The first issue of the Balkan Journal of Dental Medicine was published in 2014 The Journal continues the tradition of the Balkan Journal of Stomatology which was published between 1997 and 2013 Publisher: BALKAN STOMATOLOGICAL SOCIETY

Editor-in-Chief Prof. Dejan Marković, DDS, PhD, School of Dental Medicine, University of Belgrade, Serbia balkan.@hotmail.com Editorial Assistant Res. Asst. Bojana Ćetenović, DDS, PhD, Institute for Nuclear Sciences „Vinca“ [email protected] Associate Editors Prof. Ruzhdie Qafmolla, DDS, PhD, Faculty of Dentistry, University of Medicine-Tirana, Albania [email protected] Prof. Sedin Kobaslija, DDS, PhD, Faculty of Dentistry, University of Sarajevo, Bosnia and Herzegovina [email protected] Assoc. Prof. Nikolai Sharkov, DDS, PhD, Faculty of Dental Medicine, Medical University-Sofia, Bulgaria [email protected] Assoc. Prof. George Pantelas, DDS, PhD, The School of Medicine, European University Cyprus, Cyprus [email protected] Prof. Ana Minovska, DDS, PhD, Department of Dentistry,Goce Delcev University of Štip, FYROM [email protected] Prof. Anastasios Markopoulos, DDS, PhD, School of Dentistry, Aristotle University, Greece [email protected] Assoc. Prof. Mirjana Đuričković, Faculty of Medicine, University of Montenegro, Montenegro [email protected] Prof. Forna Norina Consuela, DDS, PhD, Faculty of Dentistry, Grigore T. Popa U. M. Ph. Iasi, Romania [email protected] Prof. Slavoljub Živković, DDS, PhD, School of Dental Medicine, University of Belgrade, Serbia [email protected] Prof. Ender Kazazoglu, DDS, PhD, Dental School, University of Yeditepe, Turkey [email protected] Editorial Board Assoc. Prof. Edit Xhajanka, DDS, PhD, Faculty of Medical Dentistry, Albania Assoc. Prof. Merita Bardhoshi, DDS, PhD, Faculty of Medical Dentistry, Albania Assoc. Prof. Elmedin Bajric, DDS, PhD, Faculty of Dentistry, University of Sarajevo, Bosnia and Herzegovina Dr. Mihael Stanojević, DDS, MSc, Medical Faculty Foca, Bosnia and Herzegovina Prof. Andon Filtchev, DDS, PhD, Faculty of Dental Medicine, Medical University, Bulgaria Prof. Georgi Todorov, DDS, PhD, Faculty of Dental Medicine, Medical University, Bulgaria Dr. Irodotos Irodotou, DDS, Private Dental Practice, Cyprus Prof. Spyros Papachalarambous, DDS, PhD, University of Nicosia Medical School, Cyprus Assoc. Prof. Ilijana Muratovska, DDS, PhD, Department of Dentistry, Goce Delcev UN of Štip, FYROM Assoc. Prof. Vera R. Nikolovska, DDS, PhD, Department of Dentistry, Goce Delcev UN of Štip, FYROM Prof. Lambros Zouloumis, DDS, PhD, School of Dentistry, Aristotle University, Greece Prof. Athanasios Poulopoulos, DDS, PhD, School of Dentistry, Aristotle University, Greece Assoc. Prof. Zoran Vlahović, DDS, PhD, V Dental Centar, Montenegro Prof. Andrei Iliescu, DDS, PhD, Faculty of Dentistry, Grigore T. Popa U. M. Ph. Iasi, Romania Assoc. Prof. Paula Perlea, DDS, PhD, Faculty of Dentistry, Carol Davila University of Medicine and Pharmacy, Romania Assoc. Prof. Tamara Perić, DDS, PhD, School of Dental Medicine, University of Belgrade, Serbia Dr. Slobodan Anđelković, DDS, Private Dental Practice- Belgrade, Serbia Prof. Gül Işik Özkol, DDS, PhD, Istanbul University, Turkey Assoc. Prof. Zeynep Ozkurt Kayahan, DDS, PhD, Dental School, University of Yeditepe, Turkey Balk J Dent Med, Vol 23, 2019

