Dental and Medical Problems

QUARTERLY ISSN 1644-387X (PRINT) ISSN 2300-9020 (ONLINE) www.dmp.umed.wroc.pl 2018, Vol. 54, No. 1 (January–March)

Ministry of Science and Higher Education – 11 pts. Index Copernicus (ICV) – 113.75 pts.

ISSN 1644-387X (PRINT) ISSN 2300-9020 (ONLINE) www.dmp.umed.wroc.pl

QUARTERLY Dental and Medical Problems is a peer-reviewed open access journal published by Wroclaw Medical 2017, Vol. 54, No. 1 University and Polish Dental Society. Journal publishes articles from different fields of dentistry and other medical, biological, deontological and historical articles, which were deemed important to dentistry by the (January-March) Editorial Board. Original papers (clinical and experimental), reviews, clinical cases, letters to the Editorial Board and reports from domestic and international academic conferences are considered for publication.

Editor-in-Chief Secretary Address of Editorial Office Tomasz Konopka Anna Paradowska-Stolarz Marcinkowskiego 2–6 50-368 Wrocław, Poland Vice-Editor-in-Chief tel.: +48 71 784 11 33, +48 71 784 15 86 Raphael Olszewski e-mail: [email protected] Thematic Editors Andrzej Wojtowicz (Oral Surgery) Teresa Bachanek (Cariology) Marcin Kozakiewicz (Maxillofacial Surgery) Publisher Mariusz Lipski (Endodontics) Teresa Sierpińska (Prosthodotics) Wroclaw Medical University Urszula Kaczmarek (Pedodontics Jolanta Kostrzewa-Janicka (Disorders Wybrzeże L. Pasteura 1 and Dental Prevention) of Mastification System) 50-367 Wrocław, Poland Renata Górska (Oral Pathology) Beata Kawala (Orthodontic) Alina Pürienè (Periodontology) Ingrid Różyło-Kalinowska (Dental Radiology) Polish Dental Society Piotr Majewski (Implantology) Montelupich 4 31-155 Kraków, Poland International Advisory Board (Russia), Piotr Majewski (Poland), Joseph Teresa Bachanek (Poland), Einar Berg Nissan (Israel), Leszek Paradowski (Poland), © Copyright by Wroclaw Medical University (Norway), Wojciech Blonski (USA), Maria Hyo-Sang Park (Korea), Alina Pürienè and Polish Dental Society, Wrocław 2017 Buscemi (Italy), Maria Chomyszyn-Gajewska (Lithuania), Małgorzata Radwan-Oczko (Poland), Ewa Czochrowska (Poland), (Poland), Monique-Marie Rousset-Caron Online edition is the original version of the journal Petr Dítĕ (Czech Republic), Marzena (France), Mykola Mychajlovych Rozhko Dominiak (Poland), Barbara Dorocka- (Ukraine), Ingrid Różyło-Kalinowska -Bobkowska (Poland), Omar El-Mowafy (Poland), Teresa Sierpińska (Poland), (Canada), Katarzyna Emerich (Poland), Jerzy Sokalski (Poland), Jerzy Sokołowski Thomas Gedrange (Germany), Hanna Gerber (Poland), Franciszek Szatko (Poland), Jacek (Poland), Jakub Gołąb (Poland), Renata C. Szepietowski (Poland), Selena Toma Górska (Poland), David Herrera (Spain), (Belgium), Danuta Waszkiel (Poland), Michał Jeleń (Poland), Urszula Kaczmarek Andrzej Wojtowicz (Poland), Dariusz (Poland), Milan Kamínek (Czech Republic), Wołowiec (Poland), Krzysztof Woźniak Beata Kawala (Poland), Kazimierz Kobus (Poland), Grażyna Wyszyńska- (Poland), Krystyna Konopka (USA), Jolanta -Pawelec (Poland), Anna Zalewska (Poland), Kostrzewa-Janicka (Poland), Marcin Marek Ziętek (Poland), Elena Borisovna Zueva Kozakiewicz (Poland), Tadeusz F. Krzemiński (Uzbekistan) (Poland), Nazan Küçükkeleş (Turkey), Mariusz Lipski (Poland), Marina V. Maevskaya Statistical Editor Krzysztof Topolski Technical Editorship Paulina Kunicka Aleksandra Raczkowska Alicja Wojciechowska English Language Copy Editors Sherill Howard-Pociecha Jason Schock Marcin Tereszewski

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Circulation: 115 copies Dental and Medical Problems ISSN 1644-387X (PRINT) ISSN 2300-9020 (ONLINE) QUARTERLY 2017, Vol. 54, No. 1 (January-March) www.dmp.umed.wroc.pl Contents

7 From Editor-in-Chief 9 New Members of the Editorial Board

Original papers 13 Ludmiła Halczy-Kowalik, Robert Kowalczyk, Anna Rzewuska, Violetta Posio Peripheral blood saturation and pulse rate during swallowing in patients with oral cavity neoplasm and after its excision 21 Aneta Neskoromna-Jędrzejczak, Bogusław Antoszewski, Katarzyna Bogusiak Animal related facial trauma 29 Paulina Czarnecka, Monika Rutkowska, Paweł Popecki, Grzegorz Grodoń Chronic odontogenic paranasal sinusitis in the material provided by the Otorhinolaryngology Unit of the 4th Military Teaching Hospital in Wroclaw 35 Jolanta E. Loster, Aneta Wieczorek, Wojciech I. Ryniewicz Condylar guidance angles obtained from panoramic radiographic images: An evaluation of their reproducibility 41 Magdalena Sulewska, Jan Pietruski, Agnieszka Tycińska, Włodzimierz Musiał, Ewa Duraj, Małgorzata Pietruska Evaluation of non-surgical periodontal treatment in patients with a past history of myocardial infarction 49 Raoul Bationo, Wendpouiré P. L. Guiguimdé, Hamidou Ouédraogo, Blintim Somé Dental emergencies in Burkina Faso Armed Forces 53 Radosław Markowski, Sławomir Ledzion, Halina Pawlicka Evaluation of marginal integrity of materials used in root postresorption cavities 59 Magdalena Sulewska, Jan Pietruski, Renata Górska, Edyta Sulima, Rafał Świsłocki, Agnieszka Paniczko, Elżbieta Sokal, Małgorzata Pietruska Evaluation of the incidence of gingival recession in the citizens of a large urban agglomeration of the Podlaskie Province in the chosen age groups of 35–44 years and 65–74 years 67 Gülsüm Duruk, Hulya Aksoy, Taskın Gurbuz, Esra Laloglu, Huseyin Tan Oral hygiene in children with epilepsy: Effect of interleukin-1β and VEGF levels in gingival crevicular fluid 73 Katarzyna Sopińska, Natalia Olszewska, Elżbieta Bołtacz-Rzepkowska The effect of dental anxiety on the dental status of adult patients in the Lodz region

Reviews 79 Przemysław Leszczyński, Jerzy Sokalski The use of fractal analysis in medicine: A literature review

Clinical cases 85 Suwarna Dangore-Khasbage Clinical aspects of oral cancer: A case report series 91 Patrycja Proc, Małgorzata Zubowska, Anna Janas-Naze A dentigerous cyst in a patient treated for an odontogenic myxoma of the maxilla: A case report 97 Kamakshi L. N. V. Alekhya, David Kadakampally Reccurent peripheral giant cell granuloma: A case report

101 Jacek Matys, Katarzyna Świder, Rafał Flieger Laser instant implant impression method: A case presentation 107 Valentyn Makeyev, Nataliya Pylypiv, Volodymir Shybinskyy Characteristic features of orthodontic treatment of tooth retention caused by hyperdontia

Letter to Editor 115 Siddharth Mehta Letter to the Editor on the article „Soft tissue profile changes after mandibular setback surgery” (Dental and Medical Problems 2016, 53, 4, 447–453) 117 Katarzyna Bogusiak, Marek Kociński, Adam Łutkowski, Andrzej Materka, Aneta Neskoromna-Jędrzejczak Reply to the Letter to the Editor on the article „Soft tissue profile changes after mandibular setback surgery” (Dental and Medical Problems 2016, 53, 4, 447–453) Dental and Medical Problems ISSN 1644-387X (PRINT) ISSN 2300-9020 (ONLINE) Kwartalnik, 2017, tom 54, nr 1 (styczeń-marzec) www.dmp.umed.wroc.pl Spis treści

7 Od Redaktora 9 Nowi członkowie Rady Naukowej Prace oryginalne 13 Ludmiła Halczy-Kowalik, Robert Kowalczyk, Anna Rzewuska, Violetta Posio Nasycenie krwi obwodowej tlenem i tętno podczas przełykania u pacjentów z nowotworem jamy ustnej oraz po jego wycięciu 21 Aneta Neskoromna-Jędrzejczak, Bogusław Antoszewski, Katarzyna Bogusiak Urazy twarzy wywołane przez zwierzęta 29 Paulina Czarnecka, Monika Rutkowska, Paweł Popecki, Grzegorz Grodoń Przewlekłe zębopochodne zapalenie zatok przynosowych w materiale Poradni Otolaryngologicznej 4. Wojskowego Szpitala Klinicznego we Wrocławiu 35 Jolanta E. Loster, Aneta Wieczorek, Wojciech I. Ryniewicz Wartości kątów drogi stawowej uzyskiwane ze zdjęć pantomograficznych – ocena powtarzalności metody 41 Magdalena Sulewska, Jan Pietruski, Agnieszka Tycińska, Włodzimierz Musiał, Ewa Duraj, Małgorzata Pietruska Ocena niechirurgicznego leczenia periodontologicznego u pacjentów z przebytym zawałem mięśnia sercowego 49 Raoul Bationo, Wendpouiré P. L. Guiguimdé, Hamidou Ouédraogo, Blintim Somé Nagłe przypadki stomatologiczne u żołnierzy sił zbrojnych Burkina Faso 53 Radosław Markowski, Sławomir Ledzion, Halina Pawlicka Ocena szczelności brzeżnej materiałów stosowanych do odbudowy tkanek korzenia zęba utraconych w wyniku resorpcji 59 Magdalena Sulewska, Jan Pietruski, Renata Górska, Edyta Sulima, Rafał Świsłocki, Agnieszka Paniczko, Elżbieta Sokal, Małgorzata Pietruska Ocena występowania recesji dziąseł u mieszkańców dużego miasta województwa podlaskiego w wybranych grupach wiekowych 35–44 oraz 65–74 lat 67 Gülsüm Duruk, Hulya Aksoy, Taskın Gurbuz, Esra Laloglu, Huseyin Tan Higiena jamy ustnej dzieci chorych na epilepsję a stężenie interleukiny 1β i czynnika wzrostu naczyniowo-śródbłonkowego w płynie dziąsłowym 73 Katarzyna Sopińska, Natalia Olszewska, Elżbieta Bołtacz-Rzepkowska Wpływ lęku stomatologicznego na stan uzębienia dorosłej populacji regionu łódzkiego

Prace poglądowe 79 Przemysław Leszczyński, Jerzy Sokalski Zastosowanie analizy fraktalnej w medycynie – przegląd piśmiennictwa

Prace kazuistyczne 85 Suwarna Dangore-Khasbage Kliniczne uwarunkowania raka jamy ustnej – opis przypadków 91 Patrycja Proc, Małgorzata Zubowska, Anna Janas-Naze Torbiel zawiązkowa zęba u pacjenta leczonego z powodu śluzaka zębopochodnego szczęki – opis przypadku 97 Kamakshi L. N. V. Alekhya, David Kadakampally Nawrotowy nadziąślak olbrzymiokomórkowy – opis przypadku

101 Jacek Matys, Katarzyna Świder, Rafał Flieger Metoda wycisku w implantacji natychmiastowej z użyciem lasera (LIIIM) – prezentacja przypadku 107 Valentyn Makeyev, Nataliya Pylypiv, Volodymir Shybinskyy Charakterystyka leczenia ortodontycznego zębów zatrzymanych z powodu ich nadliczbowości

Letter to Editor 115 Siddharth Mehta List do Redakcji dotyczący pracy pt. „Zmiana profilu tkanek miękkich po jednoszczękowych zabiegach korekcji progenii” (Dental and Medical Problems 2016, 53, 4, 447–453) 117 Katarzyna Bogusiak, Marek Kociński, Adam Łutkowski, Andrzej Materka, Aneta Neskoromna-Jędrzejczak Odpowiedź na list do Redakcji dotyczący pracy pt. „Zmiana profilu tkanek miękkich po jednoszczękowych zabiegach korekcji progenii” (Dental and Medical Problems 2016, 53, 4, 447–453) From Editor-in-Chief

Editors of Dental and Medical Problems would like to take this opportunity to thank the following people for their long-lasting contribution to the journal and for their work on the Editorial Board: – Prof. dr hab. Ryszard Koczorowski – Editorial Board member in 2010–2016 and the Thematic Editor for Gerodontology in 2012–2015 and Prosthetic Dentistry in 2016; – Dr hab. Zdzisław Bereznowski – Editorial Board member in 2009–2016; – Prof. José Duran von Arx – Editorial Board member in 2004–2016; – Prof. Charles Pilipili – Editorial Board member in 2007–2016; – Prof. Rostyslav Stupnytsky- Editorial Board member in 2011–2016. New Members of the Editorial Board

Barbara Dorocka-Bobkowska

Dr Barbara Dorocka-Bobkowska (MD, DDS, PhD) is a professor at the Poznan University of Medical Sciences and Head of the Department of Oral Mucosa Diseases. She graduated from the Medical Academy in Poznan where she completed her medical degree (1988), followed by a degree in dentistry (1991). She completed her medical residency in the Medical Academy Clinic in Poznan after which she joined the staff as a dentist in the Department of Prosthodontics of the Institute of Dentistry in Poznan (1992–2013). During this period, she received a PhD (dentistry) from the Poznan University of Medical Sciences in 1996 based on the research thesis entitled “Non-insulin dependent diabetes mellitus as a risk factor in the development of denture stomatitis – a mycological study”. The thesis received an award from the University Rector. In 1997 she completed her specialization in prosthodontics. In 2012 she received her habilitation based on the thesis entitled “Candida-associated denture stomatitis in patients with type 2 diabetes – clinical and laboratory studies” and in 2016 she was awarded the title of professor at the Poznan University of Medical Sciences. She is a specialist in clinical dentistry and prosthodontics, while her teaching interests include prosthodontics and oral mucosa diseases. She was also a tutor for the Students Research Group in the Department of Prostho- dontics and one of the principal initiators of the program within the prosthodontics course in the DDS program in Poznan Center of Medical Studies in English. Her principal research interest involves the association between oral infections and general health, etiopathogenesis of denture stomatitis in patients with diabetes mellitus. She has particular interests in oral candidosis, while the problems related to the treatment and resistance of Candida biofilm and oral candidosis have been the subjects of collaboration with the Department of Biomedical Sciences, University of the Pacific in San Francisco, USA. Dr Dorocka-Bobkowska has published 64 peer-reviewed original research publications and reviews. She has received three science awards from the Rector of Poznan University of Medical Sciences. Currently, she supervises three doctoral candidates and one habilitation candidate. She is a reviewer for the International Journal of Prosthodonitcs, Archives of Oral Biology, Advances in Clinical and Experimental Medicine, Diabetes Research and Clinical Practice, Dental Medical Problems and Dental Prosthetics. In the years 1997–2001, she was Secretary of the Poznan Branch of Polish Dental Association. In 2001 she was awarded The New York Kosciuszko Foundation Fellowship, for study in the Department of Microbiology, School of Dentistry, University of the Pacific (UOP), San Francisco (Head – Prof. Nejat Dűzgűneş). This was followed by four attachments (2007–2012) as Visiting Professor at University of the Pacific. Other international attachments include the Department of Removable Dentures and Gerodontology, University of Geneva, Switzerland (1995, Head Prof. Ejvind Budtz- Jōrgensen), Postgraduate Dental Institute, University of Edinburgh, UK (2009) and Universita degli Studi di Milano-Bicocca, Milano, Italy (2015). Since 1997, she has been a member of International Association for Dental Research and Polish Dental Association. 10 New Members of the Editorial Board

Jolanta Kostrzewa-Janicka

Associate Professor in the Department of Prosthodontics, Medical University of Warsaw. She obtained diploma of dentistry in 1989 at the University of Warsaw (specialization in general dentistry and dental prosthetics). In 2007 she obtained a PhD, and in 2013 the habilitation. Jolanta Kostrzewa-Janicka participates in numerous internships and trainings abroad on topics such as physiology and pathology of stomatognathic system, with an emphasis on the treatment of functional disturbances within the masticatory organ and prosthetic rehabilitation of patients. She is a member of the Polish Dental Association, Polish Society of Masticatory Organ Dysfunction, the International Academy of Advanced Interdisciplinary Dentistry and the European Academy of Craniomandibular Disorders. Main research and achievements in scientific activities relate to the epidemiology of functional disorders of the masticatory organ, general and local etiological factors of temporomandibular disorders, its diagnosis and treatment, prosthetic rehabilitation of patients with tooth wear, malocclusion, and prevention of functional disturbances within the masticatory organ. Scientific work and everyday practice is supported by the cooperation with foreign centers of dental sciences involved in the areas of interest. This results in the implementation of the most up-to-date methods of the masticatory organ rehabilitation.

Selena Toma

Selena Toma graduated in general dentistry in 2006 and in 2010 she obtained magna cum laude MSc in Periodontology at the Université catholique de Louvain in Brussels. In 2010–2016 she took part in the doctoral research program entitled “New insights in the treatment of periimplantitis” at the Université catholique de Louvain. Since 2016 she has been Assistant Professor at Cliniques Universitaires Saint Luc at the Université catholique de Louvain and Internship Coordinator for MSc in Periodontology. She is a member of many scientific committees such as the International Asso- ciation for Dental Research (IADR), IADR Periodontal Research Group, and the European Federation of Periodontology (EFP). Selena Toma is a past president of the junior section of the Belgian Society of Periodontology, and a board member and representative of Université catholique de Louvain at the Belgian Society of Periodontology. Her main research interests include periimplant diseases, immuno-inflammatory response in periodontal diseases, dental biofilm, and periodontal medicine. Dent Med Probl. 2017;54(1):00–01 11

Grażyna Wyszyńska-Pawelec

Grażyna Wyszyńska-Pawelec (DDS, PhD) graduated at the Division of Dentistry, Faculty of Medicine, Medical Academy in Kraków. She is a 2nd degree specialist in oral and maxillofacial surgery. She obtained her doctoral and postdoctoral degrees in dentistry at the Medical Faculty of the Jagiellonian University (Kraków). Since 1986 she has worked at the Department of Craniomaxillofacial, Oncologic and Reconstructive Surgery of the Jagiellonian University (Kraków) as a senior assistant and an adjunct. Since 2013 she has been a regional consultant in maxillofacial surgery and, since 2014, head of the Head and Neck Tumor Board (The Oncology Centre of the Ludwig Rydygier Hospital in Kraków). Her principal research interests include reconstructive and orbital surgery, head and neck oncology and oncologic surgery. She has authored 50 publications, 2 textbook chapters, and 1 monograph, has been a co-editor of 1 textbook (in press), author and co-author of 110 congress presentations, including 31 international. Her main didactic achievements are focused on practical exercises and seminars for students of the 4th and 5th years of dentistry and medicine including classes in English for foreigners. At the Jagiellonian University, she is a coordinator of dental externships, a tutor of the Student’s Scientific Association (Department of Cranio- maxillofacial, Oncologic and Reconstructive Surgery) and a supervisor of summer undergraduate practical trainings. She has supervised trainees in oral and maxillofacial surgery and organized postgraduate trainings for dentists and doctors. Since 2005 she has been a lecturer in postgraduate courses organized at the Depart- ment of Craniomaxillofacial, Oncologic and Reconstructive Surgery at the Jagiello- nian University. From 1993 to 2016 she won a scholarship in maxillofacial surgery at “La Sapienza” University in Rome and Wurzburg University and she participated in the following courses: “The North East Plastic Surgery Flap Course” (Department of Plastic Surgery, Newcastle University), “Free Flap Course. Head and Neck Reconstructive & Oncologic Surgery” (The Netherlands, SORG Academy) and “International Practical Course in Microsurgery” (Romania, Timisoara University). She was training brachytherapy of head and neck tumors at the Department of Radiother- apy, Lubecka University (Germany). She is a member of the Polish Dental Society, Polish Association for Maxillofacial Surgery, Oral Surgery and Implantology and the European Association for Cranio- maxillofacial Surgery. Grażyna Wyszyńska-Pawelec received Silver Medal for Longtime Service (2011), “Honoris gratia” badge of the President of Kraków (2005) and is an ordinary member of Pierre Fauchard Academy (2010). 12 New Members of the Editorial Board

David Herrera

David Herrera is a full-time professor of Periodontics at the Faculty of Odontology, University Complutense of Madrid (Spain) and a co-director of EFP Graduate Pro- gram in Periodontology (Madrid). David Herrera obtained a degree in dentistry at the University Complutense of Madrid where he also postgraduated in periodontology. He is a European Doctor (PhD) in dentistry (from the University Com- plutense of Madrid), a former president of the Spanish Society of Periodontology (SEPA), and a board member of the Continental European Division of the Interna- tional Association for Dental Research (IADR). His scientific interests focus on microbiology and antimicrobials in periodontology. David Herrera has more than 80 scientific publications in SCI journals and participated in many courses and congresses. He has been a speaker at more than 60 international and national congresses.

Original papers Peripheral blood saturation and pulse rate during swallowing in patients with oral cavity neoplasm and after its excision Nasycenie krwi obwodowej tlenem i tętno podczas przełykania u pacjentów z nowotworem jamy ustnej oraz po jego wycięciu

Ludmiła Halczy-Kowalik1, A–D, F, Robert Kowalczyk2, A, E, Anna Rzewuska2, B, E, Violetta Posio3, A, F

1 Independent Laboratory of Postoperative Rehabilitation in Maxillofacial Surgery, Pomeranian Medical University of Szczecin, Szczecin, Poland 2 Clinic of Maxillofacial Surgery, Pomeranian Medical University of Szczecin, Szczecin, Poland 3 Department of Imaging Diagnostics and Interventional Radiology, Pomeranian Medical University of Szczecin, Szczecin, Poland

A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation; D – writing the article; E – critical revision of the article; F – final approval of article

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):13–19

Address for correspondence Abstract Ludmiła Halczy-Kowalik E-mail: [email protected] Background. Breath holding during swallowing enables safe transport of bolus from the oral cavity to the esophagus without threat of aspiration into the lower airways. Inter-deglutition apnea elongation needed Funding sources none declared for the performance of several swallows supporting non-efficient lower pharynx emptying in the patients after oral cavity neoplasm excision, may be the cause of the peripheral blood saturation decrease. Conflict of interest Objectives. The aim of the study was to assess peripheral blood saturation during swallowing in patients none declared with oral cavity neoplasm and after its excision. Acknowledgment Material and methods. One hundred fifty-six patients with oral cavity neoplasm were scheduled for We are very grateful to Barbara Zaborek, PhD for her help in thorough statistical assessment of the results. surgical treatment. Pulse oximetry was performed before surgery, and 2 and 4 weeks post-surgically. Vi- deo fluoroscopic swallowing examination was performed 2 and 4 weeks post-surgically, simultaneously with pulse oximetry. Received on August 24, 2016 Revised on October 11, 2016 Results. After neoplasm excision, desaturation was indicated by time percentage of saturation lower than Accepted on October 14, 2016 95% increase and pulse rate acceleration. We recorded improved saturation 4 weeks after surgery and after the rehabilitation of swallowing; there was an increase in the lowest saturation value and a decrease in time percentage of saturation lower than 95%. Post-deglutition retention correlated most with the saturation. Time percentage of saturation lower than 95% for post-deglutition retention was a sensitive test in 82%, and a specific test in 70%. Conclusions. The course of act swallowing improves in patients subjected to swallowing rehabilitation after oral cavity neoplasm excision as time passes by after surgery. Desaturation during swallowing in patients after oral cavity excision improves as time passes by in patients subjected to swallowing rehabilitation. Post-deglutition retention indicating that inefficient swallowing and aspiration threat are present is DOI a feature of disturbed swallowing act which correlates the most with desaturation, especially with time 10.17219/dmp/65831 percentage of saturation lower than 95%. Copyright Key words: deglutition disorders, saturation, oral cancer excision, post-deglutition retention © 2017 by Wroclaw Medical University and Polish Dental Society Słowa kluczowe: zaburzenia połykania, nasycenie tlenem, wycięcie raka jamy ustnej, zaleganie po This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License połknięciowe (http://creativecommons.org/licenses/by-nc-nd/4.0/) 14 L. Halczy-Kowalik, et al. Swallowing vs SaO2 after oral cancer excision

Breathing, one of the most important life functions, The index finger of a patient’s right hand was placed may be temporarily restricted during phonation and swal- in the pulse oximeter sensor. The measurement was per- lowing. In proper deglutition the larynx closure lasts from formed with the use of Pulse Oximeter Palmsat® 2500 0.4 to 0.6 s and generally does not lead to desaturation1, (Plymouth, USA) and based on the assessment of the except for in older patients.2–5 red and sub-red light absorbance by the red blood cells Oral neoplasm excision changes the anatomy and func- flowing through a blood vessel. The result was diversi- tions of organs responsible for swallowing, speech cre- fied accordingly with oxyhemoglobin content in the red ation and breathing. A decrease in the organ mass, move- blood cell. The changes in the light absorbance produced ment limitation and limited sensory efficiency disturb by the blood pulse in a blood vessel were used to assess swallowing by preventing patients from feeding them- the pulse rate. The recording of examination was stored selves orally. Reconstruction of excised structures, even in the Pulse Oximeter device memory, and then entered if performed in one-step surgical procedure, does not into a database created by the manufacturer. The data- guarantee the recovery of efficient swallowing and eligible base was able to gather any number of examination re- speech6. Teaching patients saliva swallowing, especially sults. We chose 5 scores from the gathered data: basal long breath-holding, creates a new pattern of swallowing. saturation, minimum saturation, the average number of Such an elongated, mid-swallowing apnea can lead to re- pulse rate per min, the minimum number of pulse rate duced peripheral blood saturation. The level of desatura- per min, and the percentage of time period with saturation and its duration may indicate the necessity of some tion lower than 95%. changes in planned swallowing reeducation. Saturation and pulse rate were examined before surgery The aim of this study was to assess saturation as one in 75 patients, 2 weeks post-surgically in 133 patients, of the significant conditions in swallowing rehabilitation and 4 weeks post-surgically in 66 patients. Saturation as- after oral cavity neoplasm excision. sessment in the group of 156 patients was possible due to the following reasons: 1) only 75 patients spent the night before surgery in the hospital; 2) 23 patients with oral nu- Material and methods trition left hospital no later than 2 weeks after surgery; 3) 90 patients decided for oral nutrition no later than One hundred fifty-six patients were treated surgi- 4 weeks after surgery. cally due to oral cavity neoplasm: 110 men aged 22–86 Two weeks after surgery, 133 patients fed with nasogas- years (mean age 56.7), and 46 women aged 37–77 years tric tube who did not start oral feeding, were subjected (mean age 57.35). The criterion of inclusion into the study to the swallowing rehabilitation. It was preceded by video group was histopathologically diagnosed primary squa- fluoroscopic examination performed as in Dodds, Loge- mous cell carcinoma of its origins in oral cavity mucosa. man and Steward’s research.7,8 The examination showed Patients with cancer recurrence or with respiratory, heart aspiration, leakage into the larynx vestibule, post-degluti- or blood vessels diseases were not included into the study tion retention in the lower pharynx, and oral cavity out- group. The patients were not diagnosed nor treated due flow apart from jaws occlusion. The examination verified to breathing or swallowing disturbances before surgery. the compensatory mechanisms applied spontaneously Neoplasm, the range of excision, and reconstruction data by patients during swallowing, enabled checking the ef- are presented in Table 1. fectiveness of new maneuvers recommended during the Pulse oximetry of the peripheral blood saturation was examination such as changing the posture, apnea elonga- performed in patients with oral cavity cancer before sur- tion, epiglottal and supra-epiglottal swallowing. Each pa- gery, and 2 and 4 weeks post-surgically. All patients were tient was provided with their swallowing recording with advised to learn how to swallow their saliva freely; in the the information on the causes of swallowing disturbances early post-surgical period they were asked for planned and rehabilitation recommendations. Peripheral blood saliva swallowing every hour. Two weeks after surgery, saturation assessment performed during video fluoro- patients considered their saliva swallowing as effortless. scopic swallowing examination facilitated the observation Before surgery, saturation assessment was performed and recording of saturation of which parameters were in the early hours, between 9 and 10 a.m. For the first changing during swallowing. 15 min, peripheral blood saturation was examined in pa- Four weeks after surgery, 66 patients still fed through tients during their usual daily activities; a further part of nasogastric tube were subjected to video fluoroscopic ex- examination was performed as the patient drank 25 mL amination of swallowing. The examination enabled us to of still mineral water; another 15 min of the examination check the effectiveness of previous swallowing rehabilita- was performed during patients’ usual daily activities. Two tion and possible changes which could be applied in the and 4 weeks after surgery, saturation assessment began further course of rehabilitation. The changes were dis- 15 min before video fluoroscopic swallowing examina- cussed with every patient during watching the recorded tion, continued during the examination, and finished swallowing act. The assessment of saturation completed 15 min after video fluoroscopic swallowing examination. the observation made during the examination 3. Dent Med Probl. 2017;54(1):13–19 15

Table 1. Characteristic of squamous oral cavity cancer; treatment reported statistically significant differences (p = 0.0001) Tumor localization, clinical advancement, in the rate of the slowest pulse. In post-surgical examina- Number of patients treatment tions, the rate was on average 10 beats per min higher in Tumor tongue 48 women than in men. localization tongue root 16 During examination 1, before the surgery performed on floor of the mouth 42 73 patients, we reported that the neoplasm localization mandible, lower gingiva 21 retromolar trigone 19 in the front part of the oral cavity was statistically signifi- others 10 cantly correlated (p = 0.0053) with the lowest peripheral Clinical I 32 blood saturation during swallowing. Neoplasm infiltrat- advancement II 40 ing the tongue was statistically significantly correlated III 58 IV 26 (p = 0.0315) with longer lasting time of peripheral blood saturation lower than 95% during swallowing compared to Treatment surgical (only) 28 surgical + radiotherapy 44 patients with other localizations of the neoplasm. Table 2 surgical + radiotherapy 84 presents the medium values of saturation and pulse rate + chemotherapy measurements from examinations performed in patients The range of reconstruction with oral cavity neoplasm, and after 2 and 4 weeks post- oral cavity yes no surgically. tissues excision 1) front of part of tongue, 23 14 9 floor of mouth, mandible In examination 2, performed on 133 patients 2 weeks 2) lateral part of tongue, 58 24 34 after surgery, we reported the percentage elongation floor of mouth, mandible of saturation time lower than 95% (p = 0.0374), as well 3) a half of mandible and 7 5 2 half of tongue along as a statistically significant increase in the pulse rate 4) together as in 1 and 2 2 0 (p = 0.0075) in comparison with the pre-surgical exami- 3 group nation recorded. Moreover, we observed a minor and 5) whole tongue 4 4 0 6) a half of the tongue 11 4 7 statistically insignificant decrease in basal and minimum along saturation. 7) ramus of mandible, 51 16 35 In the examination 3, performed on 66 patients 4 weeks lateral pharynx part, root after surgery, we reported a statistically significant im- of tongue provement in measurements concerning the saturation in comparison with the examination 1; the lowest saturation increased (p = 0.0027), and the percentage of saturation time was lower than 95% decrease (p = 0.0047). Statistical methods Video fluoroscopic examination Pulse oximeter recordings were gathered in a database, and after compiling them with the parameters of features In the examination conducted 2 weeks after surgery we of the disturbed swallowing act, analyzed with the use of: reported a disturbance of bolus formation in the oral cav- zzStudent’s t-test of the dependent variables or the Wil- ity, inefficient oral bolus transport, premature bolus entry coxon test of 2 related samples from the same patient in the pharynx, post-deglutition retention in the oral cav- in 2 examinations. ity and pharynx, ineffective lower airways closure during zzAnalysis of variance (ANOVA) or Kruskal-Wallis test. swallowing, leakage into the laryngeal vestibule, and aspi- zzStudent’s t-test for independent variables or the Mann- ration. Table 3 presents the chosen features of disturbed Whitney U test. act of swallowing recorded in patients after 2 and 4 weeks zzThe Kolmogorov-Smirnov test. following oral cavity neoplasm excision. The number of zzSpearman’s rank correlation test. patients with disturbances in examination 3 was lower in The results were described with the use of the correla- comparison to examination 2. tion coefficient r and p value. P < 0.05 was considered as The most serious swallowing disturbance, aspiration, statistically significant in all of the aforementioned tests. did not correlate in a statistically significant manner with the age or gender of patients. Aspiration correlated statistically significantly with the range of tumor excision, i.e., Results it was recorded more often after the excision of more than a half of the movable part of the tongue (p = 0.00585) – Pulse oximetry assessment group 4, and after the excision of the root of the tongue (p = 0.00785) – group 7. Aspiration correlated with post- In the study group of 156 patients, there were no statis- deglutition retention in the lower larynx (p = 0.00001). tically significant correlations between peripheral blood The number of patients with aspiration decreased from saturation and the patient’s age or gender. However, we 10 to 7 during a 4-week observation. 16 L. Halczy-Kowalik, et al. Swallowing vs SaO2 after oral cancer excision

Table 2. Chosen values of saturation measured during swallowing in patients after oral cavity neoplasm excision

Variable Examination Compared p Mean 1 Mean 2 N1 N2

Basal O2 1 2 0.1187 96.21 95.74 73 133 1 3 0.1719 96.21 95.77 73 66 2 3 0.9140 95.74 95.77 133 66

min. O2 1 2 0.0562 90.22 88.00 73 133 1 3 0.3616 90.22 91.11 73 66 2 3 0.0083 88.00 91.11 133 66 avg. p.r. (bpm) 1 2 0.0075 80.98 86.41 73 133 1 3 0.0007 80.98 89.50 73 66 2 3 0.1646 86.41 89.50 133 66 low p.r. (bpm) 1 2 0.6247 60.36 61.33 73 133 1 3 0.0775 60.36 64.53 73 66 2 3 0.1512 61.33 64.53 133 66 % of swallowing time when saturation < 95% 1 2 0.0374 17.21 26.43 73 133 1 3 0.7804 17.21 16.09 73 66 2 3 0.0215 26.43 16.09 133 66

Examination 1 – before surgery, examination 2–2 weeks post-surgically, examination 3–4 weeks post-surgically; basal O2 – basal peripheral blond saturation min. O2 – minimal peripheral blood saturation; avg. p.r. – average number of pulse beats per min; low. p.r. – lowest number of pulse beats per min; % of time O2 < 95% – time percentage when saturation is lower than 95%; N – number of patients in study group; p – level of statistic significance of differences

Table 3. Chosen swallowing disturbances in patients after oral cavity centage of lasting time of peripheral blood saturation neoplasm excision diagnosed in a video fluoroscopic examination lower than 95%. Examination 2: Examination 3: Time percentage of saturation lower than 95% was the Features of disturbed 2 weeks post- 4 weeks post- swallowing act most differentiating value of peripheral blood saturation surgically surgically during swallowing in patients with outflow from the oral Oral cavity outflow 15*–11% 11–17% cavity, leakage into the laryngeal vestibule, and post-de- Post-deglutition retention 38–28% 28–43% glutition retention, from the patients in whom the afore- Leakage into laryngeal 26–20% 12–18% mentioned disturbances were not present. vestibule Aspiration 10–8% 7–11% Nutrition of patients’ choice Number of patients 133 66 or recommended by the doctors * the number of patients representing a feature. Before 2 weeks passed after the surgery, 23 patients were able to start oral nutrition with a liquid diet. These patients belonged to group 2 due to the range of surgery Disturbed swallowing features (their tumor was excised along with the lateral part of the vs saturation tongue, floor of mouth, and a segment of mandible of full thickness); in all of these cases the continuity of mandibu- In examination 3, oral cavity outflow, post-deglutition lar arch was reconstructed in one stage with neoplasm retention in the lower pharynx, leakage into the laryngeal excision. vestibule and aspiration were present in fewer patients, Two weeks after surgery and a video fluoroscopic ex- but the frequency of disturbances (except the leakage into amination, 67 patients started oral nutrition, and 66 of the the laryngeal vestibule) was higher. The aforementioned patients were further subjected to the nasogastric tube features of the disturbed swallowing act were juxtaposed feeding and then swallowing rehabilitation was applied with the measurements of its saturation (Table 4). Post- to them. Four weeks after surgery and video fluoroscopic deglutition retention was accompanied with statistically examination, another 39 of the patients started oral nutri- significant saturation in terms of basal saturation, mini- tion. Feeding through the nasogastric tube or temporary mal saturation, and lasting time percentage of peripheral gastrostomy with further swallowing rehabilitation were blood saturation which was lower than 95%. Outflow suggested in 27 of the patients. from the oral cavity and leakage into the laryngeal ves- Saturation values of patients who were able to return to tibule were accompanied by statistically significant per- oral nutrition were compared with the adequate values of Dent Med Probl. 2017;54(1):13–19 17

Table 4. Disturbed features of swallowing act vs. chosen values of saturation in examination performed 4 weeks post-surgically

Chosen values of saturation Disturbed The number % of time with swallowing features of patients basal O p min. O p p 2 2 sat. < 95% Outflow yes 11 95.02 0.1002 89.64 0.1172 32.48 0.0029 no 55 95.92 91.44 12.75 Retention yes 28 94.49 0.0000 88.46 0.0000 33.30 0.0000 no 38 96.72 93.07 13.06 Leakage yes 12 95.15 0.1878 90.09 0.3367 27.45 0.0072 no 54 95.90 91.32 13.77 Aspiration yes 7 95.75 0.5493 91.10 0.9101 11.50 0.8792 no 59 96.60 91.50 16.23 p – the level of statistically significant differences.

patients who needed nutrition through nasogastric tube eral part of the tongue, floor of the mouth, and mandible), or gastrostomy. Saturation time lower than 95% was re- where the level of statistical significance was p = 0.0015, ported in patients who, according to a video fluoroscopic and group 7 (excised ramus of mandible, lateral part of the examination of swallowing assessment, were able to re- pharynx, and a part of root of the tongue), where the level turn to oral nutrition, and a higher percentage of last- of statistical significance was p = 0.0002. Fig. 1 shows the ing time of peripheral blood saturation which was lower comparison of percentage of lasting time of saturation to than 95%, was reported in patients who needed to be fed be lower than 95% in patients who were fed naturally and through a nasogastric tube or gastrostomy. The difference in patients with a maintained nasogastric tube, consider- was clear in examination 2 and highly statistically signifi- ing the range of surgery; groups 3, 4 and 5 (the range of cant in examination 3. Table 5 includes the comparison surgery concerned more than a half of the tongue) were of time percentage of saturation lower than 95% during joined into one group to facilitate the compilation. swallowing in particular examinations and suggested way Additionally, we performed a comparison of distri- of nutrition on the basis of video fluoroscopic examina- bution of dependent variables with the Kolmogorov- tion complemented by pulse oximetry. Smirnov test for outflow, retention and leakage. ROC We complied the range of surgery, time percentage of curves analysis was performed for the variables which in saturation lower than 95% in examination 3, and the rec- the Kolmogorov-Smirnov test were significant to achieve ommended method of nutrition. Minimum differences the cut-off point which differentiates the distributions the between the compared time percentages of saturation best. The best cut-off (≥ 12.2%) was chosen for the maxi- lower than 95% in patients with maintained nasogastric mum value of the defined difference on the basis of ROC tube and patients who were able to start oral nutrition curves; sensitivity array was 82%, and specificity array was amounted to 6.1% in the group 3 (after resection of half 70%. For the percentage of lasting time of measurements of mandible and the tongue); the greatest differences of equal or higher than 12.2%, sensitivity array of retention 30.35% were recorded in the group 7 (after the resection was 82%, i.e. in 82% of patients with retention lasting time of mandibular ramus, lateral wall of pharynx and a part of of saturation lower than 95% was equal or greater than root of the tongue). Statistically significant differences of 12.2%, and only 30% of patients without retention showed the compared values concerned group 2 (the excised lat- such time.

Table 5. Time percentage of saturation lower than 95% during swallowing vs. recommended way of nutrition in patients after oral cavity neoplasm excision

Mean time percentage Statistical significance Examination The way of nutrition The number of patients of saturation < 95% of differences 1 oral 73 16.84 2 planned oral 87 (out of 133) 22.78 0.0836* feeding tube maintained 46 (out of 133) 33.24 3 planned oral 39 (out of 66) 11.97 0.0000 feeding tube maintained 27 (out of 66) 26.12

* in comparison to the results of patients who took part in both examinations. 18 L. Halczy-Kowalik, et al. Swallowing vs SaO2 after oral cancer excision

Mean values of percentage of lasting time of peripheral blood saturation Fig. 1. The necessity for nasogastric tube feeding lower than 95% depending on the range of the surgery and the possibility of oral nutrition vs time l percentage of saturation lower than 95% in patients after oral cavity neoplasm excision concerning the range of tissues excision

blood saturation lower than 95% tube feeding percentage of time lasting periphera no yes groups

Discussion the saturation after neoplasm excision, and improvement after 2 weeks of swallowing rehabilitation. The value which The role of pulse oximetry in diagnostics of swallowing changed the least was basal peripheral blood saturation; its disturbances is highly valued, especially in bedridden pa- fluctuations were less than 3%. The value which changed tients.9–11 A decrease in the peripheral blood saturation more (increasing) was the pulse rate; differences between during swallowing, known as the aspiration index, is not the mean pulse rate in examination 1 and 2 was almost only highly appreciated in diagnosing and treating swal- 6 beats per minute, and between examination 2 and 3 it lowing disturbances, but also significant in aspiration diag- was more than 3 beats per minute. The differences be- nosis.10,12,13 The significance of desaturation in aspiration tween the mean peripheral blood saturation which was recognition in patients with swallowing disturbances after decreased, in examination 1 and 2 during swallowing ex- cerebrovascular accidents and nasopharyngeal cancer post- ceeded 2%, and in examination 2 and 3 they exceeded 1%. radiation was assessed by Wang, after performing statistical The mean percentage of lasting time of saturation lower anylysis which did not show to be a test of high sensitiv- than 95% decreased of more than 10% during swallowing ity (58.3%), nor specificity (66.7%).14 However, Collins et al. rehabilitation, and it was increased of 9% after the surgery. reported that a decrease in saturation stands for a sensi- Higher values of minimal saturation, lower percent- tive array for aspiration in patients after a stroke, there- age of lasting time of saturation lower than 95%, and fore, the decrease in saturation was present in 81% of the accompanying pulse rate acceleration were recorded in patients with aspiration.15 The authors emphasize the need the examination 4 weeks post-surgically. Certainly, the for careful interpretation of pulse oximetry results in elderly saturation increase is associated with an improvement of patients, smokers, or patients affected by chronic lung dis- a patient’s general condition, but also with putting their eases. swallowing act in order of its course. Video fluoroscopic Lack of time synchronization between the activities of examination of swallowing plays a key role in enabling the oral and pharyngeal swallowing phase, which is present physician and the patient to assess the threat of aspira- after oral cavity neoplasm excision, is one of the causes of tion, the best position to lower the aspiration risk, and swallowing disturbances. Long-lasting apnea, which be- the time of essential mid-swallowing apnea. Providing the gins long before the swallowing trial and lasts even several patient with a recording of their swallowing act course seconds, is an aspiration that prevents auto-regulatory enables us to determine the moment of apnea and first mechanism applied by the majority of patients. It is ac- after-swallow breathe-in with the patient. Deliberate and companied by desaturation, which may be assumed to be conscious breathing prevention during swallowing, which an aspiration sensitive array (especially important in cases lasts long enough to push the bolus into the esophagus of ‘silent aspiration’), and it is present in the patients who but no longer than it is needed, shortened the time of pe- expect to aspirate.7,12,16,17 ripheral blood saturation lower than 95%. In our study group of patients after oral cavity neoplasm Reports on the unfavorable influence of the activities excision, aspiration was not accompanied by the lowest which improve the inefficient swallowing on the circu- value of peripheral blood saturation during swallowing. latory system (e.g. elongated apnea) called for some ad- The measurements show post-surgical time-dependent ditional caution as far as their application in the elderly variability of the peripheral blood saturation in the pa- patients and in patients with heart and vessels diseases tients with oral cavity neoplasm, a significant decrease in is considered.1,4,16,17 The possibility of saliva aspiration as Dent Med Probl. 2017;54(1):13–19 19

well as ‘silent saliva aspiration’ reported by Takahashi in Systematic recording and an analysis of the swallow- the elderly patients discourages from creating a situation ing acts disturbances in patients after excising the ad- in which a patient makes decision on how to swallow on vanced oral cavity neoplasm and accompanying changes his/her own, especially when there may be other diseases in peripheral blood saturation will facilitate monitoring of co-existing with the oral cavity neoplasm which may com- swallowing rehabilitation. plicate swallowing rehabilitation if the rehabilitation is not monitored.18 The results of Colodny’s research show References different general diseases as the cause of desaturation, and 1. Colodny N. Effects of age, gender, disease, and multisystem involvement on oxygen saturation levels in dysphagic persons. negate the advanced age importance in low peripheral Dysphagia 2001;16:48–57. 1,12 blood saturation. Morton et al. finding, based on their 2. Hirst LJ, Ford GA, Gibson GJ, Wilson JA. Swallow – induced altera- research performed in patients with neurologically con- tions in breathing in normal older people. Dysphagia 2002;17;152– 161. ditioned oral phase disturbances, that there is a need for 3. Hiss SG, Strauss M, Treole K, Stuart A, Boutilier S. Swallowing apnea research on the influence of breathing control improve- as a function of airway closure. Dysphagia 2003;18:293–300. ment on aspiration reduction in the patients makes the 4. Hiss SG, Treole K, Stuart A. Effects of age, gender, bolus volume, relationship between saturation and oral nutrition possi- and trial on swallowing apnea duration and swallow respiratory 19 phase relationships of normal adults. Dysphagia 2001;16:128–135. bility worth considering. 5. Palmer JB, Hiiemae K. Eating and breathing: Interactions between Despite the fact that our patients were not diagnosed respiration and feeding on solid food. Dysphagia 2003;18:169–178. nor treated due to any cardiovascular system disease, the 6. Schliephake H, Maximilian UJ. Impact of intraoral soft tissue reconstruction on the development of quality of life after ablative sur- need for determination of saturation and pulse rate chang- gery in patients with oral cancer. Plast Reconstr Surg. 2002;109:421– ing during swallowing is justified. Saturation decrease of 430. 62%, pulse rate acceleration to 128 beats per minute, and 7. Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR Am J saturation lower than 95% and lasting for over 50% of ex- Roentgenol. 1990;154:953–963. amination time recorded during swallowing are the unfa- 8. Dodds WJ, Logemann JA, Stewart ET. Radiologic assessment of vorable conditions for oral nutrition. The aforementioned abnormal oral and pharyngeal phases of swallowing. AJR Am conditions support the idea of changing the current com- J Roentgenol. 1990;154:965–974. 9. da Freitas Cardoso MC, Toniolo da Silva AM. Pulse oximetry: Instru- pensatory maneuvers which make the swallowing more mental alternative in the clinical evaluation by the bed for the dys- efficient, as well as performing the video fluoroscopic ex- phagia. Int Arch Otorhinolaryngol. 2010;14:692–699. amination of swallowing once again. 10. Ramsey DJC, Smithard DG, Kalra L. Can pulse oximetry or a bedside swallowing assessment be used to detect aspiration after stroke? Pulse oximetry as a complementing method for the Stroke 2006;37:2984–2988. video fluoroscopic examination of swallowing in patients 11. Sherman B, Nisenboum JM, Jesberger BL, Morrow CA, Jesberger after oral cavity neoplasm excision yielded more informa- JA. Assessment of dysphagia with the use of pulse oximetry. Dys- phagia 1999;14:152–156. tion to the examination in our patients. Pulse oximetry 12. Colodny N. Comparison of dysphagic and nondysphagic on pulse showed decreased peripheral blood saturation and in- oximetry during oral feeding. Dysphagia 2000;15:68–73. creased pulse rate in the examination performed 2 weeks 13. Leder SB. Use of arterial oxygen saturation, heart rate, and blood pressure as indirect objective physiologic markers to predict aspi- post-surgically in comparison with the pre-surgical ex- ration. Dysphagia 2000;15:201–205. amination, and the lack of statistically significant correla- 14. Wang TG, Chang YC, Chen SY. Pulse oximetry does not reliably tion between the decrease in peripheral blood saturation detect aspiration on video fluoroscopic swallowing study. Arch and aspiration. The examination enabled us to emerge Phys Med Rehabil. 2005;86:730–734. 15. Collins MJ, Bakheit AM. Does pulse oximetry reliable detect aspira- 3 features of disturbed swallowing in the examination tion in dysphagic stroke patients? Stroke 1997;28:1773–1775. performed 4 weeks post-surgically; post-deglutition re- 16. Rogers B, Msall M, Shucard D. Hypoxemia during oral feedings in tention, leakage into the laryngeal vestibule, and oral cav- adults with dysphagia and severe neurological disabilities. Dyspha- gia 1993;8:43–48. ity outflow were accompanied by significant saturation 17. Dharmarajan TS, Unnikkrishnan D. Tube feeding in the elderly. Post- decrease. The feature which had the greatest correlation grad Med. 2004;115:51–61. with desaturation was post-deglutition retention accom- 18. Takahashi N, Kikutani T, Tamura T, Groher M, Kuboki T. Video endoscopic assessment of swallowing function to predict the panied by the highest percentage of lasting time of satura- future incidence of pneumonia of the elderly. J Oral Rehabil. 2012; tion lower than 95%. 39:429–437. Shortening the time of saturation lower than 95% dur- 19. Morton R, Minford J, Ellis R, Pinington L. Aspiration with dysphagia: The interaction between oropharyngeal and respiratory impair- ing swallowing after oral cavity neoplasm excision was ment. Dysphagia 2002;17:192–196. only possible thanks to achieving full understanding of the patients swallowing act recording, as well as teaching patients when to hold breath and perform the first breath- in after swallowing.

