therapy series of times (e.g. 1000), allowing estima- or tunnelling was mainly provided in molars tion of both the per‐patient and per‐popula- with advanced bone loss which had received tion variance. In general, such models allow endodontic treatment, as well as for molars investigation of several groups over a longer with furcation caries (Figure 12.2). time than most clinical trials (randomized Tunnelling was only performed for lower trials rarely follow up patients for decades), molars with both lingual and buccal FI degree with high validity given that most data are II, or FI degree III with limited access for oral from reviews and meta‐analyses. They have, hygiene, often combined with persistent however, limited applicability to other set- inflammation, if resection was not possible. tings than the one analysed, and are only as Different retrospective studies demonstrated valid as the assumptions made. They need long‐term stability for molars with such a validation via sensitivity analyses, assessing treatment strategy during regular SPT the impact the uncertainties have on the (Graetz et al. 2017b, 2013, 2015; Figure 12.3). finding of a study. Costs were assessed in the context of The available health economic studies on German healthcare. As such, any costs molars with FI are mainly cost‐of‐disease occurring to payers (regardless if this was the studies, with data collection in prospectively statutory insurance, the patient, or their pri- or retrospectively assessed cohorts, or cost‐ vate insurer) were estimated using fee items effectiveness studies, using models to dem- of German item catalogues. The authors onstrate the costs and cost‐effectiveness of quantified the resources provided based on different strategies of retaining or replacing the number of periodontal, restorative, furcation‐involved molars. endodontic, or prosthetic treatments, which had been ascertained via case records. Resources and fee item–based costs were 12.3 The Costs of calculated per tooth. Services provided to Furcation Involvement more than one tooth (e.g. examination, anti- biotics) were distributed among the teeth Several clinical studies have attempted to present. Items charged per tooth (like SRP) measure the costs of retaining furcation‐ were not distributed. involved molars. Most of these have followed The study (Schwendicke et al. 2016a) molars after successful active periodontal assessed 2306 molars in 379 patients (mean treatment (APT), which were regularly initial age 45.7, standard deviation [SD] retreated as part of the SPT. 10.0 years). The majority of molars (72.8%) For example, a German study retrospec- had no PPD > 4 mm after APT. Molars were tively assessed molars in patients who all had followed up for 16.5 (SD 6.8) years. Over this received initial or follow‐up periodontal period of SPT, a mean of 0.07 (SD 0.12) SRP (a) (b)
(c) (d)
Figure 12.1 Man, aged 42 years and non‐smoker, diagnosed with chronic periodontitis and horizontal bone loss in both jaws with furcation involvement degree II up to III (Hamp et al. 1975) on all first and second molars (a: initial status). He received scaling and root planing and open‐flap debridement of all posterior teeth. After 22 years of regular supportive periodontal therapy (b), endodontic treatment was required, with trisection of the upper right molars and prosthetic reconstruction being performed. Afterwards, furcation cleaning with interdental brushes (c) was possible. The situation remained stable for a further seven years (d, last observation).
(a) (b)
(c) (d)
Figure 12.2 Woman, aged 36 years and non‐smoker, diagnosed with aggressive periodontitis and horizontal bone loss in both jaws and furcation involvement degree III (Hamp et al. 1975) of all upper molars and tooth 14 (UR4), as well as degree II (Hamp et al. 1975) of all lower molars (a: initial status). Initial periodontal therapy with scaling and root planing was followed by open‐flap debridement of all premolars and molars. After re‐ evaluation, supportive periodontal therapy was commenced and after 1.5 years the buccal roots of all upper molars were resected and fixed dental prostheses provided (b). Two (c) and 17 years later (d), no further attachment loss was noted. Tooth 46 (LR6) had to be extracted due to a fracture.
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(a) (b)
Figure 12.3 Man, aged 47 years and smoker; chronic periodontitis and horizontal bone loss in both jaws with furcation involvement degree II (Hamp et al. 1975) on all upper molars and right lower molars, as well as degree III (Hamp et al. 1975) on all left lower molars (a: initial status). Open‐flap debridement of all molars, including tunnelling of the left lower molars, was provided. The patient stopped smoking after the 8th year during SPT. After 28 years of regular supportive periodontal therapy (b), the periodontal situation remained stable. had been prov ided per year (Table 12.1). €137.86 (SD 370.03). There was a significant Similarly, a mean of 0.04 (SD 0.11) flap association between these costs and smoking debridements (FD) had been provided per status (costs being higher in current smokers year. This number was increased in older than non‐smokers). subjects, molars with PPD ≥ 5 mm, mobile Another study assessed the tooth‐retention molars, and those with prosthetic treatment efforts in periodontally compromised but initially present. Resections had been mainly successfully treated subjects over 10 years of performed in upper molars, molars with SPT, again within German healthcare (Pretzl mobility grade 3, FI degree III, bone loss, and et al. 2009). This study found that 0.34 SRP those with endodon tic treatment, periapical had been provided over the 10 years (includ- lesions, or previous prosthetic treatment. ing the first SRP). What can be seen from Few molars received endodontic, restorative, both studies is the low number of treatments or prosthetic treatments, with prosthetically needed to retain compromised molars. Total restored molars being more likely to receive periodontal treatment costs for tooth reten- endodontic therapy or prosthetic retreat- tion ranged between €6 and €13, which is low ment. The last component assessed was SPT, given the costs of alternative options (like with a mean of 2.49 (SD 0.12) SPT visits per implants or fixed dental prostheses). What year and per patient. was further shown was that periodontal Based on these estimates for the resources treatment costs made up around two‐thirds used, annual costs per molar were €18.28 (SD of the total long‐term costs; that is, most 16.91) for all treatments and €13.04 (SD 9.58) molars did not generate significant costs for for periodontal treatments only (Table 12.2). endodontic or restorative treatment (furca- The robustness of these estimates was dem- tion caries, for example, was found in only onstrated by calculating costs for patients 2% of teeth over the whole observation with different health insurances (which period). In both studies, the periodontal allows for different charges being claimed by treatment efforts were higher in teeth with dentists). Total treatment costs increased bone loss, severe FI, prosthetic abutment sta- significantly for molars with FI, PPD ≥ 5 mm, tus, and maxillary molars, but not patients bone loss, endodontic or prosthetic treat- with aggressive versus chronic periodontitis. ment, and periapical lesions. If analysed on a Practitioners should be aware of these patient level, mean costs per year were predictors, as they determine not only the Table 12.1 Mean ( SD) number of treatments provided per year of retention. Differences of number of treatments between groups are indicated in bold (p < 0.05, ANOVA). For more than two groups, different superscript letters indicate a significantly different number of treatments according to the Bonferroni post‐hoc test (p < 0.05).
Deep scaling/ Surgical flap Supportive Endodontic Restorative Prosthetic Parameter N root planing debridementRoot resection therapy treatment treatment treatment
Patients’ age at T0 <50 7380.09 (0.17) 0.04 (0.09) 0.01 (0.04)2.48 (0.12) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) ≥50 15680.06 (0.08) 0.05 (0.12) 0.01 (0.04) 2.51 (0.12) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) Gender Male 950 0.07 (0.10) 0.04 (0.12) 0.01 (0.05) 2.48 (0.12) 0.01 (0.05) 0.00 (0.01) 0.01 (0.03) Female 1356 0.07 (0.10) 0.04 (0.11) 0.01 (0.03) 2.49 (0.13) 0.01 (0.03) 0.00 (0.01) 0.01 (0.03) Diagnosis Aggressive periodontitis 453 0.07 (0.13) 0.04 (0.12) 0.01 (0.03) 2.49 (0.10) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) Chronic periodontitis 1853 0.06 (0.09) 0.05 (0.09) 0.01 (0.04) 2.49 (0.10) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) Number of teeth at T0 ≥24 1760 0.06 (0.12) 0.04 (0.10) 0.01 (0.03) 2.49 (0.10) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) <24 546 0.08 (0.12) 0.05 (0.11) 0.01 (0.06) 2.50 (0.10) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) Smoking status Non‐smoker 1458 0.07 (0.09) 0.04 (0.10) 0.00 (0.04) 2.48 (0.11) 0.01 (0.04) 0.00 (0.01) 0.01 (0.03) Former smoker 547 0.07 (0.13) 0.05 (0.15) 0.00 (0.06) 2.49 (0.15) 0.01 (0.04 0.00 (0.01) 0.01 (0.03) Smoker 301 0.07 (0.10) 0.05 (0.11) 0.00 (0.02) 2.50 (0.11) 0.01 (0.02 0.00 (0.01) 0.01 (0.03) Jaw Maxilla 1108 0.07 (0.14) 0.05 (0.11)0.01 (0.06) 2.49 (0.13) 0.01 (0.05) 0.00 (0.01) 0.01 (0.03) Mandible 1198 0.07 (0.09) 0.03 (0.11)0.00 (0.02) 2.48 (0.12) 0.01 (0.03) 0.00 (0.01) 0.01 (0.03) Maximum PPD at T1 <5 mm 16780.06 (0.08) 0.03 (0.108) 0.01 (0.03) 2.47 (0.09) 0.01 (0.03) 0.00 (0.01) 0.01 (0.03) ≥5 mm 6280.09 (0.19) 0.08 (0.16) 0.01 (0.06) 2.52 (0.17) 0.01 (0.05) 0.00 (0.01) 0.01 (0.03)
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Table 12.2 Mean (SD) periodontal and total treatment costs per retention year. Base case (privately insured patient) and sensitivity (publically insured patient) analyses are shown. Differences of costs between groups are indicated in bold (p < 0.05, ANOVA). For more than two groups, different superscript letters indicate significantly different costs according to the Bonferroni post‐hoc test (p < 0.05).
Base case analysis Sensitivity analysis
Total Periodontal Periodontal treatment treatment costs Total treatment treatment Parameter N costs per year per year costs per year costs per year
Patients‘ age at T0 <50 738 19.45 (17.71) 13.74 (11.98) 21.08 (21.77) 15.99 (16.66) ≥50 1568 17.70 (16.52) 12.62 (8.22) 18.44 (17.22) 14.05 (10.23) Gender Male 950 17.44 (16.83) 12.61 (7.25) 18.48 (16.91) 14.18 (8.66) Female 1356 18.82 (16.90) 13.26 (10.90) 19.83 (19.99) 15.01 (14.84) Diagnosis Aggressive periodontitis 453 17.11 (13.64) 13.25 (6.41) 18.15 (13.99) 14.81 (7.99) 18.51 (17.59) Chronic periodontitis 1853 12.93 (10.25) 19.55 (19.79) 14.64 (13.52) Number of teeth at T0 ≥24 1760 17.33 (16.20) 12.61 (8.99) 18.23 (17.99) 14.10 (14.66) <24 546 21.19 (18.74) 14.20 (11.23) 22.82 (20.91) 16.55 (14.97) Smoking status Non‐smoker 1458 18.33 (17.51) 12.91 (10.39) 19.32 (19.82) 14.58 (14.14) Former smoker 547 17.64 (16.51) 13.28 (8.97) 19.10 (18.29) 15.07 (10.82) Smoker 301 18.73 (14.49) 12.90 (5.89) 19.40 (14.02) 14.41 (6.55) Jaw Maxilla 1108 19.04 (18.49) 13.60 (11.12) 20.51 (21.19) 15.56 (15.00) Mandible 1198 17.50 (15.33) 12.50 (7.86) 18.15 (16.27) 13.88 (9.91) Maximum PPD at T1 <5 mm 1678 17.34 (15.69) 12.38 (9.26) 17.96 (17.12) 13.82 (12.49) ≥5 mm 628 20.62 (19.50) 14.71 (10.32) 22.92 (22.33) 16.96 (12.98) Mobility at T0 a a a a 0 1833 17.33 (14.27) 12.38 (6.49) 17.96 (14.60) 13.82 (8.60) a b b b 1 332 21.12 (21.17) 14.41 (12.23) 22.82 (23.39) 16.61 (15.78) a b b b 2 77 21.00 (22.45) 15.59 (13.01) 23.27 (26.46) 17.29 (14.03) b c c c 3 64 26.98 (37.77) 20.12 (32.67) 37.01 (54.486 27.77 (47.66) FI at T1 a a a a 0 1105 16.50 (13.27) 11.95 (6.75) 17.04 (14.69) 13.19 (8.91) a a a b 1 652 16.72 (11.72) 12.49 (5.12) 17.64 (11.36) 14.00 (6.45) b b b b 2 356 20.60 (16.99) 14.20 (9.07) 22.06 (18.29) 16.04 (11.14) c c c c 3 193 29.07 (35.69) 18.64 (23.59) 33.69 (42.37) 23.35 (32.62) Health Economics of Furcation Involvement 237
Table 12.2 (Continued)
Base case analysis Sensitivity analysis
Total Periodontal Periodontal treatment treatment costs Total treatment treatment Parameter N costs per year per year costs per year costs per year
Bone loss at T0 a a a >50% 980 19.71 (19.25) 14.28 (13.02) 21.74 (23.54) 16.55 (17.51) b b b 25‐50% 882 17.68 (16.47) 12.51 (6.49) 18.15 (16.14) 13.81 (8.12) b b b <25% 444 16.15 (11.00) 11.16 (3.23) 16.25 (9.13) 12.34 (3.55) Endodontic treatment Not present 2163 17.52 (14.84) 12.50 (6.23) 18.25 (15.09) 13.83 (7.42) Present 143 29.28 (33.97) 21.20 (28.77) 35.84 (45.82) 27.95 (40.89) Peri‐apical lesion Not present 2243 17.70(14.66) 12.74 (7.68) 18.67 (15.92) 14.28 (9.78) Present 63 36.19 (49.92) 22.15 (34.36) 42.75 (60.09) 29.50 (49.65) Prosthetic treatment Not present 1460 13.80 (12.71) 12.99 (10.05) 15.90 (17.53) 14.58 (13.30) Present 846 25.91 (20.25) 13.04 (8.89) 25.14 (19.43) 14.81 (11.41)
ANOVA = analysis of variance; FI = furcation involvement; N = number of molars; PPD = probing pocket depth; SD = standard deviation; T = time. chance of clinical success, but also the efforts indicates not only periodontal treatment needed to ensure this success, and should needs, but also the necessity of retreating guide decision making towards retaining prosthetically (due to caries, fractures, or replacing teeth. It should be noted that porcelain chippings) or endodontically prosthetically involved molars were generally (Goodacre et al. 2003; Walton 2013; see also found to be more expensive to retain, which Figure 12.4).