International Editorial Board Prof. Nitzan Bichacho, DDS, PhD, The Hebrew University- Hadassah School of Dental Medicine, Israel Dr. Borko Čudović, DDS, Angle Society of Europe, Germany Prof. George Freedman, DDS, PhD, BPP University School of Health, Faculty of Dentistry, United Kingdom Assoc. Prof. Alex Grumezescu, PhD, Polytechnic University of Bucharest, Romania Prof. James Gutmann, DDS, PhD, Texas A&M University Baylor College of Dentistry, USA Prof. Christoph Hämmerle, DDS, PhD, Center of Dental Medicine, University of Zurich, Germany Dr. Chris Ivanoff, College of Dentistry, University of Tennessee Health Science Center, USA Dr. Barrie Kenney, DDS, Private practice- Los Angeles, USA Dr. Predrag Charles Lekic, DDS, PhD, University of Manitoba, Canada Prof. Joshua Moshonov, DDS, PhD, The Hebrew University- Hadassah School of Dental Medicine, Israel John Nicholson, PhD, DSc, Bluefield Centre for Biomaterials, United Kingdom Prof. Kyösti Oikarinen, DDS, PhD, University of Oulu, Finland Assoc. Prof. Sangwon Park, DDS, PhD, Chonnam National University, South Korea Prof. George Sandor, PhD, University of British Columbia, Canada Prof. Ario Santini, DDS, PhD, Faculty of General Dental Practice, United Kingdom Prof. Riitta Suuronen, DDS, PhD, Institute for Regenerative Medicine, University of Tampere, Finland Dr. Michael Weinlaender, DDS, Private Practice- Vienna, Austria Prof. Virgjini Mulo, DDS, PhD, Faculty of Dentistry, University of Medicine-Tirana, Albania Publications Committee Chair Prof. Ljubomir Todorović, DDS, PhD, Academy of Medical Sciences, Serbian Medical Society, Serbia [email protected] Editorial Medical Staff Assoc. Prof. Elizabeta Gjorgievska, DDS, PhD, Faculty of Dentistry, Ss. Cyril and Methodius UN, FYR of Macedonia Prof. Bojan Petrović, DDS, PhD, Faculty of Medicine, University of Novi Sad, Serbia Dr. Marijan Denkovski, DDS, FYR of Macedonia Dr. Georgios Tsiogas, DDS, Greece Dr. Ana Jotić, DDS, Private Dental Practice, Belgrade, Serbia Dr. Raša Mladenović, DDS, Faculty of Medicine, University of Priština, Serbia Translations supervisor Gordana Todorović Publishing Managers Jelena Jaćimović, PhD, School of Dental Medicine, University of Belgrade, Serbia [email protected] Assis. Ana Vuković, DDS, PhD, School of Dental Medicine, University of Belgrade, Serbia [email protected] Statistical Advisor Prof. Biljana Miličić, MD, PhD, School of Dental Medicine, University of Belgrade, Serbia

Editorial Office: School of Dental Medicine, Clinic for Paediatric and Preventive Dentistry, Dr. Subotića 11, 11000 Belgrade, Serbia e-mail: [email protected], Tel: +381641149773, Fax: +381112685361 Papers published in the Balkan Journal of Dental Medicine are indexed in: Baidu Scholar, Case, Celdes, CNKI Scholar (China National Knowledge Infrastructure), CNPIEC, EBSCO DiscoverBaidu Scholar, Case, Celdes, CNKI Scholar (China National Knowledge Infrastructure), CNPIEC, EBSCO Discovery Service, Google Scholar, J-Gate, JournalTOCs, KESLI-NDSL (Korean National Discovery for Science Leaders), Naviga (Softweco), Primo Central (ExLibris), ReadCube, Sherpa/RoMEO, Summon (Serials Solutions/ProQuest), TDOne (TDNet), WorldCat (OCLC). Printed by: Forma B d.o.o., Belgrade, Čika Miše Ðurića 20 (1500 copies per issue)

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VOLUME 23 NUMBER 1 MARCH 2019 PAGES 1-53