Original papers Animal related facial trauma Urazy twarzy wywołane przez zwierzęta

Aneta Neskoromna-Jędrzejczak1, A, E, F, Bogusław Antoszewski2, E, F, Katarzyna Bogusiak1, A–D

1 Department of Craniomaxillofacial and Oncological Surgery, Medical University of Lodz, Łódź, Poland 2 Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Lodz, Łódź, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):21–27

Address for correspondence Abstract Katarzyna Bogusiak E-mai: [email protected] Background. According to ICD-10 classification, animal related injuries may result from being bitten or hit, not to mention being stung or crushed by an animal. Funding sources none declared Objectives. The aim of the study is to analyze and characterize animal related injuries.

Conflict of interest Material and methods. 35 patients (13 men and 22 women) treated at Craniomaxillofacial and On- none declared cological Surgery Department in MU of Lodz between 2004 and 2012 due to animal related injuries were enrolled into the study. The age of patients ranged between 15 and 75 years. A retrospective analysis focus- Received on October 1, 2016 ing on medical documentation enabled us to collect data concerning the following: age of patients, gender Revised on January 8, 2017 of patients, animal that caused the injury, the site of the accident, alcohol consumption by the injured Accepted on January 9, 2017 individual prior to the incident, as well as the period of hospitalization. Additionally, the FISS scale (Facial Injury Severity Scale) was used to evaluate the severity of facial injuries. Results. Results lead to observations making it possible to declare that men suffered from injuries reported as severe according to the FISS scale much more frequently than women. More severe injuries also occurred significantly more often in agricultural farms. Injuries caused by large home animals are related with the incidence of the so-called high-energy injuries and stand as frequent multi-organ and multi-site injuries. Conclusions. Animal related injuries are often multi-organ and multi-site injuries that require specialist treatment. More severe injuries were observed both in the masculine group and within the area of agricultural farms. The greater value of the FISS scale was associated with a longer period of hospitalization. Alcohol consumption is emphasized as a factor prompting the attack of the animal, as well as animal aggression against a human being. Key words: animal related injuries, face trauma, Facial Injury Severity Scale Słowa kluczowe: urazy odzwierzęce, uraz twarzy, Skala Ciężkości Urazów Twarzy

DOI 10.17219/dmp/68379

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 22 A. Neskoromna-Jędrzejczak, B. Antoszewski, K. Bogusiak. Animal related facial trauma

According to ICD-10 classification, animal related inju- Table 1. Facial Injury Severity Scale ries may result from being bitten or hit, not to mention be- Parameter Points ing stung or crushed by an animal. The frequency and type Soft tissue injuries (facial laceration) of animal related injuries differ depending on the region of ≤ 10 cm 0 the world, which is related with the occurrence of specific fauna within a given area. In the United Arab Emirates fre- > 10 cm 1 quently reported injuries include the ones caused by cam- Upper face height injuries els (212 such traumas have been reported during the years Fracture of orbital roof/rim 1 2003–2012), whereas in Kashmir bear attacks seem to be Fracture of frontal sinus/bone displaced 5 the most problematic issue (on average, causing about 50 nondisplaced 1 1,2 injuries a year). In the USA, where statistical information Middle face height injuries associated with animal related injuries has the best docu- Maxillary fracture Le Fort I 2 mentation, about 1.3 million animal related injuries are reported annually, where the most common reasons why Le Fort II 4 injured people report to physicians include traumas caused Le Fort III 6 by arthropods – 50%, dogs – 24% of all injuries. It has been Unilateral maxillary fracture are appointed half of points calculated that about 200–500 people die every year due Dento-alveolar injury 1 to animal related injuries. As far as the global perspective Naso-orbital-ethmoid complex 3 is concerned, we can observe an increasing number of dog fractures bites, and in the USA about 9,500 patients are hospitalized Zygomatico-maxillary complex 1 for longer than one day because of being bitten by a dog, fractures and what is more, in the USA and Canada more than 500 Isolated nasal bone fracture 1 3–5 deaths are reported due to the above. Lower face height injuries According to the data provided by the Agricultural So- Dento-alveolar injury of mandible 1 cial Insurance Fund (pol. Kasa Rolniczego Ubezpiecze- Fractures of mandible body, ramus/ 2 x number of nia Społecznego – KRUS), more than 2,800 people were symphysis fracture fissures treated in Poland in 2012 as a result of being hit, bitten or Fracture of mandibular subcondyle, 1 crushed by animals.6 Literature indicates a slight percent- condyle or coronoid process age of deadly dog bites – several cases each year.7 Such injuries constituted from about 2.5 to 8% of all reasons underlying traumas in Poland.7,8 The aim of this study was to analyze and characterize Statistical analysis animal related injuries. In order to verify statistical dependencies, all collected results were analyzed with a c2 test. P < 0.05 value was Materials and methods assumed as a predetermined significance level.

35 patients (13 men and 22 women) treated at Cranio- maxillofacial and Oncological Surgery Department in MU Results of Lodz between 2004–2012 due to animal related injuries were enrolled into the study. The age of patients ranged The group of hospitalized patients suffered injuries between 15 and 75 years of age – the average age in the caused by the following animals: dog (26 cases), horse whole group equaled 38.56 years ± 16.6, whereas in the (8 cases) and a bull (1 case). The majority of traumas group of women the average age was 40.14 years ± 16.62 caused by animals resulted in the occurrence of bite and in the male group it reached 25.92 years ± 16.01. wounds (26 people) (Fig. 1 and 2). Facial bone fractures A retrospective analysis focusing on medical documen- were diagnosed in the case of 9 individuals. 4 patients tation enabled us to collect data concerning the follow- with facial bone fractures also suffered from facial wounds ing: age of patients, gender of patients, animal that caused (Fig. 3). the injury, the site of the accident, alcohol consumption The majority of people, namely 27 (0.77 fraction), ex- by the injured individual prior to the incident, as well as perienced light injuries that were evaluated as 0–1 on the the period of hospitalization. Additionally, the FISS scale FISS scale. Facial wounds dominated within this group of (Facial Injury Severity Scale) was used to evaluate the se- patients (21 people), and they most commonly covered verity of facial injuries, as it enumerates 4 main groups more than just one area of the face. No concomitant in- covering certain traumas: soft tissue injuries, upper face juries were reported in this group of patients. As far as height injuries, middle face height injuries and lower face 8 people are concerned, traumas were classified as points height injuries (Table 1).9 2–6 on the FISS scale. Men dominated this group. 3 pa- Dent Med Probl. 2017;54(1):21–27 23

Fig. 1. Woman, 37 years old. The wounds of the lower lip with tissue loss caused by dog bites. Reconstruction of the lower lip

Fig. 2. Man, 36 years old. Numerous facial wounds of all facial regions

tients had concomitant soft tissue injuries, whereas 5 in- Within the whole examined group, 18 patients were individuals suffered from injuries covering other areas of toxicated. From among 22 examined women, 12 of them the body. The most frequently observed concomitant in- (0.55 fraction) suffered from injury after alcohol consump- juries include chest injuries (including rib and collarbone tion. As far as masculine group is concerned, 7 men (0.54 fractures). fraction) were sober, whilst 6 people (0.46 fraction) were 24 A. Neskoromna-Jędrzejczak, B. Antoszewski, K. Bogusiak. Animal related facial trauma

Fig. 3. Man, 54 years old – patient was hit by the horse’s head. The wounds of the upper lip, nose, the mucous membrane of the oral cavity. Fracture of tooth crowns 14, 15. The total dislocation of teeth 12–26. The comminuted fracture of the nose, maxilla, left orbital floor fracture, zygomatico-maxillo-orbital fracture on the left side and fracture of left zygomatic arch

Fig. 4. Severity of the injuries according to the FISS scale in relation to alcohol consumption before the accident

intoxicated at the moment when the incident happened. What was also observed is the fact that intoxicated Nevertheless, no statistically significant dependence be- people tended to have more than one area covered by the tween alcohol consumption and the severity of the injury injury when compared with sober patients (fractions: 0.78 was stated (only 2 people suffered from injuries evaluated and 0.59) (Table 3). This difference did not prove statisti- between 2 and 6 points on the FISS scale following alco- cally significant (p > 0.05). hol consumption). Observations revealed that men experi- Analysis focusing on the dependence between the se- enced more severe injuries, as far as the FISS scale is con- verity of the trauma and the site of the accident revealed cerned, significantly more often than women (Fig. 4). statistical significance (p < 0.01). It was proved that men The statistical significance between alcohol consump- were much more often injured in accidents taking place tion and the animal responsible for the injury was de- on agricultural farms than women (fraction 0.54 vs 0.09). clared (p < 0.05). It was observed that significantly more On the other hand, women more often suffered from inju- intoxicated people than sober individuals suffered dog ries in sites other than agricultural farms, such as: streets bites (0.89 fraction vs 0.59 fraction) (Table 2). and households (0.91 vs 0.46). It was also observed that Dent Med Probl. 2017;54(1):21–27 25

Table 2. Alcohol consumption and the animal that caused the injury Table 4. Severity of trauma in relation with the site of the accident (based on the pie chart) Alcohol Animal that Severity of trauma caused the yes no Total Site of the injury FISS 0-1 FISS 2-6 Total N fraction n fraction accident n fraction n fraction Horse 2 0.11 6 0.35 8 Agricultural farm 0 0 8 0.23 8 Bull – – 1 0.06 1 Other sites where 26 0.74 1 0.03 27 Dog 16 0.89 10 0.59 26 accidents happen: Total 18 1,00 17 1.00 35 city, streets, home p < 0.05. Total 26 0.74 9 0.26 35

Table 3. Number of injured facial areas depending on alcohol consumption slight wounds that do not require surgical intervention. Chomel et al.state that up to 37.5 people per 100,000 will Alcohol 10 Number suffer from animal related injuries. On the basis of the of injured yes no Total available literature, it is essential to emphasize that the facial areas n fraction n fraction kind of animals causing injuries depends on the environ- 1 4 0.22 7 0.41 11 mental and demographic factors. Depending on the cli- > 1 13 0.78 6 0.59 19 matic zone, as well as the scope of urbanization within the Total 17 1.00 13 1.00 30 given region, authors tend to write about injuries caused by animals such as camels, snakes or scorpions in their 2 c = 2.915; p > 0.05. research.11,12 When injuries that city dwellers suffer from are taken into consideration, other animals are cited as the cause of injuries – the most commonly mentioned animals in this case include home animals, such as dogs and injuries of greater severity were significantly more fre- cats, etc. Quite different animals cause injuries among ru- quently associated with agricultural farms (Table 4). ral inhabitants, which is due to the prevalent dominance Observations focusing on the subgroup of patients with of larger animals (farm animals such as horses, cows, facial wounds revealed that intoxicated people had more etc.).13 The literature also covers injuries associated with than one area injured when compared with sober patients human migration.13 (fractions: 0.78 and 0.59). However, this occurred only The majority of research, similarly to our study, men- slightly more frequently and this difference did not prove tions dogs as being the animal that most frequently causes statistically significant (p > 0.05). injuries to people (amounting up to more than 80% of all As far as the study group is concerned, the average hos- cases).13–18 This is due to the popularity of dogs as home pitalization period in the case of patients treated for animal animals – according to studies, there are more than related injuries lasted 5 days (standard deviation reaching 77.5 million dogs registered only in the USA. This is also 7.92 days). The length of the hospitalization period de- the country where about 9,500 incidences of hospitaliza- pended on the severity of the trauma. In the case of more tion exceeding 1-day period due to dog bites is observed. severe injuries (FISS 2–6), the period of patients’ hospi- Dogs mainly cause slight injuries. Despite this fact, we can talization was considerably longer (z = 3.928; p < 0.001) see alarming data reported in North America, where until than it was the case among patients, whose injuries were the year 2006 more than 500 deaths related to dog bites evaluated as 0–1 on the FISS scale. Respective averages were noted.4,5,19 equal 14.6 ± 12.8 days vs 2.2 ± 1.96 days. Half of the pa- Slightly more than a half of injuries among patients tients with more severe injuries stayed in the hospital for from the discussed group involved intoxicated people. longer than 9 days, whereas individuals suffering from A noteworthy majority of injuries caused by dogs hap- 0–1 FISS injuries were hospitalized for 1 day. pened to people who drank alcohol prior to the accident. The studied group revealed a tendency indicating that alcohol consumption was related to the occurrence of more Discussion severe injuries, next to a greater number of injured areas. Certain authors emphasize that repeatedly; the attack There is not a considerable number of titles in litera- of the animal was preceded by certain factors evoking ture related to the topic of animal related injuries – espe- animal aggression. Circumstances favoring the attack of cially as far as injuries of the head and neck are concerned. the animal include: feeding, taking care of the offspring, This seems to be a result of the noticeable prevalence of playing, as well as protecting against another animal.20 such injuries, which only involve epidermal abrasions and Patronek emphasizes that, apart from the lack of proper 26 A. Neskoromna-Jędrzejczak, B. Antoszewski, K. Bogusiak. Animal related facial trauma

behavior in human-animal relation, abuse of psychoac- Conclusions tive drugs, including alcohol, by the animal owner or bite victims, stand as important factors underlying deadly dog Animal related injuries are often multi–organ and bite related injuries.21 The available literature lacks proper multi–site injuries that require specialist treatment. More research concerning the dependence between the sever- severe injuries were observed both in the masculine group ity of animal related injuries and the fact that the victim and within the area of agricultural farms. The greater val- drank alcohol before the accident. ue of the FISS scale was associated with a longer period In most of our patients, we introduced antibiotic pro- of hospitalization. Alcohol consumption is emphasized phylaxis with the use of amoxycillin with clavulanic acids as factor prompting the attack of the animal, as well as and we did not observe any inflammation complication. animal aggression against a human being. However, the literature data on this topic is not consistent. Some authors indicate that there is no statistical References evidence that antimicrobial prophylaxis is effective.22,23 1. Abu-Zidan FM, Hefny AF, Eid HO, Bashir MO, Branicki FJ. Camel- related injuries: Prospective study of 212 patients. World J Surg. Others, recommend such therapy for older patients and 2012;36:2384–2389. patients with comorbidities, high-risk injuries like cats, 2. Shafaat R, Gh N, Manzoor A, Bashir A. Injuries from bear (Ursus thibet- horses, and birds bites, puncture wounds, extensive inju- anus) attacks in Kashmir. Turk J Trauma Emerg Surg. 2009;15:130–134. 3. Adams A, Suton J, Elixhauser A. Emergency department visits and ries, trauma in babies and infants and in the case of de- hospitalization associated with animal injuries. 2009. HCUP Statis- 22,24–27 layed surgical treatment of animal related wounds. tical Brief 134, 2012, May. Some authors strongly contraindicate antibiotic prophy- 4. Holmquist L, Elixhauser A. Emergency department visit and inpa- laxis in case of scratch wounds and excoriations.28 Oth- tient stays involving dog bites, 2008. Agency for Healthcare Research and Quality, Rockville, 2010, November. ers state that prophylaxis should be administered to all 5. Sacks JJ, Sinclair L, Gilchrist J, Golab GC, Lockwood R. Breeds of bite wounds after primary closure.29,30 Based on above- dogs involved in fatal human attacks in the United States between mentioned articles, it seems also that there is a great va- 1979 and 1998. J Am Vet Med Assoc. 2000;15:836–840. 6. Accidents at work, occupational diseases of farmers and pre- riety of antibiotics chosen for prophylaxis. All clinically ventive actions of KRUS in 2012. Kasa Rolniczego Ubezpieczenia 31 infected wounds should be cultured. From the studies Społecznego (KRUS). Warszawa, 2013. that have examined bacterial isolates from bite wounds it 7. Rzepecka-Woźniak E. Fatal dog bites. Arch Med Sąd Krym. 2006;56: 56–60. is known that cat and dog bite infections are polimicro- 8. Manowska B, Arkuszewski P, Tyndorf M. Review of post-traumat- 32,33 bial. Pasteurellae and Bacteroides spp. predominate ic injuries in patients who received ambulatory emergency treat- in early wounds, and, in those presenting after 24 h after ment. Czas Stomatol. 2009;62:134–140 [in Polish]. the event, staphylococci or anaerobes are frequently pres- 9. Bagheri SC, Dierks EJ, Kademani D, et al. Application of a facial 34,35 injury severity scale in craniomaxillofacial trauma. J Oral Maxillofac ent. Therefore, the prophylactic antibiotic should be Surg. 2006;64:408–414. a broad spectrum antibiotic, in which case co-amoxiclav 10. Chomel BB, Trotignon J. Epidemiologic surveys of dog and cat bites seems to be a drug of choice.36 The alternative prophylax- in the Lyon area, France. Eur J Epidemiol. 1992;8:619–624. 11. Ugboko VI, Olasoji HO, Ajike SO, Amole AOD, Ogundipe OT. Facial is for patients allergic to penicillin include tetracyclines, injuries caused by animals in northern Nigeria. Br J Oral Maxillofac a second generation of cephalosporin with anaerobic ac- Surg. 2002;40:433–437. tivity, or combination therapy with clindamycin and fluo- 12. Alavi SM, Alavi L. Epidemiology of animal bites and stings in 31 Khuzestan, Iran, 1997–2006. J Infect Public Health. 2008;1:51–55. roquinolone. 13. Nogalski A, Jankiewicz L, Ćwik G, Karski J, Matuszewski L. Animal In the case of bite wounds, there is a threat of inflam- related injuries treated at the Department of Trauma and Emergen- matory complications, so careful debridement of necrotic cy Medicine, Medical University of Lublin. Ann Agric Environ Med. 37–40 2007;14:57–61. tissue and wound toilet are always required. Primary 14. MacBean CE, Taylor DM, Ashby K. Animal and human bite injuries closure seems to be the method of choice. The more com- in Victoria 1998–2004. Med J Aust. 2007;186:38–40. plicated soft tissue injuries should be reconstructed with 15. Weis HB, Friedman DI, Coben JH. Incidence of dog bite injuries local flaps, mucosa advancement, full thickness grafts.41 treated in emergency departments. JAMA 1998;279:51–53. 16. Hon KL, Fu CC, Chor CM, Tang PS, Leung TF, Man CY. Issues asso- In some cases, microvascular reconstructions with free ciated with dog bite injuries in children and adolescents assessed flaps are good treatment options.42,43 at the emergency department. Pediatr Emerg Care. 2007;23: Results of this report lead to observations enabling us to 445–449. 17. Ndon JA, Jack GV, Wehrenberg WB. Incidence of dog bites in Mil- declare that men suffered from injuries reported as severe waukse, Wis. Wis Med J. 1996;95:237–241. according to the FISS scale much more frequently than 18. Shetty RA, Chaturvedi S, Singh Z. Profile of animal bite cases in women. More severe injuries also occurred significantly Pune. J Commun Dis. 2005;37:66–72. 19. Dog bite prevention. Injury prevention & control: Home and recre- more often in agricultural farms. The obtained data are ational safety. Centers for Disease Control and Prevention, 2009, May. compliant with those presented by other authors. It was 20. Injuries associated with dog bites and dog attacks. Canadian Hos- also observed that a greater risk of animal caused inju- pitals Injury Reporting and Prevention Program – CHIRPP data- 44,45 base, 1996. ry and death relates to men than to women. Injuries 21. Patronek GJ, Sacks JJ, Delise KM, Cleary DV, Marder AR. Co-occur- caused by large home animals are related with the inci- rence of potentially preventable factors in 256 dog bite-relat- dence of the so-called high-energy injuries and stand as ed fatalities in the United States (2000–2009). J Am Vet Med Assoc. frequent multi-organ and multi-site injuries.13,45–48 2013;243:1726–1736. Dent Med Probl. 2017;54(1):21–27 27

22. Wolff KD. Management of animal bite injuries of the face: Experi- 37. Harris D, Imperato P, Oken B. Dog bites;an unrecognised epidemic. ence with 94 patients. J Oral Maxillofac Surg. 1998;56:838–843. Bull N Y Acad Med. 1974;50:981–984. 23. Callaham M. Prophylactic antibiotics in common dog bite 38. Sacks JJ, Lockwood R, Hornreich J, Sattin RW. Fatal dog attacks wounds: A controlled study. Ann Emerg Med. 1980;9:410–414. 1981–94. Pediatrics 1996;9:891–895. 24. Correira K. Managing dog, cat, and human bite wounds. JAAPA. 39. Barnham M. Once bitten twice shy; the microbiology of animal 2003;16:28–37. bites. Rev Med Microbiol. 1991;2:231–236. 25. Scheithauer MO, Rettinger G. Bite injuries in the head and neck 40. Wright JC. Reported cat bites in Dallas. Characteristics of the cats, the area. HNO 1997;45:891–897. victims and the attack events. Public Health Rep. 1990;105:420–424. 26. Goldstein EJ. Current concepts on animal bites: Bacteriology and 41. Javaid M, Feldberg L, Gipson M. Primary repair of dog bites to the therapy. Curr Clin Top Infect Dis. 1999;19:99–111. face: 40 cases. J R Soc Med. 1998;3:414–416. 27. Metzger R, Kanz KG, Lackner CK, Mutschler W. After cat bite anti- 42. Burt JD, Burns AJ, Muzaffar AR, Byrd HS, Hobar PC, Beran SJ. Total biotics are obligatory acute management of bite injuries. MMW soft-tissue reconstruction of the middle and lower face with mul- Fortschr Med. 2002;144:46–49. tiple simultaneous free flaps in a pediatric patient. Plast Reconstr 28. Dire DJ, Hogan DE, Walker JS. Prophylactic oral antibiotics for low Surg. 2000;105:2440–2447. risk dog bite wounds. Pediatr Emerg Care. 1992;8:194–199. 43. Lengele BG, Testelin S, Bayet B, Devauchelle B. Total lower lip func- 29. Baxter DN. The deleterious effects of dogs on human health: Dog- tional reconstruction with a prefabricated gracilis muscle free flap. associated injuries. Commun Med. 1984;6:29. Int J Oral Maxillofac Surg. 2004;33:396–401. 30. Moore F. I’ve just been bitten by a dog. BMJ. 1997;314:88–89. 44. Morris JA Jr, MacKenzie EJ, Damiano AM, Bass SM. Mortality in trau- 31. Morgan M. Hospital management of animal and human bites. ma patients: The interaction between host factors and severity. J Hosp Infect. 2005;61:41–50. J Trauma. 1990;30:1476–1482. 32. Weber DJ, Hansen AR. Infections resulting from animal bites. Infect 45. Presutti RJ. Bite wounds. Early treatment and prophylaxis against Dis Clin North Am. 1991;5:663–680. infectious complications. Postgrad Med. 1997;101:243–244, 246– 33. Brook I. Microbiology of human and animal bite wounds. Am Fam 252, 254. Phys. 1987;141:703–705. 46. Wiggins P, Schenker MB, Green R, Samuels S. Prevalence of hazard- 34. Goldstein EJC, Barones MF, Miller TA. Eikenella corrodens in hand ous exposures in veterinary practice. Am J Ind Med. 1989;16:55–66. infections. J Hand Surg (Am). 1983;8:563–567. 47. Busch HM Jr, Cogbill TH, Landercasper J, Landercasper BO. Blunt 35. Lion C, Lozniewski A, Rosner V, Weber M. Lung abscess due to bovine and equine trauma. J Trauma. 1986;26:559–560. beta-lactamase producing Pasteurella multocida. Clin Infect Dis. 48. Conrad L. The maul of the wild. Animal attacks can produce signifi- 1999;29:1345–1346. cant trauma. Emerg Med Serv. 1994;23:71–72, 76. 36. Goldstein EJ, Citron DM. Comparative susceptibilities of 173 aerobic and anaerobic bite wound isolates to sparfloxacin, temafloxa- cin, clarithromycin and older agents. Antimicrob Agents Chemother. 1993;37:1150 –1153.

Original papers Chronic odontogenic paranasal sinusitis in the material provided by the Otorhinolaryngology Unit of the 4th Military Teaching Hospital in Wroclaw Przewlekłe zębopochodne zapalenie zatok przynosowych w materiale Poradni Otolaryngologicznej 4. Wojskowego Szpitala Klinicznego we Wrocławiu

Paulina Czarnecka1, A–D, Monika Rutkowska2, A–D, Paweł Popecki3, A–D, Grzegorz Grodoń3, A–D

1 Otorhinolaryngology Unit, 4th Military Teaching Hospital, Wroclaw, Poland 2 Maxillofacial Surgery Unit, 4th Military Teaching Hospital, Wroclaw, Poland 3 Dental Outpatient Clinic, 4th Military Teaching Hospital, Wroclaw, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):29–34

Address for correspondence Abstract Czarnecka Paulina MB E-mail: [email protected] Background. The aim of this work is to prepare a dental diagnostic standard that would enable us to distinguish patients with chronic odontogenic sinusitis (COS) from patients with sinusitis of other origin. We Funding sources none declared also wanted to determine a realistic number of COS in the Polish population. Objectives. The diversity of symptoms presented in COS does not differ from chronic sinusitis of other Conflict of interest origin. However, the microbiological and pathophysiological differences extort a specific diagnostic ap- none declared proach and treatment. This is why odontogenic sinusitis is considered to be an independent disease. The basic method used to diagnose odontogenic foci is an orthopantomogram (OPM), but CB-CT is currently Received on March 10, 2016 Revised on December 13, 2016 becoming a more common option. A proper diagnostic route enables correct problem identification and Accepted on January 5, 2017 implementation of the best treatment method. Endoscopic sinus surgery (ESS) is an effective way of treating up to 85% of patients. Postoperative lack of success may be associated with odontogenic foci, which is why it is highly important to exclude this infection focus in the preliminary qualification for surgery. Material and methods. Our study group consisted of 72 patients preliminary qualified for ESS on the Otolar- yngological Unit of the 4th Military Teaching Hospital in Wroclaw because of chronic sinusitis. Patients after initial qualification were referred to dental surgery outpatient clinic for exclusion of potential odontogenic changes. The evaluation was performed by a group of qualified doctors and based on a clinical examination and radiological imaging (sinus CT, ortopantomogram, other radiograms). Acquired data was analyzed statistically. Results. Odontogenic foci were found in 86.1% patients (62 cases) with chronic sinusitis. Lack of odonto- DOI genic foci was stated only in 13.9% patients (10 cases). There were no statistical differences in the number 10.17219/dmp/68297 of inflammatory foci between men and women.

Copyright Conclusions. The lack of treatment standards in COS forces us to create good interdisciplinary preoperative © 2017 by Wroclaw Medical University cooperation between head and neck surgeons, radiologists and chronic sinnsitis and Polish Dental Society This is an article distributed under the terms of the Key words: chronic odontogenic sinusitis, odontogenic complications, endoscopic sinus surgery Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) Słowa kluczowe: przewlekłe zębopochodne zapalenie zatok, powikłania zębopochodne, endoskopowa operacja zatok 30 P. Czarnecka, et al. Chronic odontogenic paranasal sinusitis

The sinonasal mucosa constitutes a morphological and Odontogenic infections spread either directly from the functional whole. Paranasal sinusitis is a disease with oral cavity, once the maxillary sinus floor is damaged, or a complex etiology; however, bacterial biofilm and the indirectly by the alveolar process of the jaw, through the obstruction of the ostiomeatal complexes constitute the Haversian and Volkmannian canals.6 The inflammation main pathogenic factors. Untreated local inflammatory starts in the alveolar recess of the maxillary sinus and process in one space begins to spread, eventually encom- then progresses, causing consequently an obstruction of passing the remaining structures. Of all the sinuses, the the ostiomeatal complex and the involvement of the ante- maxillary sinuses are the largest and they are most com- rior ethmoidal sinuses, together with the frontal sinuses, monly affected by inflammation. Possible etiology in- at the side where the lesion occurs. cludes both local and systemic factors. Wanyura et al. suggested dividing the odontogenic si- Sinusitis may be acute, subacute or chronic. The first nusitis into two types: primary and secondary.7 The pri- two types are usually related to an infection or nasal al- mary type included complications from tooth decay, pulp lergy, though the growing role of odontogenic infections necrosis and impacted teeth. The secondary type encom- is frequently mentioned among the etiological factors of passed oro-antral communications, odontogenic cysts chronic sinusitis.1 The division and treatment of indi- and other causes, such as foreign objects in the sinuses, vidual inflammatory states are presented in numerous pa- root-related inflammatory processes and periodontal dis- pers, prepared by groups of rhinologists. In Poland, EPOS eases. Some papers divide the tooth-related inflamma- is used, the last version of which dates back to 2012.2 tory states into iatrogenic and non-iatrogenic. The most Chronic paranasal sinusitis is an inflammatory state of common iatrogenic infections include post-implantation the nasal mucosa and paranasal sinuses characterized by sinusitis.8 The remaining ones are related to the mechani- the presence of two or more symptoms, one of which is cal damage inflicted to the mucous membrane of the defined as nasal obstruction or runny nose and the other maxillary sinus, occurring as a post-effect of the root ca- as the lack of the sense of smell, lasting for more than 12 nal treatment, dental material being forced into sinuses or weeks. Moreover, X-ray images and endoscopic examina- improper augmentation of the sinus. tions should also reveal changes. Longhini et al. noted that in the literature devoted to The impact of odontogenic periapical lesions on in- paranasal sinusitis, published after 2010, odontogenic flammatory changes in the maxillary sinus was described maxillary sinusitis (OMS) is being omitted as the cause in 1943 by Bauer.3 During the microscopic examination of paranasal sinusitis.9 It also seems that oroantral com- on corpses, tooth samples as well as samples of sinuses munications, as well as post-extraction complications, and alveolar processes were investigated. It has been including post-extraction alveolitis, are more and more proven that odontogenic inflammatory changes related often viewed as the underlying causes of acute sinus- to the mucous membrane may appear regardless of the itis. In the remaining cases, odontogenic lesions lead to damage inflicted to the cortical plate of the floor of the chronic sinusitis. The literature on this topic is incon- sinus. Odontogenic sinusitis is described as a reactive in- clusive and the general access to the CT scan technology flammatory process of the maxillary sinuses, secondary to forced rhinologists to revise the well-established schemes tooth infection, tooth and alveolar process damage, tooth concerning the etiopathogenesis that have been in use for extraction, procedures carried out within the area of the numerous years. Therefore, the paper presented below alveolar process or endodontic treatment, which may af- refers primarily to the literature published within the last fect the integrity of the Schneiderian membrane. 7 years. Maillet et al.4 have recently defined radiological criteria It is difficult to diagnose a tooth-related sinusitis, since for odontogenic changes within the maxillary sinus as “lo- the progression of the infection often takes place in a very cal thickening of the maxillary sinus mucosa related to ex- slow manner, with few visible clinical signs and without tensive tooth decay or dental filling, with co-existing peri- any tooth pain experienced by the patient. Moreover, apical change, or a tooth, whose condition precludes the dental clinical examination may exclude the presence of implementation of a dental treatment.” Based on a CB-CT odontogenic inflammation. analysis, Maillet et al.4 assessed that almost 50% of changes CT scans are most useful when assessing odontogenic in the maxillary sinus area are related to odontogenic foci. sinusitis; however, radiologists do not always describe Odontogenic maxillary sinusitis (OMS) is one of the dental pathologies. Meanwhile, errors made during estab- earliest detected causes of paranasal sinusitis, which lishing the etiology of a mucosal inflammation and para- is completely different in etiology from the remaining nasal sinusitis lead to errors in the treatment – patients types.1 For almost 100 years, it has been estimated that are qualified for endoscopic sinus surgery without the odontogenic sinusitis constitutes approximately 10% of all implementation of causal treatment. inflammatory diseases.5 The advancement in X-ray and Even though odontogenic sinusitis is a relatively com- endoscopic technology has led to a situation in which mon disease, its pathogenesis remains unclear. Until now, odontogenic etiology is identified as the main cause of si- no consensus has been reached concerning the clinical nusitis in almost 40% of all cases.5 approach, treatment and preventive actions that could be Dent Med Probl. 2017;54(1):29–34 31

taken to avoid the disease. The treatment of odontogenic Wroclaw. Based on the initial diagnosis and radiological paranasal sinusitis focuses on causes. examination patients were preliminary qualified for the An odontogenic inflammatory process is a condition, endoscopic sinus surgery under general anaesthesia. the prevention and treatment of which should depend on, Prior to the planned procedure, all patients were directed above all, dentists, especially given the fact that within the to the Oral Surgery Unit of the 4th Military Teaching Hospi- available literature, dental treatment complications con- tal to exclude the presence of odontogenic foci. Orthopan- stitute the main cause of OMS. tomography (panoramic radiography) was performed in all In light of the fact that the treatment is different from the cases. The doctors also carried out thorough clinical and ra- one applied in other cases, odontogenic sinusitis is a sepa- diological examinations (CT scan of the paranasal sinuses). rate disease. The treatment of chronic odontogenic sinusitis From September 2014 to October 2016, the aforesaid consists in a causal therapy, the goal of which is to eliminate procedures were performed on 147 patients. The group odontogenic foci in the first instance. When pharmacothera- consisted of 73 women and 74 men aged 19–77, with le- py is applied, one should remember that odontogenic sinus- sions in the paranasal sinuses area visible on the CT scans itis, as any odontogenic infection, is usually a heterogenous of the paranasal sinuses, and with symptoms of chronic infection, in which both anaerobic as well as aerobic bacteria paranasal sinusitis. Following the initial otolaryngologi- are involved. Antibiotic therapy is recommended mainly in cal examination, they were qualified for endoscopic sinus the cases when the underlying disease flares up and when surgery. The patients also underwent dental examination, odontogenic abscesses appear.10 It may also be considered both clinical and radiological. Odontogenic foci were when the causal dental treatment is completed, to accelerate identified by means of panoramic X-ray images, as well as the recovery process. The available literature lacks in stan- a detailed assessment of teeth, alveolar process and sinus dards related to the period, throughout which antibiotics cavity, based on a CT scan and clinical examinations. should be administered to patients with OMS. The following aspects were considered during the as- As regards the odontogenic infections treated in a hos- sessment: periodontal inflammatory states, periapical pital, the parenteral use of penicillin is still the preferred changes, teeth that were subject to improper endodontic method, with doses reaching even 20 million units per treatment, impacted teeth, and cysts related to teeth with- day. In the case of patients who are allergic to penicillin, in the jaw. Next, the results underwent a statistical anal- clindamycin is a valid alternative.10 As far as surgical treat- ysis, performed with the use of GraphPad Prism 7. The ment is concerned, the Caldwell-Luc procedure should be normality of distribution was measured by D’Agostino- considered. This would provide the surgeon with better ac- Pearson test. The difference between groups was tested cess to changes present within the maxillary sinuses. In the by Mann-Whitney test for quantitative variables and case of oroantral communication, it is possible to perform Fisher’s exact test for qualitative variables. Correlation of the revision of the sinus cavity and its drainage, from the selected parameters was tested by the Spearman test. side of the oral cavity, with subsequent surgical procedure, All patients without ostiomeatal complex obstruction aimed at closing the fistula. In some cases, endoscopic sinus and with odontogenic foci present in the alveolar process surgery may be required. This would enable us to control of the maxilla were offered surgical treatment via an intra- and monitor all sinuses and to clean them under direct vi- oral approach in the Oral Surgery Unit of the 4th Military sion, with a low percentage of complications and relapses (if Teaching Hospital. Prior to surgical treatment all patients the underlying dental cause of the disease is eliminated).11 underwent oral cavity sanitation. In most patients who underwent treatment in the De- partment of Otorhinolaryngology of the 4th Military Teaching Hospital, the decision about an endoscopic si- Results nus surgery had been based solely on a certificate issued by regional dental clinics, until the cooperation with an The average age of the patients was determined as 47.78 oral surgery unit started. years (standard deviation ± 14.55). Women constituted A vast number of relapses during the first several months 49.7% of the sample group (73 out of 147), whereas 50.3% following the surgeries impelled the doctors of the 4th Mili- of the subjects (74 out of 147) were men. tary Teaching Hospital to create standard dental prepara- Odontogenic foci were detected in the case of 85.7% of tion for sinus surgery. A group of doctors and dentists was the patients, i.e. 126 subjects. They were present in 82.2% properly trained to be able to assess odontogenic foci. of male and 89.2% of female patients. The lack of odontogenic foci was shown in the case of 14.3%. No significant differences in the number of odontogenic foci between Material and methods male and female patients were found. 32.7% of the sample group had full dental arch. Dental profile of the group is The sample group consisted of patients who were sent presented on Fig. 1 and 2. from regional ENT outpatient clinics to the Otorhinolar- The results of the clinical and radiological examinations yngological Unit of the 4th Military Teaching Hospital in were as follows: 48.9% of all odontogenic foci were teeth 32 P. Czarnecka, et al. Chronic odontogenic paranasal sinusitis

Fig. 1. Dental profile of the sample group – right maxilla

Fig. 2. Dental profile of the sample group – left maxilla

after improper endodontic treatment; 17.3% were roots re- Another positive correlation exists between the amount maining in the alveolar processes of maxilla; 9.1% showed of odontogenic foci, extracted teeth and teeth after end- inflammatory states in periodontium, visible on X-ray and odontic treatment (r = 0.674). Endodontic treatment was in clinical tests. 7.4% of all odontogenic foci were impact- usually performed also because the tooth is a dental focus. ed teeth that could potentially institute odontogenic foci In the entire group of 147 people, 16 patients (10.9%) un- (Fig. 3). 4.2% of foci consisted of endodontic material pres- derwent an endoscopic sinus surgery more than once. 15 pa- ent in maxillary sinus lumen. In the case of two patients, tients were diagnosed with multiple odontogenic foci after dental roots were present inside the maxillary sinus and a detailed clinical and radiological examination of the oral one 1 patient was diagnosed with an oroantral fistula. cavity. 30 patients (20.4%) were treated in the Oral Surgery A radiological examination revealed that only 26.8% of Unit of the 4th Military Teaching Hospital. In this group, 10 all endodontically treated teeth have shown signs of prop- subjects underwent maxillary sinus surgery via an intraoral er endodontic treatment. approach. This has proven to be the only treatment needed The relationship between the patients’ age and the num- in this group. All other patients underwent or await an endo- ber of absent teeth exists in a positive correlation (r = 0.708). scopic sinus surgery under general anesthesia in the Otorhi- The older the patient, the fewer teeth remain. In the case of nolaryngological Unit of the 4th Military Teaching Hospital. the subjects’ age and the presence of odontogenic foci, no positive correlation was determined. The situation changes if we consider the fact that the absent teeth may have been Discussion extracted as an active odontogenic focus that may have caused sinusitis in the past. Then the age and the amount of To our knowledge, there are no publications that would odontogenic foci increased by the number of removed teeth present a similar group of patients, so it is difficult to refer stay in a positive relationship with one another (r = 0.67). to results obtained by other authors. Dent Med Probl. 2017;54(1):29–34 33

Fig. 3. Distribution of patients according to odontogenic foci

The existing literature shows that the presence of in- ysis developed by Arias-Irimia et al., performed on 770 flammatory changes on the X-ray image is indicative of patients with odontogenic paranasal sinusitis, described odontogenic aetiology, present in approximately. 70% of in 41 articles written between 1986 and 2007, showed all cases.12 In a group of 172 patients, Troeltzsch et al.13 that women constitute 57.7% of all patients suffering from diagnosed the underlying odontogenic causes in 92.5% of odontogenic paranasal sinusitis.20 55.97% of patients pre- all cases, whereas the most common cause was post-den- sented odontogenic changes of an iatrogenic profile. Peri- tal treatment complications (75% of all cases). The fact odontal disease was detected in 40.38% of the patients, that the disease involved one or both maxillary sinuses while 6.66% of the patients exhibited odontogenic cysts. cannot be the main diagnostic criterion since in most Because the qualification of odontogenic foci was based cases, the inflammatory process develops and affects the mostly on X-ray techniques, which are not currently rec- remaining paranasal sinuses.14 ommended, we may assume that the above results are Bomeli et al. noted that 79% of all cases of acute maxil- understated. However, the results concerning the sex are lary sinusitis may be related to the presence of an odonto- virtually identical to those of patients treated in the 4th Mili- genic focus.15 The development of the X-ray technology, tary Teaching Hospital (with 53% of cases with a iatrogenic as well as the availability of CT scans led to a situation aetiology). Nonetheless, the statistical analysis shows that in which it is currently estimated that almost 86% of all there are no significant differences in the number of foci cases of sinusitis may have an odontogenic character.16 between men and women in the sample group. A reduced These results correspond with the percentage shown in sensitivity of X-ray techniques could have an impact on our sample group – 86.1%. significant discrepancies between the percentage of iatro- Longhini et al.indicated a group of patients with acute genic changes that were detected (ranging from 57.7% in sinusitis who received surgical treatment.17 The treat- the Arias-Irimia et al. study to 83.87% in the case of the ment was ineffective until odontogenic foci were re- research carried out at the 4th Military Teaching Hospital). moved. They also noted that in some cases, dentists who The available literature lists complications after the performed clinical tests and OPG excluded the potential insertion of dental implants as the most common cause presence of teeth-related pathologies. The changes were of odontogenic maxillary sinusitis (OMS).8 However, the confirmed only by CB-CT scans.17 sample group did not include any patients who under- Obayashi et al.noted that 71.3% of tooth infections went the aforesaid procedure. It is also quite difficult to related to the jaw were associated with changes in the assess the actual percentage of the oroantral communica- maxillary sinus.16 What is important, in most cases, the tions, since patients suffering from this condition are usu- clinical tests ruled out the presence of odontogenic infec- ally directly sent to a maxillofacial surgery unit and not to tions. These were only diagnosed with CT scans. Wang the otorhinolaryngological departments. et al. carried out a retrospective analysis of 55 patients, Rodrigues et al. notes that the lack of teeth in the maxilla where chronic odontogenic sinusitis was diagnosed and does not rule out odontogenic changes as the cause of si- teeth-related pathologies were recorded and confirmed nusitis.21 Endodontic materials, fragments of tools left after by computer tomography.18 These authors noted that in root canal treatment or even root fragments may all provide 65% of all cases, the radiological description did not con- favorable conditions for the sinus inflammation to develop. sider odontogenic pathologies. Longhini et al.17 noticed Recently, it has been agreed that the obstruction of the a similar problem in 67% of cases. ostiomeatal complex is an essential factor in the patho- While reviewing the literature on chronic odontogenic genesis of sinusitis. This led to a situation in which en- sinusitis, Lechien et al. stated that almost 67.5% of cases doscopic sinus surgery, which helps to both cleanse the have an iatrogenic background.19 Etiological meta-anal- sinuses and widen the ostiomeatal complex, has a signifi- 34 P. Czarnecka, et al. Chronic odontogenic paranasal sinusitis

cant advantage over other surgical methods used in the longer be recommended. Dentists must be trained in the treatment of chronic sinusitis. Endoscopic treatment and assessment of odontogenic changes in OPG and CT scans. the significance of nasal septum, tonsils and adenoids, The standard examination to qualify a patient for sinus sur- which is related to the patency of the ostiomeatal com- gery should be CT, which makes it possible to review the plex, led to the marginalization of the role of maxillofacial condition of the teeth and paranasal sinuses. surgeons who use, above all, the classic access point, located within the front wall of the maxillary sinus. When References 1. Hoskison E, Daniel M, Rowson JE, Jones NS. Evidence of an increase the qualification for a surgical treatment is carried out in the incidence of odontogenic sinusitis over the last decade in properly, patients with sinusitis secondary to oroantral the UK. J Laryngol Otol. 2012;126:43–46. fistula and odontogenic sinus cysts are referred to maxil- 2. Fokkens WJ, Lund VJ, Mullol J, et al. EPOS 2012: European position lary surgeons. Patients showing symptoms of acute sinus- paper on rhinosinusitis and nasal polyps 2012. A summary for oto- rhinolaryngologists. Rhinol. 2012;50:1–12. itis, for whom a sinus puncture supported by antibiotics is 3. Bauer WH. Maxillary sinusitis of dental origin. Am J Orthod Dentofa- the preferred treatment, are usually attended in an accident cial Orthop. 1943;29:133–151. and emergency pathway. A similar situation may be ob- 4. Maillet M, Bowles WR, McClanahan SL, John MT, Ahmad M. Cone- beam computed tomography evaluation of maxillary sinusitis. served in the case of patients suffering from chronic sinus- J Endod. 2011;37:753–757. itis, who are treated in the 4th Military Teaching Hospital. 5. Patel NA, Ferguson BJ. Odontogenic sinusitis: An ancient but Thus, based on this group of patients, it is only possible to under-appreciated cause of maxillary sinusitis. Curr Opin Otolaryn- gol Head Neck Surg. 2012;20:24–28. determine the scale of the problem related to odontogenic 6. Uliasz M, Wanyura H. Osteomeatal complex in pathomechanism of infections in patients suffering from chronic sinusitis. The odontogenous maxillary sinusitis. Czas Stomatol. 2009;62:735–751 real percentage of cases with sinusitis may be, in fact, deci- [in Polish]. 7. Wanyura H, Uliasz M. The aetiopathogenesis of maxillary sinusitis sively larger than the one described in this paper. in the material of the I Clinic of Maxillofacial Surgery, Medical Uni- In the case of advanced changes in numerous sinuses, it versity of Warsaw. Czas Stomatol. 2002;55:448–459 [in Polish]. is very difficult to determine whether the dental condition 8. Lee CK. Clinical features and treatmants of odontogenic sinusitis. constitutes the primary etiologic factor. However, there is Yonsei Med J. 2010;51:932–937. 9. Longhini AB, Branstetter BF, Ferguson BJ. Otolaryngologists’ per- no doubt that the presence of odontogenic foci intensifies ceptions of odontogenic maxillary sinusitis. Laryngoscope 2012;122: the inflammatory processes, contributing to the loss of 1910–1914. the effectiveness of both preventive and surgical methods 10. Christian JM. Odontogenic infections. In: Flint PW, Haughey BH, Lund VJ, Niparko JK, Richardson MA, Robbins KT, Thomas JR, eds. of treatment, which results in relapses. Cummings Otolaryngology – Head & Neck Surgery. 5th ed. Philadel- Regardless of this, the scale of the problem shows the key phia, Mosby Elsevier, 2010:177–190. role dentists play both when it comes to the prevention and 11. Chemli H, Mnejja M, Dhouib M, Karray F, Ghorbel A, Abdelmoula M. Maxillary sinusitis of odontogenic origin: Surgical treatment. Rev treatment of acute sinusitis. Meanwhile, a consistent lack Stomatol Chir Maxillofac. 2012;113:87–90. of diagnosis of odontogenic foci in the studies devoted to 12. Matsumoto Y, Ikeda T, Yokoi H, Kohno N. Association between the treatment of sinus problems, published in papers rec- odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx 2015;42:288–293. ommended by rhinologic associations, seems to have an 13. Troeltzsch M, Pache C, Troeltzsch M, et al. Etiology and clinical char- influence on the low success rate of the treatment admin- acteristics of symptomatic unilateral maxillary sinusitis: A review of istered to patients with sinusitis, which constitutes a social 174 cases. J Craniomaxillofac Surg. 2015;43:1522–1529. problem. Low efficiency of endodontic treatment indicates 14. Crovetto-Martínez R, Martin-Arregui FJ, Zabala-López-de-Matura- na A, Tudela-Cabello K, Crovetto-de la Torre MA. Frequency of the that not only diagnostic but also dental treatment quality odontogenic maxillary sinusitis extended to the anterior ethmoid has to be improved and controlled on X-rays periodically. sinus and response to surgical treatment. Med Oral Patol Oral Cir Incorrect interpretations of CT scans by dentists and of Bucal. 2014;19:409–413. 15. Bomeli SR, Branstetter BF, Ferguson BJ. Frequency of a dental source pantomograms by laryngologists expose patients to inef- for acute maxillary sinusitis. Laryngoscope 2009;119:580–584. fective treatment of sinusitis. 16. Obayashi N, Ariji Y, Goto M, et al. Spread of odontogenic infection originating in the maxillary teeth: Computerized tomo- graphic assessment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2004;98:223–231. Conclusions 17. Longhini AB, Branstetter BF, Ferguson BJ. Unrecognized odontogenic maxillary sinusitis: A cause of endoscopic sinus surgery failure. Am J Rhinol Allergy. 2010;24:296–300. Bearing in mind that there are no standards for the treat- 18. Wang KL, Nichols BG, Poetker DM, Loehrl TA. Odontogenic sinus- ment of chronic odontogenic paranasal sinusitis, it seems itis: A case series studying diagnosis and management. Int Forum that it would be a good solution to establish a pre-surgical, Allergy Rhinol. 2015;5:597–601. inter-disciplinary cooperation between the hospitals (max- 19. Lechien JR, Filleul O, Costa de Araujo P, Hsieh JW, Chantrain G, Saus- sez S. Chronic maxillary rhinosinusitis of dental origin: A systematic illofacial surgeons, laryngologists, radiologists) and outpa- review of 674 patient cases. Int J Otolaryngol. 2014, ID465173. tient clinics (dentist practices), covering crucial areas, main- 20. Arias-Irimia O, Barona-Dorado C, Santos-Marino JA, Martínez- ly raising awareness among dentists and patients regarding Rodriguez N, Martínez-González JM. Meta-analysis of odontogenic maxillary sinusitis. Med Oral Patol Oral Cir Bucal. 2010;15:70–73. the significance of odontogenic foci in the aetiology of re- 21. Rodrigues MT, Munhoz ED, Cardoso CL, de Freitas CA, Damante JH. current chronic sinusitis. Establishing a diagnosis of odon- Chronic maxillary sinusitis associated with dental impression mate- togenic foci based only on a clinical examination should no rial. Med Oral Patol Oral Cir Bucal. 2009; 14:163–166. Original papers Condylar guidance angles obtained from panoramic radiographic images: An evaluation of their reproducibility Wartości kątów drogi stawowej uzyskiwane ze zdjęć pantomograficznych – ocena powtarzalności metody

Jolanta E. LosterA–D, F, Aneta WieczorekB, F, Wojciech I. RyniewiczA, C, E, F

Department of Dental Prosthetics, Institute of Dentistry, Jagiellonian University, Kraków, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):35–40

Address for correspondence Abstract Jolanta E. Loster E-mail: [email protected] Background. The method of using panoramic radiographic images to obtain numerical data on the condylar guidance angle has been described in the literature. Funding sources none declared Objectives. The aim of the study was to verify the reproducibility of this technique.