(a) (b) (c)
Figure 12.4 First lower molar with furcation involvement degree III (Hamp et al. 1975) after treatment with tunnelling for cleaning at home (a). The situation remained stable for over 9 years (b), while after 13 years (c) a carious lesion in the furcation developed, leading to endodontic involvement and, eventually, extraction. 238 Chapter 12
Such increased risks of reinterventions for costs (Yi et al. 1995; Lulic et al. 2007; Fardal prosthetically restored teeth was shown and Linden 2010; Graetz et al, 2013; see also mainly if prosthetics had been placed prior to Figure 12.5). periodontitis treatment (Pretzl et al. 2008; Overall, the very limited available evi- Graetz et al. 2013), while prosthetics inserted dence finds retention of FI molars to require after successful initial therapy and during more effort than non‐molar or non‐FI teeth, systematic SPT were not necessarily found which has impacts on the costs required for to generate more treatment efforts and retention. This is truer in molars with severe
(a)
(b) (c)
(d) (e)
Figure 12.5 Man, aged 59 years and non‐smoker, diagnosed with generalized chronic periodontitis and horizontal bone loss up to one‐quarter of the root length in both jaws and furcation involvement degree I (lower molars) and II (upper molars) (Hamp et al. 1975) (a and b). Initial periodontal therapy using scaling and root planing followed by open‐flap debridement of all pre/molars with extraction of tooth 17 (UR7) (as a result of a root carious lesion) was provided. After re‐evaluation, a regular supportive periodontal therapy was started and after one year a fixed dental prosthesis was fitted. Seven years later, tooth 11 fractured (c) and a fixed dental prosthesis was provided in the front (d). This situation remained stable for 29 years (e, last observation). Health Economics of Furcation Involvement 239 furcation involvement (FI degree III), The study simulated an initially 50‐year‐ but not necessarily for FI degree I. More old male patient with an average remaining important, however, is the fact that overall life expectancy of 29.7 years. The model used retention costs were very limited, with only consisted of the initial and various follow‐up a few euros per year being required to retain health states (Figure 12.6), simulating the such molars. Based on this finding, it is now natural history of a periodontally affected relevant to compare these costs with those tooth or an ISC. generated by other, alternative treatments. As to the costs assessed, the following assumptions had been made: 12.4 Cost‐effectiveness of ●● All initial therapies comprised full case Retaining Furcation‐involved assessment including oral hygiene assess- Molars ment, advice and motivation, radiographs, scale and polish, re‐evaluation, and the necessary treatment as already outlined, There are only very few data comparing the including anaesthesia, possible endodon- cost‐effectiveness of different strategies to tic, surgical, or prosthetic procedures, and retain molars with FI. One recent study short‐term post‐operative care. (Schwendicke et al. 2014) used a mathemati- ●● Supportive periodontal or implant treat- cal model to assess the cost‐effectiveness of ment involved biannual re‐revaluation, treatment alternatives for periodontally scale and polish, subgingival retreatment, affected, vital molars with furcation FI, com- and antiseptic irrigation, as well as radio- paring tooth‐retaining strategies with tooth graphic reassessment every two years. For removal and replacement via implant‐ teeth but not implants, fluoridation of root supported crowns (ISCs). Categories of surfaces was assumed to be additionally tooth‐retaining strategies were performed. ●● Conservative, non‐surgical furcation ther- ●● Modelling involved fatal complica- apy involving SRP. tions – that is, those leading to loss of the ●● SRP with surgical access (i.e. FD). tooth or implant (for example periodontal ●● For teeth with FI degree II or III, root complications or untreatable root caries, resection (RR; i.e. hemisection, trisection, or untreatable peri‐implantitis or implant or amputation), as well as fracture, respectively) – and non‐fatal ●● Guided tissue regeneration (GTR, including complications – for instance treatable insertion of bone‐substitute material and caries at restoration margins, treatment‐ placement of a resorbable membrane), and responsive peri‐implantitis, or loss of ●● Tunnelling (TU, for mandibular molars crowns or abutments. Mending of compli- only). cations was assumed to generate costs, and involved repair or renewal of restorations, Tooth‐retaining strategies were compared recementation or refixing of crowns or with the removal and replacement of teeth abutments, and peri‐implant treatment via ISCs. (Mombelli and Lang, 1998). This study assessed cost‐effectiveness as lifetime treatment costs (initial plus follow‐ For molars with FI degree I, SRP was both less up treatments) per retention time of the costly and more effective than ISC. Compared tooth or implant (in years). All analyses were with FD, ISC was always more costly, but also performed separately for molars with FI more effective (i.e. implants were retained degree I, lower molars with F degree II/III, longer). Regardless of the dental arch, treat- and upper molars with FI degree II/III, again ing molars with FI degree II/III via tooth‐ in the context of German healthcare. retaining options was found to be more 240 Chapter 12
Molars with Fl I Molars with Fl II or Ill
SRP FD ISC RR GTR TU
Periodontal/Endodontic/ Technical/Biological Periodontal/Endodontic/Restorative Restorative Complications Complications Complications
RCT Refill/repair/ CIST Recement/ RCT Refill/repair/ crown -crown crown
Tooth loss Implant loss Tooth loss
Replace with ISC Replace with ISC Replace with ISC
Figure 12.6 State transition diagram. Molars with furcation involvement (FI) degrees I and II/III were analysed separately, with different treatments being compared. All periodontal treatments were compared with implant‐supported crowns (ISC). For all teeth, periodontal, endodontic, and restorative complications were modelled, with fatal (leading to tooth loss) and non‐fatal (mendable) complications being simulated separately. For implants, we modelled technical (loss of crowns, abutment fracture, implant fracture) and biological complications (peri‐implantitis), again with separate simulation of fatal and non‐fatal failures. If complications were mendable, teeth and implants were allocated to follow‐up treatments, which generated costs. In case these treatments were not final, i.e. another retreatment was possible (for example re‐restoration after repair), this was modelled as well. Eventually, lost teeth or implants were assumed to be replaced using implant‐supported crowns. Note that within base case analysis, all failed teeth or implants were assumed to be (re‐)replaced. To explore the effects of this assumption, sensitivity analyses were performed. CIST = cumulative supportive interceptive therapy; FD = flap debridement; GTR = guided tissue regeneration; RCT = root canal treatment; RR = root resection; SRP = scaling and root planing; TU = tunnelling.
effective and less costly than tooth removal This finding is in line with a number of and replacement via ISC (Figure 12.7). observational studies from another health- This cost‐effectiveness ranking – with care setting as well (Fardal and Grytten 2013; implants being more costly than tooth‐ Martin et al. 2014). retaining strategies – did hold even under More specifically, it is unlikely that remov- the worst‐case assumptions modelled, and ing and replacing molars with FI degree I will was also stable regardless of how costs were be cost‐effective (the 10‐year survival rate for estimated. molars treated via SRP and SPT was 97% in Retaining teeth was significantly less costly this study). This is in line with FI degree than removing and replacing them, mainly as I being found to have only limited impact on ISCs are so costly initially, but also as retreat- tooth success when compared with FI degree ments on ISCs (which are not needed very 0 (Salvi et al. 2014; Graetz et al., 2015), but frequently) are relatively costly. For example, also to only limited impact on required treat- treating peri‐implantitis is not only challeng- ment efforts (as has been shown already and ing but costly, as is mending non‐biological in Tables 12.1 and 12.2). FD seems less effec- complications (ceramic chippings, crown de‐ tive than ISCs, while being more costly than cementations, fractures), which usually SRP. It is therefore doubtful if such a strategy involve costly materials and often generate can be more cost‐effective than SRP in molars further staff costs for dental technicians. with FI degree I (Heitz‐Mayfield et al. 2002). Health Economics of Furcation Involvement 241
(a) (b) 2500 ISC 2500 GTR ISC 2100 ISC 2100 RR FD 1700 1700 ISC 1300 SRP 1300 RR Cost in Euro FD Cost in Euro SRP 900 900 GTR 22 24 26 28 30 22 24 26 28 30 Effectiveness in years Effectiveness in years
(c) 2500 ISC GTR ISC 2100 RR TU 1700 RR
1300 GTR Cost in Euro TU 900
22 24 26 28 30 Effectiveness in years
Figure 12.7 Cost‐effectiveness of different strategies to treat molars with furcation involvement (FI). For FI degree I, we compared conservative scaling and root planing (SRP) and flap debridement and SRP (FD) with implant‐supported crowns (ISC). For molars with FI degrees II or III, root resection (RR), guided tissue regeneration (GTR), and tunnelling (TU, for lower molars) were compared with ISC. The presented cost‐effectiveness planes (a, b, c) demonstrate the discounted lifetime costs (y‐axis) per effectiveness (in years of tooth or implant retention). In the case of FI degree I (a), SRP was more effective and less costly than ISC, while FD was both less effective and less costly than ISC. For upper (b) or lower (c) molars with FI degree II or III, ISC was dominated by all tooth‐retaining strategies.
In general, there is debate around the cost‐ already – RR might be mainly applied to effectiveness of FD versus SRP, as the effec- molars which had received endodontic tiveness gain seems limited (also in non‐FI therapy earlier) and crown placement degree I teeth) while the additional costs are (Carnevale et al. 1991; Huynh‐Ba et al. 2009; substantial (Antczak‐Bouckoms and Schwendicke et al. 2013). When considering Weinstein 1987). There is, however, some the range of estimated survival rates for indication that the need for maintenance RR – 91% after 10 years in Schwendicke et al. visits seems reduced after FD compared with (2013); 93% after 3.5 years in Helldén SRP, which could offset initially higher treat- et al. (1989); 68% after 10 years in Blomlöf ment costs (Miremadi et al. 2015). et al. (1997); and 83% after 7 years in There is greater uncertainty as to how best Little et al. (1995; reviewed in Chapter 8), it to treat molars with FI degree II or III (or remains uncertain whether the high costs whether to replace them). Treatment options for RR are truly justified. have been discussed extensively in this book What is clear from the existing studies is (mainly in Chapters 7, 8, and 9). RR espe- that one cannot really attempt to compare cially was relatively costly, as costs occur not most periodontal treatments with one only for the periodontal procedure, but also another, since their indications differ (RR will root canal treatment (note that – as dis cussed not be applied to the same teeth as SRP etc.). 242 Chapter 12
What should be further borne in mind is retained teeth, which would allow different that different periodontal treatments strategies to be properly compared. require different degrees of patient motiva- tion and compliance. For example, tunnel- ling might require highly motivated patients 12.5 Research Gaps to maintain the tunnel and prevent root caries (Hamp et al. 1975). That said, doubts Adhesive dentistry increases the number of remain regarding the postulated high risk options for dealing with furcation‐involved of caries within tunnels (Little et al. 1995; teeth. Splinting of different teeth or (resected) Dannewitz et al. 2006b; Feres et al. 2006), as roots, or even using extracted teeth as was seen in the German cohort study dis- adhesive bridge pontic, has been performed cussed, which reported such caries in only not only in the anterior region, but also 2% of molars over 16.5 years (Schwendicke posteriorly (Figures 12.8 and 12.9). Clinical et al. 2016a). Lastly, retention and replace- experience allows the hypotheses that using ment are not the only viable options for glass fibre–enforced ribbons could allow treating molars with FI; shortened dental similar retention periods to be achieved to arches might also yield sufficient function- conventional adhesive (Maryland) bridges ality and subjective oral health (Wolfart used normally in the front, with similar et al. 2014), while generating limited initial complications of debonding and fracture and long‐term costs (Faggion et al. 2011; (Miettinen and Millar 2013). However, Wolfart et al. 2012). Here again, the availa- reliable efficacy data and any data on cost‐ ble data are insufficient to assign monetary effectiveness or the value patients place on or utility values to missing, replaced, or such treatments are missing at present.
(a) (b)
(c) (d)
Figure 12.8 Man, aged 46 years, with generalized chronic periodontitis after extraction with immediately re‐fixation of tooth 31 (LL1) (a, b: before extraction) and long‐term stability of the situation during supportive periodontal therapy over 10 years (c, d). Health Economics of Furcation Involvement 243
(a) (b) (c)
(d) (e) (f)
Figure 12.9 Woman, aged 47 years, with generalized chronic periodontitis and root resorption of the mesial root of tooth 46 (LR6) (a). After successful endodontic treatment and resection of the mesial root (b), a fibre‐ enforced pontic was directly placed (c), allowing splinting of teeth 46 and 45 (LR5). Long‐term stability was achieved during supportive periodontal therapy over 11 years (d–f).
In general, there are growing data on cost‐ A range of study types has been employed in effectiveness, largely stemming from either this field, mainly to describe the costs of cohort or modelling studies. Recording of retaining these molars, but also to compare efficiency data alongside randomized trials is the cost‐effectiveness of different retention not common at present and can be recom- and replacement strategies. Based on these mended. Cost–utility or cost–benefit analy- studies, retaining molars with FI might ses are even less common, mainly since the require more effort than retaining non‐FI subjective value that patients place on single teeth. However, the resulting annual treat- retained, replaced, or missing teeth is not ment costs are nevertheless very limited. known at present. The larger proportion of these costs is for periodontal, not other (restorative, endodon- tic, prosthetic) treatments. There are a 12.6 Conclusions number of factors which are associated with greater effort being needed, resulting in Given both the demographic changes in higher costs, like bone loss, severe FI, mobil- many rich countries as well as the epidemio- ity, or status as prosthetic abutment. Dentists logical shift in older populations – who retain should consider these factors in treatment more teeth than ever before – retaining decisions. If comparing different strategies molars with FI is highly relevant from a pub- for managing molars with FI, tooth retention lic health and health economic perspective. seems probably less costly than tooth 244 Chapter 12
replacement via ISC. This is mainly because tain treatments (which are, for example, very implant placement but also maintenance is high for implants). Instead, they should con- relatively costly compared to costs for tooth sider the long‐term consequences and extent retention. of possible retreatments, as well as their feasi- In conclusion, dentists should not focus only bility and costs. Retaining molars with FI is on the reported success or survival rates of cer- likely to be both achievable and cost‐effective.
Summary of Evidence
●● Teeth with furcation involvement (FI) can ●● However, removing and replacing teeth be retained in the long term, but at higher using implant‐supported crowns does not costs than teeth without FI. seem to be less costly. ●● These costs increase with higher degrees ●● Dentists should consider these risk factors of FI, bone loss, and mobility. and the required treatment needs for plan- ning the retention or removal of teeth.