Contents

RA M. Šabanović Impact of Propolis on the Oral Health 1 S. Saltović A. Avdić Mujkić M. Jašić Z. Bahić

RA A. Sovtic How to Maintain Oral Health in Children with Review 10 T. Peric Respiratory Diseases –Literature P. Minic D. Markovic

OP B. Mroczek Change in Patients’ Self-Reported Quality of Life 15 M. Anna Lichota before and after Dental Implantation G. Trybek A. Grzywacz

OP B. Ozmen Evaluation of Permanent First Molar in 20 Young Population from North Turkey

OP Z.D. Tzima A Prospective Clinical Study of the Efficacy of 24 N. Economides Hyflex CM Rotary Instruments in C. Gogos an Endodontics Undergraduate Program I. Kolokouris

OP S. Živković Efficiency of XP Endo Shaper (XPS) and 31 M. Jovanović-Medojević Irrigation Protocol on the Quality of J. Nešković Cleaning the Apical Third of : SEM Study M. Popović Bajić M. Živković Sandić

OP L. Intzes Comparative Evaluation of Resistance to Cyclic Fatigue of 36 Z.D. Tzima Three Rotary Endodontic Ni-Ti Instruments C. Gogos

CR A. Đorđević Modern Trends in Prosthetic Implant Rehabilitation of Patients: 40 M. Mikić Case Report with 5-Year Follow-Up J. Stanišić F. Đorđević

CR H.M.M. Hegazi Mini-Implants and Zirconium Crowns in Treating Congenitally 45 Missing Maxillary Lateral Incisors: Case Report

CR T. Uzun Papillon-Lefévre Syndrome: Case Report and Genetic Analysis 50

O. Toptas

10.2478/bjdm-2019-0001

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Impact of Propolis on the Oral Health

SUMMARY Marizela Šabanović1, Semir Saltović2, Azra Propolis is a natural resinous substance collected by honey bees Avdić Mujkić2, Midhat Jašić1, Zerina Bahić1 from buds and exudates of plant species, mixed with bee enzymes, pollen 1 Faculty of Technology, University of Tuzla, and wax. It has a complex composition with a wide range of effects, Univerzitetska 8, Tuzla, Bosnia and Herzegovina including antibacterial, antiviral, antifungal, antiflogistic, antioxidant, 2 Faculty of Pharmacy, University of Tuzla, hepatoprotective, carcinostatic and immunomodulatory properties. It is Univerzitetska 8, Tuzla, Bosnia and Herzegovina often applied in the treatment of diseases involving the oral cavity and . The aim of this paper is to describe the therapeutic properties of propolis, chemical composition and its application in the oral cavity. Literature and systematic information on the composition and the effects of propolis on health were collected, with particular reference to the use in the treatment of oral cavity diseases. The chemical composition of propolis is very complex. The health impact depends on the biologically active components it contains. A particularly important application is in the treatment of diseases of the oral cavity. Studies show that propolis can help prevent dental caries and control and plaque. It reduces halithosis (bad breath) and symptoms of periodontosis. It is also effective in fighting viruses. It can have significant application in orthodontics and restorative dentistry. A wide range of effects allows the multiple uses of propolis-based products. Recent research has been increasingly focused on diseases of the oral cavity. The development of novel propolis-based pharmaceutical forms could significantly reduce the use of antibiotics in conventional treatment of diseases of the oral cavity. REVIEW PAPER (RP) Key words: Propolis, Oral Health, Apitherapy, Oral Cavity Balk J Dent Med, 2019;1-9