Conflict of interest Material and methods. One panoramic radiographic image was randomly chosen from a group of 191 none declared images. The digital image was converted to analog and printed. The study involved 21 dentists, who posi- tioned 4 dots on each side of the image (the orbitale and the porion, as well as the most superior and the Acknowledgments most inferior points of the jaw’s articular surface). The points on each side were connected with 2 lines, The authors wish to thank their colleagues from the Prosthodontic Department, Institute of Dentistry, A and B. To evaluate the accuracy of the lines, the equation of the straight lines was calculated and their Jagiellonian University in Kraków for their participation slopes compared. The condylar guidance angle between the lines was calculated. in the study. Results. The spread of the results for the condylar guidance angle on the right side was 30 degrees; on the left side it was more than 40 degrees. The SD for the slope of line A was 0.01 on both sides. The slope of Received on August 30, 2016 Revised on September 10, 2016 line B varied from 0.25 to 0.34. Accepted on September 15, 2016 Conclusions. The use of panoramic images to obtain the condylar guidance angle is not recommended in clinical use. Key words: reproducibility, guidance angle, panoramic image, condylar guidance Słowa kluczowe: powtarzalność metody, kąt stawowy, zdjęcie tomograficzne, droga stawowa

DOI 10.17219/dmp/65837

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 36 J. Loster, A. Wieczorek, W. Ryniewicz. Condylar guidance angles

The definition of condylar guidance that appears in The Material and methods Glossary of Prosthodontic Terms has two parts.1 The first is anatomical, and is expressed in terms of the glenoid fos- One panoramic radiographic image was randomly sae, which are bone parts of the skull. The second part chosen from a group of 191 images produced during ex- focuses on the mechanical relationship between the parts aminations of volunteers who had participated in a larger of the articulator. This clearly shows the application of research project. These volunteers were free of the signs clinical data to prosthetic laboratory procedures with the and symptoms of temporomandibular disorders, as deter- aim of duplicating jaw function and the occlusal relation- mined by the Polish version of the Research Diagnostic ship of the teeth. Criteria for Temporomandibular Disorders (RDC/TMD) Different clinical procedures have been used to obtain questionnaire; they also possessed intact dentition.16,17 the numerical data for individual condylar guidance val- All the participants expressed their unforced consent to ues. Some of these require intraoral wax records or ex- participate in the study and signed the appropriate state- traoral measurements using pantographic equipment.2–8 ment. The examination was performed in accordance The study by Gilboa et al. introduced the method of using with the Declaration of Helsinki and Good Clinical Prac- panoramic images in a clinical setting to provide the ana- tice (GCP). The consent of the Bioethics Committee of tomical incline of the auricular eminence.9 This method the Jagiellonian University, Kraków, Poland, was obtained generated much interest and was encouraged on account (number KBET/89/B/2009). of its simplicity and availability. Panoramic images are The panoramic radiographic image was taken with among the most frequently made radiographic exami- the Frankfurt horizontal plane parallel to the floor of the nations before the treatment is planned.10–12 Using this mouth; a cephalostat was used to align the head in that method, Gilboa et al. obtained a mean difference in the position, as in Tannamala et al.14 The radiograph was inclination of the condylar guidance angle of 7 degrees.13 made using a ProMax radiographic unit (Planmeca, In the molar area, such a discrepancy could lead to a dif- Helsinki, Finland 2005) ®at 74 kVp and 10 mA.9,14 ference in position of the mandible of 0.25 to 0.5 mm. The The method was the same as that described previously pilot study of Tannamala et al. compared the condylar by Loster et al.15 The chosen digital image was converted angles set in the semi-adjustable articulator using an in- to analog and printed on A4 size (ISO 216) paper using traoral protrusive record to those from the panoramic ra- an Epson Stylus Photo 1400 (Seiko Epson Corporation, diographic image, and showed that the method is a simple Japan, 2007) inkjet printer; the resolution used was 2880 and easy way to program the articulators and is capable of × 1440 dots per inch. One copy was provided to each of producing clinically acceptable restorations.14 The study the participants, who were recruited from the Prosth- was performed on a group of 10 patients who were free odontic Department of the Jagiellonian University. All of the signs and symptoms of temporomandibular disor- the departmental members gave their verbal voluntary ders, and who also possessed intact dentition. The study consent to participate in the study. The prosthodontists involved different individuals, with specific anatomy, and (SP), trainees (T), and general dental practitioners (GDP) each image was examined only once; the condylar angles who contributed to the study were asked to place dots in were compared, with results being received after intraoral 4 places on both sides of the printed standardized pan- registration. The results for the condylar angles vary with oramic radiographic image. Prior to this, definitions of the patients’ sides and the methods of calculation. Some the expected points (the orbitale and porion) were pre- results were greater on both sides in the radiographic sented to the participants. Afterwards, an image from method, some were greater on one side, and some were Gilboa et al. was presented to illustrate the differences be- smaller. The reproducibility of the radiographic method tween the position of the zygomatic arch and the auricu- was not evaluated here, and the authors suggested that lar eminence on the panoramic radiographic image.9 The further studies should be carried out. We conducted participants were then asked to mark the most superior a study to evaluate the reproducibility of that method in point of the mandibular fossa and the most inferior point a group of final-year dental students. Using the described of the curvature of the articular tubercle, following the method, these students analyzed a single radiographic procedure of Tannamala et al.14 The study was conduct- image.9 The results proved inadequate from the clinical ed simultaneously with all participants. The annotated point of view.15 To verify the method in the group of more photographs were numbered and scanned (Digital Photo experienced dental practitioners, the present study was Scanner Epson Perfection V370 Photo, Seiko Epson Cor- implemented. poration, Japan, 2012) to produce a digital image. A scan- The aim of the study was to compare the condylar guid- ning resolution of 1440 dots per inch was used. The co- ance angles obtained by different dentists from the same ordinates of the measuring points were then determined. panoramic radiographic image, and to investigate the The zero (0.00) point was set to the left-upper corner of problems of the method where discrepancies were found each image. Using Adobe Photoshop CS2, the orbitale in the results. O(XO, YO) and porion P(XP, YP) points were connected Dent Med Probl. 2017;54(1):35–40 37

Fig. 1. Example of a radiographic image marked with four dots (in red) and connected by lines A and B

by a line marked A to the Frankfurt horizontal plane. The Statistical analysis most superior point, W(XW, YW), and the most inferior point, N(XN, YN), of the curvatures were connected with All the data was analyzed using Statistica data analysis the mean curvature line (that is, the mean condylar path software v. 10 (StatSoft, Inc., 2011; www.statsoft.com). inclination) by line B, following Tannamala et al.14 This Data normality was tested using the Shapiro-Wilk test. procedure was carried out on both sides of each image Homogeneity was tested using Levene’s test. The de- (see Fig. 1 for an example). scriptive statistics and ANOVA test were used, and the To evaluate the accuracy of each line, the equation of multiple independent samples were compared using the the line, y = ax + b, was used, with “a” representing the Kruskal-Wallis U-test. The results are shown in the tables slope and “b” the y-intercept. We calculated the slope and charts. The level of statistical significance was set at of each line in order to compare the repeatability of the 5% (p = 0.05). points. The points O and P were thus on the same line A, and the equations of these lines A can be written as: Results YO = aOP XO + bOP and YP = aOP XP + bOP Twenty-one dentists participated in the study; of these, where the slope of A is: 7 were specialists in prosthodontics (SP), 8 were trainees (T), and 6 were general dental practitioners (GDP). The aOP = (YP – YO)/(XP – XO) marks from 1 trainee were excluded from the analysis due to outlying results. The average value, median, standard and the slope of B (which passes through points N and W) is: deviation, minimum, and maximum for the slopes of the line A on both sides are presented in Tables 1 and 2. In aWN = (YN – YW)/(XN – XW). Tables 3 and 4, the same data is shown for the slopes of line B. The slope values for both lines and for both sides A discrepancy between the slope values would be sig- did not significantly differ between the groups of par- nificant for the reproducibility of the pairs of analyzed ticipants. The dispersion in the slopes of lines A and B, points. separately on both sides, is graphically presented for all The condylar guidance angle between the lines A and participants in Fig. 2. The minimum and maximum values B was calculated using the equation: of the condylar guidance angle determined by each group of participants are presented in Fig. 3. aOP – aWN tanj = 1 + aOP × aWN Discussion and then the angle: The results show that the method developed by Gilboa 9 aOP – aWN et al. of using panoramic images to obtain the condylar j = arctan 1 + aOP × aWN guidance angle is unacceptable in dental practice. In each

38 J. Loster, A. Wieczorek, W. Ryniewicz. Condylar guidance angles

Table 1. Slope of the line A (right side)

Average Median SD Min Max SP 0.14 0.14 0.02 0.11 0.15 T 0.14 0.14 0.01 0.12 0.16 GDP 0.14 0.14 0.02 0.11 0.16 Mean 0.14 0.14 0.01 0.11 0.16 Kruskal-Wallis U-test; p = 0.9349

SP – specialists in prosthodontics; T – trainees; GDP – general dental practitioners; SD – standard deviation.

Table 2. Slope of the line A (left side)

Average Median SD Min Max SP –0.13 –0.13 0.01 –0.14 –0.11 T –0.14 –0.14 0.01 –0.15 –0.12 GDP –0.13 –0.13 0.01 –0.15 –0.12 Mean –0.13 –0.13 0.01 –0.15 –0.11 Kruskal-Wallis U-test; p = 0.3505

SP – specialists in prosthodontics; T – trainees; GDP – general dental practitioners; SD – standard deviation.

Table 3. Slope of the line B (right side)

Average Median SD Min Max SP 0.84 0.86 0.20 0.58 1.14 T 0.92 0.94 0.13 0.70 1.06 GDP 0.93 0.92 0.40 0.42 1.46 Mean 0.89 0.92 0.25 0.42 1.46 Kruskal-Wallis U-test; p = 0.7446

SP – specialists in prosthodontics; T – trainees; GDP – general dental practitioners; SD – standard deviation.

Table 4. Slope of the line B (left side)

Average Median SD Min Max SP –0.70 –0.85 0.39 –1.25 –0.11 T –0.98 –0.93 0.20 –1.23 –0.65 GDP –0.81 –0.93 0.40 –1.23 –0.08 Mean –0.83 –0.89 0.34 –1.25 –0.08 Kruskal-Wallis U-test; p = 0.3735

SP – specialists in prosthodontics; T – trainees; GDP – general dental practitioners; SD – standard deviation.

group of participants in this investigation, the standard difference in the molar region would be more than 1 mm, deviation (SD) of the angular value was above 4 degrees. following Craddock’s results, which showed that a posi- The clinical use of this method would, therefore, seem to tive 10 degree change in the condylar guidance angle be not indicated. The spread of the values of the condylar would move the molars 0.5 mm further, while a nega- guidance angle in the results on the right side was 30 de- tive 10 degree change would bring the mandible 0.5 mm grees, while on the left side it was more than 40 degrees. closer.13 In Weinberg’s results, a 9-degree decrease in the There were no significant statistical differences between condylar guidance angle resulted in a 0.2 mm reduction the groups of dentists. In clinical use, this means that the in the nonworking cusp height.18 Such differences, which Dent Med Probl. 2017;54(1):35–40 39

Fig. 2. Average value of slopes of lines A and B on both sides, all participants. AR: slope of line A on the right side; BR: slope of line B on the right side; AL: slope of line A on the left side; BL: slope of line B on the left side

Fig. 3. The range of condylar guidance angles (minimum and maximum values) obtained by each group of participants on both sides. Yellow line – line A; blue lines: SP condylar guidance angle range of values; green lines: T condylar guidance angle range of values; red lines: GDP condylar guidance angle range of values; T: trainees; SP: specialists in prosthodontics; GDP: general dental practitioners

were indeed found in this study, may lead to occlusal point, located in the mandibular fossa, is not easy to rec- disturbances in prosthetic restorations in an articulator ognize in the panoramic image. The standard deviation setting. in the slope of line A in the present study was 0.01 on The cause of this imprecision in the angle value was both sides, which can be compared with the slope of B, the lack of accuracy in drawing one pair of the examined which varied from 0.25 to 0.34 (Tables 1–4). Very simi- points. After analyzing the slopes of the lines that sub- lar results were presented in our previous investigation, tend the condylar guidance angle, it was shown that the where much less experienced final-year dental students inaccuracy in the results arose from the nonrepeatable were included.15 designation of the points on line B, presented in Fig. In the research of Prasad et al. the values for the con- 1 and explained in Fig. 2. These are the most superior dylar guidance angle obtained from the panoramic image and the most inferior points of the curvatures that cre- were compared with those from the semi-adjustable artic- ate the jaw’s articular surface, temporal eminence, and ulators by using the protrusive interocclusal records of 69 fossa. These structures are not very visible on the pan- patients.19 The average of 2 examiners’ results was taken oramic radiographic image. Even the study by Gilboa et as the condylar guidance angle. These examiners calcu- al.9 showed the localization of the articular tubercle very lated the angle using the same method described above. well, compared to the zygomatic arch; the most superior Interexaminer reliability was very high. The examiners 40 J. Loster, A. Wieczorek, W. Ryniewicz. Condylar guidance angles

concluded that this method of calculating the condylar 7. Galagali G, Kalekhan SM, Nidawani P, Naik J, Behera S. Compara- tive analysis of sagittal condylar guidance by protrusive interocclu- guidance angle from a radiographic image may have clini- sal records with panoramic and lateral cephalogram radiographs in cal relevance in setting the condylar guidance settings for dentulous population: A clinico-radiographic study. J Indian Prosth- semi-adjustable articulators. Going by our results, their odont Soc. 2016;16:148–153. 8. Shreshta P, Jain V, Bhalla A, Pruthi G. A comparative study to mea- results were too optimistic and it would be interesting to sure the condylar guidance by the radiographic and clinical meth- see the results of the panoramic radiography evaluated by ods. J Adv Prosthodont. 2012;4:153–157. more researchers. 9. Gilboa I, Cardash HS, Kaffe I, Gross MD. Condylar guidance: Corre- lation between articular morphology and panoramic radiographic On the other hand, the average value for the condylar images in dry human skulls. J Prosthet Dent. 2008;99:477–482. guidance angle obtained using the method described here 10. Wieczorek A, Loster J, Majewski S. Assessment of suitability of was about 30 degrees. It may be that this method would orthopantomographs in dental diagnostics of temporomandibu- be useful for population screening studies. Further inves- lar joints. J Stoma. 2012;65:845–854. 11. Napier ID. Reference doses for dental radiography. Br Dent J. tigations in this field are also recommended. 1999;186:392–396. On the basis of our results, the use of panoramic images 12. Williams JR, Montgomery A. Measurement of dose in panoramic in calculating the condylar guidance angle is not recom- dental radiology. Br J Radiol. 2000;73:1002–1006. 13. Craddock FW. The accuracy and practical value of records of con- mended in clinical use due to lack of repeatability of its dyle path inclination. J Am Dent Assoc. 1949;38:697–710. results. 14. Tannamala PK, Pulagam M, Pottem SR, Swapna B. Condylar guidance: Correlation between protrusive interocclusal record and pan- References oramic radiographic image: A pilot study. J Prosthodont. 2012;21: 181–184. 1. The glossary of prosthodontic terms. J Prosthet Dent. 2005;94:10–92. 15. Loster JE, Ryniewicz W, Ryniewicz J, Wieczorek A. Assessment of 2. dos Santos J Jr, Nelson S, Nowlin T. Comparison of condylar guid- the repeatability of condylar guidance angles obtained from pan- ance setting obtained from a wax record versus an extraoral trac- oramic radiographic images. J Stoma. 2014;67:841–849. ing: A pilot study. J Prosthet Dent. 2003;89:54–59. 16. Loster JE, Osiewicz MA, Groch M, Ryniewicz W, Wieczorek A. The 3. Ogawa T, Koyano K, Suetsugu T. The influence of anterior guid- prevalence of tmd in polish young adults. J Prosthodont. 2015 Dec 8. ance and condylar guidance on mandibular protrusive movement. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26646470. J Oral Rehabil. 1997;24:303–309. 17. Osiewicz MA, Lobbezoo F, Loster BW, Wilkosz M, Naeije M, Ohrbach R. 4. Petrie CS, Woolsey GD, Williams K. Comparison of recordings Research diagnostic criteria for temporomandibular disorders (rdc/ obtained with computerized axiography and mechanical pantog- tmd) – the polish version of a dual-axis system for the diagnosis of raphy at 2 time intervals. J Prosthodont. 2003;12:102–110. tmd. Rdc/tmd form. J Stoma. 2013;66:576–649. 5. Pelletier LB, Campbell SD. Comparison of condylar control settings 18. Weinberg LA. An evaluation of basic articulators and their concepts. using three methods: A bench study. J Prosthet Dent. 1991;66:193–200. Part II: Arbitrary, positional, semiadjustable articulators. J Prosthet 6. Thakur M, Jain V, Parkash H, Kumar P. A comparative evaluation Dent. 1963;13:645–663. of static and functional methods for recording centric relation 19. Prasad KD, Shah N, Hegde C. A clinico-radiographic analysis of sag- and condylar guidance: A clinical study. J Indian Prosthodont Soc. ittal condylar guidance determined by protrusive interocclusal 2012;12:175–181. registration and panoramic radiographic images in humans. Con- temp Clin Dent. 2012;3:383–387. Original papers Evaluation of non-surgical periodontal treatment in patients with a past history of myocardial infarction Ocena niechirurgicznego leczenia periodontologicznego u pacjentów z przebytym zawałem mięśnia sercowego

Magdalena Sulewska1, B–D, Jan Pietruski2, C, D, Agnieszka Tycińska3, B, Włodzimierz Musiał3, E, F, Ewa Duraj1, B, Małgorzata Pietruska1, A, E, F

1 Departmant of Periodontal and Oral Mucosa Diseases, Medical University of Bialystok, Białystok, Poland 2 Private Dental Practice, Białystok, Poland 3 Department of Cardiology, Medical University of Bialystok, Białystok, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):41–47

Address for correspondence Abstract Małgorzata Pietruska E-mail: [email protected] Background. The cohort study revealed a relationship between chronic periodontitis and the risk of developing coronary heart disease (CHD) and myocardial infarction. Funding sources none declared Objectives. The aim of the study was to evaluate the influence of periodontal treatment on periodontal status in patients with past history of acute myocardial infarction. Conflict of Interest none declared Material and methods. The study comprised 45 patients with chronic periodontitis hospitalized due to acute myocardial infarction treated with coronary angioplasty. The patients were randomized to the gro- Received on October 18, 2016 up of non-surgical periodontal treatment (group 1; 25 individuals) or the group of periodontal prophylac- Revised on November 3, 2016 tics (group 2; 20 individuals). The following aspects were evaluated in clinical study: plaque index (PI), ap- Accepted on November 20, 2016 proximal plaque index (API), bleeding on probing (BOP), probing depth (PD) and clinical attachment level (CAL). The study was carried out 1–2 weeks following discharge from hospital and 6, 7 and 12 months after the initial examination. Results. High values of PI, API and BOP were observed in both groups, which indicated poor oral hygiene and a considerable percentage of inflamed pockets. Those values significantly decreased with further control examinations, yet the obtained values were still very high. No significant changes in time were observed in PD and CAL in both groups. A significant PD reduction in the examinations performed 7 and 12 moths from the baseline was detected only in the group of younger patients who underwent non-surgical periodontal treatment. Conclusions. The patients with past history of acute myocardial infarction show an abnormal periodontal status which does not significantly change due to constant hygienic negligence despite prophylactic-therapeutic intervention. DOI 10.17219/dmp/67265 Key words: periodontitis, cardiovascular disease, non-surgical periodontal treatment

Copyright Słowa kluczowe: zapalenie przyzębia, choroby układu sercowo-naczyniowego, niechirurgiczne leczenie © 2017 by Wroclaw Medical University periodontologiczne and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 42 M. Sulewska, et al. Non-surgical periodontal treatment

Periodontitis is a chronic multifactor inflammatory dis- The exclusion criteria comprised: cancer, rheumatoid ease which involves progressive damage to the periodon- disease, autoimmune disease, chronic hepatic disorder, tium resulting in the loss of teeth. It constitutes a serious chronic renal disease in 4th and 5th stage, past cerebral issue in public health, the origin of social inequality, lower stroke, disorders accompanying the increase in the in- quality of life, reduced chewing function and esthetic de- flammatory indexes and terminal diseases. fects. Moreover, it is related to increased cost of dental When discharged from the Department of Cardiology, treatment and general health condition.1,2 the patients (n = 124) were referred to the Department Numerous research has shown a relationship between of Periodontal and Oral Mucosa Diseases, Medical Uni- chronic periodontitis and the risk of developing cardio- versity of Białystok, where the first periodontal examina- vascular disorders regardless of other known risk fac- tion was carried out in order to evaluate the periodontal tors.3–5 According to the analysis of epidemiology data, status and to possibly diagnose periodontitis. The exami- the incidence of coronary heart disease increases by 25– nation was carried out 1–2 weeks after discharge from 72% depending on the age of the persons with periodon- hospital. The following aspects were assessed: number of tal disease. The risk of developing coronary heart diseases teeth, hygiene – plaque index (PI) according to O’Leary, in periodontal patients increases by 25% compared with approximal plaque index (API) according to Lange et al., the individuals with a healthy periodontium, while in the bleeding on probing (BOP) according to Ainamo & Bay, group of men under 50 years of age this risk increases to probing depth (PD) and clinical attachment level (CAL) at 72%. In the case of smokers with advanced periodontal 4 measuring points.12–14 Also, the number and percentage disorder, the risk of developing cardiovascular disease of pockets of PD ≥ 4 mm were established. The study was increases 8 times.3,6,7 Meta-analysis by Bahekar et al.8 performed with the use of a periodontal probe PCPUNC showed a correlation between the presence of deep peri- 15 (Hu-Friedy, USA). odontal pockets and the occurrence of cardiovascular ep- Only the patients diagnosed with periodontitis at the isode. Patients with periodontal disease show 1.14–1.59 initial examination were qualified to the study. Next, the fold higher risk of developing atherosclerotic diseases patients were randomized into 2 groups and were asked compared to healthy individuals. to report for an appointment in 6 months. All the 124 According to the outcomes of intervention research, patients having undergone initial test were diagnosed effective periodontal treatment may have a positive in- with periodontitis. Only 45 individuals reported for the fluence on the primary and secondary prophylactics of examination after 6 months, although multiple phone cardiovascular diseases. D’Aiuto et al. and Matilla et al. interventions were done. Group 1 comprised 25 persons showed that treatment of periodontitis is related to the (mean age 55.95 ± 4.37 years), while group 2 comprised decrease in C-reactive protein concentration (CRP), im- 20 persons (mean age 52.64 ± 6.81 years). At the sec- provement in endothelial function and thus decreased ond appointment (6 months after the initial examina- risk of developing myocardial infarction.9–11 However, no tion) after a periodontal examination, the study group intervention studies providing the data on the impact of (group 1) was given non-surgical periodontal treatment treatment of periodontitis on the incidence of cardiovas- which involved oral hygiene education and scaling with cular incidents (myocardial infarction) in a long term ob- root planing (SRP). During the procedure the patients servation can be found. Also, no data on the effectiveness were administered antibiotics (amoxicillin 2.0 g 1 h be- of periodontal therapy in coronary disease patients can fore the procedure or in the case of allergy to penicillin be found. – clindamycin 600 mg 1 h before the procedure). More- The aim of the study was to evaluate the influence of over, modified full mouth disinfection (FMD) was per- periodontal treatment on the periodontal status in pa- formed: double rinsing with 0.2 chlorhexidine solution tients with a past history of acute myocardial infarction. for 1 min and 3 subgingival pocket irrigations for 10 min using a gel with chlorhexidine. Periodontal examination and oral hygiene education were conducted in patients Material and methods from the control group (group 2). Oral cavity sanitation was also recommended to patients from both groups. The research comprised 45 patients including 10 wom- Further control periodontal examinations were carried en and 35 men aged 35–64 years (mean 54.022 ± 5.87) out 1 and 6 months following SRP/hygiene education hospitalized in the Department of Cardiology of the appointment, which are 7 and 12 months following the Medical University of Białystok due to acute myocardial initial examination. infarction treated with coronary angioplasty. The study was carried out in accordance with the Hel- The inclusion criteria comprised: acute myocardial in- sinki Declaration of 1975, as revised in 2008. All the pa- farction, diagnosed chronic periodontitis, age under 65 tients gave their written informed consent for the clini- years, coronary angioplasty treatment and patient’s in- cal examinations. The study was approved by the Ethical formed consent (consent for participation in the study, Committee of the Medical University of Bialystok (R-I- consent for processing personal data). 002/516/2011). Dent Med Probl. 2017;54(1):41–47 43

Statistical analysis was performed with Statistica 10 of 70% during the first two examinations. In further tests, software (StatSoft, Tulsa USA). A U Mann-Whitney test the values of this index significantly decreased to approxi- was used to carry out a non-parametric comparison be- mately 50% regardless of the applied prophylactic-thera- tween groups. For the statistical evaluation of the changes peutic procedure (Table 1). from baseline to 12 months the paired t-test was used. According to the initial examination, 466 sites with PD A p-value below 0.05 was considered statistically signifi- ≥ 4 mm were observed. The total number of pockets with cant. PD ≥ 4 mm in the study conducted 12 months later was 444. A decrease by 31 sites with PD ≥ 4 mm (by 4.37%) was observed in group 1, while in group 2 the number of Results those sites increased by 9 (by 4.37%) (Table 1). In the group of patients who underwent SRP, a signifi- The results indicate the poor condition of the oral cav- cant reduction of PD in two further control examinations ity in patients with a past history of myocardial infarction was observed (p = 0.0027). According to the analysis of and the diagnosis of periodontitis. According to the initial changes in this parameter, a significant reduction of PD examination, the approximate number of teeth was 18.78 occurred only in people ≤ 55 years of age. In the case of ± 6.1 and decreased during a 12-month observation to older patients, the improvement in this parameter was 18.53 ± 5.99. 11 teeth were extracted including 6 in group statistically insignificant. In the group which received 1 and 5 in group 2. only oral hygiene education, the changes in PD were sta- It was shown that oral hygiene was poor, which was tistically insignificant and were independent of the pa- confirmed by the high mean initial values of hygiene in- tient’s age. dexes: PI – 81.33% and API – 98.46%. Those values were In both studied groups no statistically significant slightly higher in group 1 (PI – 85.12%, API – 99.12%) changes in time in CAL values were observed. Only compared to group 2 (PI – 77.83%, API – 97.82%). The an increase in this parameter was detected in both the index values significantly decreased after the second visit study and the control group. No statistically significant in both groups and remained at a similar level during the differences were observed in the mean PD and CAL de- next 6 months. High hygiene index values were accom- pending on gender. Detailed data of PD and CAL is pre- panied by high BOP values which oscillated at the level sented in Table 2.

Table 1. Changes in the number of teeth, PD ≥ 4 mm, API, PI and BOP in subsequent clinical examinations 6 month from PBaseline vs 7 month from P6 month vs 12 month P7 month vs Group Parametr Baseline baseline 6 month baseline 7 month from baseline 12 month Total number 845 ± 4.61 843 ± 4.54 0.39 841 ± 4.49 0.39 834 ± 4.38 0.38 of teeth [n] PD ≥ 4 mm [n] 466 ± 3.79 472 ± 3.72 0.39 450 ± 3.25 0.35 444 ± 3.28 0.32 PD ≥ 4 [%] 55.14 55.84 53.25 52.54 API [ %] 98.46 ± 11.64 88.19 ± 12,56 0.0 68.28 ± 14.68 0.0 71.894 ± 13.42 0.0 PI [%] 81.33 ± 18.23 61.17 ± 21.24 0.0 45.28 ± 18.21 0.0 44.89 ± 20.17 0.0 BOP[ %] 73.21 ± 18.52 72.83 ± 19.28 0.39 52.97 ± 16.29 0.0 48.08 ± 19.06 0.0 Group 1 number 465 ± 5.07 464 ± 4.97 0.39 462 ± 4.92 0.39 459 ± 4.77 0.38 of teeth [n] PD ≥ 4 mm [n] 246 ± 3.47 250 ± 3.25 0.38 227 ± 2.56 0.26 215 ± 2.42 0.14 PD ≥ 4 [%] 52.79 53.0 50.44 48.42 API [%] 99.12 ± 6.82 90.21 ± 7.37 0.0 73.35 ± 10.46 0.0 73.48 ± 11.68 0.0 PI [ %] 85.12 ± 16.41 63.73 ± 18.39 0.0 44.94 ± 19.12 0.0 43.08 ± 21.92 0.0 BOP [ %] 74.89 ± 18.04 73.48 ± 18.35 0.38 51.26 ± 19.03 0.0 49.05 ± 20.03 0.0 Group 2 number 380 ± 4.1 379 ± 3.99 0.39 379 ± 3.99 0.39 375 ± 3.85 0.38 of teeth [n] PD ≥ 4 mm 220 ± 4.15 222 ± 3.74 0.39 223 ± 2.12 0.38 229 ± 3.58 0.36 PD ≥ 4 [%] 47.21 47.0 49.56 51.58 API [%] 97.82 ± 15,68 87.48 ± 14.73 0.008 61.81 ± 16.42 0.0 67.76 ± 16.98 0.0 PI [ %] 77.83 ± 20,11 66.17 ± 19.64 0.029 46.82 ± 18.96 0.0 45.54 ± 18.45 0.0 BOP [%] 70.35 ± 19,52 68.86 ± 18.33 0.74 53.68 ± 19.46 0.003 47.83 ± 19.83 0.0

Number of teeth [n]; PD ≥ 4 mm [n]; PD ≥ 4 [%], API [w%], PI [w%], BOP [w%] – mean ± standard deviation. 44 M. Sulewska, et al. Non-surgical periodontal treatment

Table 2. Mean values, standard deviation and significance level (p) of the examined variables – PD and CAL in both groups considering time factor and patients’ age PD CAL Group Age Examination mean standard deviation p mean standard deviation p Group 1 total baseline 3.59 0.817 3.99 1.407 6 months from 3.61 0.832 0.35 4.01 1.427 0.42 baseline 7 months from 3.37 0.871 0.005 3.93 1.469 0.25 baseline 12 months 3.36 0.879 0.003 3.92 1.470 0.24 from baseline ≤ 55 baseline 3.66 0.782 3.895 0.987 6 months from 3.65 0.83 0.42 3.96 0.989 0.29 baseline 7 months from 3.37 0.862 0.009 3.84 1.048 0.38 baseline 12 months 3.35 0.861 0.007 3.802 1.049 0.30 from baseline > 55 baseline 3.57 0.856 4.15 1.771 6 months from 3.65 0.849 0.17 4.12 1.814 0.39 baseline 7 months from 3.44 0.862 0.10 4.10 1.848 0.34 baseline 12 months 3.43 0.871 0.05 4.13 1.842 0.45 from baseline Group 2 total baseline 3.61 0.585 4.05 1.253 6 months from 3.65 0.592 0.05 4.055 1.207 baseline 0.48 7 months from 3.60 0.606 0.47 4.09 1.264 0.41 baseline 12 months 3.63 0.608 0.26 4.15 1.303 0.31 from baseline ≤ 55 baseline 3.4 0.542 3.76 1.545 6 months from 3.44 0.579 0.22 4.03 1.493 0.12 baseline 7 months from 3.39 0.597 0.42 4.03 1.547 0.11 baseline 12 months 3.45 0.575 0.21 4.01 1.583 0.16 from baseline > 55 baseline 3.77 0.565 4.29 0.883 6 months from 3.83 0.524 0.07 4.07 0.908 0.23 baseline 7 months from 3.78 0.557 0.47 4.14 0.969 0.32 baseline 12 months 3.78 0.593 0.45 4.28 1.002 0.48 from baseline

There were no statistically significant differences in the Discussion examined parameters with respect to the patient’s gender. This may result from the participation of only 10 women Our obtained results indicate poor oral hygiene in pain the study (22.22% of the patients). However, it ought tients with a past history of myocardial infarction. This to be emphasized that 10 out of 13 randomized women observation was confirmed by the diagnosis of periodon- reported for control visits. titis in all the 124 hospitalized patients. Another concerning fact is that those patients neglect the necessity of applying periodontal treatment. During the first appoint- Dent Med Probl. 2017;54(1):41–47 45

ment each patient was educated about the relationship the necessity of frequent check-ups and constant re-mo- between periodontitis and the development of myocar- tivation of patients. This observation is concordant with dial infarction.4,5 Also, the patients were informed that the literature data which suggests that decreased bacterial non-surgical periodontal treatment decreases the level potential is considerably more effective by keeping nor- of inflammatory mediators including cardiovascular dis- mal oral hygiene as well as intense non-surgical periodon- eases.11,15,16 However, the patients showed negligence of tal treatment at numerous sessions than at 1 session.11 these scientific reports as only 37.5% of the qualified and Most of the studies carried out so far evaluated systemic randomized persons participated in the study. A similar and vascular consequences of the inflammatory process, problem was also observed by Offenbacher et al., who evaluated the influence of periodontal treatment at indi- suggested the need to recruit patients from cardiology rect final points of cardiovascular diseases, and observed departments.17 The authors observed the patients’ low in- numerous benefits of periodontal treatment.17,20,21 What terest in oral health in terms of the experienced myocar- is interesting, the type of therapy showed no significant dial infarction (death risk). Among the recruited patients, impact on the results. Importantly, patients undergoing 303 volunteers participated in the first study and only 37 any periodontal treatment experienced more benefits individuals reported for the examination after 1 year. compared to patients without periodontal therapy. Beck Dietrich et al. showed that the number of maintained et al. and Desvarieux et al. observed a stronger correla- teeth is a predictor of the risk of developing ischemic tion between infectious measurements (in serum, cre- heart disease.5 According to these authors, such a risk is vicular fluid) and cardiovascular disease compared to the considerably higher in edentulous men compared to those evaluation of periodontal therapy effectiveness based on with maintained dentition. Lack of maintained teeth in- clinical periodontal measurements.22,23 This is a probable dicates the severity of periodontal disease. According to cause of a small number of publications concerning the our results, none of the patients had less than 7 teeth and evaluation of periodontal parameters following non-sur- their approximate number at the first visit (1 examina- gical periodontal treatment in patients with past history tion) was 18.78 ± 6.1. The initial number of teeth was 845 of myocardial infarction. and decreased to 834 during a 12-month observation. The high initial mean values of BOP, PD and CAL ob- The patients agreed for extraction as the first appoint- tained in own study as well as the percentage of teeth with ment involved not only motivating and educating them in PD ≥ 4 mm reflect poor condition of periodontal tissues oral hygiene but they were also recommended sanitation in both groups. It may be assumed that proper periodon- of the oral cavity. 11 teeth were extracted, yet many more tal care and active treatment of periodontal diseases may were qualified for extraction due to poor prognosis. The decrease the risk of cardiovascular incidents. Therefore, patients failed to report for extraction due to fear of los- proper periodontal care ought to be an integral element ing teeth as well as, according to the history, due to the of medical care in patients with a past history of acute doctors’ concerns about performing extraction in patients coronary syndrome and in risk groups (all patients with right after myocardial infarction. The guidelines by Den- diagnosed ischemic disease). Every patient with a history tal and Cardiology Societies indicate that the majority of of myocardial infarction should be referred for a dental dental procedures are safe and do not require the need consultation as secondary prevention. According to the to discontinue dual antiplatelet therapy carried out in the available data, in the case of detecting periodontal disease first year after myocardial infarction.18 Patients’ aware- in ischemic patients and/or after myocardial infarction as ness is also reflected by the fact that 3 (27.27%) out of 11 well as after cerebral stroke, active dental and periodontal lost their teeth during a 12-month observation. treatment ought to be applied, which may lead to better The obtained high values of oral hygiene indexes (PI prognosis.24 – 81.33%, API – 98.46%) reflect poor oral hygiene in pa- In our research, a significant reduction of probing tients with the history of myocardial infarction. Accord- depth (p = 0.0027) after non-surgical periodontal treating to the medical history, the majority of patients report- ment (SRP) was obtained. These outcomes are confirmed ed to have brushed their teeth twice a day, yet as many in the study by Offenbacher et al., who observed a sig- as 35.55% (16 individuals) claimed not have brushed their nificant PD decrease in the group undergoing periodon- teeth more than once a day. The research by de Oliveira tal therapy compared to the group receiving social care et al. revealed a correlation between insufficient oral hy- only.17 Analogically to the obtained results, the authors giene and the increased risk of developing cardiovascular observed a reduction in the number of pockets over 4 and diseases.19 The patients who never or/and rarely brushed 5 mm. Our research showed a decrease in the number of their teeth showed an increased concentration of both 22 pockets with PD ≥ 4 mm. In group 1 a reduction by 31 CRP and fibrinogen. sites with high probing value was observed while in group In the presented protocol, the third control examina- 2 this number increased by 9. These changes undoubt- tion was carried out in a short, 1-month interval after the edly result from SRP therapy. According to the study by second one. The highest reduction in oral hygiene indexes Bahekar et al.,8 the reduction of the pockets with PD ≥ in both groups was obtained at that point, which indicates 4 mm reduces the risk of developing coronary heart dis- 46 M. Sulewska, et al. Non-surgical periodontal treatment

ease by 1.14–1.59, and thus the aim of periodontal thera- only on the doctor but to a great extent on the attention py ought to be elimination of the pockets over 4 mm.8 In of patients who should limit risk factors (smoking to- group 2, only a short, 1-month interval after control visits bacco) and maintain good oral hygiene at all times.34 Oral (between 2nd and 3rd appointment) led to an insignificant hygiene education comprises demonstration of brushing PD reduction, which most probably resulted from the hy- method with the recommendation of suitable duration giene education. According to other authors, longer in- and number of the procedures during the day. The dentist tervals between the appointments resulted in the increase expects that providing patients with information would in PD value, which confirms the necessity of frequent and change patients’ habits and cause the improvement of oral numerous control visits.11 hygiene. Unfortunately, this method has a limited impact According to the analysis of age, a significant PD im- on patients’ behavior and shows short-term effects.35–37 provement was observed only in younger patients ran- Therefore, frequent control visits, education and re-mo- domized to group 1. Probing depth in the younger group tivation are fundamental for successful therapy. In the (≤ 55 years) decreased by 0.31 mm, while in the older case of lack of everyday dental care, a single professional group (> 55 years) the reduction was only 0.14 mm and procedure fails to provide benefits. According to the cur- failed to reach statistical significance. The results may be rent understanding of care of periodontal cases, patients concordant with the research by other authors, who no- are responsible for the course and effect of treatment.38 ticed a strong relationship between periodontal disease in Patients with their needs, requirements, expectations and young male patients and the development of cardiovascu- values are at the center. Prevention activities evolve to- lar disorders.3,5,11,25,26 According to authors’ observations, wards more complex educational programs based on psy- this correlation constantly decreases with age and be- chological methods.39,40 This means that patients play an comes close to zero between 60–65 years of age. Dietrich active role in treating their disease and they partly take re- et al. suggest that at a younger age periodontium is an ex- sponsibility for treatment effectiveness. Thus, the dentist cellent marker of periodontal disease sensitivity.5 There- becomes the counselor who supports patients in taking fore, conducting studies on the group of male patients the right pro-health decisions. below 50 years of age would be of great benefit. However, The obtained results are indicative of the need of non- our research, as well as other studies, have been limited to surgical treatment in the group of patients with a past his- age groups below 65 years as cardiovascular incidents at tory of myocardial infarction. Continuation of random- the age below 50 are considerably rare. ized research on a larger group of patients is necessary The scope of inflammatory process tested at the first to obtain a reliable evaluation of therapy effects on the visit and expressed as BOP was extremely high. The val- periodontal status. ue of this parameter decreased statistically significantly (p = 0.0000002) during a 1-year observation in both groups References amounted to 49.05% and 47.83%, respectively. The final out- 1. Baehni P, Tonetti MS. Group 1 of the European Workshop on Peri- comes are insufficient and indicate a large number of still odontology: Conclusions and consensus statements on periodon- active pockets. The largest BOP reduction (25.84%) com- tal health, policy and education in Europe: A call for action-con- pared to the baseline value was observed in the group 1, sensus view 1. Consensus report of the 1st European Workshop on which is undoubtedly related to the mechanical removal Periodontal Education. Eur J Dent Educ. 2010;14(Suppl 1):2–3. 2. Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ. Prevalence of of biofilm (SRP). Offenbacher et al. carried out a 6-month periodontitis in adults in the United States: 2009 and 2010. J Dent observation and obtained a statistically insignificant de- Res. 2012;91:914–920. crease in BOP value in the actively treated group (SRP).17 3. De Stefano F, Anda RF, Kahn HS, Williamson DF, Russel CM. Den- tal disease and risk of coronary heart disease and mortality. BMJ. The proven relationship between development of peri- 1993;306:688–691. odontal diseases and cardiovascular disorders indicates 4. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal the necessity to prevent and treat inflammation in peri- disease and cardiovascular disease. J Periodontol. 1996;67:1123– 1137. odontal tissues. Basic periodontal treatment is mecha- 5. Dietrich T, Jimenez M, Krall Kaye EA, Vokonas PS, Garcia RI. Age- 27–29 notherapy, which is scaling and root planing. SRP is dependent associations between chronic periodontitis/edentu- aimed at breaking the structure of bacterial biofilm and lism and risk of coronary heart disease. Circulation 2008;117:1668– 1674. thus at the reduction of pathogens in periodontal pock- 6. Hyman JJ, Winn DN, Reid BC. The role cigarette smoking in the ets. Maintenance of hygiene regimen by the patient is an association between periodontal disease and coronary heart dis- indispensable element of the therapy. SRP effectiveness is ease. J Periodontol. 2002;73:988–994. well documented and expressed by the reduction of prob- 7. Górska R. Relationship between periodontitis and systemic disor- derd. Dent Med Probl. 2009;46:379–383 [in Polish]. ing depth, gain in clinical attachment level as well as re- 8. Bahekar AA, Singh S, Saha S, Molnar J, Arora R. The prevalence and duced bleeding of probing.30–33 According to own study, incidence of coronary heart disease is significantly increased in no above mentioned benefits were observed apart from periodontitis: A meta-analysis. Am Heart J. 2007;154:830–837. 9. D’Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, Tonetti PD reduction. The failure may be explained by a single MS. Periodontitis and systemic inflammation: Control of the local SRP procedure and lack of patients’ cooperation. Chapple infection is associated with a reduction in serum inflammatory et al. showed that treatment effectiveness depends not markers. J Dent Res. 2004;83:156–160. Dent Med Probl. 2017;54(1):41–47 47

10. Mattila K, Vesanen M, Valtonen V, Nieminen M, Palosuo T, Rasi V, 25. Geismar K, Stoltze K, Sigurd B, Gyntelberg F, Holmstrup P. Periodon- Asikainen S. Effect of treating periodontitis on C-reactive protein tal disease and coronary heart disease. J Periodontol. 2006;77:1547– levels: A pilot study. BMC Infect Dis. 2002;10:2–30. 1554. 11. Tonetti MS, Van Dyke TE. Periodontitis and atherosclerotic car- 26. D’Aiuto F, Orlandi M, Gunsolley JC. Evidence that periodontal treat- diovascular disease: Consensus report of the Joint EFP/AAP Work- ment improves biomarkers and ACVD outcomes. J Clin Periodontol. shop on Periodontitis and Systemic Diseases. J Periodontol. 2013;84 2013;40(Suppl 14):85–105. (Suppl 4):24–29. 27. Sanz I, Alonso B, Carasol M, Herrera D, Sanz M. Nonsurgical treat- 12. O’Leary TJ, Drake RB, Naylor JE. The plaque control record. J Peri- ment of periodontitis. J Evid Base Dent Pract. 2012;1:76–86. odontol. 1972;43:38. 28. Meissner G, Kocher T. Calculus-detection technologies and their 13. Lange DE, Plegmann HC, Eenboom A, Promsberger A. Klinische clinical application. Periodontol. 2000;2011:55, 189–204. Bewertungsverfahren zur Objektivierung der Mundhygiene. Dtsch 29. Jepsen S, Deschner J, Braun A, Schwarz F, Eberhard J. Calculus Zahnärztl Z. 1977;32:44–47. removal and the prevention of its formation. Periodontol. 2000;2011, 14. Ainamo J, Bay I: Problems and proposals for recording gingivitis 55:167–188. and plaque. Int Dent J. 1975;25:229–235. 30. Suvan JE. Effectiveness of mechanical nonsurgical pocket therapy. 15. Rodrigues DC, Taba MJ, Novaes AB, Souza SL, Grisi MF. Effect of Periodontol. 2000;2005, 37:48–71. non-surgical periodontal therapy on glycemic control in patients 31. Cobb CM. Non-surgical pocket therapy: Mechanical. Ann Periodon- with type 2 diabetes mellitus. J Periodontol. 2003;74:1361–1367. tol. 1996;1:443–490. 16. Taylor GW, Burt BA, Becker MP, et al. Non-insulin dependent diabe- 32. Van Der Weijden GA, Timmerman MF. A systematic review on the tes mellitus and alveolar bone loss progression over 2 years. J Peri- clinical efficacy of subgingival debridement in the treatment of odontol. 1998;69:76–83. chronic periodontitis. J Clin Periodontol. 2002;29(Suppl 3):55–71. 17. Offenbacher S, Beck JD, Moss K, et al. Results from the Periodon- 33. Adriaens PA, Adriaens LM. Effects of nonsurgical periodontal ther- titis and Vascular Events (PAVE) study: A pilot multicentered, ran- apy on hard and soft tissues. Periodontol. 2000;2004, 36:121–145. domized, controlled trial to study effects of periodontal therapy 34. Chapple IL, Van Der Weijden F, Doerfer C, et al. Primary prevention in a secondary prevention model of cardiovascular disease. J Peri- of periodontitis: Managing gingivitis. J Clin Periodontol. 2015;42 odontol. 2009;80:190–201. (Suppl 16):71–76. 18. Pruszczyk P, Ciurzyński M, Opolski G, et al. Common dental-cardio 35. Johansson LA, Oster B, Hamp SE. Evaluation of cause related peri- position for dealing anticoagulation in patients undergoing dental odontal therapy and compliance with maintenance care recom- procedures. Kardiol Pol. 2016;74:87–98. mendations. J Clin Periodontol. 1984;11:689– 699. 19. De Oliveira C, Watt R, Hammer M. Tooth brushing, inflammation, 36. Kay EJ, Locker D. Is dental health education effective? A sys- and risk of cardiovascular disease: Results from Scottish Health Sur- tematic review of current evidence. Comm Dent Oral Epidemiol. vey. BMJ. 2010;340:2451. 1996;24:231–235. 20. Tonetti MS, D’Aiuto F, Nibali L, et al. Treatment of periodontitis and 37. Schüz B, Sniehotta FF, Wiedemann A, Seemann R. Adherence to endothelial function. N Engl J Med. 2007;356:911–920. a daily flossing regimen in university students: Effects of planning 21. Piconi S, Trabattoni D, Luraghi C, et al. Treatment of periodon- when, where, how and what to do in the face of barriers. J Clin Peri- tal disease results in improvements in endothelial dysfunction odontol. 2006;33:612– 619. and reduction of the carotid intima-media thickness. FASEB J. 38. Miller WR, Rollnick S. Motivational interviewing: Preparing people 2009;23:1196–1204. for chance. 2nd ed. New York, Guilford, 2002. 22. Beck JD, Eke P, Lin D. Associations between IgG antibody to oral 39. Clarkson JE, Young L, Ramsay CR, Bonner BC, Bonetti D. How to organisms and carotid intima-medial thickness in community- influence patient oral hygiene behavior effectively. J Dent Res. dwelling adults. Atheroscler. 2005;183:342–348. 2009;88:933–937. 23. Desvarieux M, Demmer RT, Rundek T. Relationship between peri- 40. Jönsson B, Ohrn K, Oscarson N, Lindberg P. The effectiveness of odontal disease, tooth loss, and carotid artery plaque. The oral an individually tailored oral health educational program on oral infections and vascular disease epidemiology study (INVEST). hygiene behavior in patients with periodontal disease: A blind- Stroke 2003;34:2120–2125. ed randomized-controlled clinical trial (one-year follow-up). J Clin 24. Górska R. Sprawozdanie z niezależnego panelu ekspertów na Periodontol. 2009;36:1025–1034. temat związku chorób przyzębia z chorobami ogólnoustrojowymi. Kardiol Pol. 2009;67:708–710 [in Polish].

Original papers Dental emergencies in Burkina Faso Armed Forces Nagłe przypadki stomatologiczne u żołnierzy sił zbrojnych Burkina Faso

Raoul Bationo1, A, C, D, Wendpouiré P. L. Guiguimdé2, E, F, Hamidou Ouédraogo1, B, Blintim Somé1, B

1 Medical Center of General Aboubacar Sangoulé Lamizana, Burkina Faso 2 Health Department, Ouaga I University Professor Joseph Ki-Zerbo, Burkina Faso

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017; 54(1): 49–51

Address for correspondence Abstract Raoul Bationo E-mail: [email protected] Background. Dental emergencies affect the mission of deployed units. During military operations, the definition of dental emergency is different from that which is commonly accepted in dentistry. There is Funding sources none declared no notion of seriousness or need for urgent care. A considerable number of studies concerning American, French and other armies exist in the literature. This is the first study in Burkina Faso. Conflict of interest Objectives. The purpose of this study was to quantify the dental emergency rate observed in Burkina Faso none declared soldiers deployed in Mali and to determine the percentage of dental emergencies.