References
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Chapter 13
Deep Gaps between the Roots of the Molars: A Patient’s Point of View Luigi Nibali
Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK
13.1 Introduction 13.2 Patient‐reported Outcome Measures Dentistry is moving towards a more patient‐ in Periodontology centred approach, with more attention paid to the patient’s point of view and striving Socio‐environmental measures such as func to improve the patient’s quality of life. tion and psychological well‐being have been Ultimately, as treating clinicians we should applied to dentistry in the last few decades realize that reduction of probing pocket (Locker 1988). These measures aim to assess depths and bleeding on probing are just sur parameters related to the impact of oral rogate measures of disease progression and health which are not objectively measurable they do not necessarily mirror the patient’s by the treating clinician. The World Health aims and needs. Furthermore, every patient is Organization (WHO) defines quality of life different and what works for one patient may as individuals’ perception of their position in not work for another. However, it is interest life in the context of the culture and value ing to note how most studies in the periodon systems in which they live and in relation to tal literature have focused so much on clinical their goals, expectations, standards, and con measurements, leaving aside aspects such as cerns (WHOQOL Group 1994). It is a broad‐ costs and effects on the patient’s quality of ranging concept affected in a complex way by life. Equally, previous chapters of this book the person’s physical health, psychological have focused on clinical parameters, bone state, level of independence, social relation levels, and ‘success’ as defined by the treating ships, personal beliefs, and relationship to periodontist, but not based on the patient’s salient features of their environment. The perceptions. This chapter aims to review American Dental Association emphasized studies focusing on patient quality‐of‐life the importance of quality‐of‐life measures by measures relative to furcation involvement. stating: ‘Oral health is a functional, struc Given the paucity of data on this, anecdotally tural, aesthetic, physiologic and psychosocial the feedback from some patients treated for state of well‐being and is essential to an furcation involvement will be presented, in individual’s general health and quality of life’ order to give the reader a perspective from (Glick and Meyer 2014; Glick et al. 2017). people who are on the receiving end of the Over the last decade, patient‐reported out treatment discussed in this book. come measures (PROMs) have increasingly
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
been recognized as a research priority and naire (EQ‐5D‐5 L) is a measure of HRQoL incorporated in periodontal research studies including self‐assessments of mobility, pain/ (Aslund et al. 2008; Buset et al. 2016). PROMs discomfort, self‐care, anxiety/depression, are defined as standardized measures used to and usual activities, recorded by patients on capture the subjective effect of a disease or an ordinary scale with five levels (Herdman treatment on a patient’s life, including daily et al. 2011). It is unclear whether the valua activities and well‐being (US Department of tions would refer to periodontal disease or to Health and Human Services et al. 2009). any other condition coexisting in the same Health‐related quality of life (HRQoL) and person (or their combination, for that mat oral health–related quality of life (OHRQoL) ter). Using the EuroQol Questionnaire, a are often used as measures of PROMs in cross‐sectional study on a random sample of medicine and more specifically dentistry. 709 45‐ to 54‐year‐old Australians was able While the related questionnaires provide to differentiate the impacts of varying degrees data about health or disease status (struc of periodontal diseases (from gingivitis to ture/function/activity/participation), other periodontitis; Brennan et al. 2007). For exam questionnaires such as the Oral Impacts on ple, having a pocket depth of ≥ 6 mm was Daily Performance (OIDP) and the Oral associated with a prevalence of pain/discom Health Impact Profile (OHIP‐14) assess fort in 25.8% of cases, compared with 6.1% the impacts of oral diseases on daily life pain/discomfort for patients with gingivitis. (disease prevention/dysfunction/failure) in a In a separate study, when OHIP‐14 and OIDP pre‐determined period (Adulyanon et al. structured interviewer‐administered ques 1996; Slade 1997). These are generic tionnaires, global self‐report, and perceived OHRQoL measures, so they are not specifi need for dental treatment questions were cally designed for patients with periodontitis. administered to 264 patients, the majority In other words, they measure the oral (61.0%) rated their oral health status poorly impacts of oral conditions in general, not and 203 (76.9%) perceived a need for treat attributing them to particular diseases/ ment, highlighting the importance of patient‐ conditions. However, they have been used driven treatment needs (Lawal et al. 2015). in studies of periodontal patients with A systematic review on the impact of the underlying – but largely untested – periodontitis on OHRQoL suggested that, assumption that in such a patient sample although most studies showed a negative most of the reported oral impacts would be impact of periodontitis, it is difficult to draw due to that specific oral condition; that is, a definitive conclusions due to the heterogene periodontal condition in this case. Among ity of methods and reporting and confound the generic OHRQoL measures, the OIDP ing by other oral conditions (Al‐Harthi allows also for a condition‐specific version, et al. 2013). A more recent systematic review whereby patients attribute the reported oral found a relationship between clinical perio impacts to specific ‘causes’, in other words dontal disease extent and severity and conditions. Furthermore, while most of these OHRQoL (Buset et al. 2016). No specific measures assess the frequency of oral impacts studies on furcation treatment were detected (i.e. how often they were experienced), the among those included in these reviews. OIDP measures both the frequency and the Some studies have attempted to investi severity of oral impacts. Despite their differ gate the effects of periodontal treatment on ences, all these questionnaires tend to focus patient‐centred outcomes. In a study on per on covering the physical, psychological, and iodontitis patients in the UK, the OIDP social aspects of the oral impacts on daily life. index was administered to 45 patients at The relevant literature goes beyond the baseline and one month after treatment oral health field and extends to generic (Tsakos et al. 2010); 17 of the patients HRQoL measures. The EuroQol Question received intensive and 28 received A Patient’s Point of View 251
‘conservative’ periodontal care. Both the 87 patients with chronic periodontitis assessed generic and condition‐specific versions of OHRQoL with two different generic meas the OIDP for periodontal conditions were ures: the General Oral Health Assessment used, and one of the aims of the study was to Index (GOHAI), which assesses the presence estimate the minimally important difference of symptoms, and the UK oral health‐related for this measure among periodontal patients. quality‐of‐life measure (OHQoL‐UK), which The mean OIDP score after treatment was assesses the impact of oral health using significantly lower than at baseline, indicat a conceptualization of health beyond ing improvements in quality of life, with no the absence of disease. Improvements in differences between treatment groups. In OHRQoL for both the GOHAI and the general, the generic and condition‐specific OHQoL‐UK were detected after non‐ versions of the OIDP performed similarly, surgical periodontal therapy in both study but the differences were more distinct, with groups, without any significant difference a higher effect size, when the condition‐spe between the two groups. This research also cific version was used. This provided evi assessed the minimally important difference dence in favour of the condition‐specific for these measures, again providing some version, even in a population of patients with context for the differences observed (Jonsson severe periodontitis where no such differ and Öhrn 2014). An earlier systematic review ence would be expected, as almost all oral investigated the effect of surgical periodontal impacts would be due to the periodontal therapy on OHRQoL. At that time, only three condition (rather than any other oral condi studies qualified following full‐text screening tion). A difference of five points in the OIDP and the results were conflicting. Again, no was estimated to correspond to clinically specific assessment of furcation intervention meaningful differences, thereby providing was tested (Shanbhag et al. 2012). context for changes in OHRQoL when using this measure (Tsakos et al. 2010). In a randomized controlled clinical trial, 13.3 Patient‐reported both the OIDP and OHRQoL questionnaires were given to 90 patients divided into two Outcome Measures groups: scaling and root planing (SRP, n = 45) in Furcation Involvement and one‐stage ‘full‐mouth disinfection’ (FMD, n = 45). All patients were then reas Helldén and co‐workers (1989) presented sessed at two time points: 30 days and 180 clinical and patient‐reported outcomes days after treatment. Patients treated by from a retrospective study on molars with both SRP and FMD showed improvement furcation involvement treated with tunnel in all periodontal clinical parameters and preparations. A total of 156 teeth among OHRQoL after treatment, with no significant 107 patients had been treated surgically with differences between treatment groups tunnel preparations from 1977 to 1985. (Santuchi et al. 2016). In a study by Makino‐ In 1986, all patients were asked to return for Oi and co‐workers (2016), improvements in a re‐evaluation, and 102 attended. All teeth OHRQoL (in the domains pain and eating/ involved were affected by degree III furcation chewing function) mirrored clinical improve involvement and were treated with tunnel ments after non‐surgical and then surgical ling surgery. In particular, following eleva treatment of moderate to severe chronic tion of full‐thickness flaps, the furcations periodontitis. A greater improvement was were widened by round burs at the entrance noted following surgical therapy, with no fur and then by bone files to create space for ther improvements during maintenance care. post‐surgical inter‐radicular plaque control, A randomized controlled trial evaluating after which the flaps were apically positioned, two educational programmes including sutured, and covered with surgical dressing. 252 Chapter 13
After removal of the dressing, the patients recently reported that none of the reviewed were shown how to use interdental brushes studies had included any patient‐reported inside the tunnelled area. The majority of the outcomes. The authors highlighted the need patients rinsed with 0.1% chlorhexidine for to introduce this aspect in furcation research 4–6 weeks and at each post‐surgical visit a (Avila‐Ortiz et al. 2015). fluoride varnish was applied to the teeth. Following three‐ to six‐monthly maintenance visits for two years, the patients returned to 13.4 Patient Feedback their referring dentists for continued follow‐ up. On average, patients were re‐examined Given the paucity of data on PROMs relative 37.5 months after surgery. Before the clinical to furcation involvement, some patients re‐evaluation, the following five questions treated by the author were asked to provide were asked of patients about their experience feedback on their experience with furcation with the furcation‐involved teeth (Helldén treatment. These are provided in this section. et al. 1989): 1) Do you have any discomfort from the tun Patient Feedback 1 (70‐year‐old nel area? Female, 10 Years After Tunnelling 2) Does the gingiva bleed in the tunnel area? Surgery) 3) Is the tooth sensitive to cold or warm ‘I was made aware of the gap between the temperatures? roots of my bottom right last tooth 4) Do you easily get access to the tunnel area 10 years ago when I had a surgical proce- for cleaning? dure on it. Now I feel that, as I go through 5) What kind of oral hygiene aids do you use the process of cleaning my teeth, I auto- in the tunnel areas? matically clean inside the roots and it At the end of the follow‐up period, 10 of 102 doesn’t feel any different than cleaning the teeth had been extracted and 7 had been other teeth. Occasionally I get some food hemisected or root resected, while 11 had stuck on that tooth. I come regularly to see developed incipient root caries and 12 teeth the hygienist and periodontist and I am showed established caries lesions. Based on used to it now.’ patient feedback, most cases were not asso ciated with any discomfort (92%), gingival Patient Feedback 2 (65‐year‐old bleeding (72%), or sensitivity to cold or Male, 12 Years After Tunnelling warm temperatures (95%). Most patients Surgeries) used a common toothbrush (98%) for the outer part of the tooth and an interdental ‘When I first saw a periodontist my mouth brush for the tunnel areas (80%). Although was in a poor state. Whenever I brushed plaque removal presented some difficulties, my teeth my gums bled, and I was afraid most such areas (70%) were found to be eas of losing my teeth but I did not know how ily accessible for cleaning procedures by to make them better. At that stage I did patients. The study by Helldén and co‐work not realize that bone loss caused by gum ers represented a pioneering attempt to disease meant that the gaps between the obtain information on subjective percep furcations in the roots were hard or impos- tions in patients affected by furcation sible to clean, and were providing a gath- involvement, although without a validated ering place for bacteria causing the disease questionnaire. A systematic review on peri to continue and worsen. The periodontist odontal regeneration of furcation defects by performed a couple of operations to open the American Academy of Periodontology up the gums to enable me to clean into A Patient’s Point of View 253
these gaps, and showed me how to do the care and this regime I have managed to cleaning using little interdental brushes. extend the life of these teeth. May this From that time on I have been able to continue!’ clean my teeth fully without any bleeding, and the disease has gone. I still lost some Patient Feedback 4 (50‐year‐old of my teeth; three of them have been Male, 6 Years After Tunnelling replaced by implants, and these together Surgery on One Molar and with what remains of my natural teeth are Extraction and Implant Placement sufficient for me to eat effectively. I have on the Contralateral Molar) always dreaded the idea of having den- tures, which seemed inevitable, but more ‘Following treatment by my dentist than 12 years later I am keeping the dis- whereby I had a tooth extraction on my ease and decay at bay and I remain hope- right lower jaw and surgery to keep a tooth ful of avoiding dentures for the foreseeable on my left lower jaw. With reference to my future.’ right jaw and tooth extraction I allowed the bone in that area of extraction to grow Patient Feedback 3 (60‐year‐old back before having an implant to secure Male, 10 Years After Tunnelling and strengthen the teeth in that area. The Surgery) additional surgery I had on my left jaw meant that my tooth was saved. My dentist ‘Having undergone surgery to my right inserted a small piece of tube between the upper teeth to combat gum disease some two roots to enable the cleaning of the tooth years ago I am very fortunate to say that and root area. All I do now on a daily basis after several years I am being able to is clean in between my teeth and roots maintain a reasonable level of health in using interdental brushes which is totally this area. Following the surgery I took the pain free and easy to do.’ view that I would work hard to maintain the situation and by diligence have, it Patient Feedback 5 (45‐year‐old seems, managed to do so. I have a cleans- Female, 10 Years After Root‐ ing regime that I adhere to rigidly and resection Surgery) includes both morning and night a pro- cess which takes me approximately ‘Soon after I was referred to the periodon- 15 minutes each time. And includes tist for treatment for my gums, a very fact‐ cleansing with an interdental brush, floss- facing appointment, back tooth removed ing, cleansing with ‘sensitive’ toothpaste and three operations to clean the roots and and good quality electric brush and more I started to realize that there was a serious work with the interdental brush to finish chance that I would lose some if not all my off. At times when the mouth is sensitive I teeth, if I did not make a change. I then brush with a specific gel. Although this started on an ongoing treatment plan of takes some time and I have to exercise seeing the periodontist every six months some personal discipline I believe it is and the hygienist every alternative six time well spent and will do anything to months, but at this point I was still smok- prevent the loss of further teeth. The ing. I was eventually able to give up smok- health of my mouth in general has also ing. Treatment is ongoing, I still have most improved greatly. I also believe that my of my teeth and I plan to keep them. I wish general health has improved as a result of there was a once and for all cure, but am this improvement in my oral health. I am resigned to having ongoing maintenance very grateful that through this regular treatment.’ 254 Chapter 13
Patient Feedback 6 (63‐year‐old The specific act of cleaning inside a tunnelled Male, 5 Years After Molar furcation area was described as a relatively Extraction and Implant Placement) easy task by these patients (‘I automatically clean inside the roots and it doesn’t feel any ‘Given my experience as a dental patient, different than cleaning the other teeth’). I consider myself an expert. I’ve had caries, The patients’ perception of the treatment gum disease and extractions, followed by carried out is also very interesting, ranging crowns and bridges. I work very hard at from what seems like a good understanding my dental hygiene, but I recognize I could of the surgical tunnelling procedure (‘the gaps probably do better. Over the years I’ve had between the furcations in the roots were hard problems around my crowns and bridges on or impossible to clean, and were providing a my back teeth, both aesthetic concerns and gathering place for bacteria causing the dis several flare‐ups with inflammation and ease to continue and worsen. The periodon discomfort. I think that this is because plaque tist performed a couple of operations to open gets stuck under the crown and bridgework. up the gums to enable me to clean into these Some years ago, one of my molars was finally gaps’) to a rather more imaginative interpre extracted and replaced with an implant. I’ve tation (‘My dentist inserted a small piece of had to wait a few months after the extraction tube between the two roots to enable the to finally have a crown on the implant, but cleaning of the tooth and root area’). I understand that is normal procedure. I feel The experience of having a dental implant to the implant like a normal tooth, like it’s replace a molar previously affected by severe always been there and I’ve no longer had any periodontal disease was also seen as very pos discomfort or inflammation.’ itive (‘I’ve had problems around my crowns and bridges on my back teeth, both aesthetic 13.5 Reflections on concerns and several flare‐ups with inflam mation and discomfort. … one of my molars Patient Feedback was finally extracted and replaced with an implant. … I feel the implant like a normal While accepting that this is by no means a tooth, like it’s always been there and I’ve no representative patient sample and that longer had any discomfort or inflammation’). reporting feedback for the treating clinician may be seen as a biased exercise, several important items emerged from this feed 13.6 Implementation of back. It is clear that these patients were highly motivated and made a long‐term PROMs in Furcation commitment to the survival of their teeth. Treatment They effectively decided to change their dental health behaviour, including giving up Given the increased recognition of the impor smoking (‘I eventually gave up smoking’) and tance of patient‐reported outcomes in medi working hard on their oral hygiene (‘I have a cine, the future should see the use of OHRQoL cleansing regime that I adhere to rigidly and measures in studies investigating furcation includes both morning and night a process treatment. The pioneering effort by Helldén which takes me approximately 15 minutes and co‐workers (1989, see earlier discussion) each time’). In some cases this did not appear to investigate patient perceptions should be to be a burden on the patient (‘All I do now extended by using validated OHRQoL on a daily basis is clean in between my teeth measures, and potentially by developing a and roots using interdental brushes which is condition‐specific validated questionnaire totally pain free and easy to do’), while which also takes into account items such as in other cases it did (‘am resigned to sensitivity, ease of cleaning inside the furca having ongoing maintenance treatment’). tion area, and the alternatives of extraction A Patient’s Point of View 255 with or without replacement. The develop clinical reality, an assessment of patient per ment of such a condition‐specific measure ceptions related to periodontal treatment would need to be driven by qualitative needs to accompany purely clinical and finan research highlighting the main concerns of cial considerations. This could be considered patients with furcation involvement. in the treatment planning stages as well as More importantly, it would be ideal to use being an outcome measure to assess the effec PROMs as outcomes in long‐term randomized tiveness of interventions. controlled trials testing different modalities of furcation treatment (for example conservative treatment vs root resection vs extraction and Acknowledgements implant therapy). This could provide answers on the effects of these procedures on patients’ The invaluable help and advice of Dr George quality of life and, together with clinical and Tsakos, University College London, in the financial considerations, could help design fur preparation and revision of this chapter is cation treatment guidelines. In the everyday gratefully acknowledged.