Introduction to eliminate the potential within the hive, the bodies of dead pests are covered with propolis and thus 4 Propolis, also referred to as bee glue, is a natural, prevent their decomposition . non-toxic, resinous and sticky substance produced by Propolis is a lipophilic material that is firm and honey bees through the mixing of hypopharyngeal gland fragile at lower temperatures, while flexible and sticky at higher temperatures. Its melting point is between 60°C secretions with digestive resin products collected from and 70°C, and for some samples the temperature can go buds and bark of trees, flowers, leaves and other botanical up to 100°C 5. The best solvent used for the preparation sources1,1. Propolis most often originates from trees such of propolis is ethanol. Other solvents such as ethyl ether, 2 as poplar, willow, beech and wild chestnut . Bees use water, methanol and chloroform can be used for the propolis to protect and strengthen their hive. With this extraction and identification of propolis components6. natural product, the hive is protected from rain and pests Gloverin and propylene glycol are used in the preparation such as insects and rodents. Propolis maintains aseptic of propolis for the pharmaceutical and cosmetic conditions and the appropriate temperature within the industries7. It has a pleasant aromatic scent and can be, hive. Propolis acts as a biocide that successfully fights depending on origin and botanical origin, red, brown, bacteria, mushrooms and larvae of certain pests3. In order yellow or green in colour8,9,10. 2 Marizela Šabanović et al. Balk J Dent Med, Vol 23, 2019

Chemical composition of propolis The action of propolis on human health

The chemical composition and content of the Propolis exhibits a wide range of biological biologically active compounds of propolis depends on the properties, and one of the most significant characteristics geographical and botanical origin, the type of bees, and is its antimicrobial activity. This is supported by a large 19 the seasons in which propolis is collected11. Raw propolis number of publications . Table 1 below describes the consists of about 50% resin, 30% wax, 10% essential oils, biological activity of propolis components. 5% pollen and 5% of various organic compounds12,13,14. Research has shown that propolis extracts, which are composed of many polyphenols, have a strong antioxidant Techniques for separating and purifying the mixture, activity20,21,22. Geographically and botanically different such as high pressure liquid chromatography - HPLC, propolis samples have a different chemical composition, thin layer chromatography - TLC15, gas chromatography- which directly affects their effect as antioxidants23. Fabris GC, as well as identification techniques such as mass 16 et al. (2013) showed that ethanolic extracts of Russian spectroscopy - MS , nuclear magnetic resonance- and Italian propolis have a similar antioxidant effect NMR, gas chromatography in combination with because they have a similar polyphenol composition, 17 mass spectroscopy- GC-MS , has identified several while, on the other , the ethanolic extract of Brazilian compounds within propolis including flavonoids, propolis exhibits significantly less antioxidant effect terpenes, phenols and their esters, sugars , hydrocarbons because it contains a smaller amount of polyphenols in and mineral elements. In contrast, relatively frequent its composition. Phenolic acids and flavonoids exhibit a phytochemicals such as alkaloids and iridoids have not strong antioxidant effect, which is closely related to the been detected18. chemical structure of the components25. Table 1. Biological activity of different propolis components26

Component, propolis type Biological activity References Almeida and Menezes, Polyphenols and flavonoid Antibacterial, antiviral, antiallergic antimicrobial, antitumor, 200227; Havsteen, 200228, (in all types of propolis) antioxidant, immunomodulatory, hepatoprotective, cardioprotective. Ghisalberti, 19792 Caffe-phenethyl ester acids Antioxidant, antitumor, antiinflammatory, antibacterial, Bankova, 200929, (Topola, Baccharis) antiviral, fungicidal, cardioprotective immunomodulatory. Bankova et al., 200730 Caffeic acid Farooqui T. and Antiviral, antioxidant, antitumor (Topola, Baccharis). Farooqui A., 201031 Artepelin C Bankova, 200929; Antioxidant, antiinflammatory, antitumor (Baccharis) Bankova et al., 200730 Terpene (terpens) Bankova, 200929; Antibacterial, antimicrobial (Greece, Croatia, Brazil) Bankova et al.,199532 Essential oils Bankova et al.199532; Antibacterial (Brazil, Poland) Zwolan and Meresta, 200033

According to research, Propolis is much more for the production of adenosine triphosphate (ATP) effective in combating Gram-positive bacteria than required for the smooth flow of the membrane transport against Gram-negative bacteria34,35. This is due to the fact and for maintaining its mobility36. The polypeptide that the membrane of Gram-negative bacteria exhibits directly affects the organisms in vitro. On the other hand, greater complexity in the material than the Gram-positive propolis can indirectly participate in the destruction bacteria. In the suspension of bacteria, certain components of microorganisms by stimulating the in vivo immune of propolis can be destroyed by hydrolytic enzyme of system and activating the mechanisms responsible for the bacteria. Some of the mechanism of action by which killing microorganisms37. The polypis can be combined propolis exhibits its’ antimicrobial effect, is through the suppression of permeability of the bacterial membrane with antimicrobial drugs because it has been proven that and inhibition of bacterial mobility. Propolis can affect propolis reduces bacterial wall resistance on antibiotics the flow of ions through the inner bacterial membrane and has a synergistic effect with antibiotics that work on and lead to disturbance of the membrane potential, that ribosome’s, but does not show interaction with antibiotics affect the electrochemical gradient that is necessary that affect DNA or folic acid38,39,40. Balk J Dent Med, Vol 23, 2019 Propolis On oral Health 3