Received on September 9, 2016 Material and methods. All the reasons for dental emergencies, between February 2015 and January Revised on November 9, 2016 2016, were documented from the data of the register of clinical activities from the dental clinic of Timbuktu Accepted on November 23, 2016 level 1 hospital. Results. Caries accounted for 47.1% of dental emergencies. The second most common reason for visiting the dental clinic was periodontal diseases (19.3%), followed by lost crowns (9.7%). Fractured teeth caries accounted for 9% of emergencies and 7.1% of emergencies were attributed to infections. The remaining visits for dental emergencies accounted for 7.8%. The dental emergency rate for Burkina Faso Forces based in Mali is 182 per 1,000 soldiers per year. Conclusions. Caries are the main reason why soldiers went to the dental clinic. Dental emergencies can significantly affect the mission of the deployed unit. Key words: dental emergencies, operational capability, deployed soldiers, Burkina Faso Army Słowa kluczowe: nagłe przypadki stomatologiczne, zdolność operacyjna, rozlokowani żołnierze, armia Burkina Faso

DOI 10.17219/dpm/67315

Dental pathologies account for a great deal of the medi- Table 1. Frequency of reasons for dental emergencies (DEs) cal emergencies encountered by the deployed military Percentage Cause of DEs Frequency personnel. It has been demonstrated that as many as 22% (n = 155) of all emergency health visits during field training exer- Caries 73 47.1 1 cises were attributable to dental problems. Infections 11 7.1 Dental emergencies can significantly affect the mission of Lost crowns 15 9.7 the deployed unit with the following repercussions2: A de- Pericoronitis 3 2 creased level of the soldiers’ individual performance, inability Periodontal diseases 30 19.3 of the soldiers to accomplish their mission, unavailability of the soldiers with dental problems in case of a visit to a dental Fractured teeth no caries 2 1.3 care facility is necessary, unavailability of the soldiers who es- Fractured teeth caries 14 9 cort a patient to a dental care facility and the potential risks Others 7 4.5 associated to the movements in theaters of operations. During military operations, there is no notion of seriousness or need for urgent care in the definition of a dental emergency. This study uses a consensus definition: One hundred fifty-five (155) dental emergency visits “A condition of oral disease, trauma or loss of function, were recorded. This accounts for 182 per 1,000 soldiers or other concern that causes a patient to seek immediate per year. Most of the emergencies (47.1%) were due to dental treatment”.3 caries. The mission of the military dentists will be to preserve Periodontal diseases were the second most common the operational capability of troops by avoiding time loss- reason for visiting the dental clinic (19.3%), followed by es due to a dental issue. lost crowns (9.7%). Fractured teeth caries accounted for So far, there have been many studies concerning dental 9% of emergencies and 7.1% of emergencies were attribut- emergency rates of soldiers in theaters of operations.4–8 ed to infections. The remaining combined visits for dental The most recent, by Gunepin et al.,6 was conducted in emergencies accounted for 7.8%. Mali, as is this study. Our study aims to assess the impact of dental problems on the operational capability of Burkina Faso armed Forc- Discussion es by counting the reasons for dental emergencies. Caries appear as the main dental problem of deployed military personnel, accounting for 47.1% of causes of den- Material and methods tal emergencies. Data from our study shows that caries, periodontal dis- The present study investigated the rate of dental emer- eases and lost crowns are the 3 most common causes of gency visits from a patient population of 850 Burkina dental emergencies in Burkina Faso Army. The results of Faso soldiers deployed as part of the United Nations Mul- American, English, Australian and French studies6,9–12 are tidimensional Integrated Stabilization Mission in Mali different; with caries, fractured teeth and/or crowns with- (MINUSMA) from February 2015 to January 2016. out caries and pulpitis as the most common reasons for The register of clinical activities from the dental clinic of the dental emergency. Timbuktu level 1 hospital served as a basis for data collection. A dental literature review shows that caries are the Only the causes of dental emergencies in Burkina Faso main cause of dental emergency regardless of the nation- soldiers have been taken into account. ality of soldiers, the theater of operations and the deploy- The rate of dental emergencies per 1,000 soldiers was ment time (Table 2). calculated by dividing the total number of initial emer- The dental emergency rate expressed the difference be- gency visits by the total number of deployed soldiers and tween armies opposite to the percentage of each cause of then multiplying by 1,000. dental emergencies. The values were analyzed using Epi Info v. 3.5.3 soft- The literature reported rates from 293 to 700 per 1,000 ware. The statistical test was Mantel-Haenszel Chi-square soldiers per year for French Army,2,4,6,13 and from 86 to and the corresponding odds ratios were presented with 259 per 1,000 soldiers per year for U.S., Canadian and p < 0.05. British Forces.9–12,14 So Burkina Faso soldiers have the same dental problems than the other armies, but in small number comparatively to the French Forces. Results Studies by Chaffin et al.7 and Moss8 supported these findings, as caries were responsible for more than 1/2 of The frequency of each cause of the dental emergency is all dental emergencies, if the defective restorations are in- presented in Table 1. cluded in the caries category. Dent Med Probl. 2017;54(1):49–51 51

Table 2. Rate of the dental emergency (DE) at the operations and frequency of caries in Armies

Authors Army Place Duration Supported population Number of DE DE rate % of caries Gunepin et al4 FR Afghanistan 2 months 3,750 210 293 43 Gunepin et al.6 FR Mali 10 months NR 556 NR 44.6 Dunn15 US Oman 6 months 1,972 137 NR 38.4 Bationo et al. BFA Mali 12 months 850 155 182 47.1

Our frequency of caries in dental emergencies (47.1%) per 1,000 soldiers per year. This statistic is lower than re- is not significantly different from the results observed in ports of French Forces. The primary etiologic factor in the the French Army in Mali (44.6%) (p = 0.71).6 current study was caries (47.1%). Every effort is made to give deployed military personnel To prevent the occurrence of these emergencies, all a dental examination to identify correctable conditions or soldiers must have access during missions to oral hygiene disease before their arrival to theaters of operations. commodities. The military dentists must provide soldiers The objective of the examination is to assess for each with emergency and non-emergency care prior to their soldier their oral condition and the risk of a dental emer- deployment and also schedule routine visits during op- gency occurrence during the next 12 months.16 erations. After a fitness examination, soldiers with dental pathol- References ogies must undergo dental care prior to their deployment. 1. Grover PS, Carpenter WM, Allen GW. Dental emergencies occurring In theaters of operations, dental emergencies for cari- among United States Army recruits. Milit Med. 1983;148:56–57. ous reasons are related to preexisting lesions may worsen 2. Gunepin M, Derache F. Impact opérationnel et prise en charge des during missions because of the deterioration of living pathologies bucco-dentaires dans le cadre des opérations extéri- conditions (decrease of oral hygiene). eures. Médecine et Armées 2009;37:313–318 [in French]. 3. Simecek J. Consensus statements. Milit Med. 2008;173:59. All soldiers must have access during missions to oral 4. Gunepin M, Derache F, Ausset I, Berlizot P, Simecek J. The rate of hygiene commodities that can contribute to the improve- dental emergencies in French Armed Forces deployed to Afghani- ment of their oral health. stan. Milit Med. 2011;176:828–832. 5. Fenistein B. Pourquoi tant de consultants dentaires en Opex? These commodities can be available as a dental kit Médecine et Armées 2004;32:123–126 [in French]. included in a field hygiene kit. The U.S. Army uses the 6. Gunepin M, Benmansour A, Derache F, Maresca S, Blatteau JE, Health and Comfort Pack (HCP) type I.17 Risso JJ. Motifs de consultation en urgence au cabinet dentaire du groupement médico-chirurgical de Gao: Quelles leçons en tirer? The individual combat pack for each deployed soldier from Médecine et Armées 2015;43:345–351 [in French]. Burkina Faso Armed Forces includes 1 toothbrush with tooth- 7. Chaffin J, King JE, Fretwell LD. U.S. Army dental emergency rates in paste. This is very insufficient for a 12-month long mission, so Bosnia. Milit Med. 2001;166:1074–1078. 8. Moss DL. Dental emergencies during SFOR 8 in Bosnia. Milit Med. the renewal of this mini kit is the soldier’s responsibility. 2002;167:904–906. Dental care was only given to soldiers who came for a visit. 9. Dunn WJ, Langsten RE, Flores S, Fandell JE. Dental emergency rates It would therefore be desirable for a dentists to schedule rou- at two expeditionary medical support facilities supporting opera- tine visits at least every 6 months so as to allow them to treat tions enduring and Iraqi Freedom. Milit Med. 2004;169:510–514. 10. Mahoney G, Coombs M. A literature review of dental casualty rates. dental pathologies and also perform routine teeth cleaning. Milit Med. 2000;165:751–756. Unfortunately, in Burkina Faso the oral health program 11. Mahoney D. The operational dental officer in the ADF. ADF Health does not take into account the strategy of fluoride appli- 2003;4:40–44. 12. Moss D. Dental emergencies during Stabilization Force 8 in Bosnia. cation on the teeth. Thus, it would be beneficial for the Milit Med. 2002;167:904–906. Armed Forces to adopt this strategy for the prevention of 13. Gunepin M, Limonet A, Derache F. Intérêts et limites de l’utilisation caries in deployed military personnel. de la classification internationale des maladies dans le recueil de l’activité dentaire en opération. Médecine et Armées 2010;38:417–424 The use of xylitol in addition to daily oral hygiene can [in French]. also help reduce the frequency of dental emergencies 14. Simecek JW, Colthirst P, Wojcik BE, Eikenberg S, Guerrero AC, among soldiers in operations. Finland and the USA have al- Fedorowicz A, Szeszel-Fedorowicz W, DeNicolo P. The incidence of 18 dental disease nonbattle injuries in deployed U.S. Army personnel. ready incorporated this molecule in their Armed Forces. Milit Med. 2014;179:666–673. 15. Dunn WJ. Dental emergency rates at an expeditionary medical support facility supporting operation enduring Freedom. Milit Med. 2004;169:349–353. Conclusions 16. NATO standard. AMedP-4.4. Dental fitness standards for military personnel and the NATO dental fitness classification system. Edi- Dental emergencies of soldiers have a direct effect on tion A Version 1, 2014. the capability of a deployed Force to accomplish its as- 17. Gunepin M, Derache F. Approche militaire américaine de l’optimi- sation de la mise en condition dentaire des forces. Médecine et signed mission. Armées. 2008;36:323–331 [in French]. The dental emergency rate for Burkina Faso Army 18. Gunepin M, Derache F. Impact du xylitol sur le risque carieux – impli- peacekeeping operation in Mali was determined to be 182 cations militaires. Médecine et Armées. 2010;38:369–380 [in French].

Prace oryginalne Ocena szczelności brzeżnej materiałów stosowanych do odbudowy tkanek korzenia zęba utraconych w wyniku resorpcji Evaluation of marginal integrity of materials used in root postresorption cavities

Radosław Markowski1, A–D, Sławomir Ledzion2, A, D, E, Halina Pawlicka2, E, F

1 Prywatna praktyka, Bełchatów, Polska 2 Zakład Endodoncji, Katedra Stomatologii Zachowawczej i Endodoncji, Uniwersytet Medyczny w Łodzi, Łódź, Polska

A – koncepcja i projekt badania, B – gromadzenie i/lub zestawianie danych, C – analiza i interpretacja danych, D – napisanie artykułu, E – krytyczne zrecenzowanie artykułu, F – zatwierdzenie ostatecznej wersji artykułu

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):53–58

Adres do korespondencji Streszczenie Sławomir Ledzion E-mail: [email protected] Wprowadzenie. Resorpcja zęba jest jedną z chorób prowadzących do utraty twardych tkanek zęba. Pro- ces zachodzi z udziałem specyficznych interakcji między komórkami układu odpornościowego a tkankami Zewnętrzne źródła finansowania Z badań statutowych 503/2-044-02/503-21-001 twardymi. Rozpoznanie najczęściej jest przypadkowe, dzięki zdjęciom rentgenowskim. Leczenie jest ukie- runkowane na zatrzymanie procesu resorpcyjnego i w miarę możliwości na odtwarzanie utraconych tka- Konflikt interesów nek zęba. Najstarszym materiałem używanym do tego celu jest amalgamat. Dzięki rozwojowi materiało- Nie występuje znawstwa powstały nowe materiały, które ze względu na swoje właściwości coraz częściej są stosowane do uzupełniania utraconych tkanek zęba. Obecnie, ze względu na swoje właściwości, a zwłaszcza dużą bio- Praca wpłynęła do Redakcji: 5 października 2016 r. zgodność, najbardziej polecane jest MTA. Po recenzji: 17 listopada 2016 r. Zaakceptowano do druku: 28 grudnia 2016 r. Cel pracy. Określenie, który z najczęściej stosowanych materiałów do wypełnień jam resorpcyjnych zapewnia najlepszą szczelność. Materiał i metody. Do badań użyto 50 usuniętych zębów ludzkich. W każdym zębie w części środko- wej korzenia wykonywano 4 nacięcia imitujące jamy resorpcyjne, które następnie wypełniano: amalgamatem GS-80, IRM®, ProRoot® MTA oraz Fuji® IX. Ocenę szczelności tych materiałów badano metodą penetracji barwnika, posługując się czterostopniową skalą Mayera. Wyniki. Najmniejszą penetrację barwnika, a tym samym najlepszą szczelność, uzyskano w przypadku ubytków wypełnionych ProRoot MTA, a największy przeciek barwnika, prawie dwukrotnie większy, dla Fuji IX. Uzyskane wyniki poddano analizie statystycznej. Wnioski. Ze względu na dużą szczelność brzeżną MTA, amalgamat oraz IRM mogą być z powodzeniem stosowane do wypełnienia ubytków poresorpcyjnych. Słowa kluczowe: MTA, resorpcja korzenia, szczelność brzeżna, test penetracji barwnika DOI 10.17219/dmp/68133 Abstract

Copyright Background. Tooth resorption is a disease which can lead to the loss of dental hard tissue. The process of © 2017 by Wroclaw Medical University resorption is mediated by specific interactions between immune cells and hard tissues of the tooth. Recognition and Polish Dental Society of this process is mostly random thanks to an x-ray examination, and the treatment involves stopping the pro- This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License cess and restoring the lost tissues of the tooth if possible. Amalgam is the oldest material used for this purpose. (http://creativecommons.org/licenses/by-nc-nd/4.0/) Currently, the MTA is the most recommended material, due to its properties, especially high biocompatibility. 54 R. Markowski, S. Ledzion, H. Pawlicka. Szczelność brzeżna wypełnionych resorpcji

Objectives. The aim of the study is to evaluate which of the most commonly used materials for filling postresorption cavities provides the best seal. Material and methods. 50 extracted human teeth were used in the study. Four cuts imitating postresorption cavities were performed in the middle part of the root of each tooth and were further filled with: amalgam GS-80, IRM®, Pro-Root® MTA and Fuji® IX. The evaluation of leakage of these materials was tested by the dye penetration method using the four-level Mayer scale. Results. The lowest dye penetration, and thus the best sealing, was obtained using ProRoot MTA. The largest leakage of dye-almost double-was obtained using Fuji IX. The results were statistically analyzed. Conclusions. MTA, amalgam and IRM can be successfully used to fill postresorption cavities due to their high marginal integrity. Key words: MTA, root resorption, marginal integrity, dye penetration test

Jedną z patologii stomatologicznych, która może przy- jej szczelnym wypełnieniu. Skutecznym zabiegiem jest czynić się do utraty zęba, jest resorpcja korzenia. W jej chemomechaniczne opracowanie kanału korzeniowego wyniku zębina korzeniowa zostaje zastąpiona ziarniną z zastosowaniem do płukania 5,25% roztworu podchlory- resorpcyjną lub w szczególnych przypadkach tkanką po- nu sodu. Tak duże stężenie NaOCl najlepiej rozpuszcza dobną w swojej strukturze do kości. Do dzisiaj resorpcja części organiczne, włączając w to komórki resorpcyj- korzenia stanowi poważny problem dla stomatologa, a le- ne.2,3 Pomiędzy wizytami poleca się wypełnianie kanałów czenie nie zawsze kończy się pełnym sukcesem. Częstość preparatem na bazie nietwardniejącego wodorotlenku występowania resorpcji szacuje się na około 3,79% w ca- wapnia, który zmniejszając pH środowiska, wpływa na łej populacji.1 W większości przypadków jest to resorpcja zahamowanie czynności osteoklastów oraz działa litycz- zewnętrzna i w 82,44% dotyczy okolicy wierzchołka ko- nie, ułatwiając późniejsze usunięcie resztek tkanek ziarni- rzenia zęba. Częściej występuje w zębach szczęki (55,1%) nowych z jamy zęba.4,5 i u kobiet (59,04%). Na zjawisko resorpcji najbardziej po- Leczenie resorpcji zewnętrznych jest bardziej skompli- datne są zęby osób w wieku 21–30 lat, co stanowi 28,4% kowane i powinno rozpocząć się od ustalenia przyczy- wszystkich przypadków, najrzadziej jest obserwowana ny, która spowodowała ten proces. W pierwszym etapie u dzieci (5,51%).1 niezbędne jest wyeliminowanie czynnika wywołującego Bezobjawowy przebieg choroby powoduje, że objęte resorpcję. Następnie po dokładnym oczyszczeniu po- procesem resorpcji zęby są osłabione w swojej struktu- wierzchni jamy resorpcyjnej wypełnia się ją odpowiednim rze, a w wyniku zmniejszonej powierzchni przyczepu materiałem. więzadeł ozębnej słabsze jest również ich umocowanie Wypełnianie ubytków resorpcyjnych w środkowym w zębodole. odcinku korzenia sprawia największy kłopot – z powo- Proces resorpcji zęba zachodzi z udziałem specyficz- du ich umiejscowienia. Trudność jest głównie spowodo- nych interakcji między komórkami układu odpornościo- wana utrzymaniem optymalnej suchości i czystości pola wego: zapalnymi, resorpcyjnymi a tkankami twardymi. operacyjnego. Z uwagi na środowisko szczególnie ważny Aby resorpcja zaistniała, konieczne jest działanie czyn- jest dobór odpowiednich materiałów wypełniających. ników patogennych w dwóch fazach. Po mechanicznym Należy zwrócić również uwagę na ich właściwości fizy- lub chemicznym uszkodzeniu tkanek jest niezbędna faza kochemiczne i wpływ na tkanki otaczające i cały orga- przewlekła, w której to długotrwale działający bodziec nizm. W związku z tym materiały te powinny: szczelnie zapalny lub ucisk stymuluje resorpcję. Dynamika zjawi- przylegać do ścian ubytku (tkanek zęba), zachować kształt ska jest różna i zależy od rodzaju czynnika i przebiegu i wymiar, co wiąże się z jego odpornością na rozpuszcza- wzajemnie antagonistycznych procesów destrukcji i no- nie i wypłukiwanie, być elektrochemicznie obojętne i od- wotworzenia tkanek. porne na korozję, hamować wzrost organizmów patogen- Głównymi komórkami odpowiedzialnymi za resorpcję nych, być dobrze tolerowane (nie powodować odczynów są osteoklasty. Te wielojądrzaste komórki kościogubne są zapalnych otaczających tkanek) i nietoksyczne dla orga- rodzajem makrofagów. Powstają w wyniku łączenia ma- nizmu, stymulować odbudowę tkanki ozębnej, dawać cień krofagów jednojądrowych pod wpływem działania chole- na zdjęciach rentgenowskich, dorównywać wytrzymało- kalcyferolu. ścią odbudowywanym tkankom, być łatwe w przygoto- Resorpcje najczęściej rozpoznaje się przypadkowo, waniu i zakładaniu. głównie dzięki zdjęciom rentgenowskim, a ich leczenie Biorąc pod uwagę powyższe właściwości, do wypełnień polega na zatrzymaniu procesu i w miarę możliwości od- ubytków resorpcyjnych najczęściej stosuje się następujące tworzeniu utraconych tkanek zęba. materiały: amalgamat, cementy tlenkowo-cynkowo-eu- Leczenie resorpcji wewnętrznych polega na całkowitym genolowe (ZnOE), cementy szkło-jonomerowe i agregat usunięciu ziarniny resorpcyjnej z jamy zęba, a następnie trójtlenków metali (MTA). Dent Med Probl. 2017;54(1):53–58 55

Celem pracy było określenie, który z najczęściej stoso- Po 12 dniach zęby zanurzano na 48 h w 2% roztworze wanych materiałów do wypełniania jam resorpcyjnych błękitu metylenowego. Następnie płukano je pod bieżącą zapewnia najlepszą szczelność. wodą i szlifowano poprzecznie w miejscu wypełnienia. Każdy szlif zęba oglądano pod mikroskopem endodon- tycznym, określając, na jakiej szacunkowej głębokości jest Materiał i metody widoczne zabarwienie między materiałem a zębiną. Do oceny przecieku brzeżnego metodą penetracji barwnika Do badań użyto 50 usuniętych ludzkich zębów wieloko- posłużono się czterostopniową skalą Meyera: rzeniowych. Podczas całego badania zęby przechowywa- – 0 – brak przecieku, no w cieplarce w temperaturze 37oC i 95% wilgotności. – 1 – barwnik penetruje do 1/3 głębokości ubytku, Aby zapobiec przesuszeniu zębów, czas niezbędny do – 2 – barwnik penetruje głębiej od 1/3 do 2/3 głębokości preparacji jam imitujących resorpcję oraz ich wypełnie- ubytku, nia starano się ograniczyć do minimum. W każdym zębie – 3 – barwnik penetruje głębiej niż 2/3 głębokości w środkowym odcinku korzenia wykonano wiertłem dia- ubytku.6 mentowym na turbinę (Φ = 1,8) cztery zagłębienia wzdłuż W wyniku przeprowadzonych pomiarów uzyskano korzenia o wymiarach 2 × 3 mm i głębokości 2 mm. dane zebrane w tabeli 1 i na rycinie 1. Przed wypełnieniem ubytki przemywano fizjologicznym Metoda i liczba pomiarów pozwala na statystyczną oce- roztworem chlorku sodu i osuszano jałową watką. nę otrzymanych wyników. Badania dla czterech różnych Amalgamat GS-80® (firmy SDI) rozrabiano we wstrzą- materiałów przeprowadzono na jednym zębie, dlatego sarce, zakładano i kondensowano w ubytku z użyciem też do analizy statystycznej zastosowano testy dla zmien- upychadła do amalgamatu. Po odczekaniu około 2 mi- nych zależnych. We wstępnym etapie analizy porównano nut uwolniano zarys wypełnienia za pomocą nakładacza jednocześnie wyniki dla wszystkich czterech materiałów, i przenoszono ząb do cieplarki. stosując test Friedmana. Uzyskano prawdopodobieństwo IRM® (Dentsply DeTrey) rozrabiano z użyciem łopat- p < 0,0005 (przy założonym poziomie istotności testu ki metalowej na szorstkiej powierzchni płytki szklanej, = 0,05), co oznacza, że dla niektórych z zastosowanych mieszając płyn i proszek w proporcjach zalecanych przez materiałów głębokości przecieków były inne niż w pozo- producenta. Materiał przenoszono do ubytków na nakła- stałych. Ponieważ dla testu Friedmana nie istnieją testy daczu, kondensowano i zbierano nadmiary kuleczką z ja- porównań wielokrotnych, przyjęto w pojedynczym po- łowej waty. Po odczekaniu około 2 minut zęby umieszcza- równaniu każdych dwóch materiałów konserwatywny po- no w cieplarce. ziom istotności w teście Wilcoxona równy 0,05/6 = 0,008, Cement szkło-jonomerowy Fuji IX® (firmy GC Cor- (gdzie 6 stanowi liczbę kombinacji dwuelementowych poration) rozrabiano na papierku załączonym do opako- zbioru czteroelementowego). Szczegółowe wyniki tych wania, mieszając proszek z płynem plastikową łopatką porównań przedstawiono w tabeli 2. w proporcjach zalecanych przez producenta. Nakładano do ubytku nakładaczem i kondensowano wilgotną ku- leczką z jałowej waty. Następnie po odczekaniu 2 minut Wyniki zęby umieszczano w cieplarce. Pro Rot MTA® (Dentsply DeTrey) rozrabiano na gład- Analizując uzyskane wyniki, można stwierdzić, że naj- kiej powierzchni płytki szklanej, łącząc proszek z wodą mniejszą penetrację barwnika uzyskano w przypadku destylowaną za pomocą metalowej łopatki. Zawiesinę ubytków wypełnionych MTA, gdzie w 43 przypadkach na przenoszono na nakładaczu, kondensację wykonywano 50 nie stwierdzono przecieku. Nieco gorsze właściwości kuleczką z jałowej waty, usuwając jednocześnie nadmiary posiadają: IRM (36 przypadków) i amalgamat (34 przy- materiału, a następnie umieszczano zęby w cieplarce. padki). Dwukrotnie gorszy wynik uzyskano dla Fuji IX Sposób przygotowania ubytków i materiałów oraz po- (18 przypadków). Wyniki analizy najgłębszych prze- stępowanie podczas wypełniania, jak również przetrzy- cieków (2 i 3 w skali Meyera) wynoszą odpowiednio: mywanie materiału badawczego było zoptymalizowane 5 (amalgamat), 4 (MTA), 2 (IRM). Otrzymany wynik 14 pod kątem możliwego odtworzenia warunków in vivo. dla Fuji IX jest średnio trzykrotnie gorszy w porównaniu Przed założeniem cementu szkło-jonomerowego odstą- z pozostałymi materiałami. piono od zalecanego przez producenta kondycjonowania Materiałem, dla którego występują istotnie różne wy- zębiny. Zmiana procedury była podyktowana zbliżeniem niki, jest cement szkło-jonomerowy Fuji IX. W porów- postępowania do trudnych warunków panujących w polu naniu z amalgamatem głębokość przecieku była większa operacyjnym podczas zabiegu klinicznego. przy wypełnieniu cementem szkło-jonomerowym w 50% Ocenę szczelności wypełnień badano metodą penetra- obserwacji, w 40% przypadków głębokość przecieku jest cji barwnika. W tym celu powierzchnię zębów pokrywa- porównywalna z amalgamatem, a jedynie w 10% cement no dwukrotnie lakierem do paznokci, pozostawiając mi- szkło-jonomerowy okazał się lepszy. W porównaniu limetrowy margines wokół zarysu wypełnionego ubytku. z IRM również głębokość przecieku była większa w 50% 56 R. Markowski, S. Ledzion, H. Pawlicka. Szczelność brzeżna wypełnionych resorpcji

Tabela 1. Wyniki pomiaru głębokości penetracji barwnika według czterostopniowej skali Meyera

Table 1. Results of dye penetration method using the four-level Mayer scale

Nr zęba Amalgamat Fuji IX IRM MTA 1 1 0 1 0 2 0 1 1 0 3 2 1 0 0 4 2 2 2 0 5 0 2 0 0 6 0 3 2 0 Ryc. 1. Głębokość penetracji barwnika w zależności od materiału: 0 – brak 7 1 3 1 0 przecieku, 1 – przeciek do 1/3 głębokości ubytku, 2 – przeciek od 1/3 do 8 0 0 1 1 2/3 głębokości ubytku, 3 – przeciek powyżej 2/3 głębokości ubytku 9 0 0 0 0 Fig. 1. The depth of dye penetration depending on the material: 0 – no 10 0 0 0 0 leakage, 1 – leakage to 1/3 of the depth of the cavity, 2 – leakage from 1/3 11 2 3 0 0 to 2/3 of the depth of the cavity, 3 – leakage above 2/3 of the depth of the 12 0 3 1 2 cavity 13 0 1 0 0 14 0 0 0 0 Tabela 2. Analiza statystyczna głębokości przecieku testem Wilcoxona 15 0 1 0 0 Table 2. Statistical analysis of the leakage depth by the Wilcoxon test 16 0 0 0 0 Porównywane 17 1 2 0 0 Liczba % Prawdopodobieństwo materiały 18 0 3 0 0 Fuji IX vs amalgamat 19 0 1 0 0 Fuji IX < amalgamat 5 10 < 0,0005 20 1 1 0 0 Fuji IX > amalgamat 25 50 21 0 0 0 0 Fuji IX = amalgamat 20 40 22 0 1 0 0 IRM vs Amalgamat 23 0 1 0 0 IRM < amalgamat 11 22 0,37 24 1 0 0 0 IRM > amalgamat 9 18 25 0 1 0 0 IRM = amalgamat 30 60 26 0 1 0 0 MTA vs amalgamat 27 0 0 0 0 MTA < amalgamat 14 28 0,18 28 0 0 0 0 MTA > amalgamat 6 12 MTA = amalgamat 30 60 29 0 1 0 0 IRM vs Fuji IX 30 0 0 0 0 IRM < Fuji IX 25 50 < 0,0005 31 1 3 0 0 IRM > Fuji IX 3 6 32 0 1 0 0 IRM = Fuji IX 22 44 33 0 0 0 0 MTA vs Fuji IX 34 3 2 0 1 MTA < Fuji IX 29 58 < 0,0005 35 0 1 1 0 MTA > Fuji IX 5 10 36 1 1 0 0 MTA = Fuji IX 16 32 37 0 0 0 0 MTA vs IRM 38 2 0 0 0 MTA < IRM 10 20 0,41 39 0 1 1 2 MTA > IRM 6 12 MTA = IRM 34 68 40 0 3 1 0 41 1 2 0 3 42 0 1 1 0 43 1 2 0 0 obserwacji i tylko w 3 przypadkach (co stanowi 6%) jest 44 0 0 0 0 odwrotnie. Odsetek pomiarów głębszej penetracji barw- 45 1 1 1 0 nika w wypełnieniach z cementu szkło-jonomerowego 46 1 1 1 2 w porównaniu z MTA wynosił 58%, a tylko w 32% głębo- 47 0 0 0 1 kości penetracji są porównywalne. W 10% badanych zę- 48 0 0 1 0 bów przeciek okazał się większy w wypełnieniach z MTA 49 0 0 0 0 niż z Fuji IX. We wszystkich omówionych powyżej po- 50 0 2 0 0 równaniach prawdopodobieństwo uzyskania mniejszej Dent Med Probl. 2017;54(1):53–58 57

penetracji przez Fuji IX było mniejsze od 0,0005, co ozna- zabiegu resekcji.12–14 Szczelność i wpływ tych materiałów cza, że była to różnica statystycznie istotna. na tkanki okołowierzchołkowe były porównywalne lub Porównując pozostałe materiały, w około 60% zaob- różniły się tylko nieznacznie. serwowano podobną penetrację barwnika, a pomiędzy Wypełnienie wsteczne kanału korzeniowego po resekcji IRM i MTA nawet w 68% obserwacji. Mimo że podczas wierzchołka pod względem umiejscowienia i postępowa- zastosowania MTA barwnik w najmniejszej liczbie przy- nia jest podobne do wypełnienia ubytku resorpcyjnego padków był obserwowany między wypełnieniem i zębiną na powierzchni korzenia. Z tego powodu stosuje się ta- (7 przypadków), to nie jest to wartość świadcząca o istot- kie same materiały. W większości badań materiały te były nej statystycznie różnicy w porównaniu z IRM lub amal- porównywane pod względem przydatności do wypełnień gamatem. W piśmiennictwie za prawidłowe uznaje się wstecznych kanału, a otrzymane wyniki potwierdzały wypełnienia z przeciekiem brzeżnym 0 i 1.6 W związku skuteczność tylko wybranych preparatów. Na uwagę za- z tym przeprowadzono analizę statystyczną, biorąc pod sługuje MTA, który w badaniach własnych wykazywał uwagę te dwie wartości jako akceptowalne dla wypełnie- najlepszą szczelność. Autorzy badający szczelność w wy- nia oraz stopnie 2. i 3. według skali Meyera jako nieak- pełnieniach wstecznych kanałów również potwierdzali ceptowalne. Do tych obliczeń zamieniono wartości z ta- mniejszy przeciek dla MTA niż amalgamatu lub IRM.15,16 beli 1 na kod zero-jedynkowy. Różnica ta bywa czasami statystycznie istotna, czego nie Obliczenia wskazują również istotną statystycznie potwierdzono w badaniach własnych. Szczelność tego różnicę między wypełnieniem z cementu szkło-jonome- preparatu nie zależy również od sposobu przygotowania rowego a pozostałymi materiałami na niekorzyść tego ubytku przed wypełnieniem. Płukanie 17% EDTA, 35% pierwszego. Pozostałe materiały podobnie jak we wcześ- kwasem fosforowym lub 24% żelem EDTA daje takie same niejszej analizie wykazują zbliżoną szczelność. wyniki w uzyskaniu szczelności jak płukanie ubytku fizjologicznym roztworem chlorku sodu.17 Powyższe właści- wości w połączeniu z odpornością na wilgoć i największą Omówienie biozgodnością spowodowały, że MTA stał się materia- łem z wyboru w leczeniu ubytków w obrębie korzenia Otrzymanie znacząco gorszych wyników szczelności zęba.18 Odnosi się to zarówno do resorpcji, wstecznych w przypadku cementu szkło-jonomerowego Fuji IX może wypełnień kanałów po resekcji, jak też perforacji furkacji być spowodowane niestosowaniem się do zaleceń pro- lub korzenia zęba. Używane dawniej do tego celu amal- ducenta podczas przygotowywania próbek. Podobnie jak gamaty zostały zastąpione właśnie przez MTA, cementy postępuje się w trudnych warunkach panujących w polu ZnOE i szkło-jonomerowe. Wielu autorów porównywało operacyjnym, celowo odstąpiono od kondycjonowania wymienione materiały z amalgamatem. Wyniki wskazują, zębiny przed założeniem cementu oraz zaniechano po- że MTA i cementy tlenkowo-cynkowo-eugenolowe, do krycia izolatorem powierzchni wypełnienia.7 Pokrycie których jest zaliczany IRM, mają lepszy wpływ na otacza- izolatorem z użyciem pędzelka lub wacika jest mało pre- jące tkanki niż amalgamat, ale jest to różnica statystycznie cyzyjnie, a podczas rozdmuchiwania w czasie suszenia nieistotna.11,19 płyn izolujący zostaje przemieszczony na otaczające tkan- Cementy szkło-jonomerowe w badaniach porównaw- ki, co może zaburzać gojenie w tej okolicy.8 czych z amalgamatem wykazują mniejszy przeciek brzeż- Brak uzdatnienia zębiny i odstąpienie od pokrycia many i są dobrze tolerowane przez tkanki otaczające. Wy- teriału izolatorem przyczyniły się do gorszego przylegania stępowanie istotnych różnic nie jest pewne. Mimo że wypełnienia i zwiększonego przecieku brzeżnego, co po- odsetek wypełnień amalgamatowych, w przypadku któ- twierdzają i inni autorzy.9,10 De Bruyne et al.8 porównując rych stwierdzono przeciek, jest większy niż w porówny- cementy szkło-jonomerowe z uzdatnianiem zębiny i bez wanych cementach, to badana liniowo głębokość przecie- niego, jak również z MTA i cementami ZnOE, uzyskali ku jest mniejsza. Zjawisko to tłumaczy się zwiększaniem podobne wyniki. Mikroprzeciek w wypełnieniach bez za- objętości podczas twardnienia amalgamatu, co zmniejsza stosowania uzdatniacza zębiny był znacząco większy niż szczelinę brzeżną.20 Cement szkło-jonomerowy wykazu- w analogicznych wypełnieniach po jego użyciu. Zwraca- je dobrą adhezję do ścian ubytków, jednak jest bardziej no także uwagę na wpływ powstałego w wyniku trawienia wrażliwy na wilgoć i czynniki zewnętrzne podczas zara- kwaśnego środowiska na otaczające tkanki i późniejsze biania i w trakcie wiązania.20 Podczas zabiegów chirur- procesy gojenia. Chong i Ford11 opisali jednakowo dobre gicznych trudno utrzymać idealne warunki potrzebne do efekty lecznicze po zastosowaniu cementu szkło-jonome- wypełnienia i wiązania. Część badań potwierdza skutecz- rowego i amalgamatu. Są one porównywalne z wynikami ność wypełnień z cementów szkło-jonomerowych, które uzyskanymi dla MTA i IRM. Autorzy ci nie podali jednak pod względem szczelności ustępują jedynie MTA, zacho- szczegółów dotyczących sposobu wypełniania i przygo- wując lepsze przyleganie od IRM i amalgamatu.15,16 towania materiału. Porównania wybranych materiałów Obserwacje te powinny być poddane pogłębionej ana- dokonywano również w okolicy wierzchołka korzenia lizie, gdyż istnieją prace potwierdzające skuteczność le- zęba jako wsteczne wypełnienie kanału korzeniowego po czenia po zastosowaniu wszystkich wymienianych ma- 58 R. Markowski, S. Ledzion, H. Pawlicka. Szczelność brzeżna wypełnionych resorpcji

teriałów.6,11,15,21 Większe zainteresowanie amalgamatem 10. Titley KG, Torneck CD, Smith DC, Applebaum NB. Adhesion of glassionomer cement to bleached and unbleached bovine dentin. w dużej mierze było podyktowane bardziej względami Dent Traumatol. 1989;6:132–135. ekonomicznymi i związanymi z łatwością zarabiania niż 11. Chong B, Ford T. Root-end filling materials: Rationale and tissue wpływem na proces zdrowienia. response. End Topics 2005;11:114–130. 12. Gondim EJr, Kim S, de Souza-Filho FJ. An investigation of microle- Ze względu na dobrą szczelność brzeżną MTA, amal- akage from root-end fillings in ultrasonic retrograde cavities with gamat oraz IRM mogą być z powodzeniem stosowane do or without finishing: A quantitative analysis. Oral Surg Oral Med Oral wypełniania ubytków poresorpcyjnych, jednak ze wzglę- Pathol Oral Radiol Endod. 2005;48:755–760. 13. Pereira CL, Cenci MS, Demarco FF. Sealing ability of MTA, Super du na swoje właściwości (w szczególności dużą biozgod- EBA, Vitremer and amalgam as root-end filling materials. Pesqui ność) to MTA powinien być materiałem z wyboru w le- Odontol Bras. 2004;18:317–321. czeniu resorpcji. 14. Xavier CB, Weismann R, de Oliveira MG, Demarco FF, Pozza DH. Root-end filling materials: Apical microleakage and marginal adap- Piśmiennictwo tation. J Endod. 2005;31:539–542. 15. Adamo HL, Buruiana R, Schertzer L, Boylan RJ. A comparison of MTA, 1. Opacić-Galic V, Zivković S. Frequency of the external resorption of Super-EBA, composite and amalgam as root-end filling materials the tooth roots. Arh Celok Lek. 2004;132:152–158. using a bacterial microleakage model. Int Endod J. 1999;32:197–203. 2. Ledzion S, Markowski R, Pawlicka H. Resorption, causes and treat- 16. De Bruyne MA, De Moor RJ. The use of glassionomer cements ments. Stomatol Współ. 2005;12,1:8–12 [in Polish]. in both conventional and surgical endodontics. Int Endod J. 3. Lindskog S, Pierce AM, Blomlof L. Chlorhxidine as a root canal 2004;37:91–104. medicament for treating inflammatory lesions in the periodontal 17. Kubo CH, Gomes AP, Mancini MN. In vitro evaluation of apical seal- space. Endod Dent Traumatol. 1998;14:186–190. ing in root apex treated with demineralization agents and retro- 4. Ford GS, Baisden M, Haen M, Quigley N, Camp J. A case of severe filed with mineral trioxide aggregate through marginal dye leak- external resorption. J Can Dent Assoc. 1994;60:503–510. age. Braz Dent J. 2005;3:187–191. 5. Postek-Stefańska L, Brzoza M, Kalacińska J. Applying of calcium 18. Koh ET. Celluar response to Mineral Trioxide Aggregate. J Endod. hydroxide in dentistry – literature review. Stomatol Współ. 2004;11, 1998;24:543–547. 2:50–55 [in Polish]. 19. Pistorius A, Willershausen B, Marroquin B. Effect of apical root- 6. Jodkowska E. Evaluation of marginal sealing composite Filtek and filling materials on gingival fibroblasts. Int Endod J. 2003;36: Supreme 3M-ESPE. Stomatol Współ. 2004;11, 2:21–24 [in Polish]. 610–615. 7. Barkhordar RA, Pelzner RB, Stark MM. Use of glassionomers as ret- 20. Gladys S, Van Meerbeek B, Lambrechts P, Vanherle G. Microleakage rofilling materials. Oral Surg Oral Med Pathol. 1989;16:734–743. of adhesive restorative materials. Am J Dent. 2001;14:170–176. 8. De Bruyne MAA, De Bruyne RJE, De Moor RJG. Long-term assess- 21. Felippe WT, Felippe MCS, Rocha MJC. The effect of mineral trioxide ment of the seal provided by root-and filling materials in large cav- aggregate on the apexification and periapical healing of teeth with ities trough capillart flow porometry. Int Endod J. 2006;39:493–501. incomplete root formation. Int Endod J. 2006;39:2–9. 9. Ansari SR, Qayym Z, Khitab U. A comparison of sealing capabilities of amalgam, GIC and zinc oxide eugenol cement when used as retrograde filling materials (in vitro study). J Ayub Med Coll Abbottabed. 2003;15:43–49. Original papers Evaluation of the incidence of gingival recession in the citizens of a large urban agglomeration of the Podlaskie Province in the chosen age groups of 35–44 years and 65–74 years Ocena występowania recesji dziąseł u mieszkańców dużego miasta województwa podlaskiego w wybranych grupach wiekowych 35–44 oraz 65–74 lat

Magdalena Sulewska1, B–D, Jan Pietruski2, C–F, Renata Górska3, A, Edyta Sulima4, B, Rafał Świsłocki5, B, Agnieszka Paniczko6, B, Elżbieta Sokal7, B, Małgorzata Pietruska3, C, E, F

1 Department of Periodontology and Oral Mucosa Diseases, Medical University of Białystok, Białystok, Poland 2 Private Dental Office, Białystok, Poland 3 Department of Periodontology and Oral Mucosa Diseases, Medical University of Warsaw, Białystok, Poland 4 Private Dental Practice, Wasilków, Poland 5 Private Dental Practice, Dobrzyniewo Duże, Poland 6 Agmed Non-Public Healthcare Institute, Białystok, Poland 7 Private Dental Practice, Ełk, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):59–65

Address for correspondence Abstract Małgorzata Pietruska E-mail: [email protected] Background. Gingival recession is a condition affecting all of society. Epidemiological studies on recession incidence in the population are difficult to conduct and interpret due to the complex etiology of this abnormality. Funding sources none declared Objectives. The aim of the study was to establish the incidence of gingival recession in adult citizens of a large urban agglomeration of the Podlaskie Province. Conflict of interest none declared Material and methods. The study was carried out on randomly selected citizens of Białystok in 2 age groups. 115 individuals aged 35–44 years and 72 aged 65–74 years were examined. The clinical trial in- Received on October 26, 2016 volved an evaluation of the following aspects: recession incidence, extent (depth) and localization. Ad- Revised on October 31, 2016 ditionally, Plaque Index (PI) and Bleeding on Probing (BOP) were analyzed. Accepted on November 23, 2016 Results. Gingival recession was observed on at least one surface in about 79.14% of the individuals analyzed. The most common recession localization was the buccal surface in both the group of 35–44 years (5.29 ± 5.23) and of 65–74 years (6.24 ± 5.40). The lesions were statistically significantly more common on the lower teeth (mandible 7.38 ± 5.7 vs maxilla 4.75 ± 4.67) and lingual surface (lingual surface 3.47 DOI ± 3.11 vs buccal surface 1.77 ± 2.39) in the older group. In patients aged 35–44 years, the mean recession 10.17219/dmp/67323 depth was 1.54 ± 0.55, while in the case of patients aged 65–74 years, it was 2.28 ± 0.9.