Summary of Evidence
●● The attention to patients’ preferences and ●● There is a paucity of data on PROMs in points of view needs to take centre stage patients with furcation involvement. in treatment planning. As such, patient‐ ●● Investigation of PROMs relative to furca reported outcome measures (PROMs) are tion involvement should, together with fast becoming essential outcomes of any clinical and financial considerations, form periodontal research study. the basis of furcation treatment planning.
References
Adulyanon, S., Vourapukjaru, J., and regeneration – furcation defects: Sheiham, A. (1996). Oral impacts A systematic review from the AAP affecting daily performance in a low dental Regeneration Workshop. Journal of disease Thai population. Community Periodontology 86 (Suppl. 2), S108–S130. Dentistry and Oral Epidemiology 24, Brennan, D.S., Spencer, A.J., and Roberts‐ 385–389. Thomson, K.F. (2007). Quality of life and Al‐Harthi, L.S., Cullinan, M.P., Leichter, J.W., disability weights associated with and Thomson, W.M. (2013). The impact of periodontal disease. Journal of Dental periodontitis on oral health‐related quality Research 86, 713–717. of life: A review of the evidence from Buset, S.L., Walter, C., Friedmann, A. et al. observational studies. Australian Dental (2016). Are periodontal diseases really Journal 58, 274–277. silent? A systematic review of their effect on Aslund, M., Suvan, J., Moles, D.R. et al. (2008). quality of life. Journal of Clinical Effects of two different methods of non‐ Periodontology 43, 333–344. surgical periodontal therapy on patient Glick, M., and Meyer, D.M. (2014). Defining perception of pain and quality of life: A oral health: A prerequisite for any health randomized controlled clinical trial. Journal policy. Journal of the American Dental of Periodontology 79,1031–1040. Association 145, 519–520. Avila‐Ortiz, G., De Buitrago, J.G., and Glick, M., Williams, D.M., Kleinman, D.V. et al. Reddy, M.S. (2015). Periodontal (2017). Reprint of: A new definition for oral 256 Chapter 13
health supported by FDI opens the door to a Santuchi, C.C., Cortelli, J.R., Cortelli, S.C. universal definition of oral health. Journal of et al. (2016). Scaling and root planing per Dentistry 57, 1–3. quadrant versus one‐stage full‐mouth Helldén, L.B., Elliot, A., Steffensen, B., and disinfection: Assessment of the impact of Steffensen, J.E.M. (1989). Prognosis of chronic periodontitis treatment on quality tunnel preparations in treatment of class III of life – a clinical randomized, controlled furcations: A follow‐up study. Journal of trial. Journal of Periodontology 87, 114–123. Periodontology 60, 182–187. Shanbhag, S., Dahiya, M., and Croucher, R. Herdman, M., Gudex, C., Lloyd, A. et al. (2012). The impact of periodontal therapy (2011). Development and preliminary on oral health‐related quality of life in testing of the new five‐level version of adults: A systematic review. Journal of EQ‐5D (EQ‐5D‐5L). Quality of Life Research Clinical Periodontology 39, 725–735. 20, 1727–1736. Slade, G.D. (1997) Derivation and validation of Jönsson, B., and Öhrn, K. (2014). Evaluation of a short‐form oral health impact profile. the effect of non‐surgical periodontal Community Dentistry and Oral treatment on oral health‐related quality of Epidemiology 25, 284–290. life: Estimation of minimal important Tsakos, G., Bernabé, E., D’Aiuto, F. et al. differences 1 year after treatment. Journal of (2010). Assessing the minimally important Clinical Periodontology 41, 275–282. difference in the oral impact on daily Lawal, F.B., Taiwo, J.O., and Arowojolu, M.O. performances index in patients treated for (2015). Comparison of two oral health‐ periodontitis. Journal of Clinical related quality of life measures among adult Periodontology 37, 903–909. dental patients. Oral Health and U.S. Department of Health and Human Preventative Dentistry 13, 65–74. Services, Food and Drug Administration, Locker, D. (1988). Measuring oral health: Center for Drug Evaluation and Research A conceptual framework. Community (CDER) et al. (2009). Guidance for industry: Dental Health 5, 3–18. Patient‐reported outcome measures: Use in Makino‐Oi, A., Ishii, Y., Hoshino, T. et al. medical product development to support (2016). Effect of periodontal surgery on oral label claims. Rockville, MD: FDA. health‐related quality of life in patients who WHOQOL Group (1994). Development of the have completed initial periodontal therapy. WHOQOL: Rationale and current status. Journal of Periodontal Research 51, International Journal of Mental Health 212–220. 23, 24–56. 257
Chapter 14
Assessment of Two Example Cases Based on a Review of the Literature Luigi Nibali
Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK
In an attempt to apply the knowledge gained in favour of longer root cones. High root throughout this book to the treatment of divergence appears on teeth 16 (UR6) and cases with furcation involvement, two 26 (UL6), while the roots of 17 (UR7) and example cases are presented. They will be 27 (UL7) are less divergent. Among predis- discussed in light of the evidence gained in posing factors described in Chapter 1, each of the previous 13 chapters. bifurcation ridges, enamel projections, and enamel pearls do not seem to be present. 14.1 Case 1 (Maxillary) 14.1.2 Diagnosis (Chapter 2)
A 50‐year‐old male patient presented with a Although two‐dimensional radiographic complaint of bleeding on brushing and gum examination is not completely reliable for fur- recessions. He was medically healthy, never cation diagnosis, the areas of radiolucency smoked, and was not aware of any family between roots, coupled with interproximal history of periodontal disease. His oral bone levels apical to the furcation entrances, hygiene was good, with full mouth plaque indicate a likely triple through‐and‐through scores < 10%; he had generalized gingival furcation involvement (FI) for teeth 16, 17, and recessions and localized probing pocket 27. Doubts exist about possible FI on tooth 26. depths (PPD) > 4 mm only on upper molars. Clinical examination with a curved Nabers The case will be dissected based on the probe confirms this, with a diagnosis of triple evidence provided in each of the previous (buccal, mesial, and distal) degree III FI on chapters before reaching a treatment plan- teeth 16, 17, and 27 (Hamp et al. 1975). The ning decision. same diagnosis would be given when using the Glickman (1953) classification and the classi- 14.1.1 Anatomy (Chapter 1) fication modified by Ammons and Harrington (2006; see Table 2.4). Degree I FI was recorded The maxillary first and second right and left only distal of 26. Vertical subclassification molars in Figure 14.1 present a relatively (Tarnow and Fletcher 1984) is reported in ‘normal’ anatomy, with three roots each, all Table 14.1. The comprehensive diagnosis apparently distally curved to varying degrees. system in the table summarizes clinical and The root trunks appear reasonably small, radiographic findings on example tooth 16.
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
(a)
(b)
(c) (d)
Figure 14.1 Case 1, clinical photograph of frontal (a) and upper right palatal (b), followed by baseline periapical radiographs of upper molars (c and d), the only teeth with probing pocket depth > 4 mm at first visit.
14.1.3 Initial Therapy (Chapter 3) hygiene levels, it is crucial that further oral hygiene reinforcements are given as part of Most furcation areas, including probably initial periodontal therapy. Research shows those in this case, have narrow entrances that in interproximal sites, bristled or rubber (<0.75 mm). Ultrasonic scalers, especially interdental brushes remove more plaque with slimline tips, have been shown to be than flossing or brushing alone (Christou better suited than hand instruments for the et al. 1998; Abouassi et al. 2014). Therefore, debridement of narrow furcation areas the use of interdental brushes of the correct (Matia et al. 1986; Sugaya et al. 2002), par- size and shape in the molar region should be ticularly in degree II and III FI (Leon and encouraged and discussed with the patient. Vogel 1987). Micro Mini Five® Gracey curettes could also be helpful in narrow furcation entrances (see Chapter 3 for details). 14.1.4 Endodontics (Chapter 4) However, interproximal FI is likely to respond less favourably to mechanical debridement Although all four maxillary molars have res- compared to buccal furcations (Del Peloso torations, they are not large enough to Ribeiro et al. 2007) and more residual calcu- endanger the endodontic status of the teeth. lus will be left with a closed (non‐surgical) However, accessory canals in the furcation approach compared to an open approach region are frequent and might represent a (Matia et al. 1986; Fleischer et al. 1989). communication pathway between endodon- Although this patient exhibits very good oral tic and periodontal pathologies through Assessment of Two Example Cases 259
Table 14.1 Case 1, diagnosis of furcation on 16 based on Muller and Eger (1999).