Propolis has also been shown to have a significant the steps in the viral replication cycle, and leading to antiviral effect. It acts at different levels and impedes degradation of the RNA virus before penetration in a the replication of certain viruses such as or after its release into the supernatant43. Certain clinical type 1 and 2, adenovirus type 2, influenza virus, human trials in the male and female populations have shown immunodeficiency virus (HIV), and others. By research, that application of fat containing propolis can result in propolis can exhibit antiviral activity by causing partial faster healing in genital herpes compared to conventional blocking of viral penetration into the cell, affecting acyclovir treatment42.

Table 2. Pathogenic bacteria, fungi, viruses and parasites on which propolis acts19

Bacillus cereus, Bacillus mesentericus, Corynebacterium sp., Corynebacterium diphtheriae, Diplococcus Gram-positive bacterias pneumoniae, Enterococcus sp., Mycobacteria sp., Mycobacterium tuberculosis, Staphylococcus aureus, Streptococcus: critecus, epidermis faecalis, mutans, pyogenes, viridans, sobrinus Branhamella catarrhalis, E. coli, Helicobacter pylori, Klebsiella ozaemae, Proteus vulgaris, Gram-negative bacterias Pseudomonas aeruginosa, Salmonella: choleraesuis, dublin, enteritidis, exneri, gallinarum, pullorum, paratyphi-A, paratyphi-B, Shigella: dysinteriae, sonnei Aspergilus sp., Candida: albicans, guiliermondi, parapsilosis, tropicalis; Cryptococcus sp., Cyptococcus neoformans, Histoplasma encapsulatum, Madurella mycetomi, Microsporum: Fungus audoinini, canis, cepleo, distortum, ferrugeneum, gypseum; Piedra hortae, Phialophora jeanselmei, Saccharomyces sp., Trichophyton: sp., Mentagrophytes, rubrum, Trichosporon cutaneum Adenovirus, Coronavirus, Hepres simplex, Infulenca A and B virus, virus Newcastleske desease, Polio Viruses virus, Vaccinia, Rotavirus; Vesicular , Coronavirus Cholomonas paramecium, Eimeria: magna, media, perforans; Parasites Giardia lambia, Giardia duodenalis, Trichomonas vaginalis, Trypanosoma cruzi, Trypanosoma evansi Banskota et al., (2001)43; Burdock (1998)12; David et al (2012)44; Ghisalberti (1979)2; Gressler et al., References (2012)45; Marcucci (1995)9;Tikhonov et al., (1998)46