Copyright Conclusions. Gingival recession is a common abnormality in the population of adult citizens of large ur- © 2017 by Wroclaw Medical University ban agglomerations in the Podlaskie Province. and Polish Dental Society This is an article distributed under the terms of the Key words: epidemiology, gingival recession, adult population Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) Słowa kluczowe: epidemiologia, recesje dziąsła, populacja osób dorosłych 60 M. Sulewska, et al. Gingival recessions

Apical displacement of the soft tissue margin in relation of over 30 thousand American people, these changes are to the cemento-enamel junction (CEJ), called gingival represent in approximately 23% of individuals with 10% cession, is a frequently observed abnormality in persons frequency in the age group of 30–39 years and over 60% with various oral cavity hygiene. The individuals who ex- in the group of 80–90 years.22 Due to the complex etiol- cessively care about hygiene show gingival recession (GR) ogy of gingival recessions, it is very difficult to perform mainly on the buccal surface of teeth while people with and interpret epidemiology studies evaluating recession poor oral hygiene and/or untreated periodontitis show incidence in the population. So far, the epidemiological recession on every tooth surface. Exposed cement surfac- studies performed consider selected etiological aspects es lead to root caries, non-carious lesions and increased or a coincidence of many factors through the creation of dentine sensitivity. Unfavorable gingival morphology may multiple regression models and the introduction of in- lead to the accumulation of dental plaque and inhibits dependent variables which can influence the occurrence preservative and prosthetic treatment. Gingival recession and number of recessions.3,4,6,9,23–28 An analysis of these located within the front teeth is the most problematic, es- models proves that they are inadequate and the knowl- pecially in the times of aesthetic dentistry.1–4 edge on recession-causing factors is still insufficient.29 Gingival recession develops for many reasons which in- The aim of this study was to evaluate the incidence of clude: an abnormal, traumatizing way of brushing teeth, gingival recession in adult citizens of a large urban ag- plaque and calculus, anatomical conditions (abnormal glomeration of the Podlaskie Province. setting of a tooth in the arch, thin gingival phenotype, bone dehiscence, high muscle and frenulum attachment) and iatrogenic factors (periodontal procedures, orth- Material and methods odontic treatment, improper preservative and prosthetic treatment).5–14 Exposure of the root surface may result The study was carried out in the city of Białystok on from a localized inflammation caused by dental plaque randomly chosen citizens aged 35–44 years and 65–74 or a generalized form of periodontal inflammation.9,15 years. The invitation to the study was sent to 1000 indi- Zucchelli and Mounssif indicate that GR may be related viduals from each age group. 115 persons aged 35–44 in- to a healthy periodontium with lack of bone loss in the cluding 60 women and 55 men as well as 72 persons aged interdental spaces or may develop in the course of peri- 65–74 years including 51 women and 21 men reported for odontal inflammation accompanied by the loss of bone of the examination. The clinical study was carried out with the alveolar process.15 In both cases, the etiologic factor the use of a periodontal probe (PCPUNC 15, Hu-Friedy related to its development may be the lack of buccal bone Mfg., Chicago, USA) calibrated every 1 mm. The examin- of the alveolar process at the site of the recession, which ers (doctors, dentists) had undergone training in standard may have an anatomical origin or be acquired (patho- calibration. logical or physiologic).16 As regards anatomical causes of The study was performed under a program financed by a lack of the bundle bone of the alveolar process, Alldritt the Ministry of Health, the ‘Evaluation of the health con- suggested the following aspects: presence of fenestration dition of the oral cavity and its conditioning in the Polish and dehiscence of the alveolar process, abnormal setting population aged 35–44 and 65–74 years’, approved by the of a tooth in the arch, individual tooth shape and atypi- Bioethics Commission of the Medical University of Bialy- cal tooth eruption.17 Zucchelli and Mounssif15 defined the stok (R-I-002/266/2009). acquired pathological causes as: improper brushing and The physical examination comprised the evaluation of flossing, intraoral and perioral piercing, direct trauma re- gingival recession localization (buccal surface, palatal/lin- lated to malocclusion, partial dentures, presence of dental gual surface) and depth, Plaque Index (PI, by O’Leary) and plaque, subgingival cavity margin and prosthetic fillings Bleeding on Probing (BOP). PI and BOP were assessed in as well as herpes. The major acquired physiological cause 4 aspects: buccal, palatal/lingual, mesial and distal). Third is orthodontic tooth movement beyond the alveolar pro- molars were not taken into consideration in the study. Re- cess which leads to bone dehiscence and constitutes locus cession height was measured from CEJ to gingival margin. minoris resistentiae for the development of gingival reces- In the case of teeth with reconstructions, the gingival edge sion.15 Dominiak and Gedrange report that in today’s clas- of the reconstruction was taken as the point of reference. sification, there are 5 groups of etiological factors leading The obtained values were expressed in an approximation to development of GR, which are: primary morphological to the nearest millimeter. The clinical data was also evalu- conditions, functional factors, inflammation factors, age ated depending on the patient’s level of education. and sex, as well as general diseases.18 The statistical analysis was performed with use of Sta- The outcomes of epidemiology research on the inci- tistica 12.0 (StatSoft, Tulsa, USA) software. For compari- dence of gingival recessions indicate that this condition son between groups, the non parametric U Mann-Whit- affects all of society. The frequency of GR fluctuates be- ney test was used. The Spearman’s rank order correlation tween 6.3 and 100% depending on age and increases with coefficient was also determined. The results were consid- age.2,3,4,9,19–21 According to a study on a large population ered statistically significant at p < 0.05. Dent Med Probl. 2017;54(1):59–65 61

Results In the group aged 65–74, a greater advancement of the lesions was observed. Statistically significantly (p < 0.05) Gingival recessions were diagnosed in 91 patients aged higher values of mean gingival recession depth compared 35–44 and in 57 patients aged 65–74. In the younger to the younger group were observed regardless of the lo- group, recessions were detected in 20.5% of teeth (608 calization of the analyzed pathology in the oral cavity. surfaces) while in the older group in 44.8% (449 surfaces). Also, significant differences between the groups were In the group of younger women, recessions were found in found in terms of PI and BOP values. A statistically sig- 21.7% of teeth (335 surfaces), while in men in 19.2% (273 nificantly higher PI (p = 0.001) was found in the group surfaces). In the group of older women, recessions were aged 35–44 years, 40.51 ± 23.59%, compared to the older observed in 40.3% of teeth (268 surfaces), while in older population where PI was 28.47 ± 20.7%. Analogically, men in 47.8% (181 surfaces). the BOP value was higher in the group aged 35–44 years The analysis of the 2 age groups demonstrated that GR (45.03 ± 28.45%) compared to the older group (23.96 ± is more common on mandibular teeth (5.76 ± 5.24), pre- 18.95%). Detailed data is presented in Table 2. disposed to the localization on the buccal surface (3.34 ± A statistically insignificant increase in the number of 3.22). Recession depth was greater in the mandible (1.82 ± gingival recession surfaces in relation to education was 0.87) compared to the maxilla (1.73 ± 0.74). found. The lowest number of GR was noted in persons Also, apical displacement of the gingival margin was with basic education (5.55 ± 6.01) while the highest was more advanced in lower teeth in both the buccal surface in persons with higher education (9.64 ± 8.1). However, (lower teeth – 18.0 ± 0.87 vs upper teeth – 1.76 ± 0.76) the analysis of the number of recessions in the maxilla and lingual surface (lower teeth – 1.95 ± 1.05 vs upper indicated a statistically significant (p = 0.0294) increase teeth – 1.82 ± 1.01). The values indicating oral hygiene in their number in persons with higher education (3.82 suggest quite poor hygiene in the studied population. PI ± 4.04) compared to the individuals with basic educa- was 35.88 ± 23.22 while was BOP 36.92 ± 27.18. The val- tion (1.09 ± 1.70). A statistically significant increase (p = ues of the evaluated variables are presented in Table 1. 0.0474) in the number of gingival recessions was also In the group aged 65–74 years, a statistically signifi- observed in higher education persons in comparison to cantly higher number of tooth surfaces affected by gin- people with secondary education (2.64 ± 3.59). gival recession (p = 0.012) and mean gingival recession The comparison of gingival recession extent suggested extent (p = 0.000) were observed in comparison with the a reverse dependency – the individuals with basic educa- group aged 35–44 years. tion showed significantly (p = 0.0035) more extensive gin- The most common gingival recession (GR) localization gival recessions (2.27 ± 1.60 mm) compared to higher ed- was the buccal surface in both the group aged 35–44 years ucated persons (1.65 ± 0.57). The most extensive lesions (5.29 ± 5.23) and the group aged 65–74 (6.24 ± 5.40). The were observed on mandibular teeth on lingual surfaces in differences between the groups were insignificant. A sig- persons with basic education (2.58 ± 1.85 mm) while the nificant difference (p = 0.000) was observed in the case smallest gingival recessions (1.33 ± 0.58 mm), localized of lesions localized on palatal/lingual surfaces, affecting on palatal surfaces of upper teeth, were also observed in a smaller number of surfaces of the upper teeth (2.50 ± the individuals with basic education. Detailed data is pre- 3.09) compared to the lower teeth (4.53 ± 3.61). GR on sented in Table 3. the lingual surface of the lower teeth was significantly more common in the older group (3.47 ± 3.11) than in the group aged 35–44 years (1.77 ± 2.39). Discussion

The studies on gingival recession epidemiology most Table 1. Localization and advancement of gingival recession as well commonly take into consideration frequency, which is as PI and BOP in the 2 examined age groups of Bialystok citizens the percentage of persons with gingival recessions in the (mean ± standard deviation) examined population, scope (range), which corresponds

Gingival recessions Maxilla Mandible Total to the number of surfaces (alternatively the number of teeth), severity (intensity, advancement), indicating the Number of tooth surfaces 3.17 ± 3.82 5.76 ± 5.24 8.94 ± 7.88 scope of exposed root surfaces (vertical extent of reces- Buccal surface 2.31 ± 2.78 3.34 ± 3.22 5.65 ± 5.36 sion in mm), gingival recession localization in particular Lingual surface 0.86 ± 1.51 2.42 ± 2.81 3.28 ± 3.43 teeth and Miller’s classification.9,23–26,30–32 Despite fre- Depth (in mm) 1.73 ± 0.74 1.82 ± 0.87 1.82 ± 0.79 quent observation of gingival recession in adults, epide- Buccal surface 1.76 ± 0.76 1.80 ± 0.87 1.82 ± 0.82 miology outcomes suggest great differences depending on 30 Lingual surface 1.82 ± 1.01 1.95 ± 1.05 1.87 ± 0.93 the population studied. According to our own research, PI (%) 35.88 ± 23.22 gingival recession was observed on at least one surface in about 79.14% of the individuals and in 20.5% of teeth in BOP (%) 36.92 ± 27.18 the group of 35–44 year olds and in 44.8% of teeth in the 62 M. Sulewska, et al. Gingival recessions

Table 2. Localization and advancement of gingival recession as well as PI and BOP depending on age (mean ± standard deviation) Adult population Adult population Gingival recession p age 35–44 age 65–74 Number of surfaces Maxilla buccal surface 2.30 ± 2.87 2.32 ± 2.65 0.971 with gingival Maxilla palatine surface 0.74 ± 1.43 1.06 ± 1.63 0.165 recession Mandible buccal s. 2.98 ± 3.10 3.92 ± 3.34 0.053 Mandible lingual s. 1.77 ± 2.39 3.47 ± 3.11 0.000 Total buccal surface 5.29 ± 5.32 6.24 ± 5.40 0.239 Total palatine/ling. s. 2.50 ± 3.09 4.53 ± 3.61 0.000 Total maxilla 3.04 ± 3.75 3.38 ± 3.94 0.565 Total mandible 4.75 ± 4.67 7.39 ± 5.70 0.001 Total 7.79 ± 7.43 10.76 ± 8.27 0.012 Gingival recession Maxilla buccal surface 1.59 ± 0.63 2.00 ± 0.87 0.005 depth (in mm) Maxilla palatine surface 1.53 ± 0.75 2.16 ± 1.18 0.009 Mandible buccal s. 1.49 ± 0.53 2.23 ± 1.06 0.000 Mandible lingual s. 1.56 ± 0.8 2.41 ± 1.13 0.000 Total buccal surface 1.56 ± 0.57 2.22 ± 0.99 0.000 Total palatine/ling. s. 1.53 ± 0.69 2.32 ± 1.01 0.000 Total maxilla 1.55 ± 0.61 2.01 ± 0.84 0.001 Total mandible 1.49 ± 0.57 2.31 ± 1.01 0.000 Total 1.54 ± 0.55 2.28 ± 0.90 0.000 PI (%) PI 40.51 ± 23.59 28.46 ± 20.70 0.001 BOP (%) BOP 45.03 ± 28.45 23.96 ± 18.95 0.000

group aged 65–74 years. The outcomes obtained are con- results, which showed a similar incidence amounting to sistent with the epidemiological study carried out in the 79.13%. According to Khocht et al., gingival recession in USA by Gorman, who detected GR in 78–100% of middle- the USA develops in 69.6% of persons aged 30–40 years, aged individuals.33 The lesions affected 22–53% of the ex- which is consistent with the study by Zawada et al., who amined teeth. In Finland, gingival recession was observed observed this abnormality in 69.9% of Wrocław citizens in 68% of the examined individuals present in 11% of the aged 35–44 years.25,29 Previous research published in 1989 examined teeth.5 In Norway (Oslo), a lower frequency and 1999 involving similar age groups indicates a lower of lesions, 51%, in adults was observed,34 while in New frequency of lesions – 55.1% and 56.5%, respectively.5,21 Guinea this percentage was even smaller and referred to According to cohort research, this phenomenon is caused 11–40% of adults.35 by a constant increase in both the occurrence and num- Marini et al. showed a higher frequency of lesions com- ber of gingival recessions.3 Therefore, observations con- pared to our research.30 The authors examined 380 per- ducted at the same time are of the highest comparative sons over 20 years of age and detected GR on at least one value. surface of teeth in approximately 89% of persons. In the According to the observations, the majority of the epi- group aged 30–39 years, the pathology developed in 96% demiological studies indicated that the frequency, scope of the population while in the group older than 50 years, and severity of gingival recession gradually increase with 98.8% of the individuals. age.2,5,21,30,33 The influence of age on GR frequency increase According to the comparison of gingival reces- should probably be explained by the accumulation of nu- sion presence (% of persons) in persons aged 30–50 merous recession-contributing factors in time.6,21,30,33,36,37 years,2,3,5,10,21,25,30,32 the highest frequency was observed in According to our research, a higher frequency of gin- the Brazilian research. Susin et al. showed the presence of gival recession and greater lesion advancement were ob- lesions in 97.3% of patients aged 30–49 years, while Mari- served in the older age group (65–74 years). Statistically ni et al. showed in 96% of patients aged 30–39 years.10,30 significantly higher values of gingival recession depth A high (85%) frequency of lesions was also shown in compared to the younger group were obtained regardless Norwegians aged 34–45 years in the study by Löe et al.2 of the localization of the analyzed pathology in the oral In France, Sarfati et al. reported 75.6% while in Sweden, cavity. In the case of the younger age group (35–44 years), Serino et al. reported 75% of gingival recession cases in mean recession depth was 1.54 ± 0.55 mm, while in pa- this age group.32,3 The last 2 studies correspond with our tients aged 65–74 years, it was 2.28 ± 0.55 mm. These out- Dent Med Probl. 2017;54(1):59–65 63

Table 3. Localization and advancement of gingival recession depending on level of education (mean ± standard deviation) Education p Gingival recession basic – 1 secondary – 2 higher – 3 p1 vs 2 p1 vs 3 p2 vs 3 Number of Maxilla buccal surface 0.73 ± 1.35 1.68 ± 2.29 2.97 ± 3.06 0.1828 0.0183 0.0026 surfaces with Maxilla palatine surface 0.36 ± 0.67 0.96 ± 1.61 0.85 ± 1.51 0.2304 0.2953 0.6369 gingival recession Mandible buccal s. 2.55 ± 3.01 3.29 ± 3.21 3.46 ± 3.28 0.4715 0.3765 0.7243 Mandible lingual s. 1.91 ± 2.77 2.62 ± 2.93 2.35 ± 2.74 0.4529 0.6110 0.5395 Total buccal surface 3.27 ± 3.85 4.97 ± 4.77 6.43 ± 5.82 0.2623 0.0821 0.0775 Total palatine/ling. s. 2.27 ± 3.0 3.58 ± 3.49 3.20 ± 3.44 0.2427 0.3916 0.4764 Total maxilla 1.09 ± 1.70 2.64 ± 3.59 3.82 ± 4.04 0.1627 0.0294 0.0474 Total mandible 4.45 ± 4.59 5.91 ± 5.65 5.82 ± 5.02 0.4182 0.3907 0.9118 Total 5.55 ± 6.01 8.55 ± 7.79 9.64 ± 8.10 0.2234 0.1075 0.3737 Gingival recession Maxilla buccal surface 1.42 ± 0.38 1.99 ± 0.85 1.63 ± 0.67 0.2521 0.5869 0.0128 depth (in mm) Maxilla palatine surface 1.33 ± 0.58 2.09 ± 1.20 1.60 ± 0.78 0.2869 0.5647 0.0469 Mandible buccal s. 2.36 ± 1.76 2.00 ± 0.99 1.60 ± 0.59 0.4456 0.0160 0.0060 Mandible lingual s. 2.58 ± 1.85 2.18 ± 1.17 1.73 ± 0.82 0.5255 0.0721 0.0226 Total buccal surface 2.3 ± 1.72 1.99 ± 0.92 1.64 ± 0.59 0.4842 0.0346 0.0082 Total palatine/ling. s. 2.18 ± 1.58 2.1 ± 1.02 1.67 ± 0.74 0.8563 0.1518 0.0086 Total maxilla 1.35 ± 0.41 1.99 ± 0.88 1.60 ± 0.59 0.1618 0.4221 0.0052 Total mandible 2.32 ± 1.61 1.99 ± 0.99 1.64 ± 0.64 0.4777 0.0321 0.0127 Total 2.27 ± 1.60 2.02 ± 0.897 1.65 ± 0.57 0.5431 0.0319 0.0035 PI% PI 21.02 ± 16.99 33.87 ± 22.09 38.60 ± 23.72 0.0682 0.0188 0.1798 BOP% BOP 25.65 ± 23.89 40.46 ± 28.69 35.82 ± 25.98 0.1068 0.2174 0.2649

comes clearly correspond to French studies. Marini et al. giva and gingival recession development.4 According to observed mean GR depth of 2.16 ± 0.79 mm in the group other authors, the areas with gingival deficit in terms of older than 50 years of age.30 The analyzed pathology was thickness are more susceptible to GR development due detected in over 60% of the examined teeth. to a smaller amount of connective tissue in this site and The most common gingival recession localization in thus a faster inflammation progression due to the factors our study was found on the buccal tooth surface in both that induce and contribute to gingival recession develop- age groups. According to the analysis of lesion development.36,37,39 This data may also explain more frequent GR ment depending on the localization in the upper or lower development on the lingual surfaces of bottom teeth at dental arch, a more common localization was observed older age. According to our research, a significantly high- within the lower teeth. Moreover, the number of lower er frequency of gingival recession on lingual surfaces in tooth surfaces affected by recession in patients aged 65– older individuals was observed. Also, a significantly high- 74 years old was statistically higher compared to patients er presence of this pathology was observed in patients aged 35–44 years (7.39 ± 5.7 vs 4.75 ± 4.67, p = 0.001). aged 65–74 years (4.53 ± 3.61) compared to patients aged Marini et al. also observed the most common (56.33%) 35–44 years (2.5 ± 3.09). It ought to be emphasized that gingival recession localization in mandibular teeth, which the distribution of gingival recession is related to other was also previously observed by Vehkalahti.30,5 A simi- etiologic factors. The gingival recession present on lower lar (56%) frequency of GR development was observed by incisors is mostly connected with poor oral hygiene, while Gorman on upper teeth which, according to the author, on premolars it is with traumatic brushing.9,20 is caused by the presence of dehiscence and/or fenestra- Despite the discrepancies related to the main tooth af- tion of buccal bone.33 Kozłowski et al. and Zawada et al. fected by gingival recession, the literature provides unani- also noticed a more frequent GR development on upper mous indications that buccal surfaces are the most com- teeth.4,29 monly affected site.21,30,33 This correlation was also found The common development of gingival recession on in our research. Gingival recession development on buc- mandibular teeth is probably related to the characteristics cal surfaces is most of all related to an improper (trauma- of keratinized gingiva which is wider and probably thicker tizing) habit of brushing teeth while on the lingual and in the maxilla than in the mandible.38 Mendonça observed approximal surfaces it has mostly to do with poor oral a high correlation between the depth and quality of gin- hygiene.2 64 M. Sulewska, et al. Gingival recessions

Although the distribution pattern may be a vital indica- sion in students, amounting to almost 35%, ought to be tion of the major etiologic factors, the cause of the devel- considered high. Excessive hygiene in this group indicated opment such changes has not yet been clearly identified. the necessity of reeducation in pro-health behaviors. Final diagnosis and interpretation ought to be preceded In the study by Zawada et al. on Wroclaw citizens aged by correlating a number of variables, which is often diffi- 35–44 years, no impact of education on gingival recession cult and involves the exclusion of potentially predisposing development was observed.29 According to our research, factors.18 Due to the multifactorial gingival recession eti- the analysis of GR number in the maxilla showed a statis- ology, it is difficult to establish which combination of re- tically significant increase in persons with higher educa- cession-contributing factors reflects the displacement of tion (3.82 ± 4.04) compared to the individuals with basic the gingival margin below the cemento-enamel junction education (1.09 ± 1.70). A statistically significant increase and the progression (or not) of the vertical extent of gin- (p = 0.0474) of GR number was also observed in persons gival recession. Most commonly, an interaction of predis- with higher education compared to patients with second- posing (anatomical) and precipitating (acquired) factors ary education (2.64 ± 3.59). In the comparison of gingi- occurs leading to gingival recession as a final result.18,29 val recession extent, a reverse dependency was observed. In order to show the relevance of the interaction of the Persons with basic education showed significantly (p = numerous factors on recession development, multiple 0.0035) more extensive gingival recession (2.27 ± 1.60 regression models were constructed and independent mm) compared to persons with higher education (1.65 variables were introduced. Khocht et al. explained 19% ± 0.57 mm). The greatest changes were observed on the of gingival recession number changeability on a multiple lingual surfaces of mandibular teeth in persons with basic regression model taking into consideration only age and education – 2.58 ± 1.85 mm. The smallest (1.33 ± 0.58 gender.25 The changeability of 31% was explained by age, mm) GR, localized on the palatine surfaces of upper teeth, brushing frequency, gender and the time of using a hard was also observed in persons with basic education. toothbrush. Also, Checchi et al. used multiple regression in a study on dentistry students and demonstrated that education level in terms of pro-health behaviors may be Conclusions a crucial factor of developing gingival recession.6 Serino et al. reported that 58% of gingival recession Gingival recession is a common abnormality in the number changeability on buccal surfaces may be ex- population of adult citizens of large urban agglomerations plained by a loss of clinical attachment level on interprox- in the Podlaskie Province. Due to the complex etiology of imal surfaces and the increased severity of inflammation gingival recession, epidemiology studies evaluating reces- on buccal surfaces as a result of improper hygiene in the sion incidence in the population are difficult to carry out entire oral cavity.3 Dominiak et al. calculated that 29% of and interpret. gingival recession number changeability depends on the influence of 10 variables.27 Matas et al. showed that an in- References crease in GR depth within 10 years was 21% dependent 1. Löe H, Anerud A, Boysen H, Smith M. The natural history of peri- on 4 variables including the presence of dental plaque.26 odontal disease in man: The rate of periodontal destruction before The model of a multiple regression proposed by Waw- 40 years of age. J Periodontol. 1978;49:607–620. 2. Löe H, Anerud A, Boysen H. The natural history of periodontal dis- rzyn-Sobczak explains 41% of gingival recession number ease in man: Prevalence, severity, and extent of gingival recession. changeability while a study by Kozlowski et al. explained J Periodontol. 1992;63:489–495. 18% of this changeability.28,4 3. Serino G, Wennström JL, Lindhe J, Eneroth L. The prevalence and distribution of gingival recession in subjects with a high standard According to many authors’ observations, there is of oral hygiene. J Clin Periodontol. 1994;21:57–63. a clear correlation in the relationship between improper 4. Kozłowski Z, Konopka T, Karolewska E, Mendak M, Szulc M. Occur- or excessive oral hygiene and gingival recession develop- rence of gingival recessions in students from the first and the last 3,4,6,25–28 year of dentistry. Dent Med Probl. 2003;40:391–397 [in Polish]. ment. Although they are significant factors, they 5. Vehkalahti M. Occurrence of gingival recession in adults. J Peri- constitute only a part of the etiopathologic factors. The said odontol. 1989;60:599–603. relationship is presented by our research. A significantly 6. Checchi L, Daprile G, Gatto MRA, Pelliccioni GA. Gingival recession and toothbrushing in an Italian School of Dentistry: A pilot study. higher PI value was observed in patients aged 35–44 years J Clin Periodontol. 1999;26:276–280. (40.51 ± 23.59%) compared to older patients who showed 7. Löst C. Depth of alveolar bone dehiscences in relation to gingival a PI value of 28.47 ± 20.7%. Despite this frequency of de- recessions. J Clin Periodontol. 1984;11:583–589. veloping dental plaque in the younger group of patients, 8. Kassab MM, Cohen RE. The etiology and prevalence of gingival recession. J Am Dent Assoc. 2003;134:220–225. the presence and advancement of lesions displayed lower 9. Van Palenstein Helderman WH, Lembariti BS, Van Der Weijden GA, values compared to the population aged 65–74 years. The Van’t Hof MA. Gingival recession and its association with calculus study by Kozłowski et al. demonstrated that a very good in subjects deprived of prophylactic dental care. J Clin Periodontol. 1998;25:106 –111. oral hygiene in first- and fifth-year students of the Medical 10. Susin C, Haas AN, Oppermann RV, Haugejorden O, Albandar JM. Academy in Wroclaw (PI – 21%) failed to prevent gingival Gingival recession: Epidemiology and risk indicators in a represen- recession development.4 The frequency of gingival reces- tative urban Brazilian population. J Periodontol 2004;75:1377–1386. Dent Med Probl. 2017;54(1):59–65 65

11. Lindhe J, Nyman S. Alterations of the position of the marginal soft 27. Dominiak M, Konopka T, Szajowski K. Gingival recession with tissue following periodontal surgery. J Clin Periodontol. 1980;7:525– regard to the potential etiopatological factors. Stomatol Wspoł. 530. 2002;9:22–28 [in Polish]. 12. Lang NP. Periodontal considerations in prosthetic dentistry. Peri- 28. Wawrzyn-Sobczak K. Gingival recession – etiology, incidence and odontol 2000. 1995;9:118–131. treatment. Doctoral thesis, Białystok 2003 [in Polish]. 13. Matthews DC, Tabesh M. Detection of localized tooth-related fac- 29. Zawada Ł, Konopka T, Chrzęszczyk D. Prevalence of the gingi- tors that predispose to periodontal infections. Periodontol 2000. val recessions in adult residents of Wrocław. Dent Med Probl. 2004;34:136–150. 2012;49:383–390 [in Polish]. 14. Smith RG. Gingival recession. Reappraisal of an enigmatic condition 30. Marini MG, Greghi SLA, Passanezi E, Sant’Ana ACP. Gingival reces- and a new index for monitoring. J Clin Periodontol. 1997;24:201–205. sion: Prevalence, extension and severity in adults. J Appl Oral Sci. 15. Zucchelli G, Mounsif I. Periodontal plastic surgery. Periodontol 2004;12:250–255. 2000. 2015;68:333–368. 31. Geiser EJ, Kleisner J, Marinello CP. Gingivale Rezession. Eine Über- 16. Geiger A. Mucogingival problems and the movement of mandibu- sicht über Prävalenz, Ätiologie und Klassifikation. Schweiz Monatss- lar incisors: A clinical review. Am J Orthod. 1980;78:511–527. chr Zahnmed. 1993;103:1278–1287. 17. Alldritt W. Abnormal gingival form. Proc R Soc Med. 1968;61:137–142. 32. Sarfati A, Bourgeois D, Katsahian S, Mora F, Bouchard P. Risk assess- 18. Dominiak M, Gedrange T. New perspectives in the diagnostic of ment for buccal gingival recession defects in an adult population. gingival recession. Adv Clin Exp Med 2014;23:857–863. J Periodontol. 2010;81:1419–1425. 19. Källestal C, Uhlin S. Buccal attachment loss in Swedish adolescents. 33. Gorman WJ. Prevalence and etiology of gingival recession. J Peri- J Clin Periodontol. 1992;19:485–491. odontol. 1967;38:316–322. 20. Joshipura K, Kent R, Depaola P. Gingival recession: Intra−oral distri- 34. Sangnes G, Gjermo P. Prevalence of oral soft and hard tissue lesions bution and associated factors. J Periodontol. 1994;65:864–871. related to mechanical toothcleansing procedures. Community Dent 21. Albandar JM, Kingman A. Gingival recession, gingival bleeding Oral Epidemiol. 1976;4:77–83. and dental calculus in adults 30 years of age and older in the Unit- 35. Schamschula RG, Keyes PH, Hornabrook RW. Root surface car- ed States, 1988–1994 – National Institute of Dental and Craniofacial ies in Lufa, New Guinea. I. Clinical observations. J Am Dent Assoc. Research, National Institutes of Health. J Periodontol 1999;70:30–43. 1972;85:603–608. 22. Albander JM. Periodontal diseases in North America. Periodontolo- 36. Baker DL, Seymour GJ. The possible pathogenesis of gingival reces- gy 2000. 2002;29:31–69. sion. A histological study of induced recession in the rat. J Clin Peri- 23. Muller HP, Stadermann S, Heinecke A. Gingival recession in smok- odontol. 1976;3:208–219. ers and non-smokers with minimal periodontal disease. J Clin Peri- 37. Ericsson I, Lindhe J. Recession in sites with inadequate width of the odontol. 2002;29:129–136. keratinized gingiva. An experimental study in the dog. J Clin Peri- 24. Miller PD. A classification of marginal tissue recession. Int J Peri- odontol. 1984;11:95–103. odont. 1985;5:9–13. 38. Bednarz W, Zielińska A. Ultrasonic biometer and its usage in an 25. Khocht A, Simon G, Person P, Denepitiya JL. Gingival recession assessment of periodontal soft tissue thickness and comparison in relation to history of hard toothbrush use. J Periodontol. 1993; of its measurement accuracy with a bone sounding method. Dent 64:900–905. Med Probl. 2011;48:481–489. 26. Matas F, Sentis J, Mendieta C. Ten-year longitudinal study of gingi- 39. Kennedy JE, Bird WC, Palcanis KG, Dorfman HS. A longitudinal eval- val recession in dentists. J Clin Periodontol. 2011;38:1091–1098. uation of varying widths of attached gingiva. J Clin Periodontol. 1985;12:667–675.

Original papers Oral hygiene in children with epilepsy: Effect of interleukin-1β and VEGF levels in gingival crevicular fluid Higiena jamy ustnej dzieci chorych na epilepsję a stężenie interleukiny 1β i czynnika wzrostu naczyniowo-śródbłonkowego w płynie dziąsłowym

Gülsüm Duruk1, A–F, Hulya Aksoy2, A–D, Taskın Gurbuz3, A–C, Esra Laloglu4, A, B, Huseyin Tan5, A, B

1 Inonu University, Faculty of Dentistry, Department of Pediatric Dentistry, Malatya, Turkey 2 Private Medical Practice, Erzurum, Turkey 3 Ataturk University, Faculty of Dentistry, Department of Pediatric Dentistry, Erzurum, Turkey 4 Ataturk University, Faculty of Medicine, Department of Biochemistry, Erzurum, Turkey 5 Ataturk University, Faculty of Medicine, Department of Pediatric Neurology, Erzurum, Turkey

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):67–71

Address for correspondence Abstract Gülsüm Duruk E-mail: [email protected] Background. The biochemical parameters in gingival crevicular fluid (GCF) are affected by some systemic diseases and poor oral hygiene. Conflict of interest none declared Objectives. The aim of this study was to evaluate the total amounts of Interleukin-1β (IL-1β) and vascular endothelial growth factor (VEGF) in GCF in children with epilepsy. Funding sources The study was funded by the Scientific Research Foundation Material and methods. Eighty children with epilepsy in a seizure-free period (the test group) and 80 of Ataturk University (grant 2010/140). healthy children (the control group) were evaluated. The children with epilepsy were taking valproic acid This study had ethical approval. The acceptance number is B.30.2.ATA.0.01.00/118. (VPA), carbamazepine, phenobarbital, and the combinations of these drugs. Gingival index (GI), plaque index (PI), probing depth (PD) and clinical attachment level (CAL) were measured. GCF was collected and its Acknowledgments volume was measured. The total amounts of IL-1β and VEGF in the GCF were analyzed in the Biochemistry The authors would like to thank Prof. Zekeriya Aktürk for his Laboratory at Ataturk University. statistical assistance. Results. The biochemical (IL-1β and VEGF) and clinical parameters (GI, PI, PD and GCF volume) were sig- Received on August 29, 2016 nificantly higher in children with epilepsy compared to healthy children (p < 0.0001). When the epilepsy Revised on September 27, 2016 patients were divided into groups according to the drug used in this study, there were no significant differ- Accepted on September 29, 2016 ences in the GCF levels of IL-1β and VEGF among the drug groups. Also, a significant gingival enlargement in the patient population was not recorded. Conclusions. According to these results, it may be suggested that patients need optimal oral care in epi- DOI lepsy. 10.17219/dmp/65450 Key words: children, epilepsy, cytokine, gingival crevicular fluid, oral health Copyright Słowa kluczowe: dzieci, epilepsja, cytokiny, płyn dziąsłowy, higiena jamy ustnej © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 68 G. Duruk, et al. GCF IL-1β and VEGF in epilepsy

The World Health Organization estimates that 0.8% of ered as a sign of severe periodontitis.13,17,18 VEGF is de- the world’s population are affected by epilepsy, which is tectable in periodontal tissues within endothelial cells, a brain disorder.1 In 35% of the cases, epilepsy is due to an plasma cells and macrophages, in junctional, sulcular and identifiable central nervous system (CNS) injury, whereas gingival epithelium, and in GCF.18 Moreover, VEGF ex- in the rest of the cases, it is a result of either genetic or pression may be induced by IL-6, IL-1 and PGE2. VEGF unknown causes.2 also appears to be regulated by the oxygen concentration For preventing seizure, different drugs are used in the that cells are exposed to, with hypoxia inducing its ex- treatment of epilepsy. But there are some side effects of pression.19 these medications. For example, in 30–50% of the cases, In this study, we aimed to investigate the total phenytoin develops a significant gingival overgrowth. Al- amounts of IL-1β and VEGF in GCF in epileptic pa- though the reason of the gingival overgrowth is not fully tients in a seizure-free period and focused on the re- understood, some studies have shown that inflammatory lationship between oral hygiene and these biochemical cytokines and growth factors may play an important role parameters. in the pathogenesis of gingival changes.3,4 IL-1β, 17-kDa glycoprotein is a potent proinflamma- tory cytokine. It is produced predominantly not only by Material and methods monocytes/macrophages, but also by fibroblasts and bone cells.5 Its production may be induced by microorganisms, Patient selection microbial products, inflammatory agents and antigens.6 Several clinical studies have addressed the change of This study was performed in the Department of Pe- IL-1β levels in the blood and cerebrospinal fluid (CSF) diatric Neurology, Faculty of Medicine and Department of patients with focal epilepsy.7,8 It has been found that of Pedodontics, Faculty of Dentistry of Ataturk Univer- IL-1β plays a role in the development of a neuronal cell sity in 2012. The samples were analyzed in the Biochem- death after traumatic, ischemic, excitotoxic and seizure- istry Department. A total of 160 subjects, 80 pediatric induced brain injuries.8,9 patients (36 girls, 44 boys) with epilepsy, the test group, Gingival crevicular fluid (GCF) is an exudate that is and 80 systemically healthy children (46 girls, 34 boys), originated from gingival crevices or periodontal pock- the control group, aged 4–11, participated in this study. ets around teeth with inflamed gingiva. GCF contains The study was approved by the local ethics committee of a variety of materials, including leukocytes (mainly neu- the Medical School of Ataturk University and performed trophils), antibodies, complement proteins, various en- in accordance with good clinical practice guidelines. In- zymes, and cytokines.10–12 Therefore, GCF component or formed consent was obtained from the parents of pa- constituent measurements are useful to show the altera- tients. Children were excluded from the study if they had tions in gingival tissues. Additionally, in the oral cavity, any systemic diseases, periodontal diseases, dental caries poor oral hygiene and gingival and periodontal diseases or filling in the maxillary anterior teeth, and had taken without gingival enlargement can also modify the con- antibiotics or anti-inflammatory drugs in the previous tents of GCF. In some studies, poor oral hygiene, gingivi- one month. The children in the test group had no other tis, periodontitis or a gingival injury increases IL-1β and systemic diseases except epilepsy and they had had no sei- VEGF values in GCF.13–15 zures in the past month. IL-1β has an important role in regulating and increasing the inflammatory response in periodontal diseases. Clinical measurements IL-1β levels in periodontal tissues and GCF have been closely associated with periodontal disease severity and it Periodontal examinations were carried out and record- has been found that they significantly increase in diseased ed by the same investigator. None of the study patients sites, compared to healthy sites.15 had gingival overgrowth. Four points (mesio-buccal, A vascular endothelial growth factor (VEGF), 45-kDa mesio-oral, disto-buccal and disto-oral) of per maxillary homodimeric glycoprotein, is an angiogenesis and vas- anterior primary teeth were selected for clinical measure- cular permeability factor that increases microvascular ments. If there were no maxillary anterior primary teeth, permeability, stimulates endothelial cell (EC) prolifera- permanent maxillary anterior teeth were selected. The tion, and induces proteolytic enzyme expression and the selected teeth were caries-free and unfilled. The gingival migration of ECs, monocytes and osteoblasts, all of which conditions of the patients were evaluated using the Sil- are essential for angiogenesis.16 ness-Loe plaque index (PI), Loe gingival index (GI), clini- An increase in VEGF in GCF affects the periodontal cal attachment loss (CAL) and probing pocket depth (PD) vasculature profoundly during periodontal disease pro- to the nearest millimeter with a Williams probe (Aes- gression.13,14 The increased concentration of VEGF in culap, Inc., Center Valley, USA).20,21 The obtained® scores periodontitis may be one of the reasons for the increased were calculated by dividing the total score by the total vascularization and permeability, and it may be consid- number of scored surfaces. Dent Med Probl. 2017;54(1):67–71 69

GCF collection The Pearson correlation test was used to verify the correlations between the biochemical parameters, while The selected tooth sites were mesiobuccal sites of max- Spearman’s Rank correlation test was used between the illary central or lateral in primary or permanent dentition clinical parameters. Spearman’s Rank correlation test was for collecting GCF. A total of 160 GCF samples were ob- used to evaluate the relationship between the clinical and tained, 80 from epilepsy patients and 80 from a healthy biochemical parameters. group. The upper anterior teeth were included in the The qualitative non-parametric variable of CAL was study to improve access and to reduce the risk of salivary not analyzed because the CAL of both healthy children contamination during these processes. To avoid the blood and children with epilepsy was ≤ 2 mm. contamination and the possible stimulation of GCF flow during clinical measurements, samples were collected before any other clinical recordings except PI. Prior to sam- Results pling, each selected site was carefully isolated using cot- ton rolls. A Periopaper strip (Oraflow, Plainview, USA) In the epilepsy group, the clinical and biochemical pa- was placed in the pocket® until a mild resistance was felt rameters were significantly higher than in the control and then left in place for 30 s. In the case of visible con- group (p < 0.0001 for all) (Table 1). tamination with blood, the strips were removed. To elimi- Looking at the distribution of the drugs used in the epi- nate the risk of vaporization, the paper strips with GCF lepsy patients, in 46, 12, 10 and 12 of the 80 cases, they were immediately carried to a previously calibrated elec- were taking valproic acid (VPA), carbamazepine, pheno- tronic gingival fluid measuring device (Periotron 8000; barbital, and the combinations of these drugs, respective- Oraflow, Plainview, USA) for volume calculation.® After ly. These patients had been using their respective drugs the volume calculation, Periotron scores were converted for at least 6 months. When the patients were divided from mL to microliters (μL) via a computer conversion into groups according to the drug used in this study, there program. The samples were put into Eppendorf tubes in were not any significant differences in the clinical and bio- 300 μL phosphate buffered saline (PBS), containing 100 μL chemical parameters among the drug groups (p > 0.05). of 2% bovine serum albumin in PBS and immediately fro- There was a statistically significant positive corre- zen at –80°C until the day of the laboratory analysis. lation between total IL-1β and VEGF in both groups (p < 0.0001). Correlations between IL-1β and GI (r = 0.292, IL-1β and VEGF assay p = 0.009), IL-1β and PI (r = 0.359, p = 0.001), VEGF and GI (r = 0.419, p = 0.0001), VEGF and PI (r = 0.347, p = 0.002), The level of IL-1β (eBioscience Platinum ELISA, NY, GI and PI (r = 0.466, p = 0.0001) and PD and GCF volume USA) and VEGF (RayBio , NY, USA)® in GCF was mea- (r = 0.662, p = 0.0001) were found in the healthy children. sured by ELISA and the analysis® was performed according Regarding the children with epilepsy, correlations were to the manufacturer’s instructions using human recombi- found between IL-1β and GI (r = 0.651, p = 0.0001), IL-1β nant standards in the Biochemistry Laboratory of Ataturk and PI (r = 0.481, p = 0.0001), VEGF and GI (r = 0.635, University. The results were reported in pg/mL per sample. p = 0.0001), VEGF and PI (r = 0.534, p = 0.0001), GI and The sensitivity was 0.3 pg/mL for IL-1β ELISA while it was PI (r = 0.676, p = 0.0001) and PD and GCF volume (r = 10 pg/mL for VEGF ELISA. The samples with IL-1β levels = 0.319, p = 0.004). below the limits of the assay’s detectability were scored 0. The IL-1β results were multiplied by the dilution factor (×2). The results were converted to µL by being divided by Discussion 1000. GCF volumes were added to the dilution factor and multiplied by IL-1β and VEGF levels. The present study has shown that in epilepsy patients, the total amounts of IL-1β and VEGF in GCF were signifi- Statistical analysis cantly higher than in healthy children. To our knowledge, this is the first report measuring GCF levels of IL-1β and Data analysis was performed using the statistical pack- VEGF in epilepsy patients. age SPSS 16 (2008, SPSS Inc., Chicago, USA). The results In our study, all patients were taking anti-epileptic drugs were expressed as mean ± standard deviation. The data in a seizure-free period. Researchers have found that IL-1β was firstly analyzed for normal distribution with a Kol- and VEGF production increases in the blood and brain mogorov-Smirnov test. The biochemical parameters be- during an epileptic seizure.9,22 Vezzani et al. reported that tween the groups were compared with Student’s t-test, cytokine levels approximate to the normal values in brain while the clinical parameters between the groups were tissue in the next 3–7 days after the seizure.7 In this study, compared with a non-parametric Mann-Whitney U test. an increase in biochemical parameters in GCF couldn’t be The non-parametric Kruskall-Wallis test was used to attributed to the epileptic seizures because all the epilepsy evaluate the differences among the drug groups. cases were seizure-free. 70 G. Duruk, et al. GCF IL-1β and VEGF in epilepsy

Table 1. The mean ± SD of total amounts of IL-1β and VEGF and clinical parameters of both groups

Parameters Healthy Epilepsy p values* Statistically used tests Biochemical parameters total IL-1β (pg) 4.02 ± 0.89 17.15 ± 6.90 0.0001 Student’s t-test total VEGF (pg) 48.46 ± 10.92 124.06 ± 35.57 0.0001 Clinical parameters GI 0.26 ± 0.13 0.81 ± 0.14 0.0001 Mann-Whitney U test PI 0.35 ± 0.20 0.75 ± 0.14 0.0001 PD 0.82 ± 0.24 1.78 ± 0.17 0.0001 GCF volume (µL) 0.06 ± 0.02 0.17 ± 0.08 0.0001

* The p values show the comparison of the values in the same row.

Moreover, increased total amounts of IL-1β and VEGF and outer membrane protein from periodontopathic bac- in GCF may be due to some other causes in epilepsy pa- teria.16 In our study, it was found that total amounts of tients. Gingival enlargement may be one of the factors that IL-1β and VEGF in GCF had a positive correlation with increases IL-1β and VEGF to damage the integrity of the plaque-induced gingivitis in both groups (PI, GI). This re- gingiva. Some anti-epileptic drugs (especially phenytoin) sult may indicate that oral hygiene may be one of the fac- have side effects such as gingival enlargement. This situ- tors increasing IL-1β and VEGF in GCF that is unrelated ation was found to be rare in patients taking other anti- to epilepsy. epileptic drugs such as phenobarbital, valproic acid, car- Many systemic diseases may adversely affect oral health bamazepine, and levetiracetam. In our study, none of the due to the changes in metabolism and drug use. In some patients with epilepsy was taking phenytoin. Besides, we studies, which support our study, it was shown that epi- couldn’t find significant gingival enlargement in the pa- lepsy cases have poor oral hygiene and it has been found tient population. The authors reported that valproic acid that GI and PI scores are higher in epileptics than in prevented an inflammation, and carbamazepine could healthy children.27,28 cause an inflammation and hepatic injury as a result of Guneri et al. investigated the VEGF concentration in this.23,24 We couldn’t find any information about possible GFC in patients with periodontal diseases.17 Some of anti-inflammatory effects of phenobarbital. But, in our these patients (group I) had diabetic diseases, while the study, when patients were classified according to the use others (group II) were healthy without any systemic dis- of the drug, no differences were found in IL-1β and VEGF eases. The differences of VEGF levels were found statisti- levels of GCF among the drug groups. cally insignificant between the periodontally healthy sites We thought that the cause of the increased total of these two groups and the negative control group. But amounts of IL-1β and VEGF in GCF may be from differ- they found statistically significant differences between ent factors rather than seizure, drugs or gingival enlarge- periodontally healthy and unhealthy sites of these two ment. IL-1β is one of the most important inflammatory groups, which is similar to Booth et al.18 Guneri’s study cytokines in the oral cavity and plays a major role in gin- indicated that the oral situation is more important than givitis and periodontitis,15 while VEGF is one of the pri- systemic disease for GCF mediators, because the VEGF mary mediators of neovascularization in chronic inflam- levels in GCF were not different between periodontally mation, including periodontal disease and wound repair,25 healthy sites of diabetic patients and the control group.17 and plays a major role in periodontal diseases to increase This result indicates that oral hygiene may be one of the vascularization and permeability and help the passage of factors increasing VEGF that is unrelated to epilepsy. inflammatory cells, and it may be considered as a sign of Sandalli and Wade recorded a positive correlation be- the severity of periodontitis.8,18,19 tween PD and GCF volume in the gingiva of 3–5 year old There are various bacterial species embedded in a ma- children.29 The correlation was more statistically signifi- trix of bacterial products and host-derived factors in den- cant in a gingivitis region than in healthy gingiva. Yucel et tal biofilm or dental plaque. This biofilm can stimulate al. reported higher GCF volumes in a deep pocket com- an inflammation in gingival tissue. The increase of GCF pared to a shallow pocket.30 In our study, in addition, we volume is an indication of inflammation and subsequent found a positive correlation between PD and GCF vol- clinical signs of gingivitis.26 Studies show that plaque in- ume in both groups. creases crevicular IL-1β and VEGF.14,15 Pathogenic bacte- In this study, we found that the children with epilep- ria in subgingival plaque cause a subepithelial infiltration sy were more likely to have a periodontal disease than by inflammatory cells, which produce and release IL-1β, healthy children. We could not give any exact reasons that thus an IL-1β concentration in GCF increases in peri- this situation may be an immune system problem caused odontal tissue with gingivitis or periodontitis.15 VEGF by epilepsy or neglected oral hygiene. In our study, there is increased by gingival fibroblasts in response to vesicle was a limitation that blood specimens were not taken Dent Med Probl. 2017;54(1):67–71 71

from the patients. Thus, we could not compare these bio- 10. Lamster IB, Grbic JT. Diagnosis of periodontal disease based on analysis of the host response. Periodontol. 2000;1995:7, 83–99. chemical parameters in serum and GCF. Further studies 11. Ebersole JL, Singer RE, Steffensen B, Filloon T, Kornman KS. Inflam- are needed to clarify the effect of epileptic drugs on the matory mediators and immunoglobulins in GCF from healthy, gin- immune system. givitis and periodontitis sites. J Periodont Res. 1993;28:543–546. 12. Sakai A, Ohshima M, Sugano N, Otsuka K, Ito K. Profiling the cyto- If this situation is not a problem originating from the kines in gingival crevicular fluid using a cytokine antibody array. immune system, further research should be focused on J Periodontol. 2006;77:856–864. why these children care less about oral hygiene than 13. Unlu F, Guneri PG, Hekimgil M, Yesilbek B, Boyacioglu H. Expres- sion of vascular endothelial growth factor in human periodontal healthy children. They spend most of their lives in a hos- tissues: Comparison of healthy and diabetic patients. J Periodontol. pital and constantly have to take medication. For all these 2003;74:181–187. reasons, oral care may be difficult and tedious for them. 14. Prapulla DV, Sujatha PB, Pradeep AR. Gingival crevicular fluid VEGF levels in periodontal health and disease. J Periodontol. 2007;78:1783–1787. 15. Ishihara Y, Nishihara T, Kuroyanagi T, et al. Gingival crevicular inter- Conclusions leukin-1 and interleukin-1 receptor antagonist levels in periodontally healthy and diseased sites. J Periodont Res. 1997;32:524–529. 16. Suthin K, Matsushita K, Machigashira M, et al. Enhanced expression Our study revealed that IL-1β, an inflammation indica- of vascular endothelial growth factor by periodontal pathogens in tor, and VEGF, an angiogenesis mediator, increase in the gingival fibroblasts. J Periodont Res. 2003;38:90–96. GCF of epilepsy patients and we can say that epilepsy pa- 17. Guneri P, Unlu F, Yesilbek B, et al. Vascular endothelial growth factor in gingival tissues and crevicular fluids of diabetic and healthy tients may be at risk of periodontal disease in their future periodontal patients. J Periodontol. 2004;75:91–97. lives. 18. Booth V, Young S, Cruchley A, Taichman NS, Paleolog E. Vascular Further longitudinal clinical studies are required in or- endothelial growth factor in human periodontal disease. J Peri- odont Res. 1998;33:491–499. der to study the oral health of children with epilepsy and 19. Ben-Av P, Crofford LJ, Wilder RL, Hla T. Induction of vascular endo- the probable diagnostic value of combinations of inflam- thelial growth factor expression in synovial fibroblasts by prosta- matory mediators. glandin E and interleukin-1: A potential mechanism for inflammatory angiogenesis. FEBS Lett. 1995;372:83–87. 20. Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation References between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–135. 1. World Health Organisation (WHO) Atlas. Epilepsy care in the world. 21. Loe H. The Gingival Index, the Plaque Index and the Retention WHO, Geneva, 2005. Index Systems. J Periodontol. 1967, 38, Suppl, 610–616. 2. Pitkanen A, Sutula TP. Is epilepsy a progressive disorder? Prospects 22. Rigau V, Morin M, Rousset MC, et al. Angiogenesis is associated for new therapeutic approaches in temporal-lobe epilepsy. Lancet with blood-brain barrier permeability in temporal lobe epilepsy. Neurol. 2002;1:173–181. Brain 2007;130:1942–1956. 3. Modeer T, Domeij H, Anduren I, Mustafa M, Brunius G. Effect of 23. Kim JE, Choi HC, Song HK, et al. Levetiracetam inhibits interleu- phenytoin on the production of interleukin-6 and interleukin-8 in kin-1 beta inflammatory responses in the hippocampus and piri- human gingival fibroblasts. J Oral Pathol Med. 2000;29:491–499. form cortex of epileptic rats. Neurosci Lett. 2010;471:94–99. 4. Vahabi S, Salman BN, Rezazadeh F, Namdari M. Effects of cyclo- 24. Higuchi S, Yano A, Takai S, et al. Metabolic activation and inflamma- sporine and phenytoin on biomarker expressions in gingival fibro- tion reactions involved in carbamazepine-induced liver injury. Toxi- blasts of children and adults: An in vitro study. J Basic Clin Physiol colog Sci. 2012;130:4–16. Pharmacol. 2014;25:167–173. 25. Polverini PJ. The pathophysiology of angiogenesis. Crit Rev Oral Biol 5. Horowitz MC. Cytokines and estrogen in bone: Anti-osteoporotics Med. 1995;6:230–247. effects. Sci. 1993;260:626–627. 26. Loe H, Holm-Pedersen P. Absence and presence of fluid from nor- 6. Dagmar SP, Meley J. Interleukin-1β concentration of gingival crevic- mal and inflamed gingivae. Periodont. 1965;149:171–177. ular fluid. J Periodontol. 1994;65:423–428. 27. Gurbuz T, Tan H. Oral health status in epileptic children. Pediatr 7. Vezzani A, Moneta D, Richichi C, et al. Functional role of inflam- Internat. 2010;52:279–283. matory cytokines and antiinflammatory molecules in seizures and 28. Tan H, Gurbuz T, Dagsuyu IM. Gingival enlargement in children epileptogenesis. Epilepsia 2002;43 Suppl. 5:30–35. treated with antiepileptics. J Child Neurol. 2004;19:958–963. 8. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. 29. Sandalli P, Wade AB. Crevicular fluid flow in young children. J Peri- Nat Rev Neurosci. 2001;2:734–744. odontol. 1971, 42, 713–716. 9. Murashima YL, Suzuki J, Yoshii M. Role of cytokines during epilepto- 30. Yucel OO, Berker E, Gariboglu S, Otlu H. Interleukin-11, interleukin- genesis and in the transition from the interictal to the ictal state in 1beta, interleukin-12 and the pathogenesis of inflammatory peri- the epileptic mutant EL mouse. Gene Regul Syst Bio. 2008;2:267–274. odontal diseases. J Clin Periodontol. 2008, 35, 365–370.