Patient PL (age 50) Tooth 16
Mobility (0, 1, 2, 3) 0 Elongation (0, 1) 0 Sensibility testing (1: positive, 2: negative) 1 Endodontic dx (0: OK, 1: revision necessary) 0 Caries/restorations (0: caries free, 1: small caries or filling, 1 2: extended caries, large filling, 3: artificial crown)
Rx diagnosis Mesial root Distal root Palatal root
MDMDMD Bone loss 2 2 2 2 1 1 m/d roots m/p roots d/p roots Separation degree 1 1 1 Degree of divergence 1 1 1
Clinical diagnosis
mb b db mp p dp BOP (0,1) 1 0 1 1 0 0 Plaque (0,1) 0 0 0 0 0 1 PPD 6 6 6 6 3 7 vCAL 7 7 8 9 6 9 hCAL – 6 – 6 – 6 Degree – III B – III B – III C
Bone loss: 0 (≤ ⅓ root length), 1 (⅓–⅔ root length), 2 (≥ ⅔ root length); separation degree: 0 (< ⅓), 1 (> ⅓); degree of divergence: 0 (≤30°), 1(>30°). B = buccal; BOP = bleeding on probing; CAL = clinical attachment loss; D = distal; h = horizontal; M = mesial; P = palatal; PPD = probing pocket depth; v = vertical. the induction of inflammatory responses. comprehensive periodontal treatment (non‐ Furthermore, a small radiolucency area surgical and surgical). For degree III FI, the seems to be present on 17 (palatal root). relative risk of tooth loss is approximately Therefore, it is always advisable to test tooth three times that of degree I FI molars and vitality. Vitality testing was positive for all twice compared with degree II FI molars tested molars (16, 17, 26, and 27). Hence no (Nibali et al. 2016). In a follow‐up mainte- endodontic treatment was required, but nance programme varying from 5 to 53 years, retesting during treatment and maintenance 30% of degree III FI molars are lost (Nibali therapy was recommended. et al. 2016). Meta‐analyses providing specific data for maxillary degree III FI molars, or 14.1.5 Long‐term Prognosis specifically for first or second molars, are (Chapter 5) lacking. Based on these data, it may be con- sidered worth trying to maintain this tooth. Molars with FI have a higher risk of tooth Treatment options need to be assessed in the loss than molars with no FI (twice as likely to following sections. A strict post‐treatment be lost up to 15 years of follow‐up), following maintenance programme including three‐ to 260 Chapter 14
four‐monthly periodontal charting, supra‐ do not make root resection the preferred and subgingival debridement, and oral treatment option for teeth 16, 17, and 27. hygiene reinforcement and motivation is recommended based on the available litera- 14.1.8 Tunnelling (Chapter 9) ture (Nibali et al. 2016). The furcation tunnelling procedure should 14.1.6 Regeneration be considered at stable (no more than mobil- (Chapters 6 and 7) ity grade I) furcation‐involved molars with advanced inter‐radicular bone loss (prefera- The first aim of periodontal treatment, where bly degree III FI) when accessibility to the possible, should be to regenerate the lost per- furcation area for plaque removal is difficult. iodontal support. However, despite some As a rule of thumb, the alveolar bone sup- successful reports of regeneration of degree port should be of equal amounts at all roots III FI molars in animal models (Chapter 6), and at least cover one‐third of the root human studies do not support the use of length, with mainly horizontal bone loss. regeneration in maxillary degree III FI molars The length of the root trunk should not (Chapter 7). In particular, one randomized exceed 4 mm and the diameter of the furca- controlled trial with split‐mouth design with tion entrance should be at least 0.5 mm. 11 patients compared guided tissue regener- Fulfilment of these criteria for teeth 17, 16, ation (GTR) and open‐flap debridement and 27, this patient’s full cooperation, good (OFD) in the treatment of maxillary inter- oral hygiene dexterity and attitude, and a proximal degree III furcation defects relatively low caries risk make tunnelling (Pontoriero and Lindhe 1995). Baseline and surgery an attractive treatment option in this six‐month examinations were performed by case. However, we should bear in mind that re‐entry after flap elevation. Neither GTR very few reports of long‐term success of tri- nor OFD led to even partial closure of the ple maxillary tunnels exist in the literature 22 degree III furcations. Based on these data, (Helldén et al. 1989). these teeth are not suitable for regenerative treatment of their FI. 14.1.9 Innovative and Adjunctive Therapy (Chapter 10) 14.1.7 Resective Therapy (Chapter 8) In order to maximize the efficacy of non‐ surgical therapy of FI on the molars pre- Common sense would suggest that if you sented here, adjunctive systems such as an cannot close the furcation by regeneration, at endoscope, lasers, photodynamic therapy, least you should eliminate it surgically or air‐polishing devices, antimicrobials, or make it cleansable. The options of root sepa- probiotics could be considered. However, ration, root amputation, and root resection this should be carefully weighed in the light could be considered in a case of advanced FI, of costs and the so far poor evidence for their as for the molars in this case. However, these efficacy specific to furcations (de Andrade options are more suitable when, for example, et al. 2008; Ribeiro Edel et al. 2010; Tomasi one root is affected to a greater extent than and Wennstrom 2011; Eickholz et al. 2016). the others. Furthermore, particular caution should be taken when the teeth are intact, 14.1.10 Extraction and Implant because this is an invasive procedure involv- Placement (Chapter 11) ing a considerable biological cost that must always be carefully evaluated. For this rea- Given the extensive loss of periodontal sup- son, in this case, inadequate residual attach- port and FI and the perceived low predicta- ment on the remaining roots and tooth vitality bility of furcation treatment, teeth 17, 16, and Assessment of Two Example Cases 261
27 could be considered hopeless by some with tunnelling were not associated with any treating clinicians based on published prog- discomfort, gingival bleeding, or sensitivity. nostic systems (Becker et al. 1984; Machtei Although plaque removal presented some et al. 1989). If a decision was made to extract difficulties, most furcation areas were found them, the options of a shortened dental arch, to be easily accessible for cleaning proce- partial dentures, or implants could be con- dures by patients with interdental brushes. In sidered. Bearing in mind the high long‐term this specific case, the patient expressed his survival rates of implant‐supported restora- wish to maintain these teeth for as long as tions (Moraschini et al. 2015) and the possible, and he showed very good oral hygiene relatively young age and motivation of the and commitment. patient, implant placement was discussed as his main alternative option to tooth reten- 14.1.13 Treatment Decision tion. However, as discussed in Chapter 11, reduced quantity of bone, proximity to maxil- Based on all these considerations, backed lary sinus, need for grafting, and previous his- when possible by data from the literature, tory of periodontitis may result in reduced it was decided to maintain the molars implant‐survival rates in this case (Becker affected by FI and to carry out non‐surgical et al. 1999; Drago 1992; Graziani et al. 2004; debridement and oral hygiene reinforce- Pjetursson et al. 2008). The option of extrac- ment. Following re‐evaluation two months tion, socket preservation, and short implants later, residual pockets and FI were detected could also be considered, provided enough on the affected molars and it was decided residual bone was available to allow implant to proceed with tunnelling surgeries for 16, placement (Thoma et al. 2015). 17, and 27, followed by strict supportive periodontal therapy (see Chapter 9 for a 14.1.11 Health Economics step‐by‐step guide on the furcation tunnel- (Chapter 12) ling surgical technique). Post‐operative photos and radiographs are presented in A handful of studies have now shown that Chapter 15 (Figure 15.8). The main reasons treating molars with degree III FI via tooth‐ for this choice are summarised in retaining options was more effective and less Table 14.2). costly than tooth removal and replacement via implant‐supported restorations (Fardal and Grytten 2013; Martin et al. 2014; Table 14.2 Case 1, main reasons for treatment Schwendicke et al. 2014). Among possible choice (tunnelling surgery). treatment options, considering that all molars are still vital, it remains uncertain Factors whether the high costs for root‐resective therapy could be truly justified (Little et al. TOOTH Good root divergence 1995; Blomlof et al. 1997; see Chapter 12 Short root trunk for more details). Prevalently horizontal bone loss affecting all roots Tooth vitality and no restorative 14.1.12 Patient’s Point of View concerns (Chapter 13) Importance in masticatory function PATIENT Clear medical history In the absence of data on patient‐reported Non‐smoker outcomes on treatment of degree III FI, some Motivation to keep teeth suggestions could be drawn from the paper No financial or other concerns for on tunnelling discussed in Chapter 13 surgical treatment Good oral hygiene dexterity (Helldén et al. 1989). Most cases treated 262 Chapter 14
14.2 Case 2 (Mandibular) 14.2.2 Diagnosis (Chapter 2) Although two‐dimensional radiographic A 47‐year‐old male patient presented with a examination is not completely reliable for complaint of occasional bleeding on brush- furcation diagnosis, the area of radiolu- ing and discomfort from the lower left gingi- cency between mesial and distal roots, vae. He was medically healthy, he used to coupled with distal interproximal bone smoke (10 a day for 20 years, and gave up 10 levels apical to the furcation entrances, years before the first examination), and was suggests a likely through‐and‐through fur- not aware of any family history of periodon- cation involvement (FI). However, clinical tal disease. His oral hygiene was fair, with full examination with a curved Nabers probe mouth plaque scores of 40% (generalized only resulted in degree II buccal and lin- interproximal plaque), localized gingival gual FI (Hamp et al. 1975) and a possible recessions, and localized probing pocket degree III when using the Glickman (1953) depths > 4 mm only on the lower left first classification and the classification modi- molar (LL6). The case will be dissected based fied by Ammons and Harrington (2006; on the evidence provided in each of the pre- see Table 2.4). Probing pocket depths are vious chapters before reaching a treatment reported in Table 14.3. planning decision. Table 14.3 Case 2, evaluation. 14.2.1 Anatomy (Chapter 1) Tooth 36 (LL6) v‐PPD CAL h‐PPD The mandibular left first molar (LL6) in Figure 14.2 presents a relatively ‘normal’ Mesio‐buccal 2 2 – anatomy, with two roots (mesial and dis- Buccal 8 10 5 tal). The mesial root is slightly distally Disto‐buccal 12 15 – tilted towards the apex. The root trunks Mesio‐lingual 3 3 – and root cones appear to be of average length and root divergence seems normal. Lingual 7 7 4 Among the predisposing factors described Disto‐lingual 10 11 – in Chapter 1, bifurcation ridges, enamel CAL = clinical attachment loss; h‐PPD = horizontal projections, and enamel pearls do not seem probing pocket depth; v‐PPD = vertical probing to be present. pocket depth.
(a) (b)
Figure 14.2 Case 2, clinical photograph (a) of left mandibular first molar, followed by baseline periapical radiograph (b). Assessment of Two Example Cases 263
On vertical probing, degree C FI was diag- pulp necrosis might occur during periodontal nosed (exceeding 6 mm in both buccal and healing, root canal treatment could be pre- lingual furcations; Tarnow and Fletcher ventively performed to avoid any interference 1984). Therefore, a degree II C diagnosis was with the regeneration process in case of peri- given to both furcations, but with doubt on odontal bone loss to the apex (Cortellini and possible degree III through‐and‐through. It Tonetti 2001). However, this was not consid- is important to note that the furcation defect ered necessary in this case. Instead, retesting is combined with a very deep distal intra- of vitality after treatment was planned. bony defect, reaching the apex of the distal root, with some reduced bone support also 14.2.5 Long‐term Prognosis on the mesial aspect of neighbouring tooth (Chapter 5) 37 (LL7). In this case, due to the difficulty in probing According to the evidence discussed in the furcation, it may be worth considering a Chapter 5, following comprehensive perio- three‐dimensional radiograph to ascertain dontal treatment, as a furcation‐involved the presence of residual alveolar bone by the molar this tooth has a higher risk of tooth loss furcation fornex for treatment planning than a molar with no FI (twice as likely to be purposes. lost up to 15 years of follow‐up). According to a recent systematic review (Nibali et al. 2016), 14.2.3 Initial Therapy (Chapter 3) 18% of degree II FI molars are lost in a follow‐ up maintenance programme varying from As discussed for Case 1, due to narrow furca- 5 to 53 years, and this tooth’s relative risk of tion entrances ultrasonic scalers with slim‐ needing extraction is 1.67 compared with line tips, possibly complemented by Micro degree I FI molars. The risk could actually be Mini Five® Gracey curettes, are particularly higher for this tooth, affected at least by dou- suited for the debridement of FI. It is likely ble degree II FI and possibly by degree III FI. that residual calculus might be left with a Based on these data, it may be worth trying to closed (non‐surgical) approach compared to maintain this tooth. Treatment options need the open approach (Matia et al. 1986; to be assessed, as in the following sections. Fleischer et al. 1989), although probably not A strict post‐treatment maintenance pro- as much as in interproximal furcations. gramme including three‐ to four‐monthly Particular attention needs to be paid to the periodontal charting, supra‐ and subgingival difficult‐to‐reach concavity around the debridement, and oral hygiene reinforcement furcation fornix. An improvement in oral and motivation are recommended based on hygiene levels is necessary for this patient, the available literature (Nibali et al. 2016). with the introduction of large interdental brushes for cleaning the interproximal area 14.2.6 Regeneration between LL6 and LL7. (Chapters 6 and 7)
14.2.4 Endodontics (Chapter 4) Tooth 36 seems to be affected by degree II FI, although a degree III FI cannot be ruled out. Although the tooth is non‐restored, due to Despite some successful reports of regenera- extensive FI and a distal intrabony defect tion of degree III furcation‐involved molars reaching the apex, a neuro‐vascular bundle in animal models, according to the literature damage may have occurred (Langeland et al. reviewed in Chapter 7, human studies do not 1974). Therefore, it is advisable to test tooth support the use of regeneration in maxillary vitality. Vitality testing was positive for 36. degree III FI molars. However, in case of Some authors have even advocated that since mandibular FI II, the chances are good of 264 Chapter 14
achieving at least a partial fill of the furcation However, caution should be employed, as the defect, converting the degree II to a degree I tooth presented here is not restored, hence a FI. Treatment with either guided tissue root‐resection procedure would involve a regeneration (GTR) or enamel matrix deriva- considerable biological cost. tive (EMD) has produced histological evi- dence of regeneration (Stoller et al. 2001; 14.2.8 Tunnelling (Chapter 9) Nevins et al. 2003) and consistently more favourable clinical outcomes (reduction to As seen for Case 1, the furcation tunnelling degree I or closure) compared with access procedure should be considered for furca- flaps in degree II mandibular furcations tion‐involved molars with advanced inter‐ (Jepsen et al. 2002, 2004). The high bone sup- radicular bone loss (preferably FI degree III) port on the mesial root of 36 (above the fur- when accessibility to the furcation area for cation fornix) as well as on the mesial root of plaque removal is difficult. Indications for the adjacent 37 (next to the distal intrabony tunnelling are mainly good oral hygiene dex- defect of 36) would have a beneficial impact terity and motivation, and horizontal bone on the regeneration potential, provided that loss covering at least one‐third of the root good soft‐tissue closure of the defect could length. Therefore, this case does not seem be achieved post‐operatively. Therefore, if suitable for tunnelling surgery. degree II FI was confirmed intra‐surgically, according to the evidence reviewed in 14.2.9 Innovative and Adjunctive Chapter 7, this molar appears to be suitable Therapy (Chapter 10) to benefit from regenerative furcation ther- apy, although, due to the bilateral degree II FI As discussed for Case 1, adjunctive therapy (in the best‐case scenario), the results of to non‐surgical periodontal treatment could regenerative therapy might be less predicta- be considered, but should be carefully bal- ble than in a single degree II FI. anced with costs and the so far poor evidence for their efficacy specific to furcations (de 14.2.7 Resective Therapy Andrade et al. 2008; Ribeiro Edel et al. 2010; (Chapter 8) Tomasi and Wennstrom 2011; Eickholz et al. 2016). The options of root separation, root amputa- tion, and root resection could be considered 14.2.10 Extraction and Implant in cases of advanced FI, like this one. The Placement (Chapter 11) options of root amputation (removing the distal root and leaving the crown intact) or Given the extensive loss of periodontal sup- root resection (removing the distal root and port to the apex and FI, tooth 36 might be the relative section of the crown) are particu- considered hopeless based on published larly suitable when one root is affected to a prognostic systems (Becker et al. 1984; greater extent than the others, which is the Machtei et al. 1989; Cortellini et al. 2011). case for the tooth in question. Although the Reduced bone quantity on the distal aspect of distal root has a significantly smaller root the tooth may mean that there might be need surface area than the mesial one (Dunlap and for bone grafting after extraction; a previous Gher 1985), the mesial root has a deep con- history of periodontitis might result in a cavity, which makes it more difficult to endo- reduced implant‐survival rate in this case dontically treat and properly prepare and (Drago 1992; Becker et al. 1999; Graziani restore. The reported long‐term survival of et al. 2004; Pjetursson et al. 2008). However, it root‐resected molars is in the 60–90% range is not inconceivable to think that, instead of for studies up to 10 years (Langer et al. 1981; distal root resection, extraction of the tooth Carnevale et al. 1998; reviewed in Chapter 8). and replacement could be an option here. Assessment of Two Example Cases 265
14.2.11 Health Economics Table 14.4 Case 2, re‐evaluation. (Chapter 12) Tooth 36 (LL6) v‐PPD CAL h‐PPD As discussed earlier, studies have now shown that treating molars with degree II and III FI Mesio‐buccal 2 2 – via tooth‐retaining options was more effective Buccal 6 8 4 and less costly than tooth removal and replace- ment via implant‐supported restorations Disto‐buccal 10 13 – (Fardal and Grytten 2013; Martin et al. 2014; Mesio‐lingual 3 3 – Schwendicke et al. 2014). However, this may Lingual 6 6 4 not apply if the more invasive and expensive Disto‐lingual 9 11 – options of root resection, endodontic therapy, CAL = clinical attachment loss; h‐PPD = horizontal and restoration are chosen for tooth retention probing pocket depth; v‐PPD = vertical probing (Little et al. 1995; Blomlof et al. 1997). pocket depth.