Prace oryginalne Wpływ lęku stomatologicznego na stan uzębienia dorosłej populacji regionu łódzkiego The effect of dental anxiety on the dental status of adult patients in the Lodz region

Katarzyna Sopińska1, A–D, Natalia Olszewska2, B–D, Elżbieta Bołtacz-Rzepkowska1, A, C–F

1 Zakład Stomatologii Zachowawczej, Uniwersytet Medyczny w Łodzi, Łódź, Polska 2 Koło Naukowe przy Zakładzie Stomatologii Zachowawczej, Uniwersytet Medyczny w Łodzi, Łódź, Polska

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;26(1):73–78

Adres do korespondencji Streszczenie Katarzyna Sopińska e-mail: [email protected] Wprowadzenie. Według danych z piśmiennictwa lęk stomatologiczny, który w różnych populacjach dotyczy od 16 do 24% dorosłych, może mieć wpływ na zachowania prozdrowotne związane z leczeniem den- Zewnętrzne źródła finansowania Nie podano tystycznym oraz na stan uzębienia. Cel pracy. Ocena wpływu poziomu lęku przed leczeniem stomatologicznym na stan uzębienia dorosłych Konflikt interesów pacjentów z regionu łódzkiego. Nie występuje Materiał i metody. Do badania zakwalifikowano 140 losowo wybranych dorosłych zgłaszających się do Praca wpłynęła do Redakcji: 16 sierpnia 2016 r. Po recenzji: 20 września 2016 r. Centralnego Szpitala Klinicznego UM w Łodzi od stycznia do maja 2015 r. Badanie składało się z części Zaakceptowano do druku: 1 października 2016 r. ankietowej i radiologicznej. Kwestionariusz zawierał pytania dotyczące danych socjodemograficznych oraz oceny lęku przed leczeniem dentystycznym za pomocą skali MDAS (Modified Dental Anxiety Scale). Radio- logiczna część badania polegała na analizie zdjęć pantomograficznych. Oceniano liczbę zębów usuniętych, z próchnicą, z wypełnieniami koronowymi, leczonych endodontycznie i ze zmianami zapalnymi w tkankach okołowierzchołkowych. Wyniki. Wiek badanych zawierał się w przedziale 18–81 lat (średnia 44,5 ± 17,8). U większości ankietowanych stwierdzono mały (47%) lub umiarkowany (24%) poziom lęku. Wysoki poziom lęku odnotowa- no u 29% badanych, w tym dentofobię u 9%. W ocenianej grupie średni poziom lęku według skali MDAS wynosił 11,0 ± 5,3. W grupie osób z wysokim poziomem lęku wykazano istotnie większy odsetek zę- bów z próchnicą (21,9 vs 10,4%; p = 0,003) i ze zmianami zapalnymi w tkankach okołowierzchołkowych (13,7 vs 8,6%; p = 0,035) niż w grupie osób z niskim poziomem lęku. W ocenianych grupach nie zaobserwowano istotnych różnic w procentowym udziale zębów z wypełnieniami (27,4 vs 34,4%; p = 0,114), usuniętych (25 vs 17,2%; p = 0,114) oraz leczonych endodontycznie (10,2 vs 10,8%; p = 0,786). Wnioski. Wysoki poziom lęku przed zabiegami stomatologicznymi jest skorelowany z gorszym stanem DOI 10.17219/acem/65519 uzębienia. Lęk powinien być uwzględniany jako jeden z możliwych czynników ryzyka występowania próchnicy i jej powikłań. Copyright Słowa kluczowe: lęk przed leczeniem stomatologicznym, zmodyfikowana skala oceny lęku dentystycz- © 2017 by Wroclaw Medical University and Polish Dental Society nego (MDAS), stan jamy ustnej, próchnica zębów, zapalenie przyzębia okołowierzchołkowego This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 74 K. Sopińska, N. Olszewska, E. Bołtacz-Rzepkowska. Lęk stomatologiczny a stan uzębienia osób dorosłych

Abstract Background. According to the literature, dental anxiety, which affects from 16 to 24% of patients in different populations, can influence dental health behavior and dental status. Objectives. The aim of the study was to assess the influence of dental anxiety on the dental status of adult patients in the Lodz region. Material and methods. The survey included 140 randomly selected patients who were referred to Central Clinical Hospital Medical University of Lodz from January to May 2015. The questionnaire included questions about socio-demographic data and the level of dental anxiety using the Modified Dental Anxiety Scale (MDAS). The radiological part included an analysis of pantomographs. The number of decayed, filled, missing, endodontically treated teeth was evaluated. The presence of apical periodontitis was assessed as well.

Results. The age of the patients ranged from 18 to 81 years (mean 44.5 ± 17.8). The majority of respondents demonstrated low (47%) or moderate (24%) level of anxiety. A high level of anxiety was observed in 29% of subjects including 9% with dentophobia. The mean MDAS value in the study group was 11.0 ± 5.3. Patients with high levels of dental anxiety had a significantly higher percentage of decayed teeth (21.9 vs 10.4%; p = 0.003) and teeth with apical periodontitis (13.7 vs 8.6%; p = 0.035) than in the group with low level of dental anxiety. In both groups there was no significant difference in the percentage of filled (27.4% vs 34.4%; p = 0.114), missing (25% vs 17.2%; p = 0.114) and endodontically treated teeth (10.2 % vs 10.8%; p = 0.786). Conclusions. A high level of dental fear is correlated with poor dental status. Dental anxiety should be considered as one of the possible risk factors for caries and its complications. Key words: dental anxiety, Modified Dental Anxiety Scale (MDAS), oral health, dental caries, apical periodontitis

Strach i lęk należą do najczęściej przeżywanych stanów inne dziedziny życia, co pokazują obserwacje duńskiej emocjonalnych. Chociaż terminy te różnią się definicją, populacji cierpiącej na dentofobię. Według obserwacji często są używane zamiennie.1,2 Lęk to stan psychiczny Vermaire et al.18 27 na 30 pacjentów podających lęk przed związany z poczuciem zagrożenia, którego nie można do leczeniem odczuwa zakłopotanie z powodu stanu swoje kładnie określić. Strach występuje w obliczu rzeczywiście go uzębienia, rzadziej się uśmiecha, co obniża pewność występującego niebezpieczeństwa.3 Silniejszym uczuciem siebie i utrudnia kontakty społeczne. jest fobia. Określa się ją jako irracjonalny strach, którego Stan zdrowia jamy ustnej pacjentów odczuwających natężenie nie jest adekwatne do okoliczności i prowadzi duży lęk przed leczeniem dentystycznym był przedmio do unikania sytuacji, które ją wywołują.1 tem badań różnych populacji.9,19–22 W Polsce w ostatnich Lęk przed leczeniem stomatologicznym jest częstym latach oceniano wpływ lęku na stan uzębienia młodzieży zjawiskiem i dotyczy od 16 do 24% dorosłych w różnych szkolnej,2,23 natomiast publikacje dotyczące tego zagad populacjach,4–8 a od 12 do 16% z nich cierpi z powodu nienia w odniesieniu do ogólnej populacji są rzadkie. dentofobii, która obok lęku wysokości należy do najczę Celem pracy była ocena wpływu poziomu lęku przed ściej diagnozowanych fobii.5–7,9–11 Jej występowanie za leczeniem stomatologicznym na stan uzębienia dorosłych leży od wieku, płci, wykształcenia i statusu socjoekono pacjentów z regionu łódzkiego. micznego. Częściej dotyczy kobiet8 i osób do 30. r.ż.6 Badania przeprowadzone wśród pacjentów cierpią cych na dentofobię wykazały, że u 85% z nich rozpoczęła Materiał i metody się ona w dzieciństwie na tle negatywnych doświadczeń związanych z leczeniem stomatologicznym.12 Wśród in W badaniu wzięło udział 158 losowo wybranych do nych przyczyn wymienia się także zniechęcającą posta rosłych zgłaszających się do Centralnego Szpitala Kli wę rówieśników i członków rodziny oraz występowanie nicznego UM w Łodzi. Badana grupa stanowiła próbę dentofobii na tle innych zaburzeń psychicznych.13,14 Ir systematyczną z populacji pacjentów przyjętych w okre racjonalny strach może pojawić się z obawy przed utra sie od stycznia do maja 2015 r. Badanie składało się tą kontroli nad sytuacją podczas wykonywania procedur z części ankietowej i radiologicznej. Osoby poniżej 18. stomatologicznych. Dla pacjenta sama obecność w gabi roku życia, pacjenci bezzębni oraz ankietowani, którzy necie czy też ułożenie w pozycji leżącej w otoczeniu in nie udzielili odpowiedzi na więcej niż jedno pytanie na strumentarium może być przyczyną uczucia naruszenia skali oceniającej lęk przed leczeniem dentystycznym, zo strefy intymnej.15,16 Badania pokazują, że bodźcem wy stali wykluczeni z udziału w eksperymencie. Ostatecz zwalającym największy lęk jest podanie znieczulenia za nie analizie statystycznej poddano dane 140 dorosłych, pomocą igły i strzykawki oraz maszynowe opracowanie którzy wyrazili pisemną zgodę na udział w badaniu. Ba ubytku.12,17 danie uzyskało pozytywną opinię Komisji Bioetycznej Lęk stomatologiczny może niekorzystnie wpływać na nrRNN/24/14KE. Dent Med Probl. 2017;26(1):73–78 75

Kwestionariusz zawierał pytania dotyczące danych so 35 cjodemograficznych (wiek, płeć) oraz lęku przed lecze 30 niem dentystycznym. Poziom lęku oceniono za pomocą skali Modified Dental Anxiety Scale (MDAS),24 która 25 składa się z pięciu pytań jednokrotnego wyboru na temat 20 samopoczucia pacjenta w sytuacjach związanych z le 15 czeniem:

1) przed zaplanowaną wizytą, liczba pacjentów 10

2) w czasie oczekiwania na wizytę w poczekalni, 5 3) na fotelu przed rozpoczęciem zabiegu polegającego na maszynowym opracowaniu ubytku, 0 5791113151719212325 4) podczas usuwania kamienia nazębnego, 5) podczas znieczulenia nasiękowego podawanego wartości skali MDAS z użyciem igły i strzykawki. Ryc. 1. Rozkład badanych z poszczególnymi wartościami skali MDAS Na każde z pytań ankietowany miał do wyboru jedną Fig. 1. The number of the respondents with the respective MDAS values z pięciu możliwych odpowiedzi, którym zostały przypi sane odpowiednie wartości punktowe: nie ma to wpływu na nastrój – 1 pkt, czuję się lekko zaniepokojony – 2 pkt, dentofobia; 9% zaniepokojony – 3 pkt, zdenerwowany – 4 pkt oraz spara liżowany strachem – 5 pkt. Zgodnie z założeniem skali MDAS zastosowano na stępującą punktację oceny lęku: niski poziom – 5–9 pkt, wysoki; 20% umiarkowany – 10–14 pkt i wysoki – 15–25 pkt. Wynik niski; powyżej 19 punktów oznaczał dentofobię.24 47% Radiologiczna część badania polegała na ocenie zdjęć pantomograficznych pacjentów. Radiogramy wykona no cyfrowym aparatem firmy GendexOrthoralix 9200. Oceniano liczbę zębów usuniętych, z próchnicą,® z wy umiarkowany; pełnieniami koronowymi, leczonych endodontycznie i ze 24% zmianami zapalnymi w tkankach okołowierzchołkowych Ryc. 2. Struktura pacjentów ze względu na poziom lęku w skali MDAS (okw.). Fig. 2. The structure of patients according to the anxiety level on the MDAS Metody analizy statystycznej Średnia wartość skali MDAS badanych pacjentów wy Do opisu uzyskanych wyników użyto podstawowych nosiła 11,0 ± 5,3. Dominującymi wartościami były war miar statystycznych, takich jak minimum, maksimum, tości z dolnej części skali. Połowa wyników miała wartość średnia, mediana, dolny i górny kwartyl, odchylenie stan nie większą niż 10 punktów (mediana), natomiast 25% dardowe, błąd standardowy średniej (SEM) oraz wskaź wyników znajdowało się powyżej 15 punktów na ska nik struktury. li MDAS (górny kwartyl). Ilustracją rozkładu wyników Do porównania średnich w grupach wykorzystano w skali MDAS jest rycina 1. test t-studenta. W przypadku niespełnienia założeń te Podział pacjentów na grupy ze względu na uzyskane war stu parametrycznego stosowano ich nieparametryczny tości skali MDAS przedstawiono na rycinie 2. U większości odpowiednik, tj. test U Manna-Whitneya. Na wykresach uczestników badania stwierdzono niski (47%) lub umiarko ramkowych przedstawiono średnią ± błąd standardowy wany (24%) poziom lęku przed leczeniem stomatologicz z wąsami oznaczającymi 95% przedział ufności dla śred nym. Osób z wysokim poziomem lęku było 29%, w tym niej. Za poziom istotny statystycznie przyjęto p < 0,05. Do charakteryzujących się dentofobią – 9%. Dalszej analizie analizy statystycznej użyto programu Statistica 12.5 PL statystycznej poddano dwie grupy ankietowanych: z wyso (Statsoft Inc., USA). kim poziomem lęku – grupa I (≥ 15 pkt w skali MDAS) i niskim poziomem lęku – grupa II (≤ 9 pkt w skali MDAS). W dwóch badanych grupach na radiogramach ocenio Wyniki no 2391 zębów. Średnia liczba zębów w grupie I (wyso ki poziom lęku) wynosiła 21, a w grupie II (niski poziom Wiek badanych osób zawierał się w przedziale 18–81 lat, lęku) – 23, natomiast średnia liczba zębów brakujących średnia wieku wynosiła 44,5 ± 17,8. Wśród ankietowa odpowiednio: 7 i 4,9. nych przeważały kobiety – 58,57% (82), mężczyzn było Porównanie procentowego udziału zębów objętych pro 41,43% (58). cesem próchnicowym, z wypełnieniami koronowymi, le 76 K. Sopińska, N. Olszewska, E. Bołtacz-Rzepkowska. Lęk stomatologiczny a stan uzębienia osób dorosłych

Tabela 1. Porównanie w badanych grupach średnich odsetków zębów objętych procesem próchnicowym, wypełnionych, usuniętych, leczonych endodontycznie i ze zmianami w tkankach okołowierzchołkowych Table 1. A comparison of average percentages of decayed, restored, missing, endodontically treated teeth and teeth with apical periodontitis in studied groups

Pacjenci z wysokim poziomem lęku (grupa I) Pacjenci z niskim poziomem lęku (grupa II) Oceniany parametr p średni odsetek (± SEM) średni odsetek (± SEM) Zęby z próchnicą 21,9% (± 3,5%) 10,4% (± 1,2%) 0,003 Zęby z wypełnieniami 27,4% (± 3,5%) 34,4% (± 2,7%) 0,114 Zęby usunięte 25,0% (± 4,2%) 17,2% (± 2,6%) 0,114 Zęby leczone endodontycznie 10,2% (± 2,1%) 10,8% (± 1,3%) 0,786 Zęby ze zmianami zapalnymi 13,7% (± 2,1%) 8,6% (± 1%) 0,035 w tkankach okołowierzchołkowych

pie z wysokim poziomem lęku wynosił on 13,7%, nato miast z niskim poziomem lęku – 8,6%. Zależność tę zilu strowano na ryc. 4. W badanych grupach zaobserwowano natomiast brak statystycznie istotnych zależności w ocenie odsetków zę bów: z wypełnieniami, usuniętych i leczonych endodon tycznie.

Ryc. 3. Udział procentowy zębów objętych próchnicą w badanych grupach Omówienie Fig. 3. The share of decayed teeth in the studied groups Badanie zostało przeprowadzone w Centralnym Szpi talu Klinicznym UM w Łodzi, który zapewnia dostęp do podstawowej i specjalistycznej opieki stomatologicz nej mieszkańcom miasta i regionu. Pacjenci zgłaszający się do placówki stanowią zróżnicowaną populację pod względem wieku, wykształcenia, miejsca zamieszkania oraz potrzeb leczniczych. Szpital umożliwia komplekso we leczenie osób z różnych grup społecznych i w związku z tym był odpowiednim miejscem do przeprowadzenia niniejszego badania. W badaniu wykorzystano zdjęcia pantomograficzne, które wykonuje się w celach diagnostycznych przed roz poczęciem leczenia stomatologicznego. Dostarczają one Ryc. 4. Udział procentowy zębów ze zmianami zapalnymi w tkankach okołowierzchołkowych w badanych grupach między innymi informacji o twardych tkankach zębów, Fig. 4. The share of teeth with apical periodontitis in studied groups obecności próchnicy i wypełnień, leczeniu kanałowym oraz stanie zdrowia przyzębia wierzchołkowego. Ich za letą jest stosunkowo niska dawka napromieniowania, szybkość i łatwość wykonania oraz uwidocznienie na jed czonych endodontycznie, ze zmianami zapalnymi w tkan nym zdjęciu wszystkich zębów. Dlatego, mimo pewnych kach okołowierzchołkowych oraz usuniętych w badanych ograniczeń wynikających z powiększenia obrazu oraz grupach przedstawiono w tabeli 1, a zależności różniące nakładania się struktur anatomicznych, zdjęcia pantomo się statystycznie zilustrowano również na rycinach 3 i 4. graficzne25 znalazły szerokie zastosowanie w badaniach Jak wynika z danych przedstawionych w tabeli 1 i na epidemiologicznych.19,26,27 rycinie 3, wśród pacjentów przyznających się do strachu Według danych z piśmiennictwa strach przed lecze przed leczeniem dentystycznym odsetek zębów z próch niem stomatologicznym może mieć wpływ na zachowa nicą był istotnie wyższy (p = 0,003) niż u osób z niskim nia prozdrowotne związane z terapią oraz na stan uzębie poziomem lęku (21,9 vs 10,4%). nia.2,9,19–22 Stwierdzono statystycznie istotną różnicę (p = 0,035) Wielu pacjentów z powodu strachu nie zgłasza się re w wartości odsetków zębów ze zmianami w tkankach gularnie na wizyty do dentysty, co skutkuje brakiem okołowierzchołkowych w wyróżnionych grupach. W gru systematycznego leczenia. Kiedy po długiej przerwie Dent Med Probl. 2017;26(1):73–78 77

odwiedzają gabinet, wymagają skomplikowanego i inwa W opinii autorów opisane zachowania były przyczyną zyjnego leczenia, które dodatkowo potęguje niechęć i po stwierdzonej również u tych pacjentów większej liczby woduje utrwalenie postawy unikającej w przyszłości.1,28 brakujących zębów. W piśmiennictwie taka sytuacja określana jest mianem Obserwacje dotyczące tego zagadnienia nie są jedno „błędnego koła”. Termin ten po raz pierwszy został użyty znaczne, bowiem Coolidge et al.7 po zbadaniu hiszpań przez Berggrenai Meynerta12 w 1984 r., ale jak pokazują skiej populacji nie znaleźli podobnej zależności. Badanie badania z ostatnich lat, jest nadal obecny w wielu publi własne również nie potwierdziło związku między pozio kacjach.1,15,28 Arfmield et al.15 odnotowali, że 39% osób ze mem lęku a odsetkiem usuniętych zębów, chociaż u pa średnim i wysokim poziomem lęku znalazło się w „błęd cjentów lękowych wartość tego odsetka była wyraźnie nym kole”. Ankietowani odwiedzali dentystę tylko w przy większa (25,0 vs 17,2%). padku bólu, a gdy dolegliwości ustępowały, rezygnowali Na zdjęciach pantomograficznych ocenie poddano tak z dalszej opieki stomatologicznej. W grupie pacjentów że częstość leczenia endodontycznego. Odsetek zębów pozbawionych strachu taki model zachowania dotyczył z wypełnionymi kanałami nie różnił się u osób z wysokim tylko 1% osób. (10,2%) i niskim poziomem lęku (10,8%). W piśmiennic Lęk dentystyczny z użyciem skali MDAS oceniano twie nie znaleziono publikacji, które badałyby tę zależ w różnych populacjach na całym świecie. Średnia wartość ność. Można jednak dodać, że według wcześniejszych skali MDAS w obecnym badaniu wyniosła 11,0. Uzyskane danych dotyczących łódzkiej populacji odsetek zębów wyniki są zbliżone do obserwowanych w innych krajach. leczonych endodontycznie był porównywalny i wyno Nieco wyższą wartość średniej stwierdzono w Hiszpanii sił 9,7%.26 (11,87)7 i Iranie (12,34),8 a niższą w Grecji (10,48).29 We W badaniu oceniano także wpływ poziomu lęku na dług danych własnych wysoki poziom lęku dotyczył 29,3% obecność przewlekłych stanów zapalnych w tkankach ankietowanych, co sugeruje, że mimo coraz doskonal okołowierzchołkowych, które najczęściej są skutkiem szych metod leczenia problem pozostaje ciągle aktualny. zakażenia miazgi przez bakterie pochodzące z ogniska Z przeprowadzonych badań wynika, że u osób z wy próchnicowego.22 Nasza analiza ujawniła korelację mię sokim poziomem lęku odsetek zębów z próchnicą był dzy częstością występowania zmian zapalnych przyzębia dwukrotnie wyższy i wynosił 21,9%, podczas gdy u osób wierzchołkowego a wysokim poziomem lęku. Odsetek z niskim poziomem – 10,5%. Jest to zgodne z obserwacja zębów ze zmianami w grupie I był istotnie większy niż mi Hakeberga et al.,21 którzy badali szwedzką populację w grupie II i wynosił odpowiednio: 13,7 i 8,6%. Jest to i zauważyli, że średnia liczba powierzchni zębów objętych zgodne z obserwacjami Hakeberga et al.13, według któ próchnicą była zdecydowanie wyższa u ankietowanych rych osoby z wysokim poziomem lęku miały średnio odczuwających strach przed leczeniem dentystycznym 4 zęby ze zmianami, a osoby nieobawiające się stoma niż w grupie osób pozbawionych lęku (19,5 vs 7,9). Wen- tologa – 1,2. Takiej zależności nie potwierdzają bada stromm et al.19 oceniając zdjęcia pantomograficzne ko nia Friska i Hackeberga,22 którzy ocenili stan przyzębia biet w wieku 38 i 50 lat pod kątem występowania próch wierzchołkowego 844 kobiet w wieku 38–78 lat i nie za nicy zębów, stwierdzili gorszy stan uzębienia u pacjentek uważyli związku między lękiem przed leczeniem a czę odczuwających lęk stomatologiczny. Coolidge et al.7 za stością występowania stanów zapalnych w przyzębiu uważyli również częstsze występowanie zaawansowanej wierzchołkowym. próchnicy o ostrym przebiegu u osób cierpiących na den Zróżnicowane obserwacje dotyczące tego zagadnienia tofobię. wyjaśniają w pewnym stopniu badania Kirkevang et al.,30 Kolejnym ocenianym parametrem była obecność wy którzy zbadali grupę szwedzkich pacjentów pod kątem pełnień koronowych. Jak wynika z przeprowadzonego identyfikacji czynników ryzyka utraty zębów. Autorzy przeglądu, odsetek zębów z wypełnieniami nie różnił podczas dziesięcioletniej obserwacji zębów ze zdia się istotnie w porównywanych grupach. Odmienne dane gnozowanym na początku badania zapaleniem przyzę podali szwedzcy autorzy, których badanie ankietowe i ra bia wierzchołkowego zauważyli, że część z nich została diologiczne 180 pacjentów ujawniło, że osoby z wysokim w tym czasie usunięta, nie podlegając tym samym dal poziomem lęku miały średnio mniej wypełnionych po szej ocenie. wierzchni zębów w porównaniu z tymi, którzy nie bali Przeprowadzone badania pokazały, że wysoki poziom się stomatologa: średnie wyniosły odpowiednio 8,1 i 13,1 lęku przed zabiegami stomatologicznymi jest skorelowa i różniły się istotnie. Ich zdaniem większa liczba wypeł ny z gorszym stanem uzębienia. U pacjentów z wysokim nień świadczy o regularnym leczeniu, które pozwala poziomem lęku zaobserwowano istotnie więcej zębów na zachowanie własnego uzębienia. Pacjenci odczuwa objętych procesem próchnicowym i ze zmianami zapal jący strach przed wizytą u dentysty częściej natomiast nymi w tkankach okołowierzchołkowych. Z tego powodu zgłaszali się z zaawansowanym procesem chorobowym lęk obok nieprawidłowej higieny, diety czy też niskiego i w obawie przed skomplikowanym leczeniem decy statusu socjoekonomicznego powinien być uwzględniany dowali się na najszybszą i jednocześnie najbardziej ra jako jeden z możliwych czynników ryzyka występowania dykalną metodę postępowania, jaką była ekstrakcja.21 próchnicy i jej powikłań. 78 K. Sopińska, N. Olszewska, E. Bołtacz-Rzepkowska. Lęk stomatologiczny a stan uzębienia osób dorosłych

Piśmiennictwo 16. Crego A, Carrillo-Díaz M, Armfield JM, Romero M. From public mental health to community oral health: The impact of dental anx- 1. Beaton L, Freeman R, Humphris G. Why are people afraid of iety and fear on dental status. Front Public Health. 2014;16:1–4. the dentst? Observations and explenations. Med Princ Pract. 17. Kaczmarek U, Mysiak-Dębska M, Dębska K, Grzebieluch W. Dental 2014;23:295–301. anxiety in students of the first years of the study of dentistry and 2. Kaczmarek U, Grzesiak I, Kowalczyk-Zając M, Bader-Orłowska D. medicine faculties. Dent Med Probl. 2010;47:343–349 (in Polish). The level of dental anxiety and the dental status in 18-year-olds. 18. Vermaire JH, de Jongh A, Aartman IH. Dental anxiety and quality of J Stoma. 2008;61:81–87 [in Polish]. life: The effect of dental treatment. Community Dent Oral Epidemiol. 3. Siwy-Hudowska A, Kieszkowska-Grudny A. Machiavellian person- 2008;36:409–416. ality and its factors in gender comparisons: The role of emotional 19. Wennström A, WideBoman U, Stenman U, Ahlqwist M, Hakeberg M. intelligence and anxiety. Psychol Społ. 2010;5:27–41 [in Polish]. Oral health, sense of coherence and dental anxiety among middle- 4. Smith TA, Heaton LJ. Fear of dental care: Are we making any prog- aged women. Acta Odontol Scand. 2013;71:256–262. ress? J Am Dent Assoc. 2003;134:1101–1108. 20. Armfield JM, Slade GD, Spencer AJ. Dental fear and adult oral health 5. do Nascimento DL, da Silva Araújo AC, Gusmão ES, Cimões R. Anxi- in Australia. Community Dent Oral Epidemiol. 2009;37:220–230. ety and fear of dental treatment among users of public health ser- 21. Hakeberg M, Berggren LJ, Grondahl HG: A radiographic study of vices. Oral Health Prev Dent. 2011;9:329–337. dental health in adult patients with dental anxiety. Community 6. Kirova DG, Atanasov DT, Lalabonova CK, Janevska S. Dental anxiety Dent Oral Epidemiol. 1993;21:27–30. in adults in Bulgaria. Folia Med. 2010;52:49–56. 22. Frisk F, Hakeberg M. Socio-economic risk indicators for apical peri- 7. Coolidge T, Hillstead MB, Farjo N, Weinstein P, Coldwell SE. Addi- odontitis. Acta Odontol Scand. 2006;64:123–128. tional psychometric data for the Spanish Modified Dental Anxiety 23. Hajto-Bryk J, Dobroś K, Zarzecka J. Dental anxiety level and dental Scale, and psychometric data for a Spanish version of the Revised status in 18-year-old patients in Poland. J Stoma. 2015;68:669–680. Dental Beliefs Survey. BMC Oral Health 2010;10:2. 24. Humphris GM, Morrison T, Lindsay SJ. The Modified Dental Anxi- 8. Saatchi M, Abtahi M, Mohammadi G, Mirdamadi M, Binandeh ES. ety Scale: Validation and United Kingdom norms. Community Dent The prevalence of dental anxiety and fear in patients referred to Health. 1995;12:143–150. Isfahan Dental School. Iran. Dent Res J. 2015;12:248–253. 25. Whaites E. Zdjęcia pantomograficzne. W: Podstawy radiodiagno- 9. Kanaffa-Kilijanska U, Kaczmarek U, Kilijanska B, Frydecka D. Oral styki stomatologicznej. Redakcja wydania polskiego T.K. Różyło. health condition and hygiene habits among adult patients with Sanmedica, Warszawa, 1994;137–151. respect to their level of dental anxiety. Oral Health Prev Dent. 26. Bołtacz-Rzepkowska E, Łaszkiewicz J. Endodontic treatment and 2014;12:233–239. periapical health in patients of the Institute of Dentistry in Łódź. 10. Schuller AA, Willumsen T, Holst D. Are there differences in oral Przegl Epidemiol. 2005;59:107–115 [in Polish]. health and oral health behavior between individuals with high and 27. Różyło TK, Szczepanik-Barczewska E, Kalinowski P, Barczewski Ł. low dental fear? Community Dent Oral Epidemiol. 2003;31:116 –121. Radiological comparative evaluation of dental and oral status on 11. Armfield JM. Australian population norms for the Index of Dental panoramic radiographs of diabetics and health controls. Magazyn Anxiety and Fear (IDAF-4C). Aust Dent J. 2011;56:16–22. Stomatol. 2014;24:5, 28–32 [in Polish]. 12. Berggren U, Meynert G. Dental fear and avoidance: Causes, symp- 28. Boyle CA, Newton T, Milgrom P. Who is referred for sedation for toms, and consequences. J Am Dent Assoc. 1984;109:247–251. dentistry and why? Br Dent J. 2009;206:322–323. 13. Hakeberg M, Hägglin C, Berggren U, Carlsson SG. Structural rela- 29. Coolidge T, Arapostathis KN, Emmanouil D, et al. Psychometric tionships of dental anxiety, mood, and general anxiety. Acta Odon- properties of Greek versions of the Modified Corah Dental Anxiety tol Scand. 2001;59:99–103. Scale (MDAS) and the Dental Fear Survey (DFS). BMC Oral Health. 14. Locker D, Poulton R, Thomson WM. Psychological disorders and 2008, 30, 8, 29. dental anxiety in a young adult population. Community Dent Oral 30. Kirkevang LL, Ørstavik D, Wenzel A, Vaeth M. Prognostic value of Epidemiol. 2001;29:456–463. the full-scale Periapical Index. Int Endod J. 2015; 48:1051–1058. 15. Armfield JM, Heaton LJ. Management of fear and anxiety in the dental clinic: A review. Aust Dent J. 2013;58:390–407. Reviews The use of fractal analysis in medicine: A literature review Zastosowanie analizy fraktalnej w medycynie – przegląd piśmiennictwa

Przemysław LeszczyńskiB–D, F, Jerzy SokalskiA, E, F

Department of Dental Surgery, Poznan University of Medical Sciences, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):79–83

Address for correspondence Abstract Przemysław Leszczyński E-mail: [email protected] In many areas of science, there is a need to assess the complexity of the analyzed objects. One instrument used to assess this complexity can be fractal analysis, which provides a quantitative measure in the form of Funding sources none declared a fractal dimension. A fractal dimension is a quantitative parameter used for measuring the complexity of the examined objects. Fractal analysis is the process of information processing, where the input data is an Conflict of interest image. The generated information is stored in the form of numbers, an array of numbers, the decision of none declared the text etc. The implementation of the image processing requires a computer system. In the publications of recent years, there is increasing interest in the potential use of fractal analysis in many fields of science, Received on August 16, 2016 including medicine. Fractal analysis expands the capabilities of the diagnosis of systemic diseases, facilitat- Revised on November 23, 2016 ing and accelerating their examination. In dentistry, the calculation of the fractal dimension can be a tool Accepted on February 2, 2017 for early detection of a periapical lesion on the basic X-rays. Fractal analysis can also be a helpful indicator in predicting the primary stability of an implant. On the basis of the literature and own experience, the authors sum up the use of fractal analysis in accordance with current medical knowledge. Key words: fractal analysis, fractal dimension, fractals, dentistry Słowa kluczowe: analiza fraktalna, wymiar fraklany, fraktale, stomatologia

DOI 10.17219/dmp/67501

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 80 P. Leszczyński, J. Sokalski. The use of fractal analysis in medicine

Many areas of science require the assessment of the de- Recent studies also suggest that fractal analysis describ- gree of complexity of the analyzed areas. The tools used to ing the nonlinear dynamics of heart rhythm can provide assess this complexity include fractal analysis, which pro- stronger prognostic information than conventional index- vides a quantitative measurement in the form of a fractal es of heart rate variability. In particular, short-term fluc- dimension.1 The word fractus means “broken” or “partial”. tuation analysis can predict the risk of fatal cardiovascular Fractals are objects made of an irregular shape, character- events in different populations.8 This is also confirmed by ized by self-similarity, which means that they look alike, the study by Tapanainen et al.9 Their prospective, multi- regardless of the magnification used. A fractal dimension center study evaluated the prognostic significance of frac- is a quantitative parameter used for measuring the com- tal analysis and traditional parameters of variability of the plexity of the examined objects.2 heart rate of patients after acute myocardial infarction. Fractal analysis allows for a comparison between im- They showed that the fractal analysis of heart rate vari- ages for the presence of self-similarity.1 Fractal analysis ability is a strong predictor of mortality among patients is the process of information processing, where the input who survived acute myocardial infarction.9 data is in the form of an image. The generated information is stored as numbers, an array of numbers, the decision, the text and the like. The implementation of the Oncological applications image processing requires a computer system. The quality of the compressed images becomes an im- A recent study indicates that fractals can be used to di- portant factor, and a considerable compression ratio de- agnose cancerous lesions. This fact is not surprising, be- termines the effective image compression. Compressing cause, due to the irregular structure, cancer cells can be an image reduces the amount of redundant data from the interpreted as fractals. image. The objective of quality measures is to reflect the Fractal analysis is widely used in oncology. It enables approximate quality of the decoded images. The signal- objective classification of complex patterns of tumor tis- to-noise ratio is a quality measure which is frequently sue by examining the distribution of nuclei. Changes in used to measure the deviation between an original and fractal dimension are important in a system of classifica- a coded image.3 tion of tumors. In addition, fractal analysis makes it possi- The most important feature of the fractal dimension ble to compare with each other the complexity of increase lies in the possibility of being a fractional number. A com- and intercellular interactions in tumor tissues.10 puter representation of a radiological image is the image Daye et al. investigated the potential of mammographic matrix, where shades of gray correspond to the elements parenchymal texture as a phenotypic imaging marker of with coordinates x and y, and create a more or less com- endogenous hormonal exposure.11 They concluded that plex surface whose shape is far from being smooth. In the mammographic texture patterns may reflect the effect of case of medical images, the values of the fractal dimen- endogenous hormonal exposure on the breast tissue and sion are in the range of 2.00 < D < 3.00.4 may capture such effects beyond mammographic density. Image analysis is used in areas such as materials science Differences in texture features between pre- and post- (evaluation of porosity, grain size), medicine, forensics menopausal women are more pronounced in the cancer- (comparison of fingerprints), remote sensing (satellite affected population, which may be attributed to an in- and aerial images), quality control, automatic sorting of creased association to breast cancer risk.11 correspondence and others.5 Zheng et al. have developed a fully automated software pipeline based on a novel lattice-based strategy to extract a range of parenchymal texture features from the entire Cardiological applications breast region.12 They conclude that a lattice-based strategy for mammographic texture analysis makes it possible The studies of Lawrence et al. showed the usefulness to characterize the parenchymal pattern over the entire of fractal analysis in cardiology.6 They took advantage of breast. As such, these features provide richer information the new marker Gel Point in patients after myocardial in- compared to currently used descriptors and may ulti- farction and evaluated its therapeutic usefulness. Fractal mately improve breast cancer risk assessment.12 analysis measured the changes in the microstructure of Heymans et al. examined the differences of micro vessels blood clots. They proved that this method makes it pos- in malignant melanoma using the fractal method.13 They sible to evaluate the effectiveness of therapeutic interven- found that it is possible to distinguish the quantitative profile tions by measuring changes in the microstructure of the of blood vessels. They have demonstrated the usefulness of clot.6 Beckers et al. analyzed the nonlinear heart rate vari- the above method as a predictor of disease progression. ability.7 They obtained information about the autonomic An analysis of fractal dimensions is ancillarily used in control of the heart rate. It turned out that the fractal setting a definitive diagnosis. It helps to distinguish the dimension changes reflect physiological and pathophysi- normal structure images of histological tissue from the ological changes taking place in the myocardium.7 tissue with characteristics of malignancy.14 Dent Med Probl. 2017;54(1):79–83 81

Use in ophthalmology A fractal dimension using e.g. the method of box- counting can be calculated from a binary image. Available publications indicate the particular utility of These studies suggest that the bone tissue is of a frac- fractal analysis in the examination of the surface of the tal construction. Bone strength depends on the mass retina. The research of Frydkjaer-Oslen et al. has shown and structure of bone tissue. Research by Sindeaux et al. the relationship between early vascular changes and neu- confirmed that the fractal dimension values of corti- rogenic changes in patients with type 2 diabetes.15 They cal bone are lower in women with osteoporosis.20 They considered retinal fractal analysis an effective method proved that fractal analysis can be considered a pre-test for early identification of neurodegenerative disorders.15 to measure bone density, normally used in the diagnosis Fractal analysis is also used in studies of macular vessels. of osteoporosis.20 The study by Bianciardi et al. shows that It allows for reliable, accurate analysis of the structure of the results obtained from the analysis of the fractal im- the retina in macular degenerations – diabetic maculo ages of X-rays of bones directly correlate with the results pathy.16 obtained with ultrasound methods in patients suffering A Talu study confirmed the multifractal nature of the from osteoporosis.21 Attempts have been made to devel- network of tiny blood vessels in the retina.17 Their analy- op an automatic testing system of trabecular bone using sis allows for a non-invasive way to measure various as- fractal analysis. Selected areas were tested in tension and pects of the topography of the blood vessels. He showed compression condition. Preliminary results show that the that image analysis can be used as a potential marker for above method may have significant clinical application.22 early detection of diseases of the retina. Luo et al. transformed 3D images of bones obtained Pathological lesions in the microcirculation of the retina through CT to flat, 2-dimensional X-ray images. Using may reflect microvascular processes in the brain. Quan- a fractal analysis of the obtained radiographs, they titative analysis of the small blood vessels on the capil- showed that using this method can evaluate the architec- lary level opens a new era of microcirculation research in ture of bone tissue.23 They proved that the fractal dimen- small cerebrovascular diseases.18 sion increases as bone density decreases. Fractal analysis of conventional radiographs may become an alternative to costly and specialized imaging tests.23,24 Use in radiology

The mathematical nature of fractal analysis is widely The use in dentistry used in radiology. There are two types of image compression: ‘Lossless’ compression and Lossy compression. Currently, the literature provides relatively few reports ‘Lossy’ compression always produces an image which is on the use of fractal analysis in dentistry. Its use is based not an exact copy of the original data. It removes redun- on the finding that bone tissue has a fractal construction. dancy and creates an approximation of the original. Lossy Thus the calculation of the fractal dimension can be a tool compression are required to apply on those data where for the early detection of periapical lesion on basic X-rays. reproduction of original data is not required. This hypothesis was confirmed using artificial, chemical- The following diagrams show the processing of radio- ly-generated lesions.25 Fractal analysis can also be used to logical images for the purpose of fractal analysis proposed evaluate the periapical area after endodontic treatment.26 by White.19 Processing of radiological images deliver a bi- Sobolewska-Siemieniuk et al. assessed the quantitative nary image. changes in the bone tissue regions of reincluded teeth.4

Fig. 1. Processing radiological images using the S.C. White method19 82 P. Leszczyński, J. Sokalski. The use of fractal analysis in medicine

They found that, in the case of reincluded teeth, bone tis- 4. Sobolewska-Siemieniuk M, Grabowska S, Oczeretko E, Kitlas A, Borowska M. Fractal analysis of mandibular radiographic images in sue of the alveolar part exhibits a high degree of irregular- the region of reincluded teeth. Czas. Stomatol. 2007;60:593–600 [in ity, and fractal analysis expands the evaluation of radio- Polish]. logical images.4 Studies also suggest that comparing the 5. Gawlik J, Magdziarczyk W, Wojnar L. Fractal analysis of geometric surface structure. Komputerowo Zintegrowane Zarządzanie 2011;2: fractal dimension is a promising tool for detecting chang- 382–396 [in Polish]. es in the bone tissue associated with the patients receiving 6. Lawrence MJ, Sabra A, Thomas P, et al. Fractal dimension: A novel bisphosphonates.27 clot microstructure biomarker use in ST elevation myocardial infarction patients. Atheroscler. 2015;240:402–407. Kąkolewska’s research aimed to determine whether 7. Beckers F, Verheyden B, Couckuyt K, Aubert AE. Fractal dimension there is a relationship between the dimension of implant in health and heart failure. Biomed Tech. (Berl) 2006;51:194–197. stability and a fractal dimension of radiological images of 8. Perkiömäki JS, Mäkikallio TH, Huikuri HV. Fractal and complexity mea- bone tissue.28 She obtained a correlation between the im- sures of heart rate variability. Clin Exp Hypertens. 2005;27:149–158. 9. Tapanainen JM, Thomsen PE, Kober L, et al. Fractal analysis of heart plants primary stability and the fractal dimension, mak- rate variability and mortality after an acute myocardial infarction. ing it possible to draw the conclusion that the smaller Am J Cardiol. 2002;90:347–352. the fractal dimension of the bone, the higher the primary 10. Waliszewski P, Wagenlehner F, Gattenlöhner S, Weidner W. Fractal geometry in the objective grading of prostate carcinoma. Urologe stability obtained can be. The results of this study show A. 2014;53:1186 –1194. that the fractal dimension can be a helpful indicator in 11. Daye D, Keller B, Conant EF, Chen J, Schnall MD, Maidment AD, Kon- predicting the primary stability of an implant.28 tos D. Mammographic parenchymal patterns as an imaging marker of endogenous hormonal exposure: A preliminary study in a high- Kozakiewicz et al. analyzed how different implanted risk population. Acad Radiol. 2013;20:635–646. materials affected the healing of alveolar defects using 12. Zheng Y, Keller BM, Ray S, Wang Y, Conant EF, Gee JC, Kontos D. fractal dimension computation taken from radiographs.29 Parenchymal texture analysis in digital mammography: A fully automated pipeline for breast cancer risk assessment. Med Phys. Studies suggest that a fractal dimension varied with dif- 2015;42:4149–4160. ferent biomaterials throughout the time of observation 13. Heymans O, Blacher S, Brouers F, Piérard GE. Fractal quantification and reflected the individual character of bone remodeling. of the microvasculature heterogeneity in cutaneous melanoma. Visible changes in the structure emerge earlier in places of Dermatol. 1999;198:212–217. 14. Gheonea DI, Streba CT, Vere CC, et al. Diagnosis system for hepa- implantation of bovine bone mineral and beta-tricalcium tocellular carcinoma based on fractal dimension of morphometric phosphate in comparison to the group of biomaterials elements integrated in an artificial neural network. Biomed Res Int. constituting more stable patterns of radiotexture: algae 2014;239706. 15. Frydkjaer-Olsen U, Soegaard Hansen R, Pedersen K, Peto T, Graus- derived hydroxyapatite, biological active glass, synthetic lund J. Retinal vascular fractals correlate with early neurodegener- hydroxyapatite. The authors conclude that fractal tech- ation in patients with type 2 diabetes mellitus. Invest Ophthalmol niques can be a descriptor of bone substitutes.29 Vis Sci. 2015;56:7438–7443. 16. Thomas GN, Ong SY, Tham YC, et al. Measurement of macular frac- However, an examination of the fractal dimension is not tal dimension using a computer-assisted program. Invest Ophthal- a suitable method to be used in each case. In order to ob- mol Vis Sci. 2014;55:2237–2243. tain reliable data, the image resolution and the exposure 17. Tălu S. Multifractal characterisation of human retinal blood vessels. 30 Oftalmol. 2012;56:63–71. time must be appropriately chosen. 18. Jiang H, Debuc DC, Rundek T, et al. Automated segmentation and fractal analysis of high-resolution non-invasive capillary perfusion maps of the human retina. Microvasc Res. 2013;89:172–175. Summary 19. White SC. Oral radiographic predictors of osteoporosis. Dentomax- illofac Radiol. 2002;31:84–92. 20. Sindeaux R, Figueiredo PT, de Melo NS, et al. Fractal dimension and The publications of recent years show increasing inter- mandibular cortical width in normal and osteoporotic men and est in the potential use of fractal analysis in many fields women. Maturitas 2014;77:142–148. 21. Bianciardi G, Bisogno S, Bertoldi I, Laurini L, Coviello G, Frediani of science, including medicine. Fractal analysis expands B. Fractal dimension of bone texture in radiographs correlates to the diagnostic capabilities regarding systemic diseases ultrasound broadband attenuation T-score. Clin Exp Rheumatol. by facilitating and accelerating their diagnosis. However, 2013;31:389–393. 22. Udhayakumar G, Sujatha CM, Ramakrishnan S. Trabecular architec- fractal analysis also has its drawbacks as it is sensitive to ture analysis in femur radiographic images using fractals. Proc Inst image processing and the phenomenon of noise. This sug- Mech Eng H. 2013;227:448–453. gests the desirability of undertaking further research into 23. Luo G, Kinney JH, Kaufman JJ, Haupt D, Chiabrera A, Siffert RS. Rela- the use of fractal analysis to be used in medicine. tionship between plain radiographic patterns and three dimensional trabecular architecture in the human calcaneus. Osteoporos Int. 1999;9:339–345. 24. Linkow LI. Some variant designs of the subperiosteal implant. Oral References Implantol. 1972;2:190–205. 1. Omiotek Z. The study of images self-similarity using the method of 25. Soğur E, Baksı BG, Gröndahl HG, Sen BH. Pixel intensity and frac- fractal analysis. Barometr regionalny. 2011;23:93–105 [in Polish]. tal dimension of periapical lesions visually indiscernible in radio- 2. Kąkolewska J, Kuras M, Sokalski J, Kulczyk T. Use of fractal analysis graphs. J Endod. 2013;39:16–19. for bone assessment. Dent Forum 2014;42:104–106. 26. Huang CC, Chen JC, Chang YC, Jeng JH, Chen CM. A fractal dimen- 3. Garg A, Agrawal A, Negi A. A review on fractal image compression. sional approach to successful evaluation of apical healing. Int Int J Comp Applicat. 2014;85:25–31. Endod J. 2013;46:523–529. Dent Med Probl. 2017;54(1):79–83 83

27. Torres SR, Chen CS, Leroux BG, Lee PP, Hollender LG, Schubert MM. 29. Kozakiewicz M, Chaberek S, Bogusiak K. Using fractal dimension to Fractal dimension evaluation of cone beam computed tomogra- evaluate alveolar bone defects treated with various bone substi- phy in patients with bisphosphonate-associated osteonecrosis. tute materials. Central Europ J Med. 2013;8:776–789. Dentomaxillofac Radiol. 2011;40:501–505. 30. Baksi BG, Fidler A. Image resolution and exposure time of digital 28. Kąkolewska J. Evaluation of the alveolar bone using fractal anal- radiographs affects fractal dimension of periapical bone. Clin Oral ysis and periotest device in patients after implantation of dental Investig. 2012;16:1507–1510. implants. Doctoral Thesis, Poznań 2014 [in Polish].

Clinical cases Clinical aspects of oral cancer: A case report series Kliniczne uwarunkowania raka jamy ustnej – opis przypadków

Suwarna Dangore-KhasbageA, B, D

Oral Medicine and Radiology, Sharad Pawar Dental College, Datta Meghe Institute of Medical Sciences, Sawangi, India

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):85–89

Address for correspondence Abstract Suwarna Dangore-Khasbage E-mail: [email protected] Oral cancer is the sixth-most common cancer globally; nevertheless, there is a wide geographical variation in its incidence all over the world. In India, it accounts for about 30% of all new cases annually and the Funding sources none declared gingival-buccal complex (alveolar ridge, gingival-buccal sulcus, buccal mucosa) forms the most common subsite for cancer of the oral cavity, in contrast to cancer of the tongue that is more common in the Western Conflict of interest world. There is a trend towards increasing incidence and delayed presentation of oral cancer as approxi- none declared mately 50% of patients present at stage III or IV. Although, oral cancer is a disease of the older age groups, many patients contract it at an early age (< 40 years of age), especially in high incidence countries such as Acknowledgments We wish to thank our patients for their kind cooperation. India where the lower socioeconomic strata of society plays a vital role. Despite improvement in diagnostic and management techniques, the age-standardized mortality rates in oral cancer are constant, which is attributable to a failure to detect potentially malignant lesions and early stage oral cancer which precludes Received on November 1, 2016 Revised on November 12, 2016 successful treatment. Accepted on December 2, 2016 This article describes three cases of oral squamous cell carcinoma occurring at an early age, with more emphasis on the clinical aspects of squamous cell carcinoma and measures for the prevention and early detection of oral cancer. Key words: tobacco, squamous cell carcinoma, oral cancer Słowa kluczowe: tytoń, rak płaskonabłonkowy, rak jamy ustnej

DOI 10.17219/dmp/67499

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 86 S. Dangore-Khasbage. Clinical aspects of oral cancer

Oral cancer is the sixth-most common cancer in the world casional bleeding from the same site. There was no history and in India oral cancer ranks in the top 3 of all cancers.1 of pus discharge, trauma, anesthesia or paresthesia in the Amongst all oral cancers, more than 90% are squamous cell associated area. He had a habit of paan chewing and quid carcinomas (OSCC) while the remaining 10% of the cases keeping in the lower left buccal vestibule for 30–35 min, are mainly melanomas, sarcomas, minor salivary gland car- 8 to 10 times a day for 20 years. Oral examination revealed cinomas and metastatic cancers.2 OSCC is asymptomatic an ulcero-infiltrative lesion on the gingival margin in tooth in the early stage and thus ignored by the patient, but it is 34, 35, 36 and 37 with everted edges (Fig. 1). On palpation, known to produce high mortality and serious disturbances the lesion was tender, firm, indurated and showed mild or discomfort in the patient as a consequence of either the bleeding on manipulation. Teeth in the vicinity were tender tumor itself or of the treatment in the advanced stage. The and mobile. Extraoral examination revealed the presence incidence of OSCC is age related, which may reflect the time of a single submandibular lymph node on the same side of for the accumulation of genetic changes and duration of ex- approximately size 1 × 1.5 cm, firm, non-tender and mo- posure to initiators and promoters, cellular aging, and de- bile. Based on the clinical features, the diagnosis was ma- creased immunologic surveillance with aging.3 lignancy involving the gingiva and alveolus (TNM staging OSCC presents different clinical aspects which are re- – T4 N1 M0). Computed tomography showed evidence of lated to the etiology, location of the tumor, evolution time, a well-defined, enhancing soft tissue density in the gingi- origin from precancerous lesion or condition and various vobuccal sulcus which was eroding the outer cortex of the risk factors. Even though the frequent clinical presenta- body of the mandible on the left side. The features were tion of OSCC is a painless, rapidly increasing growth or suggestive of malignancy, supporting the clinical diagnosis a non-healing ulcer, it may occur in various clinical forms (Fig. 2). Histopathological confirmation of the disease was such as a white lesion, red lesion, mixed lesion (combi- done by performing an incisional biopsy. He was treated nation of red and white), vegetans, verrucous, and mixed by surgical excision of the lesion followed by plastic sur- forms such as ulcerous-vegetans.4 In India, ulcero-prolif- gery. The skin graft, tissue flap was used to restore tissues erative and ulcero-infiltrative presentation is quite com- removed from the surgical site. An H&E stained tissue mon. This article focuses mainly on the etiology, clinical section from the surgical specimen showed the presence presentation and diagnostic delay of OSCC. of neoplastic epithelial cells in the outer connective tissue capsule. The inner stroma also showed the presence of neoplastic epithelial cells arranged in the form of sheets along Case presentation with a keratin pearl formation. The features were diagnostic of moderately-differentiated squamous cell carcinoma. Case 1

A 38-year-old male reported with the complaint of loosening of teeth and pain in the mandibular left posterior region of the jaw for 4 months. He gave a history of oc-

Fig. 1. Case 1 – an ulcero- infiltrative lesion on the gingiva and vestibule on the left side

Fig. 2. Case 1 – CT scan – axial view, showing a well-defined enhancing soft tissue mass in the gingivobuccal sulcus, eroding the outer cortex of the body of the mandible on the left side Dent Med Probl. 2017;54(1):85–89 87

Fig. 3. Case 2 – an exophytic growth on the left buccal mucosa

Fig. 4. Case 2 – post-operative photograph after six months following surgery

Case 2

A 36-year-old male reported with the complaint of a painless growth on the left buccal mucosa for 2 months. There was no history of discharge or paresthesia in the associated area. He had a habit of keeping tobacco lime quid in the same region 10–15 times a day for 18 years. On intraoral examination there was the presence of a single, sessile, exophytic, cauliflower-like growth on the left buccal mucosa of approximately 3 × 2 cm, which was white Fig. 5. Case 3 – malignant ulcer on the right lateral border of the tongue in color with distinct borders (Fig. 3). Palpation revealed that the growth was non-tender and firm. There was no regional lymphadenopathy. Considering the habit history and clinical features, the diagnosis was malignancy of the to the physician in his home town for the problem but left buccal mucosa (TNM staging – T2 N0 M0). Histo- didn’t get relief with the medications prescribed. The in- pathological confirmation of the disease was done by per- traoral ulcer increased rapidly in the course of 3 months. forming an incisional biopsy. He was treated by doing wide He also gave a history of mild pain and difficulty in masti- local excision of the lesion. An H&E stained tissue section cation on the right side due to the large ulcer and repeat- from the surgical specimen was diagnostic of moderately- ed tongue biting. There was no history of bleeding, pus differentiated squamous cell carcinoma. Clinical examina- discharge or paresthesia in the associated area. He had tion after 6 months following the surgery revealed uncom- a habit of chewing paan and tobacco 4–5 times a day for plicated recovery and no recurrence (Fig. 4). 15 years. Oral examination showed the presence of a single, large (4 × 5 cm in size) ulcer with everted edges. The Case 3 base of the ulcer was indurated and covered with necrotic slough (Fig. 5). Lymph node examination revealed lymph- A 34-year-old male reported with the complaint of adenopathy with submental and right submandibular a non-healing ulcer on the right lateral border of the groups. All lymph nodes were tender, hard and partially tongue for 3 months. The patient stated that he was fixed. The clinical features were diagnostic of tongue ma- healthy 3 months prior, but one day he had experienced lignancy (TNM staging – T3 N2b M0). He was treated by discomfort on the right side of his tongue for which he a combination of surgery and radiotherapy after undergo- had performed self oral inspection and noticed a small ul- ing all the necessary examinations for local and distant cer of a few millimeters in the same region. He reported metastases and confirmation by incisional biopsy. The 88 S. Dangore-Khasbage. Clinical aspects of oral cancer

histopathological features of the postoperative specimen For lip carcinoma, the etiology is usually chronic ex- were suggestive of moderately-differentiated squamous posure to sunlight. Meanwhile, chronic trauma due to cell carcinoma. various factors, such as a fractured tooth, sharp edged teeth, root pieces or improper denture, is the most typical reason for carcinoma of the lateral border and ventral Discussion surface of the tongue.3,10 In the present article, in case 3, it is difficult to guess the probable etiology for OSCC of Oral cancer is considered a serious public health prob- the lateral border of the tongue because, even though the lem that causes a great deal of morbidity and mortality patient has teeth with sharp cusps, he had a history of an in the population. It is often painless or asymptomatic, adverse habit for 15 years. so the patient usually reports for treatment at the ad- In most cases, OSCC is asymptomatic, and pain ap- vanced stage of the disease. Nonetheless, a diagnosis of pears only when muscles or nerves are invaded in the ad- early OSCC with a presentation of just a white lesion, red vanced stages of the disease.10 The common symptoms of lesion, in-situ or micro-invasive carcinoma represents OSCC are a painless growth, painless ulcer, loosening of a real challenge for the oral diagnostician. The clinical teeth, exfoliation of teeth, discomfort, difficulty in swal- presentation of OSCC as a white lesion with an uneven lowing, etc. granular surface or red lesion with superficially eroded The most deadly aspect of oral cancer, like any other areas may be misdiagnosed as a premalignant lesion. The cancers, is its ability to spread, or metastasize. In OSCC, oral diagnostician should be aware of the initial carcino- the spread of tumor to regional or cervical lymph nodes matous changes that may take place in a premalignant le- take place by lymphatic route usually in a sequential man- sion, as they do not respond to local treatments. ner. About two-thirds of OSCC are already of substantial Oral cancer is a disease of increasing age, with an av- size and will have clinically detectable metastases to cer- erage age at diagnosis of about 60 years and usually the vical lymph nodes at the time of diagnosis.11 The metas- etiology is deleterious habits.3 The patients described in tases to regional lymph nodes can be ipsilateral, contra- the present article are less than 40 years of age but ac- lateral or bilateral. Ipsilateral metastases are frequently cording to the habit history given by them, the presence associated with early stage of tumor while bilateral is of- of adverse habits can be considered a probable cause for ten seen in advanced stage of disease, tumors of midline the development of cancer in them. Few previous studies and posterior part of oral cavity. The higher incidence of have reported about the occurrence of OSCC in a young- regional metastases at the time of diagnosis is noted in er age group (< 40), especially in high incidence countries OSCC involving the posterior areas of oral cavity. The tu- such as India, Pakistan and Sri Lanka.5,6 However, a num- mor spread is influenced by its size. Lesions classed as T1 ber of additional factors such as genetic susceptibility, vi- may show regional spread in 10 to 20% of cases, T2 lesions ral infection and hormone and immune modulation are in 25 to 30% of cases and T3 to T4 tumors in 50 to 75%.3 to be considered responsible for the occurrence of OSCC The presence of extracapsular lymph node spread is as- in young individuals, especially in females.7,8 According to sociated with a high rate of local and regional recurrence, Fabiana Vargas-Ferreira et al., nearly 20% of OSCC cases distant metastasis and mortality.11 Patients with metasta- have unknown etiology and thus it is important to investi- sis need more-aggressive treatments such as combination gate other possible factors associated with the occurrence of surgery and radiotherapy or combination of surgery of OSCC, enabling appropriate clinical management and and chemotherapy. It is therefore important to assess as monitoring.9 reliably as possible whether a patient has metastases or The location of the OSCC directly correlates with the not. etiological factors in a particular patient. In central India, Early diagnosis is a foremost step for reducing cancer a common site for the occurrence of OSCC is the gingi- mortality, but approximately 50% of cases are diagnosed vobuccal vestibule. But in Western countries, the tongue in the late stages (stages III or IV), either due to ignorance is the commonest site. These site-wise differences in the or the inaccessibility of medical care. The diagnostic delay incidence of oral cancer between Western countries and in OSCC can be considered in three categories:4,12,13 India may be due to a difference in the habit of tobacco 1. Patient delay or primary delay – a delay in the time usage. Tobacco smoking (cigarette) is more prevalent in from the onset of symptoms to the initial visit to a den- Western countries while tobacco chewing, smoking (bidi) tal or medical professional, and snuffing, along with other ingredients like betel nut, 2. Professional delay or secondary delay – the time be- Gutkha, lime, catechu, etc., are the most prevalent habits tween the visit to a dental or medical professional and in India. The first two cases described in this paper have a final diagnosis, that is histological confirmation of the shown similar presentation. Due to these major etiologi- disease, cal factors and the increasing incidence rate, it is suggest- 3. Patient and professional delay or total delay – the pe- ed that oral cancer in India should be considered a “new riod of time between the final diagnosis and the begin- epidemic”.4 ning of treatment. Dent Med Probl. 2017;54(1):85–89 89

The time period to consider as a delay in receiving Conclusions treatment ranges from 21 days to 3 months according to various studies.12 In the 1st case of the present article, The oral physician plays a vital role in the prevention there was a delay on the patient’s side, but the 3rd case can of oral cancer by inducing healthy life styles and detect- be considered a total delay, as the patient had reported to ing the potentially malignant conditions. They can reduce the local physician who probably could not do a correct oral cancer related morbidity and mortality by diagnos- diagnosis and thus resulted in a worsening of the disease. ing an early stage oral cancer. But, to achieve this goal, The overall information affirmed in this article points they should have in-depth knowledge about the clinical to the rising prevalence of oral cancer all over the world, aspects of oral cancer. The Indian oral cancer scenario is including India, which is attributable to diagnostic de- relatively different from other parts of the world in terms lays by both parties, the patient and the professional, and of its etiology, clinical presentation, sociology, economy thus prevention and diagnosis of early oral cancers be- and diagnostic delay. comes an area of great concern. References 1. Prasad LK. Burden of oral cancer: An Indian scenario. J Orofac Sci. Prevention and diagnosis 2014;6:77. 2. Waal VI, Bree DR, Brakenhoff R, Coebergh JW. Early diagnosis in of oral cancer primary oral cancer: Is it possible? Med Oral Patol Oral Cir Bucal. 2011;16:e300–305. 3. Epstein JB. Oral cancer. In: Burket’s Oral Medicine. Diagnosis and One of the methods for the prevention of oral cancer is treatment. 10th ed. Delhi, India: Harcourt Pvt Ltd;2003:194–234. to conduct a survey to evaluate the attitude of the popula- 4. Bolesina N, Femopase FL, Silvia A, Blanc L, Morelatto RA, Olmos MA. tion regarding addiction to various adverse habits and their Oral squamous cell carcinoma clinical aspects, oral cancer. InTech. knowledge about the causative role of habits in the devel- 2012. Available from: http://www.intechopen.com/books/oral- cancer/oral-squamouscell- carcinoma-clinical-aspects opment of oral cancer. With reference to this, programs 5. Warnakulasuriya S. Global epidemiology of oral and oropharyn- should be conducted to impart awareness amongst the geal cancer. Oral Oncol. 2009;45:309–316. population related to the harmful effects of adverse habits, 6. Effiom OA, Adeyemo WL, Omitola OG, Ajayi OF, Emmanuel MM, Gbotolorun OM. Oral squamous cell carcinoma: A clinicopatholog- and also periodic de-addiction programs should be carried ic review of 233 cases in Lagos, Nigeria. J Oral Maxillofac Surg. 2008; out especially for the rural public. Another cost-effective 66:1595–1599. and feasible method to reduce overall cancer prevalence is 7. Falaki F, Dalirsani Z, Pakfetrat A. Clinical and histopathological analysis of oral squamous cell carcinoma of young patients in Mashhad, to screen the population for early cancer and presence of Iran: A retrospective study and review of literatures. Med Oral Patol precancer or potentially malignant disease. Oral Cir Bucal. 2011;16:e473–477. Sankaranarayanan et al. have reported a sensitivity of 8. Soudry E, Preis M, Hod R. Squamous cell carcinoma of the oral 67.4% for a visual examination in detecting oral cancer in tongue in patients younger than 30 years: Clinicopathologic fea- 14 tures and outcome. Clin Otolaryngol. 2010;35:307–312. their study. Screenings should basically focus on the peo- 9. Fabiana VF, Nedel F, Etges A, Gomes APN, Furuse C, Tarquinio SBC. ple of the high risk group such as people having a history of Etiologic factors associated with oral squamous cell carcinoma in habit, immuno-compromised patients, elderly males, and non-smokers and non-alcoholic drinkers: A brief approach. Braz Dent J. 2012;23:586–590. people in a low socioeconomic group. Oral self-examina- 10. Chi AC. Epithelial pathology. In: Neville BW, Damm DD, Allen CM, tion can be helpful in detecting oral cancers early.12,13 Bouquot JE, ed. Oral & Maxillofacial Pathology. 2nd ed. Noida, India: Dentists are in a unique position to promote primary Elsevier; 2002:409–421. 11. Massano J, Regateiro FS, Januario G, Ferreira A. Oral squamous cell preventative measures to high risk groups, and to aid in carcinoma: Review of prognostic and predictive factors. Oral Surg the early diagnosis and referral of suspicious oral lesions. Oral Med Oral Pathol Oral Radiol Endod. 2006;102:67–76. There should be a policy to conduct regular continuing 12. Joshi P, Nair S, Chaturvedi P, Nair D, Agarwal JP, D’Cruz AK. Delay in seeking specialized care for oral cancers: Experience from a tertia- education programs for dentist, especially budding den- ry cancer center. Indian J Cancer. 2014;51:95–97. tists, to impart knowledge about the warning signs that 13. Kerdpon D, Sriplung H. Factors related to delay in diagnosis of will aid in the diagnosis of early oral cancer. oral squamous cell carcinoma in southern Thailand. Oral Oncol. Shwetha et al. have mentioned the objectives referring 2001;37:127–131. 14. Sankaranarayanan R, Ramadas K, Thara S, Muwonge R, Thomas G, to the early diagnosis of oral cancer and various compre- Anju G. Long term effect of visual screening on oral cancer inci- hensive diagnostic modalities that can be used for early dence and mortality in a randomized trial in Kerala, India. Oral detection of oral cancer like PCR, genomics and pro- Oncol. 2013;49:314–321. 15 15. Shwetha KN, Vanishri HC, Dominic A, Sowmya SV, Roopa RS. Recent teomics, microarrays, nanodiagnostics, etc. Also, they advances in diagnosis of oral cancer. JDOR 2016;12:19–21. have stated the limitations in performing these methods routinely. Last but not the least is that patients must be encouraged to visit their dentist regularly, which will help to increase the rate of early detection of oral cancer.

Clinical cases A dentigerous cyst in a patient treated for an odontogenic myxoma of the maxilla: A case report Torbiel zawiązkowa zęba u pacjenta leczonego z powodu śluzaka zębopochodnego szczęki – opis przypadku

Patrycja Proc1, A–D, Małgorzata Zubowska2, A–D, Anna Janas-Naze3, B, E

1 Department of Pediatric Dentistry, Medical University of Łodź, Łodź, Poland 2 Department of Pediatrics, Oncology, Hematology and Diabetology, Medical University of Łódź, Łodź, Poland 3 Department and Clinic of Oral Surgery, Medical University of Łodź, Łodź, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):91–95

Address for correspondence Abstract Patrycja Proc E-mail: [email protected] Tumors of the oral cavity are of various origins and can be signs of non-invasive cysts or malignant neoplasms. Funding sources none declared The paper describes the case of a 9-year-old boy with a tumor in the right side of the maxilla. Having been treated for an odontogenic myxoma at the age of 3, the patient was included in a national program assess- Conflict of interest ing the health of children who had undergone anticancer treatment. The boy remained under oncological none declared supervision, and the tumor was found again in the same region a few years later. It was diagnosed as a dentigerous cyst and surgically excised. In addition, when the patient was 9 several changes in dentition Received on September 11, 2016 Revised on September 22, 2016 were found that were typical following anticancer therapy: no tooth germs were observed for teeth 13, 35 Accepted on September 30, 2016 and 45, and microdontic teeth 25 and 47 were noted. These changes could be attributed to the chemotherapy performed in early childhood. Tumors appearing in the oral cavity always require an in-depth assessment of their nature and origin. Chemotherapy elicits late complications in tooth development in children. Key words: child, myxoma, dentigerous cyst Słowa kluczowe: dziecko, śluzak zębopochodny, torbiel zawiązkowa

DOI 10.17219/dmp/65514

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 92 P. Proc, M. Zubowska, A. Janas-Naze. An odontogenic cyst in a cancer patient

A cyst is defined as a pathological space within soft tis- CWS protocol. By the time the diagnosis was verified, sues or bones that contains a liquid and is lined with an 3 full cycles of chemotherapy had been completed. After epithelial lining. The most common odontogenic cysts gaining a final histopathological diagnosis from the in- are radicular cysts (62%), dentigerous cysts (31%) and pri- ternational Sarcoma Coordinator for Cancer Treatment, mordial cysts (3%). They are more common in the man- the diagnosis was changed from sarcoma to myxoma, and dible (52% of cases) than in the maxilla (46% of cases), the invasive treatment was suspended. The boy remained with the remaining cases (2%) found in both jaws.1 In an under observation by the Clinic of Oncology with regular analysis of the incidence of cysts among patients treated magnetic resonance imaging (MRI) examinations; no sign between 1996 and 1999 in the Department of Dental Sur- of relapse was found in the right maxillary sinus. gery in Warszawa, Kozarzewska et al. found 340 such cas- A few days before the January 2015 visit, the patient, now es, 174 (51.2%) in women and 166 (48.8%) in men, with aged 9, had reported a change in the shape of the alveo- developmental cysts in 9.5% of them.2 lar process of the upper right side of the maxilla. An MRI Kramer and Pindborg propose that dentigerous cysts was performed in the Clinic of Oncology using T1/T2- are epithelial odontogenic cysts that arose from the dental -weighted imaging with a Fast Spin Echo (FSE) sequence, lamina following disturbances in the process of odonto- a T1-weighted FLAIR sequence with fat suppressed (FS) genesis.3 They are accompanied by impacted, embedded and a T1-weighted FS sequence following intravenous in- or otherwise unerupted teeth.4,5 The cysts may have an fusion of the contrast medium. The MRI revealed no re- inflammatory origin from a source such as periapical in- lapse of myxoma, and showed that the paranasal sinuses flammation from non-vital teeth.6 They also appear dur- were also free from changes. However, in the region of ing the course of some genetic disorders, such as Gorlin tooth 12, a 11 × 6 mm tumor was noticed with no inflam- syndrome or cleidocranial dysplasia.5,7 matory changes in the surrounding bone (Fig. 1). Digital The clinical symptoms of dentigerous cysts include palpation indicated that the submandibular and cervical expansion of dento-alveolar bone, facial asymmetry, di- lymph nodes were not enlarged, and that a small polyp of vergence of adjacent tooth roots, dislocation of teeth, mucous membrane, about 7 mm in diameter, with no neo- disturbances in teething, malocclusion or local inflamma- plastic traits, was present in the apex of the left maxillary sition.2,5,9 The cysts are typically found accidentally during nus. The polyp had been visible during earlier MR imaging. routine radiographic examinations as well-defined uni- An initial diagnosis of odontogenic cyst was made, and locular or multilocular radiolucent lesions.8 the patient was directed to the Department of Pediatric The treatment of cysts is surgical. According to tra- Dentistry of the Medical University of Łódź for further ditional terminology, Partch I refers to total excision of diagnosis and treatment. the cyst with its follicle and the tooth germ inside, while The patient was admitted to the Department of Pediatric Partch II refers to a 2-step method of marsupialization Dentistry for an urgent procedure in February 2015. A clin- or cystotomy.8 In cases of larger lesions, several modifi- ical investigation revealed the presence of a non-painful cations can be used, mostly based on decompression by fenestration of the tumor, leading to a gradual reduction of the cyst before its final excision.4 While the prognosis for surgical treatment is good, a cyst can recur if many epithelial cells remain. During surgery, the tooth germ is also removed from inside the cyst. A lack of treatment can lead to bone perforation or metaplasia of the cyst to the neoplasm.9–12

Case report

In January 2015, a 9-year-old boy (F.T.) was admitted to the Clinic of Pediatrics, Oncology, Hematology and Diabetology at the Medical University of Łodź (Po- land). He had been under regular supervision since 2009 as part of a national program supported by the National Health Ministry assessing the health of children following anticancer treatment. In 2009, at the age of 3, the boy was treated for a tumor of the right maxillary sinus. The tumor was totally excised in July 2009; the initial histopathological diagnosis of rhabdomyosarcoma led to a recommendation of chemotherapy according to the Fig. 1. CT of the head of the 9-year-old boy Dent Med Probl. 2017;54(1):91–95 93

Fig. 2. Intraoral view of the tumor in the nine-year-old boy Fig. 4. Intraoral view of the nine-year-old boy’s dentition two months after surgery

Fig. 3. Panoramic radiograph taken before treatment of the nine-year-old Fig. 5. Panoramic radiograph taken two months after treatment of the boy: cyst with the crown of tooth 12 on the right side nine-year-old boy; the absence of tooth germs for teeth 13, 35 and 45 and microdontic teeth 25 and 47 can be noted

tumor with unchanged mucous membrane in the region of cancer treatment. The inflammatory condition caused by teeth 52, 53 and 54 (Fig. 2). The teeth were not tender to the tumor, or mechanical damage to the dentigerous lam- percussion, and the reaction of their pulp was correct. In ina connected with surgery, may have initiated the cyst. addition, a retained tooth 52 was noticed, while permanent On the other hand, several studies have reported a con- tooth 22 had already fully erupted on the opposite side of nection between the occurrence of odontogenic cysts and the arch. A panoramic radiograph was performed, and an neoplasms, and various authors have noted that lesions impacted tooth 12 was observed inside the tumor (Fig. 3); which appear as dentigerous cysts may have a compo- the root of tooth 11 was displaced. On the basis of the ra- nent of ameloblastic changes in their lining.9,13,14 Mucus- diograph, a dentigerous cyst was diagnosed (cystis follicu- secreting cells or even a mucoepidermoid carcinoma may laris). The patient was directed to the Department of Oral arise in the wall of a cyst.8 It has also been documented Surgery of the Medical University of Łódź, where the cyst that a dentigerous cyst may transform, or be a predictor was excised. During the procedure, teeth 52, 53, 54 and 12 of odontogenic keratocysts in later years.8,15 These obser- were removed under general anesthesia (Figs. 4 and 5). The vations might indicate that a connection exists between histopathological results confirmed the clinical diagnosis. various pathological processes which share similar origins The radiograph also revealed several dental anomalies. in the same part of the bone. The dentition lacked germs for teeth 13, 35 and 45, and In the present case, the decision to perform total enucle- microdontic teeth 25 and 47 were found. ation of the dentigerous cyst followed a heated discussion in which the authors compared the use of total incision with a 2-stage treatment. The 2-stage treatment seemed Discussion to be more favorable, as many studies stress the advantag- es of more conservative treatment, preserving the tooth The occurrence of a dentigerous cyst in the same re- inside the cyst, especially in patients of developmental gion as a neoplasm may suggest that the presence of the age.1,4 In addition, the patient already lacked a few teeth, neoplasm is related to the inception of the cyst following including an adjacent upper canine. However, in the light 94 P. Proc, M. Zubowska, A. Janas-Naze. An odontogenic cyst in a cancer patient

of the aforementioned link between different pathological family members excluded this possibility. The etiology of processes and the fact that the boy had already suffered microdontic teeth is not well evidenced; however, micro- from cancer, it was decided to remove all the cells of the dontia is believed to be mostly caused by harmful factors cyst by more invasive treatment. It should be noted that disturbing odontogenesis.23 The patient in the present the diagnosis was not certain until the histopathological study had received anticancer treatment at the age of 3, verification. which is known to be a critical age for the development The odontogenic myxoma (OM) found in the patient at of premolar and second molar teeth. While microdontic the age of 3 is a benign neoplasm that represents around premolars are most often found in patients treated within 3–6% of all odontogenic tumors. It can be locally invasive the age range of 19–24 months, the 31–42 month period and can be found in both jaws with similar incidence.10,12,16 is also known to be one of increased risk for premolars.23 It originates from odontogenic ectomesenchyme or un- Microdontic second molars are most often found in pa- differentiated mesenchymal cells in the periodontal liga- tients treated in the 31–36 month age range, which in- ment.8 In a Polish population, Stypulkowska found myx- cludes the age at which the patient in this study under- oma to be present more commonly in the mandible than went chemotherapy. the maxilla, and more frequently in males than females (1 : 0.7).17 The majority of cases are found in the second or third decades of life, but are also occasionally found in Conclusions those below the age of 10 (5–7% of cases).8,18 While the initial recognition of the tumor is mostly based on radio- Tumors appearing in the oral cavity always require an graphs, this is followed by computer tomography (CT) or in-depth assessment of their nature and origin. MRI. The final diagnosis is based on histological results. Chemotherapy elicits late complications in tooth devel- McDonald-Jankowski et al. reported that the likelihood opment in children. of perforation and the pattern of the septa in the myxoma are better displayed by CT, while the tooth displacement References and root resorption are more reliably observed on con- 1. Pawlak W, Kubasiewicz-Ross P, Pałka Ł, Zarzycki R. Cystic lesions of ventional radiographs.19 the jaws treated surgically in the Department of Maxillofacial Sur- In the present case, both tumors were initially diagnosed gery Wroclaw Medical University in the years 2004–2007. Dent Med Probl. 2009;46:49–53 [in Polish]. by MRI. In the case of the cyst, a relapse of myxoma was 2. Kozarzewska M, Popowski W, Wojtowicz A. Epidemiological anal- excluded during MR imaging. However, the dentigerous ysis of dentigerous cysts in material of Oral Surgery Department cyst with a tooth inside was visible only in a conventional Medical University of Warsaw by years 1996–1999. Nowa Stomatol. 2001;6:2, 15–18 [in Polish]. radiograph. It is difficult to distinguish odontogenic myx- 3. Kramer IRH, Pindborg JJ, Shear M. The WHO histological typing omas from similar tumors, and a number of diagnostic er- of odontogenic tumorous. A commentary on the second edition. rors have been described.20 Myxomas might be mistaken Cancer 1992;70:2988–2994. 4. Sobczak-Zagalska H, Emerich K. Dentigerous cyst – case reports and for dentigerous inflammation or a malignant neoplasm; proposed treatment. Magazyn Stomatol. 2015;25:1, 31–37 [in Polish]. for example, Basile and Lin described a case of odontogen- 5. Puacz P, Koczorowski M, Kaczmarek I, Osmola K. Dentigerous cyst ic myxoma mimicking a fibro-osseous process.21 On the associated with maxillary canine as a reason of occlusion defect. other hand, Kali et al. reported a gnathic desmoplastic fi- Dev Period Med. 2013;1:72–76 [in Polish]. 22 6. Benn A, Altini M. Dentigerous cysts of inflammatory origin. A clin- broma mimicking a dentigerous cyst. icopathologic study. Oral Surg Oral Med Oral Pathol Oral Radiol The patient described in the present study had received Endod. 1996;81:203–209. 3 rounds of chemotherapy before the final, more favorable 7. Błochowiak K, Pluskota J, Grajewski S, Sokalski J. Rare case of a huge odontogenic cyst of the mandible. Dent Forum 2013;41:144–49 [in diagnosis of the tumor was made, and several dental anom- Polish]. alies were found in the panoramic radiograph taken a few 8. Mc Donald RE. Tumors of the oral soft tissues and cysts and tumors years after anticancer treatment. The missing upper right of the bone. [In:] Dentistry for the Child and Adolescent. Eds.: Dean JA, Avery DR, Mc Donald RE. Mosby, Elsevier, 2011, 135–141. canine (tooth 13) was probably a complication of myxoma 9. Ratajczyk M, Sowa W, Walter A. Molecular basis for formation of the excision from the upper right sinus. However, the lack of odontogenic inflammatory cysts – review of literature. Dent Med premolars 35 and 45 and the microdontia of teeth 25 and Probl. 2010;47:496–501 [in Polish]. 10. Aquillino RN, Tuji FM, Eid LM, Molina OF, Joo HY, Net FH. Odonto- 47, not directly connected with the site of the tumor, might genic myxoma in the maxilla: A case report and characteristic on have been a complication of chemotherapy. In an examina- CT and MR. Oral Oncol. 2006;42:133–136. tion of the impact of chemotherapy on the incidence of den- 11. Borgiel-Marek H, Jędrusik-Pawłowska M, Drugacz J, Malara P, tal anomalies like hypodontia, microdontia or short roots, Wodołażski A, Mazur M. Myxoma of the maxilla and mandible – a report of two cases and literature review. Czas Stomatol. Proc et al. noted a significantly higher incidence of missing 2005;56:667–672 [in Polish]. teeth in patients who had undergone chemotherapy in early 12. Tkaczuk AT, Bhatti M, Caccamese JF, Ord RA, Pereira KD. Cystic childhood than in the controls (31.14% vs 9.21%), as well as lesion of the jaw in children. JAMA Otolaryngol Head Neck Surg. 23 2015;141:834–839. a greater incidence of microdontic teeth (36.06% vs 2.87%). 13. Cankurtaran C, Branstetter BF, Chiosea SI, Barnes EL Jr: Ameloblas- Although hypodontia is most often attributed to genet- toma and dentigerous cyst associated with impacted mandibular ics, in the present case an interview with the immediate third molar tooth. Radio Graphics 2010;30:1415–1420. Dent Med Probl. 2017;54(1):91–95 95

14. Mc Millan MD, Smillie AC. Ameloblastomas associated with dentig- 19. MacDonald-Jankowski DS, Yeung RW, Li T, Lee KM. Computed erous cysts. Oral Surg. 1981;51:489–496. tomography of odontogenic myxoma. Clin Radiol. 2004;59:281–287. 15. Tsukamoto G, Sasaki A, Akiyama T, Ishikawa T, Kishimoto K, Nishiya- 20. Gupta P, Jawanda K, Narula R, Singh J. Inflammatory dentigerous ma A, Matsumura T. A radiologic analysis of dentigerous cysts and cyst mimicking a periapical cyst. J Int Clinic Dent Res Org. 2016;8: odontogenic keratocysts associated with a mandibular third molar. 63–66. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001;91:743–747. 21. Basile JR, Lin YLA. Case of odontogenic myxoma with unusual his- 16. Singaraju S, Wanjari SP, Parwani RN. Odontogenic myxoma of the tological features mimicking a fibro-osseous process. Head Neck maxilla: A report of a rare case and review of the literature. J Oral Pathol. 2010;4:253–256. Maxillofac Pathol. 2010;14:19–23. 22. Kalia V, Kaur S, Vashisht D. Gnathic desmoplastic fibroma mimick- 17. Stypulkowska J. Odontogenic tumors and neoplastic-like changes ing a dentigerous cyst: A case report J Maxillofac Oral Surg. 2015;14 of the jaw bone: Clinical study and evaluation of treatment results. (Suppl 1):150–153. Folia Medica Cracov. 1998;39:135–141 [in Polish]. 23. Proc P, Szczepańska J, Skiba A, Zubowska M, Fendler W, Młynarski 18. Noffke CE, Raubenheimer EJ, Chabikuli NJ, Bouckaert MM. Odon- W. Dental anomalies as late adverse effect among young children togenic myxoma: Review of the literature and report of 30 cases treated from cancer. Cancer Res Treat. 2016;48: 658–667. from South Africa. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104:101–109.

Clinical cases Reccurent peripheral giant cell granuloma: A case report Nawrotowy nadziąślak olbrzymiokomórkowy – opis przypadku

Kamakshi L. N. V. AlekhyaD, David KadakampallyF

Manipal College of Dental Sciences, Mangaluru, Karnataka, India

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):97–100

Address for correspondence Abstract David Kadakampally E-mail: [email protected] Peripheral giant cell granuloma is an inflammatory hyperplastic lesion that commonly occurs on peripheral tissues like gingiva, periodontal ligaments or alveolar mucosa. Clinically it is only seen in gingiva, particu- Funding sources none declared larly between the first permanent molars and incisors. It manifests itself as a benign tumor consisting of multinucleated giant cells. Conflict of interest This article reports a case of peripheral giant cell granuloma in the left mandibular premolar region in none declared a 34-year-old man. The lesion was excised and sent for histopathological examination, and was diagnosed as peripheral giant cell granuloma. The lesion was recurrent. This case report shows the importance of Received on October 1, 2016 Revised on October 24, 2016 confirming the diagnosis of the lesion by histopathological examination. Peripheral giant cell granuloma Accepted on November 4, 2016 is a reactive lesion that shows a rapid growth rate and can cause minor tooth movement. As the name suggests, there is no bony involvement and the enlargement is a soft tissue extension. Early conservative management will reduce the risk of tooth loss. Key words: peripheral giant cell granuloma, multinucleated giant cells, local trauma Słowa kluczowe: nawrotowy nadziąślak olbrzymiokomórkowy, wielojądrowe komórki olbrzymie, uraz miejscowy

DOI 10.17219/dmp/66759

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 98 K. Alekhya, D. Kadakampally. Recurrent peripheral giant cell granuloma

Peripheral giant cell granuloma (PGCG) is among the benign tumors of peripheral origin. It is also referred to as giant cell epulis, peripheral giant cell tumor, osteo- clastoma, giant cell hyperplasia or giant cell reparative granuloma. It is an inflammatory hyperplastic lesion that commonly occurs on peripheral tissues like gingiva, periodontal ligaments or alveolar mucosa. As the name indicates, it does not represent a true neoplasm, but rather a reactive hyperplastic lesion secondary to local trauma or irritation. The exact etiology is, however, unknown.1 Clinically PGCG is only seen in gingiva, particularly between the first permanent molars and incisors; it presents as a smooth surface, either sessile or pedunculated, bluish red in color. It is asymptomatic, seen as red mass of gingiva composed of fibroblasts and multinucleated giant cells with more nuclei and amorphilic cytoplasm. The giant cells Fig. 1. Pre-operative image showing the intra-oral lesion appear to be non-functional in terms of phagocytosis and bone resorption. When it occurs in edentulous areas (which is rare) it produces a cup-shaped radiolucency. It occurs in all age groups, but more commonly in 30- to 40-year-old patients; females have a greater predilection than males. It cannot be clinically separated from pyogenic granuloma.2,3

Case report

A systemically healthy 34-year-old male patient presented with a chief complaint of swelling in the lower left back region for 6 months. His history revealed that the swelling started after chewing on a fish bone 6 months previously and started increasing in size, gradually attain- ing the present size. There was occasional bleeding from the lesion while brushing. The patient was asymptomatic. Extra-oral swelling was not seen. On intra-oral examination, an intra-oral swelling was present in the lower left back region, which is illustrated in Fig. 2. Post-operative image after excision of the lesion Fig. 1. A swelling measuring 3 × 2 cm was seen adjacent to tooth number 21 (universal tooth numbering system). It was reddish pink in color, with a firm consistency, well defined and non-fluctuant; it was tender on palpation extending A routine histological examination with hematoxylin re- along both the buccal and lingual sides of the same tooth. vealed the presence of areas of multinucleated giant cells The tooth was vital; it was slightly mobile, but there was no with 6 to 8 nuclei and amorphilic cytoplasm in a back- evidence of endodontic pathology associated with it. ground of plump ovoid and spindle shaped mesenchymal A radiological examination revealed horizontal bone cells. Deposition of hemosiderin pigments along with colla- loss at tooth 21 but no evidence of bony involvement. gen fibers intermixed with chronic inflammatory cell infil- Routine blood tests including a complete hemogram, trate (chiefly lymphocytes and plasma cells), blood vessels bleeding time and clotting time and erythrocyte sedimen- engorged with RBCs and areas of hemorrhage were also tation rate (ESR) were found to be normal. seen. The zone of giant cell proliferation was delineated from the overlying hyperplastic parakeratinized stratified squamous epithelium by a zone of normal lamina propria. Treatment of the lesion The histological picture is shown in Fig. 3. The diagnosis was suggestive of peripheral giant cell Scaling and root debridement were performed as Phase I granuloma. A characteristic feature of PGCG is recur- therapy. The patient was recalled after one week for a re- rence, which is seen in 5–11% of cases.4 Recurrence of evaluation. The lesion was excised under local anesthesia peripheral giant cell granuloma was observed in the pres- (Fig. 2) and sent for histopathological examination. ent case after 3 months. Dent Med Probl. 2017;54(1):97–100 99

tein-1 (MCP1), osteoclast differentiation factor (ODF) and macrophage-colony stimulating factor (M-CSF), are monocyte chemo attractants and are essential for osteoclast differentiation. This suggests that the stromal cells stimulate the immigration of monocytes from the blood into the tumor tissue and enhance their fusion into osteoclast-like, multinucleated giant cells.2 As Abe et al. wrote, “the recently identified membrane-bound protein family, a disintegrin and metalloprotease (ADAM), is considered to play a role in the multinucleation of osteoclasts and macrophage-derived giant cells from mononuclear pre- Fig. 3. Histological picture showing multinucleated giant cells and foci of cursor cells”.10 hemorrhage There are no pathognomic clinical features that differ- entiate the peripheral giant cell granuloma from pyogenic granuloma, peripheral ossifying fibroma or giant cell fibroma. Along with clinical examinations, radiographic Discussion and histological examinations are needed to confirm the diagnosis. 11–13 Peripheral giant cell granuloma is the most common lesion in both jaws. The etiology of PGCG is still not clear. The literature indicates that PGCG has a female predilec- Conclusions tion, although the present case report concerns peripheral giant cell granuloma in a male patient, which is similar Even though the etiology is unclear, poor oral hygiene to the study by Bhaskar et al.5 could be a predisposing factor in PGCG. Early diagnosis Radiographic features in an edentulous area include and conservative management is important in such le- cup-shaped resorption of alveolar bone that is called sions, since they can become more destructive over time. a “levelling effect”; and in a dentate region there will be Peripheral giant cell granuloma can manifest as gingi- widening of the periodontal ligament space and resorp- val enlargement, which is a reactive lesion with a rapid tion of the alveolar crest in the interdental region.6 growth rate and involvement of soft tissue above under- Bischof et al. reported a case of peripheral giant cell lying bone, without any central bony lesion. This could granuloma associated with implants.7 cause minor to moderate tooth movement because of The observed recurrence of this lesion is from 5% to 11%. resorption of underlying alveolar bone. Therefore, early In the present case, recurrence was seen after 6 months, management of these lesions can prevent the risk of tooth which coincides with a case report by Prabhat.8 To pre- loss. vent recurrence, the excision of the lesion should be performed down to the periosteum. In the present case, total References excision and complete removal of the remnants of the le- 1. Rodrigues SV, Mitra DK, Pawar SD, Vijayakar HN. Peripheral giant sion was advised to prevent recurrence. cell granuloma: This enormity is a rarity. J Indian Soc Periodontol. Rodrigues et al. reported that the presence of lesions 2015;19:466–469. may cause mobility or displacement of neighboring 2. Willing M, Engels C, Jesse N, Werner M, Delling G, Kaiser E. The 1 nature of giant cell tumor of bone. J Cancer Res Clin Oncol. 2001;127: teeth. In the present case, increased mobility of the tooth 467–474. was noted after excision of the lesion. It was painless and 3. Agarwal A, Prasad UC, Jithendra KD. Peripheral giant cell granulo- it did not interfere with occlusion, hence it was not af- ma: A case report and review of literature. Guident.net/periodontics. 2011,16. fected by traumatic forces. Rodrigues et al. also stated that 4. Khan KP, Gokhale ST, Manjunath RGS, Bhattacharya HS. Recurrent the consistency of a PGCG lesion depends on its age: with peripheral giant cell granuloma – a rare case report. Indian J Dent time, there is an increase in collagen fibers, so a mature Sci. 2014;6:50–52. 1 5. Bhaskar SN, Cutright DE, Beasley JD, Perez B. Giant cell reparative lesion is firm in consistency. In the present case, the con- granuloma (peripheral): Report of 50 cases. J Oral Surg. 1971;29: sistency was firm. 110 –115. El Mofty et al. stated that these giant cells are derived 6. Flaitz CM. Peripheral giant cell granuloma: A potentially aggressive from bone marrow mononuclear cells and are present lesion in children. Pediatr Dent. 2000;22:232–233. 7. Bischof M, Nedir R, Lombardi T. Peripheral giant cell granuloma in the stroma only in response to an unknown stimu- associated with a dental implant. Int J Oral Maxillofac Impl. 2004;19: lus.9 The giant cells are short-lived and disappear early in 295–299. cultures, in contrast to the stromal cells, which show ac- 8. Prabhat. MPV. Recurrent peripheral giant cell granuloma of the gin- 9 giva – a case report. Ann Essenc Dent. 2010;2:65– 67. tive proliferation. 9. Ei-Mofty SK, Osbody P. Growth behavior and lineage of isolated Willing et al. reported that factors that are secreted by and cultured cells derived from giant cell granuloma of the mandi- stromal cells, such as monocyte chemo attractant pro- ble. J Oral Pathol. 1985;14:539–552. 100 K. Alekhya, D. Kadakampally. Recurrent peripheral giant cell granuloma

10. Abe E, Mocharla H, Yamate T, Taguchi Y, Monolages SC. Meltrin- 12. Sahingur SE, Cohen RE, Aguirre A. Esthetic management of periph- alpha, a fusion protein involved in multinucleated giant cell and eral giant cell granuloma. J Periodontol. 2004;75:487–492. osteoclast formation. Calcified Tissue Internat. 1999;64:508–515. 13. Ghimire N, Nepal P, Ghimire N. Peripheral giant cell granuloma: 11. Adlakha VK, Chandna P, Rehani U, Rana V, Malik W. Peripheral giant A case report. J Chitwan Medical College 2013;3:28–30. cell granuloma. J Indian Soc Pedodont Prevent Dent. 2010;4:293–296. Clinical cases Laser instant implant impression method: A case presentation Metoda wycisku w implantacji natychmiastowej z użyciem lasera (LIIIM) – prezentacja przypadku

Jacek Matys1–3, A–D, Katarzyna Świder3, D, Rafał Flieger4, D, E

1 Department of Dental Surgery, Wroclaw Medical University, Wrocław, Poland 2 Student of the Master in Laser Dentistry of Sapienza University of Rome, Italy 3 Private Practice, Wschowa, Poland 4 Private Dental Healthcare, Kościan, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):101–106

Address for correspondence Abstract Jacek Matys E-mail: [email protected] Dental impressions are mainly used to record the geometry of hard and soft tissue and the relations between teeth and the adjacent tissues. In implantology, precise implant impressions are necessary to obtain the best Funding sources none declared possible detailed reproduction of the implant site and the passive intraoral fit of the implant framework. However, ensuring those necessities in the interdisciplinary treatment of orthodontic patients requires re- Conflict of interest vised impression techniques and materials. In this study a modified one-stage putty-wash pick-up implant none declared impression procedure was used, incorporating the use of two additional silicone materials and modeling wax. Additionally, an Er:YAG laser was used to obtain a better emergence profile for implant restorations and Received on September 1, 2016 an immediate impression, which shortened the prosthodontic stage in patients undergoing orthodontic Revised on October 24, 2016 treatment. The technique described here for taking the impression and creating the emergence profile offers Accepted on October 26, 2016 dental practitioners additional options in implantoprosthodontic treatment of orthodontic patients, as the method is characterized by simple preparation and satisfactory implant site reproduction. Key words: dental implants, orthodontic treatment, Er:YAG laser, prosthetic impression, laser surgery Słowa kluczowe: implanty stomatologiczne, leczenie ortodontyczne, laser Er:YAG, wycisk protetyczny, chirurgia laserowa

DOI 10.17219/dmp/66363

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 102 J. Matys, K. Świder, R. Flieger. Laser instant implant impression method

The use of endosseous titanium implants has been suc- adjusted regularly.15 Azer combined the method of using cessfully implemented in the treatment of patients with a rotary instrument to reshape the stone cast with the use edentulism of various extents.1–3 Nowadays, implants are of a provisional autopolymerizing resin crown that was extensively used in several disciplines of dentistry. Pa- gradually built up each week by adding more resin to the tients affected with malocclusion and partial edentulism external gingival contours.17 frequently insist on being treated as quickly as possible. One technique that offers the possibility of executing Therefore, an interdisciplinary approach and precise plan- the impression immediately after implant exposure is the ning are needed to obtain satisfactory results. Orthodon- use of the Er:YAG laser, widely employed in surgical pro- tic treatment can contribute to the successful use of im- cedures. Identifying the patients’ periodontal biotype is plants through vertical development of the peri-implant fundamental to the optimal planning of therapeutic man- site (using tooth extrusion) and the creation of space for agement, especially in implantology.18 Matys et al. pro- implant restorations.1 In addition, osseointegrated dental posed the use of erbium lasers only in cases with sufficient implants have been used for a variety of purposes in or- keratinized tissue thickness.19 Hence, when the attached thodontics. The placement of dental implants can provide gingiva around the implants are insufficiently thick, the a good quality of anchorage control, as well as a method implants should be covered with subepithelial connective to reposition the natural teeth.1–3 tissue grafts (SCTG) or free gingival grafts (FGG).20 However, interdisciplinary treatment can entail some To the best of the present authors’ knowledge, the laser difficulties. If the implant placement takes place during instant implant impression method (LIIIM) developed by orthodontic treatment and before its finalization, a sat- the authors has not previously been described in litera- isfactory impression is hard to obtain. Elements of orth- ture. The method incorporates the use of two silicone im- odontic appliances (wires, brackets, bands) can trap and pression materials and a modeling wax strip as block-out damage the impression material. Usually the wires can be material for orthodontic brackets. An optimal emergence pulled out without problems prior to taking the impres- profile is obtained with the direct use of an Er:YAG laser. sion, but removing brackets would be time-consuming and could disturb the treatment process. To overcome this problem, clinicians have come up with different methods Case presentation to facilitate impressions of orthodontically banded teeth. The most widely used method is to cover the orthodon- A 20-year-old female patient was referred to one au- tic brackets. Consequently, when the impression tray is thor’s private practice (in Wschowa, Poland) from a gen- removed the material tearing is minimized, or even elim- eral dentist, with the aim of restoring her missing teeth inated in some cases. Maeda et al. proposed the use of 12 and 22 (FDI notation system used), in which the germs a tube as block-out material for orthodontic brackets and had been missing from birth due to hereditary agenesis. It arch wire while taking the impression for the production was decided that implantation would be the best course of a mouthguard.4 Rilo et al. suggested using small por- of action; however, as the patient wished to align her tions of utility wax; Croll and Castaldi proposed strips of teeth in the process, she was referred to an orthodontist utility wax; while Lorton recommended the use of strips of for assessment. Complete fixed orthodontic treatment occlusal indicator wax compressed over bonded brackets was planned for the correction of crowding and a lack prior to alginate impression.5–7 Sukotjo and Bocage pro- of space for future implants 12 and 22. The tooth align- posed the use of an implant surgical template.8 However, ment process meant that implant treatment would have all of these procedures involved the use of irreversible hy- to be staged. Six months before the planned termination drocoloid as impression material, which cannot yield sat- of the orthodontic treatment, two implants (Superline, isfactory impression results for implant procedures. Dentium, Suwon, Korea), 4.0 mm in diameter and 10 Another challenge the clinician can encounter dur- mm in length, were inserted under local infiltrative anes- ing implant-supported restoration treatment of an orth- thesia with articaine hydrochloride 4% plus epinephrine odontic patient is the emergence profile. Multiple meth- 1:100000 (Orablock , Pierrel Group, Capua, Italy) and ods have been described that utilize direct, indirect or cover screws were fitted® immediately. combined techniques.9 Tarlow, as well as Macintosh and After half a year, during which the adjacent bone Sutherland, formed the emergence profile on the master healed, the patient came back to continue her implanto- cast by trimming or burring the overabundance of the soft prosthodontic treatment. However, it is difficult to obtain tissue substitute before the final crown framework was accurate impressions before the completion of orthodon- made.10,11 Reike suggested surgically repositioning a split tic treatment, since (as noted earlier) the brackets of orth- flap and overcontouring the soft tissue around the healing odontic devices trap and tear the impression material. To abutment.12 Other methods incorporate the use of interim bypass these problems, a modified one-stage putty-wash restorations made of an autopolymerizing resin or direct pick-up impression technique was used, with open tray composite.13–17 Ntounis and Petropoulou proposed the (direct) procedure and an application of modeling wax for use of a screw-retained provisional restoration that was undercut coverage. Dent Med Probl. 2017;54(1):101–106 103

Fig. 1. Implants exposure and emergence profile was aquired using the Fig. 3. Placement of the implant transfers Er:YAG LiteTouch™ laser

Prior to taking the impression, the orthodontic upper arch-wire was removed. To shorten the time of final crown cementation, the implants were exposed using an Er:YAG LiteTouch™ laser (Syneron™ Dental Lasers, Syneron Medi- cal Ltd., Yokneam, Israel) (Fig. 1) with the following settings: pulse energy 300 mJ, pulse frequency 18 Hz, energy density per pulse 38.2 J/cm2, mode for soft tissue (ST), cooling spray 5 mL/min, angle of the working tip 70o, size of the tip 1.0 × 17 mm, distance from the soft tissue 2 mm. The use of the laser allowed fast homeostasis of the wound. An immediate impression for the final prosthodontic restoration was possible thanks to the lack of postoperative bleeding. Addi- tionally, the use of the Er:YAG laser resulted in an emergence profile without any visible thermal damage (Fig. 2). After this, direct transfer abutments were screwed onto Fig. 4. View of the custom tray adjustments – inner side the implants (Fig. 3). To facilitate access to the implant transfer, the open tray method was used; a custom impression tray was perforated (before the impression was taken, the hole was adjusted to line up with the position of the transfer) (Fig. 4). The undercuts around the brackets were blocked with a strip of Vertex™ Modelling wax (Vertex-Dental, Soesterberg, The Netherlands); the material was heated to obtain the necessary shape and then folded three times (Fig. 5). It is very important to leave the space near the implants and adjacent teeth free to allow the impression material to enter. Light-bodied addition silicone material (Variotime Medium Flow, Heraeus Kulzer, Hanau, Germany) was placed® around the implant with an injection tip. At the same time, putty-bodied addition silicone material (Variotime Dynamix Monophase, Heraeus Kulzer, Hanau, Germany)® was loaded onto the tray by a dental assistant, using the Variotime Dynamix Speed System (Heraeus Kulzer, Hanau, Germany). This® allowed a full-arch impression with the transfer screws protruding through the tray (Fig. 6). Subsequently, with the tray still in place, the retaining screws were removed. In consequence, when the tray was taken out of the pa- Fig. 2. Intraoral view of the emergence profile of the implant in position 22 tient’s mouth (using a swaying motion), the transfers 104 J. Matys, K. Świder, R. Flieger. Laser instant implant impression method

Fig. 5. The under cuts around the orthodontic brackets are blocket using Fig. 7. Close-up of the implant analogs in impression material the modeling wax strips – patient’s right side view

Fig. 6. View of the impression with the transfer screws protruded through Fig. 8. Implant analog in position 22 the tray

were captured in the impression material. The presence of the wax prevented the impression material from tearing, and its thickness and ductility allowed easier tray removal. The implant analogs were then connected to the transfers in the impression material (Fig. 7–9). After the impressions were taken, temporary healing screws were placed onto the implants (Fig. 10). Healing screws with a diameter matching the implant emergence profile made with the laser were used, and after 7 hours the final screw- retained crowns were made by a dental laboratory and ce- mented onto the implants (Fig. 11).