14.2.12 Patient’s Point of View Table 14.5 Case 2, main reasons for treatment choice (regenerative therapy with enamel matrix (Chapter 13) derivative). In the absence of data on patient‐reported outcomes on treatment of furcation‐involved Factors molars (in particular degree II, as in this case), patient preferences are very important. TOOTH Good mesial bone support Good bone support on neighbouring In this specific case, the patient was very keen tooth 37 to maintain 36 for as long as possible. Reduced tooth divergence Intrabony defect affecting distal root and furcation 14.2.13 Treatment Decision Tooth vitality and no restorative concerns Based on all these considerations, backed Importance in masticatory function when possible by data from the literature, it PATIENT Clear medical history was decided to maintain 36 and to carry out Non‐smoker non‐surgical debridement and oral hygiene Motivation to keep the tooth instructions. Following re‐evaluation two No financial or other concerns for surgical treatment months later, residual pockets, bleeding on probing, and FI were detected on this tooth (see Table 14.4). only a very limited layer of bone may have Given the residual FI and residual deep been present. Therefore, regenerative therapy pockets, associated with a high risk of future with EMD was provided (see Chapter 7 for a tooth loss (Matuliene et al. 2008; Nibali et al. step‐by‐step guide to the furcation regener- 2016), a decision to attempt surgical explora- ative surgical technique). Post‐opera tive tion and if possible regenerative surgery was photos and radiographs are presented in made. No through‐and through FI could be Chapter 15 (Figure 15.5). The main reasons detected intra‐surgically, although probably for this choice are summarized in Table 14.5.
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Chapter 15
Furcations: A Treatment Algorithm Luigi Nibali
Centre for Immunobiology and Regenerative Medicine, Centre for Oral Clinical Research, Institute of Dentistry, Barts and the London School of Medicine and Dentistry, Queen Mary University of London (QMUL), London, UK
15.1 Introduction 15.2 First Things First: Proper Diagnosis What do you do when facing a molar with furcation involvement (FI)? Extract? Diagnosis is the first step towards treatment. Ignore? Treat? And how? Regeneration? As in any other field of medicine, every effort Root resection? Several papers in the peri- needs to be expended for a correct diagnosis odontal literature have covered the treat- of the problem (Khullar et al. 2015). Most of ment of molars with FI. Previous chapters the mistakes I have made in my professional of this book have reviewed and carefully career or have seen made by students or col- scrutinized the evidence for no treatment, leagues were due to incorrect diagnosis. This and for conservative, regenerative, and is particularly important for furcations, since resective therapy. But how do we approach diagnosis is not straightforward. Therefore, decision‐making? How can we merge the spending more time and effort for diagnostic patient’s preferences and needs with the purposes before rushing to pick up blade or financial considerations and the clinical forceps is recommended. criteria discussed in this book to achieve a Furcation diagnosis has been covered by favourable outcome? We embark on this Eickholz and Walter in Chapter 2. Their clear chapter with a scientific evidence‐based message is that clinical and radiographic approach to try to answer these questions. diagnoses need to be combined to obtain a However, in the absence of randomized correct measure of the involvement of the controlled trials comparing different man- furcation area. A curved Nabers probe is vital agement options for molars with varying for measuring the bone loss in the furcation degrees of FI, pragmatic considerations and area, although the difference between degrees experience will complement the evidence II and III might be difficult to ascertain, espe- in order to obtain treatment guidelines. cially in maxillary molars. Three‐dimensional The main points to consider are highlighted radiography may also be needed for treat- in what follows. ment planning purposes in some cases.
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
Periodontal probe: pockets on molars
Nabers probe
Probing degree II or III
No probing in furcation Probing degree I Periapical radiograph, assessment of endodontic status, and occlusion
Complex treatment planning
Consider cone-beam CT Maintenance/treatment
Periodontal treatment
Figure 15.1 Proposed algorithm for furcation diagnosis.
Figure 15.1 shows a furcation diagnosis 15.3 Degree I Furcation algorithm, essential for treatment planning. Involvement It is suggested that a Nabers probe is used in all cases of probing pocket depths > 4 mm in The evidence from the literature, summa- molars, to establish a furcation diagnosis. In rized in a recent systematic review and dis- the case of FI degree II or III, further diag- cussed in Chapter 5, suggests that increasing nostic tests, including periapical radiographs FI degree is associated with an increased and endodontic and occlusal assessments, risk of tooth loss (Nibali et al. 2016). The may be necessary for treatment planning. long‐term risk of tooth loss appears minimal When the diagnosis and extent of FI are not in degree I FI molars undergoing regular care clear, posing doubts about the best treatment compared with molars with no FI. In fact, plan, cone‐beam computed tomography re‐examining data from that systematic (CBCT) may be justifiable as a useful review, it appears that molars with degree I FI diagnostic adjunct, especially for maxillary undergoing regular supportive periodontal molars (Walter et al. 2016; see Chapter 2 for therapy (SPT) have an identical tooth loss more details). rate to molars with no FI (0.01 teeth/patient/ The main differential diagnostic elements year; Nibali et al. 2016). For this reason, the to consider for complex treatment planning consensus opinion at present is that degree I are briefly highlighted in Table 15.1. FI is not suitable for complex treatment such Bearing in mind all the factors discussed, as periodontal regeneration. Authors of a treatment guidelines for different degrees of previous systematic review had also con- FI are proposed in the following sections. cluded that degree I FI could be success- These cannot be applied as ‘blanket’ fully managed by non‐surgical mechanical treatment guidelines, but need to be adapted debridement (Huynh‐Ba et al. 2009). to every different patient and every different Less is known about FI degree I molars not molar. undergoing regular periodontal care. Data Furcations: A Treatment Algorithm 271
Table 15.1 Main differential diagnostic elements to consider for complex furcation treatment planning.
Factors Thresholds/grades
ANATOMY Endodontic status Degree 1–5 (Ørstavik et al. 1986) Restorability Class I–III (Esteves et al. 2011) Degree of furcation involvement I–III (Hamp et al. 1975) Number of furcation Single, double, or triple involvements Vertical probing A–C (Tarnow and Fletcher 1984) Degree of separation (root 30° (Muller and Eger 1999) divergence) Separation degree ⅓ (Muller and Eger 1999) Bone loss ⅓, ⅔ of root length (Muller and Eger 1999) Position of furcation fornix Coronal or apical (Bowers et al. 2003) relative to bone crest and interproximal bone levels Furcation width Narrow or wide (Horwitz et al. 2004) Other anatomical features Length of root cone, root trunk etc.
PATIENT Medical history Healthy vs medically compromised Smoking Current/former/never Preferences/motivation Refusal to undergo surgery Financial Inability/unwillingness to pay for complex treatment Oral hygiene dexterity Inability to access furcation entrance
OPERATOR Ability/experience
STRATEGY Abutment Functional
RISK Anatomical risks, surgical risks
ALTERNATIVES Replacement with implant, prosthetic bridge, removable denture from SHIP (Study for Health In Pomerania) degree I FI and might interfere with oral show an incidence rate ratio (IRR) for molar hygiene manoeuvres (see Figure 15.2). loss of 1.73 (95% confidence interval [CI] 1.34–2.23, p < 0.001) for degree I FI versus no FI after 11 years of follow‐up, suggesting that 15.4 Degree II Furcation ‘no treatment’ worsens the prognosis of molars Involvement with FI degree I (Nibali et al. 2017a). Therefore, it could be suggested that oral The real complexity starts when considering hygiene instructions and non‐surgical therapy degree II FI, as this seems to be the threshold represent the treatment of choice for degree I at which the risk of tooth loss sharply increases FI, irrespective of location or other factors. (Nibali et al. 2016, 2017a). Therefore, treat- Odontoplasty might complement this treat- ment is needed to reduce the impact of such ment in cases where the furcation entrance FI in determining tooth loss. The main treat- anatomy might contribute to the presence of a ment goal should be the reduction of degree 272 Chapter 15
hygiene instructions and non‐surgical Furcation degree I therapy can already lead to the reduction of degree II FI to degree I FI through mecha- nisms including reduction of gingival oedema, epithelial reattachment, reduced probe penetration, and potentially radio- graphic bone fill (see the case in Figure 15.3). Oral hygiene and non-surgical However, residual degree II FI after causal maintenance therapy needs to be further addressed. (consider odontoplasty) 15.4.1 Mandibular Degree II Furcations Supportive periodontal therapy Except for cases of degree II FI after initial Figure 15.2 Proposed algorithm for furcation periodontal therapy where odontoplasty treatment (degree I furcation involvement). and/or surgical osteoplasty could lead to a reduction to degree I FI, reduction of degree II FI could be achieved via regenerative ther- II FI to degree I FI or to no FI (ideal). It is apy. Chapters 6 and 7 have presented the evi- implied that oral hygiene instructions and dence for the efficacy of regeneration in non‐surgical therapy (with or without furcations. Based on the discussion in these adjuncts) are a prerequisite for this treatment chapters, an important differentiation needs algorithm, and they should always represent to be made between maxillary and mandibu- the starting point. In some occasions, oral lar degree II furcations. Figure 15.4 shows a
(a) (b)
Figure 15.3 (a) Periapical radiographs of molars of a female 32‐year‐old aggressive periodontitis patient at periodontal diagnosis. Radiolucency inside the furcation areas is visible, particularly for UR6 and 7 (both degree II clinical furcation involvement [FI] diagnosis), UL6 and 7 (degree I FI), LL6 (degree I FI), and LR6 (degree II FI), often associated with intrabony defects. (b) Periapical radiographs of the same molars one year after initial periodontal therapy (oral hygiene instructions and supra‐ and subgingival debridement with adjunctive systemic antibiotics and extraction of UL8), showing radiographic bone fill in furcation defects and intrabony defects, associated with clinical reduction of FI degrees (now only degree I for UR6 and 7, UL6 and 7, and LR6). Furcations: A Treatment Algorithm 273
Mandibular degree II
Single Combined
II + I II + II
Regeneration Regeneration Tunnelling
Non-surgical Non-surgical maintenance, maintenance, odontoplasty Non-surgical odontoplasty maintenance, Resection/hemisection odontoplasty Access flap/apically Access flap/apically positioned flap/ positioned flap/ osteoplasty osteoplasty Access flap/apically Regeneration positioned flap/ osteplasty
Supportive periodontal therapy
Figure 15.4 Proposed algorithm for furcation treatment (degree II mandibular furcation involvement).
proposed algorithm for the treatment of are non‐surgical maintenance/SPT, access mandibular degree II FI. A hierarchy is pre- flap with or without osteoplasty, or apically sented starting from the preferred choice at positioned flap (APF), to improve access for the top, although this is rather arbitrary and professional cleaning of the furcation region. not strictly evidence based. Similar treatment options are recommended Another important differentiation to be for combined degree II and I mandibular drawn is based on whether the furcation is furcations. single (e.g. only buccal or only lingual) or However, when double degree II mandibu- double (both buccal and lingual). In a case of lar furcations are present, regeneration single degree II mandibular FI following becomes much less predictable, albeit not initial therapy, regeneration seems to be the impossible (see Figure 15.5, in relation to preferred choice. The evidence reviewed by Case 2 described in Chapter 14). Jepsen and Jepsen in Chapter 7 shows that, In contrast, tunnelling comes into play as although complete furcation closure in degree probably the preferred option. Tunnelling II FI is not a predictable outcome, treatment surgery can improve access to self‐performed, with either guided tissue regeneration (GTR) as well as professional, cleaning of the furca- or enamel matrix derivative (EMD) has pro- tion area, so it could be indicated too in cases duced histological evidence of regeneration of double degree II mandibular FI. Studies (Stoller et al. 2001; Nevins et al. 2003) and with 5–10 years follow‐up show success rates consistently more favourable clinical out- varying between 51 and 93% (Hamp et al. comes (reduction to degree I or closure) 1975; Dannewitz et al. 2006). Patient selec- compared with access flaps, especially in tion (good oral hygiene and motivation, low mandibular furcations (Jepsen et al. 2002, caries risk) and tooth selection (short root 2004). Alternatives to regenerative therapy trunk, favourable root divergence; Muller 274 Chapter 15
(a) (b)
(c) (d)
(e) (f)
Figure 15.5 Clinical photograph (a) and periapical radiograph (b) of 47‐year‐old patient diagnosed with chronic periodontitis and affected by double degree II furcation involvement and distal intrabony defect (disto‐buccal and disto‐lingual probing pocket depth [PPD] 12 mm) on tooth 36 (LL6). Following non‐surgical periodontal therapy, regenerative surgery with enamel matrix derivative was carried out (c and d, buccal and lingual intra‐operative views after full‐thickness flaps elevation), with favourable outcomes at five years after surgery, with reduction of PPD to 4 mm and only degree I furcation lingual (e) and fill of intrabony and furcation defect (f).
and Eger 1999) are vital for tunnelling, and hemisection, or access flap (or APF) are also for access reasons mandibular furcations realistic. We should bear in mind that root‐ are clearly more suitable. resection studies with follow‐ups at 5–10 Other options such as non‐surgical years showed success rates of 62–100% maintenance/odontoplasty, root resection/ (Carnevale et al. 1998; Dannewitz et al. 2006) Furcations: A Treatment Algorithm 275 and, with the exception of three studies, the such results are more predictable in buccal average survival rate of the molars treated sites (Pontoriero and Lindhe 1995a). with root separation/resection was close to Therefore, regeneration could be a good 90% (see Chapter 8). Access flap (or APF) with alternative to non‐surgical maintenance, or without ostectomy could improve access odontoplasty, and access flap surgery in for professional cleaning of the furcation area order to reduce the buccal furcation to and lead to reduction of probing pocket degree I or to achieve complete closure. The depths and inflammation (Wang et al. 1994). decision for regenerative therapy would depend on factors mentioned in the previous 15.4.2 Single Maxillary Degree II section (see Table 15.1), such as smoking and Buccal Furcations financial considerations, as well as good interproximal bone levels, reduced vertical Maxillary molars with degree II FI after furcation component, and reduced furcation initial periodontal therapy present probably width, all shown to favour regeneration in the most challenging scenario in terms of animal and human studies (Pontoriero et al. potential treatment choices and expected 1992; Bowers et al. 2003; Horwitz et al. 2004). outcome. Again, in the absence of rand- omized controlled trials comparing all 15.4.3 Single Maxillary Degree II options, we need to draw guidelines mainly Interproximal Furcations based on low‐evidence studies, experience, and common sense. Figure 15.6 shows Overall, the application of GTR, EMD, or options for degree II maxillary furcations. combination therapy (EMD/bone grafts) to Favourable results could be achieved with proximal furcations in maxillary molars GTR therapy and EMD in maxillary degree II achieved some furcation closures, but was furcations (Yukna and Yukna 1996; Casarin not as favourable as that in mandibular et al. 2010), but the evidence suggests that furcations or buccal maxillary furcations
Maxillary degree II
Single Combined
Buccal Interproximal Interproximal Buccal/interproximal
Regeneration Non-surgical Access flap/apically Access flap/apically maintenance, positioned flap/ positioned flap/ Non-surgical odontoplasty osteoplasty osteoplasty maintenance, Non-surgical odontoplasty Access flap/osteoplasty Resection/root maintenance, separation odontoplasty Access flap/apically Regeneration Tunnelling positioned flap/ Resection/ osteoplasty Resection root separation Non-surgical maintenance, Tunnelling odontoplasty
Supportive periodontal therapy
Figure 15.6 Proposed algorithm for furcation treatment (degree II maxillary furcation involvement). 276 Chapter 15
(Pontoriero and Lindhe 1995a; Avera degree II FI) is less favourable owing to ana- et al. 1998; Casarin et al. 2010; Peres et al. tomical features (see Chapter 8), and that 2013). Therefore, non‐surgical maintenance/ access to the furcation tunnel for self‐per- odontoplasty, access flap/osteoplasty (or formed hygiene is easier from a buccal access APF), and potentially also root resection (see Chapter 9). Therefore, a slightly different could be valid alternatives. The latter could hierarchy of choice is presented in Figure 15.6, be particularly suitable for previously endo- with root resection and tunnelling consid- dontically treated molars. ered to have more ‘worth’ for combined buccal–interproximal FI, and more conserva- 15.4.4 Combined Maxillary tive options probably indicated for combined Degree II Furcations interproximal furcations. The unlikely case of triple non‐through‐ Although regenerative periodontal therapy and‐through degree II furcation involvement may be a viable option for degree II maxillary could be considered within the degree III FI molars, this would be probably only limited treatment options. to single degree II maxillary defects, as the unpredictability would certainly increase several‐fold in multiple degree II maxillary FI 15.5 Degree III Furcation (which often could hide a true degree III FI). Involvement Therefore, root resection, access flap, and tunnelling procedures are probably the best When bone loss in the furcation area goes alternatives to choose from in these cases. through and through, from one root‐separation As previously discussed for mandibular area to another on the same tooth, we are degree II furcations, root‐resective surgery faced with degree III FI. The main treatment and access flap/APF with or without ostec- challenge here derives from the limitations of tomy could be good potential alternatives regenerative therapy in such cases. No clini- (Wang et al. 1994; Carnevale et al. 1998). cal study in humans has so far reported any Root resection/separation is mainly recom- degree III furcation closures with GTR, EMD, mended for previously endodontically or both combined, but only clinical reduc- treated maxillary molars with combined tions in furcation degree in some very lim- furcations degree II, particularly when the ited cases (Pontoriero et al. 1989; Pontoriero worst‐affected root is the disto‐buccal. and Lindhe 1995b; Eickholz et al. 1998, 1999; Tunnelling, given the correct patient and Jepsen et al. 2002; Donos et al. 2004). Jepsen molar selection, could be another appropri- and Jepsen in Chapter 7 reviewed the availa- ate treatment choice in selected cases. ble evidence to conclude that degree III FI When for patient or tooth reasons these cannot be improved predictably by regenera- options are not feasible or not worth pursu- tive therapy, until new developments in ing, non‐surgical maintenance with frequent regenerative material and techniques are SPT recalls based on a patient risk profile available (discussed in Chapter 6). Therefore, (Lang and Tonetti 2003) remains a valid it would be difficult to justify the use of option, with the clear limitation of difficul- regenerative surgery on degree III FI at pre- ties in achieving proper debridement of the sent. The persistence of a degree III furcation furcation area (Fleischer et al. 1989). defect which is not regenerable and is diffi- Root resection and tunnelling options may cult to clean (see Chapter 3) equals a higher be more indicated in cases of combined risk of future tooth loss than for degree I and buccal/interproximal degree II furcations, degree II FI molars (Nibali et al. 2016). Hence rather than when both are interproximal. the need to find a solution to manage these The reasons for this are that resecting the cases and to reduce the risk of tooth loss. palatal root (in cases of mesial and distal The treatment options are presented in Furcations: A Treatment Algorithm 277
Maxillary degree III Mandibular degree III
Root resection/separation Tunnelling
Non-surgical maintenance Root separation
Tunnelling Non-surgical maintenance
Root separation Root resection
Extraction Extraction
Supportive periodontal therapy
Figure 15.7 Proposed algorithm for furcation treatment (degree III furcation involvement).
Figure 15.7, divided between maxillary and avoided in cases with high caries risk, high mandibular molars. tooth sensitivity, poor compliance, or poor The difference, clearly, is that maxillary manual dexterity, as lack of proper oral molars, with three furcation entrances, could hygiene defies the purpose of this therapy. potentially have three through‐and‐through Molars with a short root trunk, high degree furcation lesions, making the access for clean- of separation (root divergence), and a large ing (both professional and self‐performed) band of keratinized gingiva are particularly very challenging. On the other hand, suitable for this procedure (see Chapter 9). mandibular degree III FI molars can only When tunnelling is not indicated, root sepa- have one through‐and‐through furcation ration (premolarization) could be considered lesion, with access both buccally and a valid alternative, especially in cases of good lingually. While bearing in mind the evidence residual bone support in the distal aspect of of success for tunnelling and root‐resection the distal root and in the mesial aspect of the procedures in long‐term clinical trials mesial root. This would again aim to improve (Helldén et al. 1989; Carnevale et al. 1998), cleaning (by removal of the furcation region), we need to stress the importance of proper but would entail extensive restorative work. diagnosis and patient and molar selection. Long‐term non‐surgical maintenance The factors highlighted in Table 15.1 need (preceded or not by surgical access) and root again to be kept in mind in order to ensure resection represent possible alternatives if long‐term success. tooth survival is chosen.
15.5.1 Mandibular Degree III 15.5.2 Maxillary Degree III Furcations Furcations
Tunnelling could be considered the treat- Root resection or non‐surgical maintenance ment of choice for mandibular degree III FI. could be considered the treatment of choice As already mentioned, tunnelling should be for degree III FI maxillary molars. These two 278 Chapter 15
procedures have different indications, as root 10–15‐year period of periodontal supportive resection is generally more advisable in the care (Nibali et al. 2016), meaning that extrac- case of a double degree III FI, mainly affecting tion of molars affected by degree III FI should one root. In this case, the resection of a root not be a given. (preferably if it is the smallest disto‐bucc al root) could leave two easily maintainable roots with no FI. As Rotundo and Fonzar dis- 15.6 Upper Premolars cussed in Chapter 6, root resection in a case of a triple degree III FI is less advisable, as it Upper first premolars are normally two‐ would anyway result in a residual difficult‐to‐ rooted, while second maxillary premolars clean furcation. In such a case (triple degree and mandibular canines are occasionally III FI), regular subgingival debridement two‐rooted. However, very little data exist in seems the most reasonable option in cases the literature about the treatment of non‐ where tooth survival is preferred. This could molar teeth with FI (Hamp et al. 1975). be preceded or not by surgical access for As discussed in Chapter 7, the majority of furcation debridement, shown to improve maxillary first premolars have fused roots. In professional cleaning efficacy (see Chapter 3). upper premolars with separated roots, the Other factors mentioned earlier, such as furcation entrance is on average 8 mm apical patient preferences and financial considera- to the cemento‐enamel junction and only tions, play an important role in the decision 7–10% of furcation entrances are in the coro- of whether to maintain such teeth or not. nal third of the root (Joseph et al. 1996; Under exceptional circumstances, tunnel- Dababneh and Rodan 2013). Furthermore, ling could be considered an option for triple root grooves and concavities are the norm in degree III FI, mainly in cases of very compli- upper premolars. Owing to these anatomical ant patients with good manual dexterity and features, root resection and tunnelling are low caries risk. Tunnelling can occur either not usually viable options for upper premo- naturally, by virtue of gingival recession, as a lars with FI, and access flap and/or non‐ result of oral hygiene and non‐surgical ther- surgical maintenance should be preferred. apy, or can be created surgically. The main reason for the failure of tunnelling is not periodontal but restorative, linked with root 15.7 Innovative Treatment caries following the exposure of the root sur- face (Helldén et al. 1989). Figure 15.8 shows a Novel treatments for furcation‐involved case of surgically created triple degree III FI teeth were discussed in Chapter 10. Some of in maxillary molars maintained for over these, such as adjunctive photodynamic 10 years with no clinical and radiographic therapy, lasers, or air‐polishing devices, signs of disease progression or caries (Case 1 could be added to the options discussed in described in Chapter 14). this chapter, although more evidence needs Root separation is also a possible option to be gathered before routinely recommend- for degree III maxillary molars, associated or ing these therapies. not with root resection. Careful endodontic and prosthetic considerations are needed before deciding on this treatment option (Carnevale et al. 1998). 15.8 So, When Should However, in making the decision on We Extract? whether to extract or not, one should take into account that, despite a higher tooth loss The emphasis of this chapter, and perhaps of risk, the majority of maxillary degree III FI the whole book, has been on tooth retention. molars could be maintained over at least a However, there are cases where even the most (a) (b) (c) (d)
(e) (f) (g) (h)
(i) (j)
Figure 15.8 Clinical photograph (a) and periapical radiographs (b and c) of 50‐year‐old patient diagnosed with chronic periodontitis and affected by triple degree III furcation involvement on 17 (UR7), 16 (UR6), and 27 (UL7). Following non‐surgical periodontal therapy, tunnelling surgery was carried out (d, intra‐operative view after full‐thickness flaps elevation and osteoplasty), with favourable outcomes at 12 years after surgery with probing pocket depths < 5 mm (e), continued good oral hygiene access to furcations (f, g, and h), and stable radiographic bone levels (i and j).
Chapter No.: 1 Title Name:
daring periodontist has to admit that a tooth (PAI) score of 4 (Ørstavik et al. 1986), or with is hopeless or irrational to treat, and extraction mobility grade III or FI degree III (Nibali et al. might be the best option. Several definitions 2017b). This new prognostic system aims to of ‘hopeless’ have been proposed in the peri- be more conservative than previous propos- odontal literature. Becker and colle agues als, based on the data discussed earlier show- (1984) reported a range of criteria for hopeless ing that degree III FI alone should not qualify teeth, including degree III FI or bone a tooth as hopeless (Nibali et al. 2016). In the loss > 75%. Machtei and co‐workers (1989) reality of everyday practice, patient‐related defined as hopeless teeth with bone loss ≥ 50%, factors (e.g. risk of caries, compliance, and or radiographic evidence of total bone loss in smoking), patient preferences, financial con- the furcation area (grade III FI). In their land- siderations, and overall strategic value need mark prognosis paper, McGuire and Nunn to accompany clinical and radiographic crite- (1996) more vaguely identified as hopeless ria in reaching a decision about maintaining teeth with ‘inadequate attachment’. Hopeless or extracting. Further considerations on has also been defined as having loss of ≥ 70% possible extraction and implant replacement bone height (Graetz et al. 2011) or as having can be found in Chapter 11. bone loss to the apex (Cortellini et al. 2011). Finally, it is important to remember that We recently assigned an ‘unfavourable’ community‐wide oral hygiene instruction prognosis to teeth with ≥ 70% bone loss which and primary prevention programmes are the were also either unrestorable (Esteves et al. best measures for reducing oral diseases and 2011), with an endodontic periapical index tooth loss.
Summary of Evidence
●● Furcation diagnosis is crucial for treat- be carefully considered before embarking ment planning purposes. on treatment or extraction. ●● Degree I, II, and III maxillary and man- ●● A holistic approach, including clinical and dibular molars have very different treat- radiographic parameters but also overall ment indications. strategic tooth value, financial considera- ●● Degree I furcation involvement (FI) has a tions, and patient preferences, needs to be good long‐term prognosis and does not pursued in order to obtain the most satis- represent a higher risk of tooth loss if factory outcome of furcation therapy. under periodontal maintenance care. ●● General dentists should bear in mind that ●● Degree II FI could benefit from periodon- referral to a periodontist is advised for tal regeneration or other conservative molars with severe FI, and that most therapy (or root resection). molars with FI can be maintained func- ●● Degree II interproximal maxillary FI is tionally in the long term. less suitable for regeneration. ●● Adherence to patient‐tailored supportive ●● Degree III FI is linked with a higher risk of periodontal therapy is crucial to reduce tooth loss and treatment options need to the long‐term tooth loss risk.