Discussion Fig. 9. Implant analog in position 12 Implant impressions during fully-banded orthodontic treatment can cause many difficulties for dental practitioners, as elements of the orthodontic appliances (brack- Dent Med Probl. 2017;54(1):101–106 105

of the material, whereas Croll and Castaldi suggested using strips.5,6 Forming small portions of wax takes a little more time than the use of strips. The method proposed by the current authors incorporates the best of both of these techniques: folded strips of modeling wax are a faster and cheaper solution. Additionally, the thickness of the folded strip of wax allows simple tray removal even when using rigid A-silicone material. The properties of the impression material (rigidity, accuracy) can influence the accuracy of the implant impression, cast and framework.21 The most frequently applied material for implant impressions is polyether; however, studies have shown that the use of A-silicon, as in the current study, yields comparable accuracy.21 The use of two A-silicone materials allows improved dimensional accu- Fig. 10. Intraoral view of interim healing screws racy and less deformation22, compared to alginate material that most clinicians use for orthodontic patients.2–8 It also permits better detail reproduction and adhesion between the impression materials, compared to irreversible hydrocolloid material or an alginate and silicone combination.22 Studies assessing the prosthetic impression quality of an implant emergence profile using the Er:YAG are scarce in the scientific literature. Matys et al. used a 3-point prosthetic impression scale (PIS) to visually assess the accuracy of the prepared soft tissue using an erbium laser.19 They found an ideal projection of the soft tissue (no bubbles or scratches: PIS1) in 4 cases; a satisfactory projection of the soft tissue (small bubbles, scratches: PIS2) in 19 cases; and an inaccurate projection of the soft tissue (cavities, large cracks in the impression material: PIS3) in 7 cases. They concluded that in 70% of the cases (21/30) Fig. 11. View of the final screw retained crowns in position 12 and 22 – the quality of the implant emergence profiles prepared without the orthodontic wire using an Er:YAG laser allowed a prosthetic impression to be taken immediately, without utilizing healing screws, which reduced the overall treatment time.19 ets, wires) can trap and tear the impression material. The The indirect techniques proposed by Tarlow or Macin- easiest proven method to overcome these difficulties is to tosh and Sutherland require cast and/or soft tissue substi- block the undercuts around the brackets with additional tute modification, which prolongs the treatment and often material. Maeda et al. proposed a use of a tube, while Su- requires excellent communication with the dental techni- kotjo and Bocage recommend the use of an implant sur- cian.10,11 The result depends mainly on skills of the techni- gical template.4,8 However, those solutions are time con- cian. Direct techniques are easier to carry out. However, suming. The use of dental wax is a quick and inexpensive the surgical intervention in soft tissue proposed by Reike method that can accommodate orthodontically banded entails extended impression waiting time due to the need patients. The plasticity of the wax depends on the tem- for local anesthesia and the postoperative bleeding.12 So- perature. Due to its ductile nature when warmed, it al- lutions that incorporate the use of interim restorations lows easy shaping and molding. When cooled, however, it very often do not ensure the ideal shape of the emergence stays in the impression material and does not change its profile (prefabricated abutments) or are dependent on the shape without extra applied force. The material has the technician’s skills (custom abutments).13–17 Nevertheless, added advantage of attaching well to brackets, in addition the addition of an Er:YAG laser introduces a fast and easy to peeling off easily. Consequently, it results in minimized method for obtaining an optimal emergence profile. The material damage when the impression tray is removed. use of a laser excludes postoperative bleeding (optimal The first author to use this material was Lorton, who ad- hemostasis), the need for suturing and local anesthesia.23 vised the use of strips of occlusal indicator wax.7 Rilo et al., Laser intervention significantly reduces postoperative along with Croll and Castaldi, proposed a cheaper mate- pain, discomfort and swelling, and causes only a minimal rial: utility wax.5,6 Rilo et al. suggested using small portions thermal rise in the bone around the implant.24–26 The ab- 106 J. Matys, K. Świder, R. Flieger. Laser instant implant impression method

sence of bleeding permits immediate implementation of 9. Alani A, Corson M. Soft tissue manipulation for single implant restorations. Br Dent J. 2011;211:411– 416. impressions for restorations, while other methods require 10. Tarlow JL. Procedure for obtaining proper contour of an implant- healing time for the soft tissue.19 supported crown, a clinical report. J Prosthet Dent. 2002;87:416–418. 11. Macintosh DC, Sutherland M. Method for developing an optimal emergence profile using heat-polymerized provisional restorations for single-tooth implant-supported restorations. J Prosthet Conclusions Dent. 2004;91:289–292. 12. Reikie DF. Restoring gingival harmony around single tooth implants. J Prosthet Dent. 1995;74:47–50. Regarding the new method presented here, the authors 13. Spyropoulou PE, Razzoog M, Sierraalta M. Restoring implants in the suggest that further comparison studies of the influence esthetic zone after sculpting and capturing the periimplant tissues on implant collar height and crestal bone loss using LIIIM in rest position, a clinical report. J Prosthet Dent. 2009;102:345–347. and traditional mucoperiosteal flap development are nec- 14. Becker W, Doerr J, Becker BE. A novel method for creating an optimal emergence profile adjacent to dental implants. J Esthet Restor essary. Furthermore, a long term randomized clinical Dent. 2012;24:395–400. trial should be performed to assess the emergence profile 15. Ntounis A, Petropoulou A. A technique for managing and accu- quality obtained using an Er:YAG laser. rate registration of periimplant soft tissues. J Prosthet Dent. 2010;104:276–279. Within the limitations of this single case study, the out- 16. Al-Harbi SA, Edgin WA. Preservation of soft tissue contours with comes could indicate that the technique described here immediate screw-retained provisional implant crown. J Prosthet for taking the impression and creating the emergence Dent. 2007;98:329–332. 17. Azer SS. A simplified technique for creating a customized gingival profile offers dental practitioners additional options in emergence profile for implant-supported crowns. J Prosthodont. the implantoprosthodontic treatment of orthodontic pa- 2010;19:497–501. tients, as the method is characterized by simple prepara- 18. Bednarz W. The thickness of periodontal soft tissue ultrasonic examination – current possibilities and perspectives. Dent Med tion and satisfactory implant site reproduction. Probl. 2011;48:303–310. 19. Matys J, Dominiak M. Assessment of pain during uncovering implants with Er:YAG laser or scalpel for second stage surgery. Adv References Clin Exp Med. 2016, doi:10.17219/acem/62456. 1. Rose TP, Jivraj S, Chee W. The role of orthodontics in implant den- 20. Hsu YT, Shieh CH, Wang HL. Using soft tissue graft to prevent mid- tistry. Br Dent J. 2006;201:753–764. facial mucosal recession following immediate implant placement. 2. Farret MM, Farret MM, Carlesso J, Carlesso O. Orthodontic treat- J Int Acad Periodontol. 2012;14:76–82. ment and implant-prosthetic rehabilitation of a partially edentu- 21. Wee AG. Comparison of impression materials for direct multi- lous patient. J Prosthodont. 2013;22:587–590. implant impressions. J Prosthet Dent. 2000;83:323–331. 3. Drago CJ. Use of osseointegrated implants in adult orthodontic 22. Peutzfeldt A, Asmussen E. Accuracy of alginate and elastomeric treatment, a clinical report. J Prosthet Dent. 1999;82:504–509. impression materials. Scand J Dent Res. 1989;97:375–379. 4. Maeda Y, Matsuda S, Tsugawa T, Maeda S. A modified method of 23. Walsh LJ. Erbium dental lasers and bone modification. Aust Dent mouthguard fabrication for orthodontic patients. Dent Traumatol. Pract. 2008;9:106–108. 2008;24:475–478. 24. Happe A, Körner G, Nolte A. The keyhole access expansion tech- 5. Rilo B, Lago L, Da Silva L, Fernández-Formoso N. Implant impression nique for flapless implant stage-two surgery, technical note. Int for full-banded orthodontic patient. J Oral Implantol. 2016;42:292–293. J Periodontics Restorative Dent. 2010;30:97–101. 6. Croll TP, Castaldi CR. Custom sports mouthguard modified for orth- 25. Al-Khayatt AS, Eliyas S. Soft tissue handling during implant place- odontic patients and children in the transitional dentition. Pediatr ment. Evid Based Dent. 2008;9:77. Dent. 2004;26:417–420. 26. Matys J, Botzenhart U, Gedrange T, Dominiak M. Thermodynam- 7. Lorton L. A method to facilitate impressions of orthodontically ic effects after diode and Er:YAG laser irradiation of grade IV and banded teeth. J Prosthet Dent. 1982;48:356. V titanium implants placed in bone – an ex vivo study. Preliminary 8. Sukotjo C, Bocage V. Simplified fabrication of surgical template for report. Biomed Engineering/Biomed Technik. 2016, doi: 10.1515/bmt- orthodontic-implant treatment. J Prosthodont. 2006;15:59–61. 2015-0135. Clinical cases Characteristic features of orthodontic treatment of tooth retention caused by hyperdontia Charakterystyka leczenia ortodontycznego zębów zatrzymanych z powodu ich nadliczbowości

Valentyn Makeyev1, A, C, E, F, Nataliya Pylypiv2, B–D, F, Volodymir Shybinskyy1, A, C, E, F

1 Department of Prosthodontics, Lviv National Medical University, Lviv, Ukraine 2 Department of Orthodontics, Lviv National Medical University, Lviv, Ukraine

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):107–113

Address for correspondence Abstract Valentyn Makeyew E-mail: [email protected] Supernumerary teeth often cause tooth retention. The presence of supernumerary teeth, depending on their shape, number and location, can create unfavorable conditions for the development of the dental arches Funding sources none declared and occlusion, resulting in significant functional and esthetic disorders. The article presents clinical cases of patients with hyperdontia and tooth retention. Each case involves a thor- Conflict of interest ough patient examination and an individual approach to the choice of treatment. The authors’ experience none declared in treating retention caused by hyperdontia allowed a range of treatment methods to be used, depending on the functional state of occlusion, the patient’s age and the characteristics and location of the impacted Received on October 7, 2016 Revised on November 6, 2016 and supernumerary teeth. In two patients with dentition in the early transitional period, the central inci- Accepted on December 4, 2016 sors erupted without a doctor’s intervention within three months after the extraction of supernumerary teeth. In both cases, the subsequent orthodontic treatment aimed at correcting the torsiversion the incisors displayed upon eruption. Another case demonstrates a method of treatment that provides minimal loss of bone tissue: the supernumerary tooth were initially shifted to the alveolar bone surface and then removed. The last case describes a complete surgical-orthodontic treatment. Bone grafting was performed after the extraction of a supernumerary tooth, and an impacted tooth was moved to the newly created bone tissue. All these methods of treatment have their specific indications and can be implemented after a thorough examination of the patient. Key words: hyperdontia, impacted teeth, tooth retention Słowa kluczowe: nadliczbowość zębów, zęby zaklinowane, zatrzymanie zęba

DOI 10.17219/dmp/67514

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc-nd/4.0/) 108 V. Makeyev, N. Pylypiv, V. Shybinskyy. Orthodontic treatment of tooth retention

Tooth retention is an abnormality that requires atten- Among 94 patients with tooth retention treated at the tion for both scientific and practical reasons. Usually, authors’ departments, 24 cases were identified as involv- this anomaly is accompanied by disturbances in the tooth ing retention of the upper central incisors. In 18 of these eruption sequence, by tooth crowding, diastema and cyst cases (75.0%) the condition was caused by supernumerary formation. Among other causes, tooth retention is of- teeth (Table 1). ten caused by supernumerary teeth (ST), which occur as The number of male patients with supernumerary teeth single, multiple, unilateral or bilateral anomalies in the preventing the incisors from erupting was 3.5 times high- maxilla, mandible or both jaws.1 A statistically significant er than the number of females. The primary therapeutic association has been found between unerupted incisors approach for patients with hyperdontia causing failure of and other inherited dental anomalies, in particular hy- incisor eruption is extraction of the supernumerary teeth. perdontia.2 The presence of supernumerary tooth is the In two patients with dentition in the early transition- most common cause of maxillary incisor eruption failure. al period, after extraction of supernumerary teeth, the Delayed eruption of associated teeth has been reported in central incisors erupted within three months without 28–60% of Caucasians with supernumerary teeth.3 a doctor’s intervention. The orthodontic treatment that The clinical manifestations of hyperdontia can vary followed in both cases was aimed at correcting the tor- widely and depend on many factors: the number of siversion the incisors displayed upon eruption. supplemental teeth, their size, shape and location in the Below, examples of different clinical approaches to su- jaws.1,4 The presence of a supernumerary tooth or teeth pernumerary tooth extraction are provided. often causes upper midline deviation, space loss, disturbed eruption or rotated central incisors.5,6 Supernu- merary teeth located in the anterior region of the maxilla Case reports are usually palatally located.7 The location of supernumerary teeth plays a major role Case 1 in the diagnosis and treatment, especially in determining the necessity of surgical intervention.8 The clinical di- A nine-year-old girl was referred to the Department of agnosis can be confirmed by radiographic examination. Orthodontics of Lviv National Medical University (Lviv, Anthonappa et al. reported that panoramic radiographs Ukraine) with a lack of left central and lateral permanent are not sufficient to reliably identify supernumerary incisors in the upper jaw. Clinical examination revealed teeth.9 Different radiographs are necessary to diagnose the early period of primary occlusion, normognathic oc- ST location. Widely used techniques for determining the clusion and a midline shift to the left; teeth 61 and 62 location of supernumerary teeth include vertical tube were present in the dental row. The intraoral radiograph shift and horizontal tube shift. In 2013, Toureno et al. and panoramic x-ray (Fig. 1) revealed retention of the left proposed “a guideline to locate and identify supernumer- central and lateral incisors and supernumerary teeth that ary teeth in two and three dimensions, which may reduce projected into the crowns of the retained teeth. treatment errors and improve communication among A CT scan was made to update and specify the location health care providers and third-party administrators”.10 of the supernumerary teeth. To extract them, the decision Surgical removal of impacted teeth requires great ac- was made to establish access to them through the open- curacy in the diagnosis and the localization of the teeth. ing that was made after extracting a deciduous incisor. Because of its 3D images, cone-beam computed tomog- The two supernumerary teeth were extracted (Fig. 2), and raphy (CBCT) has a greater potential than conventional tooth 21 erupted independently after two months. radiography for providing precisely detailed information, so the possibility of surgical errors is greatly reduced.11,12 Case 2 Each case of tooth retention, especially when caused by hyperdontia, requires an individual approach considering A nine-year-old boy with a lack of central maxillary in- the patient’s age and the location and topography of the cisors was referred to the Department of Orthodontics. teeth.13 This article presents some solutions to these is- He was in the early period of primary occlusion. There sues. were no visible lesions in the mucous membranes of the

Table 1. The distribution of patients and the location of the supernumerary teeth (selfobservation)

Hyperdontia was an obstacle to eruption Hyperdontia wasn’t an obstacle to eruption Total Patient’s sex n % n % n % Male 14 58.3 2 8.3 16 66.6 Female 4 16.7 4 16.7 8 33.4 Total 18 75.0 6 25.0 24 100.0 Dent Med Probl. 2017;54(1):107–113 109

Fig. 1. A nine-year-old girl’s panoramic x-ray: retained teeth 21 and 22 and supernumerary inclusion

Fig. 4. The same seven-year-old boy’s panoramic x-ray: a supernumerary tooth between central incisors, the left incisor in tortoanomalia Fig. 2. The same nine- year-old girl’s super- Fig. 5. Supernumerary teeth numerary which were extracted from the teeth which seven-year-old boy were extracted

Fig. 6. The seven-year-old boy’s central incisors erupted (photo seven months after treatment) Fig. 3. A seven-year-old boy in the early period of primary occlusion; retention of teeth 11 and 21 caused by hyperdontia

but were torsiverted. A removable appliance with an activation arm was used to correct the position of the central mouth. The child’s face was symmetrical and proportion- incisors. After five months positive functional and esthet- ate. ic results were achieved (Fig. 6). Clinical examination revealed the presence of a partial- In patients with permanent occlusion, crown exposure ly erupted conical tooth (Fig. 3). Radiological examination of the retained tooth is performed simultaneously with showed a supernumerary conical tooth between the cen- the supernumerary tooth extraction, immediately fol- tral incisors that was preventing them from erupting. The lowed by fixing the orthodontic element for its movement left central incisor was rotated 45o (Fig. 4). into the dental arch. After the supernumerary tooth was extracted (Fig. 5), The objective of this intervention is to gain access to the the central incisors erupted independently within months, crown of the retained tooth without damaging the mar- 110 V. Makeyev, N. Pylypiv, V. Shybinskyy. Orthodontic treatment of tooth retention

ginal edge of the gum. This provides a better esthetic ef- with open springs enough space was created to move fect in the area of the retained tooth that has been moved tooth 23 into the dental arch. to the dental arch. In all cases, the central incisors were An orthodontic button was fixed to the exposed sur- accessed from the vestibular side of the alveolar process. face of the retained 23 from the palatal side of the alveolar If retention is caused by hyperdontia and after extrac- bone (Fig. 8). The double-arch method was used to move tion of the supernumerary tooth/teeth the cavity in the jaw the retained tooth, using a 0.017” × 0.022” steel rectan- bone prevents the retained tooth from initiating move- gular arch as the main stabilizing one and a 0.016” round ment, staged surgery might decided upon in some cases. NiTi arch, which provides light continuous force on the The first stage is the exposure of the crown of the retained retained tooth. tooth. Once the supernumerary tooth shifts closer to the After 5 months of tooth 23 movement, when the super- edge of the alveolar process as a result of the movement numerary tooth started emerging and visualized on the of the retained tooth, the second stage of the surgery is vestibular surface of the alveolar bone, the second surgi- carried out: extraction of the supernumerary tooth, which cal procedure was performed: removal of the supernu- is less invasive and traumatic for the bone and consider- merary tooth, after which the movement of the retained ably shortens the post-surgical treatment time. tooth continued. The total duration of the treatment was 23 months. After the treatment a removable retainer was Case 3 made. In this case, the individual treatment plan and individualized approach allowed the retained tooth to be A 22-year-old female came to the Depertment of Or- successfully moved without significant loss of volumetric thodontics complaining that an absent right upper canine bone density. caused an esthetic defect. Clinical examination revealed An- In some cases, when the supernumerary tooth is large gle’s class 1 malocclusion, left-sided cross bite, teeth 33 and in size or when a retained tooth cannot be accessed with- 34 in a vestibular position, and tooth 23 was missing. X-ray out extracting the supernumerary one, a large cavity is imaging (Fig. 7) showed the retained tooth 23 with a formed expected in the jaw bone. In this situation, orthodontic root and correct anatomical structure, and a supernumerary treatment is preceded by bone grafting. The following is tooth causing the failure of tooth of 23 to erupt. a clinical example. Non-removable Roth 0018 orthodontic appliance was fitted for the patient and after five months of treatment Case 4

A 21-year-old male came to the Department of Ortho- dontics complaining of the formation of a neoplasm on the upper left jaw. Clinical examination and x-ray (Fig. 9) led to a diagnosis of Angle’s class 1 malocclusion, insignificant crowding of the teeth in the anterior area of the lower jaw, retention of tooth 23, hyperdontia between teeth 22 and 23, and a follicular cyst. In the Surgical Department under local anesthesia a trapezoid mucoperiosteal flap above the location of tooth 23 was mobilized. The follicular cyst was extracted and the crowns of the impacted 23 and the supernumerary tooth were exposed. To reduce the trauma from extraction, the Fig. 7. A 22-year-old female’s orthopantomogram

Fig. 8. The same 22-year- old female: surgical baring of the crown of tooth 23 and supernumerary tooth extraction Dent Med Probl. 2017;54(1):107–113 111

1.5 g of Bio-Oss® (Geistlich Pharma, Wolhusen, Switzer- land) and Bio-Gide® collagen membrane (Geistlich). The mucoperiostal flap was closed and the wound was sutured (Fig. 10). Postoperative instructions and the necessary pre- scriptions were given to the patient. The healing period passed without any complications. After 6 months a second x-ray was taken, and it showed good osteointegration of the bone graft material (Fig. 11). After 7 months the retained tooth erupted by itself, but in a vestibular position and turned around its axis. A non- removable Roth 0018 orthodontic appliance with open springs was used to create sufficient space. The double arch method was used to move tooth 23 into the dental Fig. 9. A 21-year-old male’s panoramic x-ray: impacted tooth 23 and arch. Active treatment lasted for 7 months. The achieved hyperdontia result was satisfactory and stable (Fig. 12). After removing the braces the patient uses a removable retainer. It is significant that in this situation the retained tooth supernumerary tooth was divided beforehand into two erupted through the newly formed bone made of bone parts with a bur and then extracted. Given the significant substitute. This way, full dentition was maintained, with- defect of the osseous tissue of the upper jaw in the loca- out extracting tooth 24. tion of the extracted cyst and supernumerary tooth, it was decided to place a bone graft. The cavity was filled with

Fig. 10. The same 21-year-old male: the surgical stages of the treatment 112 V. Makeyev, N. Pylypiv, V. Shybinskyy. Orthodontic treatment of tooth retention

Discussion

Retention of teeth in conjunction with hyperdontia is a complex condition that requires a carefully planned approach to the treatment.14 The choice of treatment should be individualized and based on a thorough examination. As Alling et al. wrote, “Methods of management of crowding or impaction due to supernumerary [teeth] are: remove supernumerary teeth or tooth only, remove supernumerary teeth and bone overlying impacted teeth, incision of fi- brous tissue over the alveolar ridge to promote the eruption with or without orthodontic traction”.15 To bring retained Fig. 11. The 21-year-old male’s condition 6 months after osteoplasty; the demarcation line between his own bone and the bone substitute is not visible teeth into the dental arch, surgical exposure or surgical repositioning can be used in some cases.16,17 The authors’ experience providing comprehensive care to patients with retained teeth due to supernumerary teeth led to the development of algorithms of orthodontic treatment for such cases (Fig. 13). The decision of which treatment plan to choose primarily depends on the physiological status of the functional dentition (primary or permanent), and the depth and location of the supernumerary tooth. In a case of primary occlusion and both the retained tooth and the supernumerary tooth are located close to the surface, it is sufficient to extract the supernumerary tooth and wait for self-eruption of the retained tooth, if there is enough space in dental arch. In case of a delay in its eruption the use of a stimulating removable appliance is recommended. In cases of patients with primary occlusion in which the location of the retained and supernumerary teeth is deep, it is appropriate to postpone treatment until the forma- Fig. 12. The 21-year-old male’s tooth 23 has moved into the dental row tion of permanent occlusion.

retention caused by а supernumerary tooth

transitional dentition permanent dentition

supernumerary tooth supernumerary tooth supernumerary tooth supernumerary tooth is located close to surface is deep is located close to surface is deep

extraction stage 1: extraction stage 1: exposure stage 1: extraction stage 1: extraction of the of the supernumerary of the crown of the of the supernumerary of the supernumerary supernumerary tooth with exposure retained tooth tooth followed tooth with exposure tooth of the crown of the and its orthodontic by osteoplastic of the crown of the retained tooth; relocation; surgery of the bone retained tooth stage 2: orthodontic stage 2: extraction tissue defect; stage 2: orthodontic relocation of the of the supernumerary stage 2: self-eruption relocation of the retained tooth tooth after it of the retained tooth retained tooth has moved; or its orthodontic stage 3: further relocation self-eruption stimulating orthodontic of the retained removable relocation of the tooth appliance retained tooth

Fig. 13. The algorithm of action when retention caused by hyperdontia is discovered Dent Med Probl. 2017;54(1):107–113 113

In cases of permanent occlusion when the retained and References supernumerary teeth are located close to the surface, it is 1. Rajab LD, Hamdan MAM. Supernumerary teeth: Review of the liter- enough to extract the supernumerary tooth, expose the ature and a survey of 152 cases. Int J Paediatr Dent. 2002;12:244−254. 2. Bartolo A, Camilleri A, Camilleri S. Unerupted incisors – characteristic crown of the retained tooth and proceed with the orth- features and associated anomalies. Eur J Orthod. 2010;32:297–301. odontic treatment scheme, which will depend on the 3. Mitchell L, Bennett TG. Supernumerary teeth causing delayed availability of space in the dental arch. This treatment ap- eruption − a retrospective study. Br J Orthod. 1992;19:41−46. 4. Becker A, Casap N, Chaushu S. Conventional wisdom and the surgi- proach can be applied in some cases in which both teeth cal exposure of impacted teeth. Orthod Craniofac Res. 2009;12:82–93. are deep but access to them and orthodontic relocation is 5. Baart JA, Groenewegen BT, Verloop MA. Correlations between the not complicated. presence of a mesiodens and position abnormalities, diastemas, and eruption disturbances of maxillary frontal teeth. Ned Tijdschr However, in some clinical situations of a deep super- Tandheelkd. 2009;116:399–402. numerary tooth, it is advisable to carry out the exposure 6. Sant’Anna EF, Marquezan M, Sant’Anna CF. Impacted incisors asso- of the crown of the retained tooth and its orthodontic ciated with supernumerary teeth treated with a modified Haas movement in the first stage. The movement of the re- appliance. Am J Orthod Dentofacial Orthop. 2012;142:863–871. 7. Becker A. Orthodontic treatment of impacted teeth. WileyBlack- tained tooth towards the crest of the alveolar bone will well, 2012. cause the relocation of the supernumerary tooth, which 8. Mallineni SK. Radiographic localization of supernumerary teeth in can be extracted in the second stage, under less traumatic the maxilla. Doctoral thesis. University of Hong Kong, 2011. 9. Anthonappa RP, King NM, Rabie ABM, Mallineni SK. Reliability of conditions. Further orthodontic treatment is carried out panoramic radiographs for identifying supernumerary teeth in in accordance with normal practice. children. Inter J Pediatr Dent. 2012;22:37–43. Sometimes there are clinical situations where as a result 10. Toureno L, Park JH, Cederberg RA, Hwang EH, Shin JW. Identifica- tion of supernumerary teeth in 2D and 3D: Review of literature and of removing a large supernumerary tooth, or several of a proposal. J Dent Educat. 2013;77:43–50. them, and/or the removal of follicular cysts near the retained 11. Jeremias F, Bullio Fragelli CM, Di Salvo Mastrantonio S, et al. Cone- tooth, a large defect forms in the bone. In such cases, placing beam computed tomography as a surgical guide to impacted anterior teeth. Dent Res J. 2016;13:85–89. a bone graft with bone substitute and wound closure by mu- 12. Lai CS, Bornstein MM, Mock L, Heuberger BM, Dietrich T, Katsaros coperiosteal flap is advisable. The retained tooth may erupt C. Impacted maxillary canines and root resorptions of neighboring independently, or in the second stage (6–8 months later) it teeth: A radiographic analysis using cone-beam computed tomog- might be necessary to expose the crown of the retained tooth raphy. Eur J Orthod. 2013;35:529–538. 13. Das D, Misra J. Surgical management of impacted incisors in asso- and move it with the help of orthodontic treatment. ciate with supernumerary teeth: A combine case report of sponta- With retained and supernumerary teeth, providing neous eruption and orthodontic extrusion. J Indian Soc Pedod Prev comprehensive care can be achieved by the algorithms Dent. 2012;30:329–332. 14. Garvey MT, Barry HJ, Blake M. Supernumerary teeth – An overview described above, determined by the clinical situation: the of classification, diagnosis and management. J Can Dent Assoc. topographical location of the retained and supernumer- 1999;65:612–616. ary teeth, size, their shape and number, the presence of 15. Alling CA, Hellric JF, Alling R. Impacted teeth. WB. Saunders Co., Philadelphia, 1993, 46–49. follicular cysts, etc. 16. Kocadereli I, Turgut MD. Surgical and orthodontic treatment of an impacted permanent incisor: Case report. Dent Traumatol. 2005;21:234–239. 17. Kamakura S, Matsui K, Katou F, Shirai N, Kochi S, Motegi K. Surgi- cal and orthodontic management of compound odontoma without removal of the impacted permanent tooth. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2002;94:540–542.

Letter to the Editor Letter to the Editor on the article “Soft tissue profile changes after mandibular setback surgery” (Dent Med Probl 2016, 53, 4, 447–453) List do Redakcji dotyczący pracy pt. „Zmiana profilu tkanek miękkich po jednoszczękowych zabiegach korekcji progenii” (Dent Med Probl 2016, 53, 4, 447–453)

Siddharth Mehta

Department of Orthodontics & Dentofacial Orthopedics, Manipal College of Dental Sciences, Manipal University, Karnataka, India

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):115–116

Address for correspondence Respected Editor, Siddharth Mehta E-mail: [email protected] I read with great interest the article by Bogusiak et al.1 entitled “Soft tissue profile changes after mandibular setback surgery” published in issue 4, 2016 of the journal Dental and Medical Problems and I appreciate the effort of the authors to propose changes in soft tissue profile of the patients after bilateral sagittal split osteotomy vs vertical ramus osteotomy. Presently, we have seen a transition from hard tissue to soft tissue paradigm and now soft tissue drape serves as the basis for most of orthodontic and orthognathic surgeries.2 Cephalometric analysis helps us assess the profile of a patient with various linear and angular measurements. Previous studies on the effect of orthognathic surgery on the upper lip position demonstrate that

DOI 10.17219/dmp/69932

Copyright © 2017 by Wroclaw Medical University and Polish Dental Society This is an article distributed under the terms of the Creative Commons Attribution Non-Commercial License Fig. 1. Linear measurements to assess (http://creativecommons.org/licenses/by-nc-nd/4.0/) soft tissue profile changes 116 S. Mehta. Letter to the Editor

the thicker the pretreatment tissue, the less prominent is References the post-treatment change3,4. Similarly, it could have an 1. Bogusiak K, Kociński M, Łutkowski A, Materka A, Neskoromna- -Jędrzejczak A. Soft tissue profile changes after mandibular setback influence on the outcome of the following lower lip po- surgery. Dent Med Probl. 2016;53:447–453. sition surgery. Therefore, in addition to the parameters 2. Ackerman JL, Proffit WR, Sarver DM. The emerging soft tissue para- mentioned in the aforementioned study, it is important to digm in orthodontic diagnosis and treatment planning. Clin Orthod Res. 1999;2:49–52. include a few linear measurements like lip thickness, lip 3. Ayoub AF, Yahya AM. Soft tissue response to anterior maxillary oste- strain or measurements from true vertical line and to as- otomy. Int J Adult Orthod Orthognath Surg. 1999;6:183–190. sess their changes post-surgery (Fig. 1). Clarification will 4. Mansour S, Burstone C, Legan H. An evaluation of soft tissue changes be highly appreciated. resulting from Le Fort I maxillary surgery. Am J Orthod. 1983;84:37–47. Letter to the Editor Reply to the Letter to the Editor on the article “Soft tissue profile changes after mandibular setback surgery” (Dent Med Probl 2016, 53, 4, 447–453) Odpowiedź na list do Redakcji dotyczący pracy pt. „Zmiana profilu tkanek miękkich po jednoszczękowych zabiegach korekcji progenii” (Dent Med Probl 2016, 53, 4, 447–453)

Katarzyna Bogusiak1, Marek Kociński2, Adam Łutkowski2, Andrzej Materka2, Aneta Neskoromna-Jędrzejczak1

1 Department of Craniomaxillofacial and Oncological Surgery, Medical University of Lodz, Łódź, Poland 2 Institute of Electronics, Department of Medical Electronics, Technical University of Lodz, Łódź, Poland

Dental and Medical Problems, ISSN 1644-387X (print), ISSN 2300-9020 (online) Dent Med Probl. 2017;54(1):117–118

Address for correspondence Key words: soft tissue profile, cephalometry, bilateral sagittal split osteostomy (BSSO), extraoral vertical Katarzyna Bogusiak ramus osteotomy (EVRO) E-mail: [email protected] Słowa kluczowe: profil tkanek miękkich, cefalometria, obustronna strzałkowa osteotomia gałęzi żuchwy, pionowa osteotomia gałęzi żuchwy z dostępu zewnątrzustnego

The evaluation of soft tissues is an integral part of orthodontic and maxillofacial diagnosis and treatment planning of patients with orthognathic defects.1 The forehead, nose, upper and lower lip, and chin are the anatomical structures that create facial profile. Both corrective surgery and orthodontic treatment affect the patients’ appearance and facial contours. Many authors emphasized the significance of soft tissue analysis in the proper evaluation of skeletal discrepancy, which could be altered by individual differences in soft tissue thickness.2–4 Different cephalometric soft tissue analyses have been developed for clinical and experimental purposes to quantitatively and more reliably evaluate the facial morphology.5–12 Soft tissue assessment on lateral cephalograms is not as straightforward and easy to reproduce as the analysis of hard tissue structures of the face. Such quantification requires the curved surfaces of patients’ profile to be reduced to distances, angles and ratios, which makes such a procedure less precise.13 Soft tissue profile analyses are variable also because their measurements involve the construction of straight lines of facial contours between anatomic landmarks located along the soft tissue profile or by lines tangent to the curved surfaces.13 These lines form the angles and distances of cephalometric DOI methods. There are also 3D cephalometric methods that include soft tissue 14–18 10.17219/dmp/69933 landmarks, angles and distances. McNamara’s analysis is well-established and is believed to be a very practical cephalometric tool. Its norms have been Copyright studied in various populations due to their optimal efficacy.19, 20 This method, © 2017 by Wroclaw Medical University© 2017 by Wroclaw through the measurement of angles, describes the thickness of soft tissue facial Medical University and Polish Dental Society This is an article distributed under the terms of the profile. Creative Commons Attribution Non-Commercial License Data on the shift of the facial profile and on hard-to-soft tissue ratio after (http://creativecommons.org/licenses/by-nc-nd/4.0/) surgical corrective procedures affects treatment planning and is of a great im- 118 K. Bogusiak, et al. Reply to the Letter to the Editor

portance in predicting the aesthetic treatment outcome. 9. Holdaway RA. A soft tissue cephalometric analysis and its use in orthodontic treatment planning. Part II. Am J Orthod. 1984;85:279–293. Orthognathic surgery affects lips positions. Ayoub indi- 10. Williams S. A short guide on cephalometry in orthodontics. Polor- cated that the response of soft tissues of the upper lip to. Częstochowa 1998 [in Polish]. region to anterior maxillary osteotomy is related to their 11. Neger M. A quantitative method for the evaluation of the soft-tissue facial profile. Am J Orthod. 1959;45:738–751. thickness – the thicker they are, the lower is the post- 12. Lusterman EA. The esthetics of the occidental face: A study of 21 operative change. After mandibular setback surgeries, dentofacial morphology based upon anthropologic criteria. Am the position of the upper and lower lips is also changed. J Orthod. 1963;49:826–850. 13. Hwang HS, Kim WS, McNamara JA Jr. A comparative study of two The changes in the upper lip position after mandibular methods of quantifying the soft tissue profile. Angle Orthod. 2000; surgery were explained by the contraction of the orbicu- 70:200–207. laris oris muscle and soft tissue traction.22 Some authors 14. Olszewski R, Villamil MB, Trevisan DG, et al. Towards an integrated hypothesized that the thickness and posture of presur- system for planning and assisting maxillofacial orthognathic surgery. Comput Meth Prog Bio. 2008;9:13–21. gical soft tissue may affect the post-treatment position 15. Shimomatsu K, Nozoe E, Ishihata K, Okawachi T, Nakamura N. of the upper lip.23 The relation of incisors before the Three-dimensional analyses of facial soft tissue configuration of surgery should also be considered. Several factors may Japanese females with jaw deformity – a trial of polygonal view of facial soft tissue deformity in orthognathic patients. J Craniomaxil- contribute to the postoperative position of the lower lip. lofac Surg. 2012;40:559–567. It should be emphasized that lower lip position is deter- 16. Swennen GR, Schutyser F, Barth EL, De Groeve P, De Mey A. A new mined by upper and lower incisors, perioral muscles, method of 3-D cephalometry Part I: the anatomic Cartesian 3-D ref- 24–26 erence system. J Craniofac Surg. 2006;17:314–325. their thickness and tonicity. In our article, in the an- 17. Baysal A, Sahan AO, Ozturk MA, Uysal T. Reproducibility and reli- alyzed groups of patients (after EVRO and BSSO), men ability of three-dimensional soft tissue landmark identification and women did not differ significantly in terms of pre- using three-dimensional stereophotogrammetry. Angle Orthod. 2016;86:1004–1009. surgical soft tissue profile assessed with Hwang, Kim and 18. Treil J, Braga J, Aït Ameur A. 3D representation of skull and soft tis- McNamara analysis. The measurements were performed sues. Usefulness in orthodontic and orthognathic surgery. J Radiol. with an anatomical-based method.27 2009;90:634–641. We believe that more prospective studies are still need- 19. Nouri M, Hamidiaval S, Akbarzadeh Baghban A, Basafa M, Fahim M. Efficacy of a newly designed cephalometric analysis software for ed that would stratify such confounding factors as the McNamara analysis in comparison with Dolphin software. J Dent. magnitude of movement, method of osteosynthesis, sex, (Tehran) 2015;12:60–69. age, race, quality and quantity of soft tissues with suffi- 20. Hwang HS, Kim WS, McNamara JA Jr. Ethnic differences in the soft tissue profile of Korean and European-American adults with normal cient sample sizes. occlusions and well-balanced faces. Angle Orthod. 2002;72:72–80. 21. Ayoub AF, Yahya AM. Soft tissue response to anterior maxillary References osteotomy. Int J Adult Orthod Orthognath Surg. 1991;6:183–190. 1. McNamara JA Jr, Brust EW, Riolo ML. Soft tissue evaluation of indi- 22. Jung YJ, Kim MJ, Baek SH. Hard and soft tissue changes after correc- viduals with an ideal occlusion and a well-balanced face. In: Esthet- tion of mandibular prognathism and facial asymmetry by mandib- ics and the treatment of facial form. Center for Human Growth and ular setback surgery: three-dimensional analysis using computer- Development, The University of Michigan, Ann Arbor, 1993 (Mono- ized tomography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. graph 28, Craniofacial Growth Series). 2009;107:763–771. 2. Subtelny JD. A longitudinal study of soft tissue facial structures and 23. Gjørup H, Athanasiou AE. Soft-tissue and dentoskeletal pro- their profile characteristics, defined in relation to underlying skele- file changes associated with mandibular setback osteotomy. Am tal structures. Am J Orthod. 1958;45:481–507. J Orthod Dentofacial Orthop. 1991;100:312–323. 3. Burstone CJ. Integumental contour and extension patterns. Angle 24. Chunmaneechote P, Friede H. Mandibular setback osteotomy: facial Orthod. 1959;29:93–104. soft tissue behavior and possibility to improve the accuracy of the 4. Bowker WD, Meredith HV. A metric analysis of the facial profile. soft tissue profile prediction with the use of a computerized ceph- Angle Orthod. 1959;29:149–160. alometric program: Quick Ceph Image Pro: v. 2.5. Clin Orthod Res. 5. Merrifield LL. The profile line as an aid in critically evaluating facial 1999;2:85–98. esthetics. Am J Orthod. 1966;52:804–822. 25. Solow B, Tallgren A. Natural head position in standing subjects. 6. Ricketts RM. Esthetics, environment, and the law of lip relation. Am Acta Odontol Scand. 1971;29:591–607. J Orthod. 1968;54:272–289. 26. Momeni Danaei SH, Zamiri B, Khajeh F, Torkan S, Ghodsi Busheh- 7. Burstone CJ, James RB, Legan H, Murphy GA, Norton LA. Cephalo- ri S. Comparative study of facial soft tissue profile changes follow- metrics for orthognathic surgery. J Oral Surg. 1978;36:269–277. ing bilateral sagittal split and subcondylar osteotomies in patients 8. Holdaway RA. A soft tissue cephalometric analysis and its use in with mandibular prognathism. J Dent Sch. 2013; 30:248–255. orthodontic treatment planning. Part I. Am J Orthod. 1983;84:1–28. 27. Bogusiak K, Kociński M, Łutkowski A, Materka A, Neskoromna- -Jędrzejczak A. Soft tissue profile changes after mandibular setback surgery. Dent Med Probl. 2016;53:447–453. Impact Factor Listing for Journals on Dentistry (2015) First part: Journals on General Dentistry (38 titles with IF: 0.28–4.602)

Country of the Frequency IF (change Journal title Abbreviation publisher in a year vs 2012) Journal of Dental Research J Dent Res USA 12 4.602 (+ 0.46) Dental Materials Dent Mater Great Britain 12 3.931 (+ 0.16) Journal of Dentistry J Dent Great Britain 12 3.109 (+ 0.35) Molecular Oral Microbiology Mol Oral Microbiol USA 6 3.061 (+ 0.28) Journal of Orofacial Pain J Orofac Pain Canada 4 2.824 (+ 1.13) International Journal of Oral Science Int J Oral Sci China 4 2.595 (+ 0.06) Community Dentistry and Oral Epidemiology Commun Dent Oral Epidemiol New Zealand 6 2.333 (+ 0.21) Clinical Oral Investigations Clin Oral Invest Germany 6 2.207 (– 0.15) Journal of the American Dental Association JADA USA 12 1.767 (– 0.25) Archives of Oral Biology Arch Oral Biol Great Britain 12 1.733 (– 0.002) European Journal of Oral Sciences Eur J Oral Sci Denmark 6 1.607 (+ 0.12) Odontology Odontol Japan open access 1.538 (+ 0.31) Journal of Evidence-Based Dental Practice* J Evid Bas Dent Pract USA 4 1.474 Gerodontology Gerodontol Canada 4 1.396 (+ 0.28) Dental Traumatology Dent Traumatol Australia 6 1.327 (– 0.28) Australian Dental Journal Aust J Dent Australia 6 1.272 (+ 0.17) Oral Surgery Oral Medicine Oral Pathology Oral Oral Surg Oral Med Oral Pathol USA 12 1.262 (+ 0.001) Radiology and Endodontics Oral Radiol Endod Journal of Esthetic and Restorative Dentistry J Esth Restorative Dent USA 6 1.231 (+ 0.43) BMC Oral Health BMC Oral Health Great Britain open access 1.21 (+ 0.08) American Journal of Dentistry Am J Dent USA 6 1.194 (+ 0.34) Journal of Public Health Dentistry J Public Health Dent USA 4 1.182 (– 0.47) Acta Odontologica Scandinavica Acta Odontol Scand Denmark 8 1.171 (+ 0.14) Journal of Applied Oral Science J Appl Oral Sci Brazil 4 1.117 (+ 0.19) Dental Materials Journal Dent Mater J Japan 2 1.087 (+ 0.12) International Journal of Periodontics & Restorative Int J Periodontisc Restorative USA 6 1.039 (– 0.38) Dentistry Dent British Dental Journal Brit Dent J Great Britain 24 0.997 (– 0.08) International Dental Journal Int Dent J Great Britain 6 0.967 (– 0.29) Head & Face Medicine Head Face Med Germany open access 0.916 (+ 0.06) Brazilian Oral Research Braz Oral Res Brazil 4 0.859 (– 0.08) Quintessence International Quintes Int USA 10 0.821 (– 0.13) Journal of Oral Science J Oral Sci Japan 4 0.804 (– 0.12) Journal of Dental Sciences J Dent Sci China 4 0.795 (+ 0.24) International Journal of Dental Hygiene Int J Dent Hyg Sweden 4 0.791 (– 0.26) Community Dental Health Commun Dent Health Great Britain 4 0.767 (+ 0.16) Journal of Craniomandibular Practice & Sleep Practice Cranio USA 6 0.738 (+ 0.05) Oral Health and Preventive Dentistry Oral Health Prev Dent Switzerland 6 0.69 (+ 0.19) Swedish Dental Journal Swed Dent J Sweden 4 0.381 (– 0.35) Journal of the Canadian Dental Association JCDA Canada 11 0.28 (– 0.07)

* Journal has entered the list in 2015 Impact Factor Listing for Journals on Dentistry (2015) Second part: Journals on Specialist Dentistry (51 titles with IF: 0.052–4.949)

Country of Frequency IF (change Journal title Abbreviation the publisher in a year vs 2012) Oral Surgery and Maxillofacial Surgery (8 titles) Oral Oncology Oral Oncol USA 12 4.286 (+ 0.68) Journal of Oral and Maxillofacial Surgery J Oral Max Surg USA 12 1.631 (+ 0.21) Journal of Cranio-Maxillofacial Surgery J Craniofac Surg Germany 12 1.592 (– 1.34) International Journal of Oral and Maxillofacial Surgery Int J Oral Max Surg Great Britain 12 1.563 (– 0.002) British Journal of Oral & Maxillofacial Surgery Brit J Oral Max Surg Great Britain 6 1.237 (+ 0.16) Cleft Palate-Craniofacial Journal Cleft Pal-Craniofac J USA 6 1.05 (– 0.15) Oral and Maxillofacial Surgery Clinics of North America Oral Max Surg Clin North Am USA 6 0.67 (+ 0.09) Reveu de Stomatologie et de Chirurgie Maxillo-faciale Rev Stomatol Chir Max France 6 0.248 (– 0.05) Dental Radiology (2 titles) Dentomaxillofacial Radiology Dentomaxillofac Rad Germany 8 1.919 (+ 0.52) Oral Radiology Oral Radiol Japan 3 0.449 (– 0.005) Periodontology and Oral Pathology (8 titles) Periodontology 2000 Periodontol 2000 USA 3 4.949 (+ 1.31) Journal of Clinical Periodontology J Clin Periodontol Great Britain 12 3.915 (– 0.1) Journal of Periodontology J Periodontol USA 12 2.844 (+ 0.14) Journal of Periodontal Research J Periodontal Res USA 6 2.474 (+ 0.1) Oral Diseases Oral Dis Great Britain 8 2.0 (– 0.42) Journal of Oral Pathology & Medicine J Oral Pathol Med Great Britain 10 1.859 (– 0.07) Journal of Periodontal & Implant Science JPIS Korea 6 1.108 (– 0.04) Medicina Oral Patologia Oral y Cirugia Bucal Med Oral Pat Oral Cir Bucal Spain open access 1.087 (– 0.09) Implant Dentistry (7 titles) Clinical Implant Dentistry and Related Research Clin Impl Dent Res USA 6 4.152 (+ 0.56) Clinical Oral Implants Research Clin Oral Impl Res Australia 12 3.464 (– 0.42) European Journal of Implantology Eur J Implant Great Britain 4 2.328 (– 0.8) International Journal of Oral & Maxillofacial Implants IOMI USA 6 1.859 (+ 0.4) Journal of Oral Implantology J Oral Implant USA 6 1.432 (+ 0.42) Implant Dentistry Impl Dent USA 6 1.023 (– 0.15) Implantologie Implant Germany 4 0.052 (+ 0.01) Cariology and Endodontics (6 titles) Journal of Endodontics J Endod. USA 12 2.904 (– 0.47) International Endodontic Journal Int Endod J Great Britain 12 2.842 (– 0.13) Operative Dentistry Oper Dent USA 6 2.819 (+ 1.14) Caries Research Caries Res Great Britain 6 2.278 (– 0.01) Journal of Adhesive Dentistry J Adhesiv Dent Germany 6 1.594 (+ 0.28) Australian Endodontic Journal Austr Endod J Australia 3 0.885 (+ 0.3) Country of Frequency IF (change Journal title Abbreviation the publisher in a year vs 2012) Orthodontics (8 titles) American Journal of Orthodontics and Dentofacial AJO-DO USA 12 1.69 (+ 0.31) Orthopedics Orthodontics & Craniofacial Research Orthod Craniofac Res Netherlands 4 1.64 (+ 0.58) Angle Orthodontist Angle USA 6 1.579 (+ 0.35) European Journal of Orthodontics Eur J Orthod Finland 6 1.44 (– 0.04) Korean Journal of Orthodontics Kor J Orthod Korea 6 1.162 (– 0.01) Journal of Orofacial Orthopedics J Orofac Orthod Germany open access 0.789 (– 0.05) Australian Orthodontic Journal Austr Orthod J Australia 3 0.451 (+ 0.02) Seminars in Orthodontics* Sem Orthod USA open access 0.346 Pediatric Dentistry (4 titles) International Journal of Paediatric Dentistry Int J Paediatr Dent Great Britain 6 1.303 (– 0.03) Pediatric Dentistry Pediatr Dent USA 6 0.874 (– 0.9) Journal of Clinical Pediatric Dentistry JOCPD Great Britain 6 0.562 (+ 0.21) European Journal of Paediatric Dentistry Eur J Paediatr Dent Italy 4 0.421 (– 0.02) Prosthetic Dentistry (6 titles) Journal of Oral Rehabilitation J Oral Rehabil Denmark 12 1.926 (+ 0.24) Journal of Prosthodontic Research J Prosthet Res Japan 4 1.693 (+ 0.15) Journal of Prosthetic Dentistry J Prosthet Dent USA 12 1.515 (– 0.24) International Journal of Prosthodontics Int J Prosthodont Canada 6 1.487 (+ 0.02) Journal of Prosthodontics J Prosthodont USA 4 1.133 (+ 0.06) Journal of Advanced Prosthodontics J Adv Prosthodont Korea 6 0.844 (+ 0.2) Dental Education (2 titles) Journal of Dental Education J Dent Educ USA 12 0.83 (– 0.13) European Journal of Dental Education Eur J Dent Educ Great Britain 4 0.784 (– 0.15)

* Journal has entered the list in 2015 Dental and Medical Problems