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Index
Page numbers in italics refer to illustrations; those in bold refer to tables
a naturally occurring periodontitis 107, accessory canals 56–57, 57 111–112 Acute Defect Model 107, 111 ethical codes 127 Acute/Chronic Defect Model 107–108, limitations 125–127 111–112, 115–116 antimicrobial treatment air‐polishing devices 195–196 local 196–197, 198 allograft 48–49 systemic 197–199 alveolar ridge preservation 212–213 antiseptic treatment 196 amoxicillin 197–199 apical foramina 57–58 animal models of regenerative furcation therapy 105–128 b available models 105–106 barrier membranes see guided tissue dog 106 regeneration (GTR) miniature pig 106 bifurcation ridges 4–5, 4 primates 106 bite test 72 class II defects 110–117 bone grafts 48–49 bone grafts 110–113 animal models 110–113, 117–119 cell therapy 114–117 combined with enamel matrix enamel matrix proteins 13–114 derivative 147–148 growth factors 114, 115–116 combined with guided tissue guided tissue regeneration 110–113 regeneration 139–144, 145 class III defects 117–124 bone loss 232–233, 238 bone grafts 117–119 implant positioning and 212–213 cell therapy 124 bone morphogenetic proteins (BMPs), animal enamel matrix proteins 119–120, 121, models 114, 121 122, 123 bone quality 211 growth factors 120–124 bone resorption 64 guided tissue regeneration 117, 118–119 c defect types 106–108 caries, after furcation tunnelling 185, critical size defect concept 108–110 188, 237 experimentally induced defects cavity test 76 107–108 cell therapy, animal models 114–116, 124, 125
Diagnosis and Treatment of Furcation-Involved Teeth, First Edition. Edited by Luigi Nibali. © 2018 John Wiley & Sons Ltd. Published 2018 by John Wiley & Sons Ltd. Companion website: www.wiley.com/go/nibali/diagnosis
Chapter No.: 1 Title Name:
cemento‐enamel junction (CEJ) 5 disease progression 91–92 cervical enamel projections (CEPs) 6–8, 7, 8, documentation 22, 24 48, 50 classification 6 e Chronic Defect Model 107, 112 economic aspects see health economic clinical diagnosis 15–22, 23 aspects examination 72 enamel matrix derivative (EMD) reproducibility and validity 22 animal models 113–114, 119–120, 121, see also diagnosis 122, 123, 125 cone‐beam computed tomography degree II furcation defects 144–148, (CBCT) 26–28, 26, 270 273, 274 costs combination therapy 147–148 cost‐effectiveness studies 230, mandibular molars 144–146, 147 239–242, 241 maxillary molars 146–147, 148 cost‐of‐disease studies 230 versus guided tissue regeneration cost‐utility analyses 230 144–146, 147 cost–benefit analysis 230 degree III furcation defects 149 furcation involvement costs 231–239, regenerative periodontal surgery 150 234–237 enamel pearls 8–9, 8, 9 see also health economic aspects endodontic‐periodontal disease cracked tooth syndrome 58 bacteria involved 59 cracked tooth testing 73 classification 63–71 critical size defect (CSD) 108–110 primary endodontic lesion 64, 65, 65, 66 curettes 39, 45, 46 primary endodontic lesion with secondary periodontal d involvement 66–68, 68 debridement 34, 39–45, 46 primary periodontal lesion 64–66, 67 effectiveness studies 40–45, 41–44 primary periodontal lesion with healing after 33–34 secondary endodontic imperfect 34 involvement 68–70, 69 longitudinal studies 34–38, 35–37 true combined lesion 70–71, 71, 72, 78 open flap 48–49, 50 diagnosis of see diagnosis versus guided tissue regeneration 139, effect on pulp tissue 60–63, 61–62 140–142 endodontically treated teeth 77–78 versus non‐surgical closed management 77 debridement 40 see also periodontitis dental floss 47 EuroQol Questionnaire 250 dentine tubules 55–56 diagnosis 71–77, 269–271 f algorithm 270, 270 fibroblast growth factor (FGF), animal case examples 257, 262–263, 262 models 114, 120–121 clinical 15–22, 23, 72 fistula tracking 73 pre‐surgical 161–162 fistulous sinus track 73, 73 radiographic 22–28, 25, 26, 73, 74, furcation probes 16–17, 16, 269 162, 269 furcation ridges 4–5, 4 reproducibility and validity 22 furcation tunnelling 177–185, 178 differential diagnosis 271 caries after 185, 188, 237 digital subtraction radiography (DSR) case examples 260, 261, 261, 264 25, 25 degree II furcation defects 273–274, 276 Index 287
degree III furcation defects 277, 278, 279 relevance of furcation follow‐up studies 186–187 involvement 229–230 indications 177–179 research gaps 242–243 maintenance phase 185 health‐related quality of life (HRQoL) 250 oral hygiene in the furcation 182–184, 183 home care 45–47 double tunnels 183–184, 184 horizontal bone augmentation 215 patient selection 179 horizontal probing attachment loss postoperative follow‐up 182–183 (PAL‐H) 15, 23 pulp reaction 184–185 horizontal probing bone level (PBL‐H) 15 tunnelling procedure 179–182, 180, 181, 182 i upper first premolar 184, 185 iatrogenic lesions 11, 78 inferior alveolar nerve damage 213–214 g root canal perforations 58 gingivectomy 179, 180 implant placement 209–211 gingivitis 10, 33 anatomical considerations 211–213 Gracey curettes 39, 45, 46 bone loss and implant positioning case examples 258, 263 212–213, 212 growth factors, animal models 114, 115–116, bone quality 211–212 120–124 bone augmentation in maxillary molar guided tissue regeneration (GTR) 79, region 214–217 109, 273 horizontal augmentation 215 animal models 109, 110–113, 117, osteome‐mediated sinus floor 124–125 elevation 216–217, 217 bone grafts and GTR 110–113 sinus lift 215–216 degree II furcation defects 138–144 case examples 260–261, 264 animal models 110–113 complications 219–220, 219 combination therapy 139–144, 145 mandibular molar region 213–214 long‐term results 144 bone augmentation 214 non‐resorbable versus biodegradable short implants 218–219 barrier membranes 139, 143 inferior alveolar nerve damage 213–214 versus enamel matrix derivative insulin growth factor (IGF‐1), animal 144–146, 147 models 114 versus open‐flap debridement 139, interdental brushes 46–47 140–142 case examples 258, 263 degree III furcation defects 148–149 tunnelling procedure and 179, 179, animal models 117 180, 180 mandibular molars 149 intermediate bifurcation ridge (IBR) 4 maxillary molars 149 regenerative periodontal surgery 150 l laser therapy 192–193 h lateral canals 56–57 healing after debridement 33–34 local antibiotic therapy 196–197, 198 health economic aspects low‐level laser therapy (LLLT) 193 case examples 261, 265 cost‐effectiveness studies 239–242, 241 m furcation involvement costs 231–239, magnetostrictive scalers 39 234–237 mesenchymal stem cells (MSCs) 114–117 health economic analysis 230–231 metronidazole 197–199 288 Index
microbial plaque see plaque patient‐reported outcome measures minimally invasive surgical therapy 200 (PROMS) mobility test 72 furcation involvement 251–252 molars 1 periodontology 249–251 anatomical aetiological factors 6–9 overhanging dental restorations 11 cervical enamel projections 6–8, 6, 7, 8 p enamel pearls 8–9, 8, 9 palpation 72 anatomical factors in furcation patient feedback 252–254 involvement 2–6, 3 patient selection bifurcation ridges 4–5, 4 furcation tunnelling 179 furcation entrance area 3–4 regenerative furcation therapy 149 root surface area (RSA) 5 resective therapy 170 root trunk length 5–6 patient‐reported outcome measures anatomy 1–2 (PROMS) 249–252 development 2 furcation involvement 251–252 periodontal aetiological factors 9–11 implementation of in furcation iatrogenic factors 11 treatment 254–255 occlusal trauma 10 periodontology 249–251 plaque‐associated inflammation 10 percussion 72 pulpal pathology 10–11 peri‐implantitis 219–220 vertical root fractures 10, 58, 58, 59 risk factors 219–220 root resection 27 therapy 220 multi‐rooted teeth 15–16, 16 periodontal chart 24 periodontal endoscope 191–192 o periodontal ligament (PDL) 114 occlusal trauma 10, 73, 74 periodontal therapy 92, 92 open flap debridement 48–49, 50 periodontitis 10, 33, 40, 64–66, 101, 199 versus guided tissue regeneration 139, disease progression 91–92 140–142 model 239, 240 versus non‐surgical closed debridement 40 see also tooth loss Oral Health Impact Profile (OHIP‐14) 250 furcation involvement frequency 28–29 oral health‐related quality of life health economics studies 232, 233, 238, (OHRQoL) 250, 251 242, 243 implementation of in furcation treatment see also endodontic‐periodontal disease 254–255 photodynamic therapy (PDT) 193–195, 194 oral hygiene phototherapy 193 after furcation tunnelling 182–184, 183 piezoelectric scalers 39, 46 degree I furcation involvement 271 plaque 33–34 patient home care 45–47 removal 33–34 Oral Impacts on Daily Performance (OIDP) effectiveness evaluation 38 questionnaire 250, 251 see also debridement Osteogain 120 role in gingivitis and periodontitis 33 osteogenic protein‐1 (OP‐1) 121–124 plaque‐associated inflammation 10 osteoplasty 180, 181 platelet‐derived growth factor (PDGF), animal outcome measures 137–138 models 114, 121 clinical outcomes 138 platelet‐rich fibrin (PRF) 148 degree II furcation defects 137–138 platelet‐rich plasma (PRP) 114–117, 148 degree III furcation defects 138 pocket probing 73–74 histology 137 povidone‐iodine 197 Index 289 powered scalers 39 see also animal models of regenerative powered toothbrushes 45–46 furcation therapy probes 16–17, 16, 269 resective therapy 80–82, 81, 161–173 probing 73–74 anatomical considerations 161 probiotics 199–200 case examples 260, 264 pulp vitality tests 74–76, 75 contraindications 169–170 pulpal pathology 10–11 degree II furcation defects 276 necrosis 63, 69, 70, 76 degree III furcation defects 277–278 periodontal disease relationship 60–63, indications 163–167 61–62 root resection 164–167, 165 periodontal furcation therapy root separation 163–164, 164, 166–167, relationship 78–82 166, 167 non‐surgical therapy 78–79 furcation tunnelling 177–179 regenerative therapy 79–80 patient selection 170 resective therapy 80–82 pre‐surgical diagnosis 161–162 pulpitis 65, 76 procedure 170–173 reaction to tunnelling procedure 184–185 crown build‐up 171 endodontic treatment 170 r final prosthesis 173 radiographic diagnosis 22–28, 73, 74, 269 periodontal surgery 172–173 digital subtraction radiography (DSR) provisional restoration 172 25, 25 root separation/resection 171–172 pre‐surgical 162 pulp relationship 80–82 radiation exposure issues 28 recommendations 82 three‐dimensional radiography 26–28, 26 scientific studies 167, 168, 169 regenerative furcation therapy 79–80, 105, tooth selection 170 137–152 restorations, overhanging 11 case examples 260, 263–264 rizectomy 59, 78, 165, 166 challenges 150–151 rizotomy 164 degree II furcation defects 138–148, root canal 273, 275 accessory canals 56–57, 57 enamel matrix derivative 144–148 iatrogenic perforations 58 guided tissue regeneration 138–144 root complex 5 platelet concentrates 148 root cone length 6 degree III furcation defects 148–149 root dentine hypersensitivity 79 enamel matrix derivative 149 root fractures 10, 58, 58, 59 guided tissue regeneration 148–149 root resection 27 outcome measures 137–138 root resorption 58–59, 60 clinical outcomes 138 root separation 163–164, 164 degree II furcation defects 137–138 root surface area (RSA) 5 degree III furcation defects 138 mandible 5 histology 137 maxilla 5 see also patient‐reported outcome root trunk length 5–6 measures (PROMS) patient selection 149 s pulp relationship 79–80 scaling and root planing 33–34, 39 recommendations 80 case examples 258, 263 regenerative periodontal surgery 150, endoscopy‐aided 191–192 151, 152 healing after 33–34 tooth selection 149–150 see also debridement 290 Index
selective anaesthesia test 77 study procedures 95–97 short implants 218–219 treated teeth 93–99 sinus lift 215–216 untreated furcation‐involved teeth 93 osteome‐mediated sinus floor elevation tooth mobility 72 216–217, 217 tooth selection sonic scalers 39 regenerative furcation therapy 149–150 split‐mouth design 34 resective therapy 170 stellate reticulum 2 toothbrushes 45–46 surgical treatment transforming growth factor‐beta (TGF‐β), furcation regeneration 149–150 animal models 114 patient selection 149 treatment regenerative periodontal surgery 150 degree I furcation involvement tooth selection 149–150, 151 270–271, 272 innovations 200 degree II furcation involvement 271–276, minimally invasive surgery 200 273, 275 root separation/resection 170–173 mandibular 272–275, 273 crown build‐up 171 maxillary, combined 276 during preliminary prosthetic maxillary, single buccal 275, 275 preparation 171–172 maxillary, single interproximal 275–276 endodontic treatment 170 degree III furcation involvement final prosthesis 173 276–278, 277 patient selection 170 mandibular 277 periodontal surgery 172–173 maxillary 277–278, 279 provisional restoration 172 innovative treatment 278 tooth selection 170 options 162–163 tunnelling procedure 179–182, 180, treatment versus extraction and 181, 182 implants 209–211 see also open flap debridement; resective upper premolars 184, 185, 278 therapy when to extract 278–280 systemic antimicrobial treatment 197–199 see also specific treatments tunnelling see furcation tunnelling t tetracyclines 197–199 u three‐dimensional radiography 26–28, 26 ultrasonic scalers 39, 45, 47, 258, 263 tooth extraction upper premolar treatment 278 versus treatment 209–211 furcation tunnelling 184, 185 when to extract 278–280 see also implant placement v tooth loss 92–101 vertical root fractures 10, 58, 58, 59 by different furcation degree 99 by vertical furcation component 99 w risk of 98, 99–101, 100 WaterPik 47