Propolis have been shown to exhibit antifungal antitumor properties. Other distinguished components action against C. albicans, C. tropicalis and C. krusei47. include: chrysine, nemesone, galangin and cardanol51 Propolis acts on the aflatoxicogenic types of Aspergillus Propolis modifies non-specific immunity. Propolis and such as Aspergillus flavus by inhibiting the condom its constituents, such as cinnamic acid and its p-coumarinic germination48. Propolis also acts on numerous parasites derivative, stimulate the production of TNF-α (tumor- (Table 2). alpha necrosis factor) and interleukin (IL)-1β in mouse Antiparasitic and immunomodulatory activity macrophages54,55. The expression of cellular receptors of Brazilian propolis on Leishmania braziliensis was such as toll-like receptors TLR-2 and TLR-4 was also investigated49. Propolis directly affected the parasite increased in peritoneal macrophages of propolis-treated and exhibited immunomodulatory effects on murine mice56. A study on the effect on reactive oxygen species macrophages, although it has been shown that the also showed that propolis stimulates the formation of parasite continues to affect the activation pathways of the hydrogen peroxide (H2O2) through mouse macrophages cell. Components important for the antiparasitic action while reducing the production of nitric oxide (NO)38. are phenolic compounds (flavonoids, aromatic acids, In a second study however, the inhibitory effect on the benzopyrene), di- and triterpenes; and essential oils found production of superoxide anions by rabbit neutrophils was in the propolis sample49. demonstrated by the propolis compounds57. In humans, Various in-vitro studies have demonstrated the propolis can exhibit immunomodulatory effects on cellular cytotoxic effect of propolis on tumor cells. In-vivo receptors, as well as in the production of cytokines and studies have also shown that there is potential for the the fungicidal activity of monocytes, depending on the development of new antitumor drugs; showing no adverse concentration. It increases the expression of TLR-4 and effects when tested on rats50. This natural product is able CD80 receptors, influences the production of TNF-α and to block oncogenic signaling pathways, which in turn IL-10 and increases the fungicidal activity of monocytes58. leads to decreased proliferation and cell growth. It also Cinnamic acid reduces the number and activity of TLR-2, reduces the population of tumor stem cells by increasing HLA-DR and CD80 receptors, and increases the activity apoptosis, preventing angiogenesis and modulating tumor of TLR-4 receptors. High concentrations of cinnamic micro-circulation51,52,53. Caffe-phenethylether acids and acid inhibit the production of TNF-α and IL-10, while the artepelin C are distinguished as components possessing same concentrations encourage stronger fungicidal activity 4 Marizela Šabanović et al. Balk J Dent Med, Vol 23, 2019 against C. albicans59. Propolis stimulates the production of Propolis and oral cavity health antibodies; independent of the year of propolis collection and its origin. This was confirmed by a 2005 study in Early animal studies have shown that propolis which scientists used Brazilian and Bulgarian propolis as an significantly reduces dental caries in rats as a result auxiliary in rats immunized with bovine serum albumin60. of multiple effects on the bacterial flora. It limits the Propolis can exhibit pro-inflammatory and anti- number of microorganisms, slows down the synthesis inflammatory effects depending on the concentration, of insoluble glucans, and slows down the activity of entry period and experimental conditions and can glucosyltransferase enzyme64. This natural product has stimulate or inhibit certain processes. However there is oral cavity activity due to its high fatty acid content such still little evidence of the clinical efficacy of propolis in as oleic, linoleic, palmitic and stearic acids which slows this manner60. the production of acid by Streptococcus mutans and Propolis also has a beneficial effect in the treatment reduces the tolerance of microorganisms to the acidic of wounds due to its antifungal and antibacterial abilities pH65. Propolis also have a lower cytotoxic effect on in view of the presence of certain components such as: fibroblasts (found in gums) compared to flavonoids, phenolic compounds, terpenes and enzymes. (also used in caries prevention), suggesting that propolis It reduces the amount of free radicals (reactive oxygen can be used as an ingredient in mouthwash66. Majority species) and thus facilitates the wound healing process. of studies uses propolis as a in the form It participates in collagen by increasing of aqueous and alcoholic solution67,68 or in the form the synthesis of collagen type I and type III collagen of toothpaste69. Propolis can be used in the form of in tissues. Propolis is a potential apitherapy agent that a solution for the decontamination of fibers on the has the ability to modify the metabolism of fibronectin. toothbrush69. It develops a fibrous network of extracellular matrix Bacteria such as Tannerella forsythensis, and inhibits the fibronectin disintegration. Components and Treponema denticol make such as quercetin and resveratrol inhibit the fibronectin up a of microorganisms that increases the biosynthesis and TGF-β (transforming growth factor β) depth of the periodontal pocket and causes bleeding of dependent production of fibronectin in C2C12 myoblasts. the gums. The propolis extract shows high efficacy in Both components play an important role in the expression preventing the growth of bacteria belonging to the red of fibronectin. Studies have shown that the mobility complex68. Clinical examination has shown that the 3% of epithelial cells depends on the reduced content of ethanolic propolis extract in the form of gel and paste fibronectin in the extracellular matrix. Reduced amounts slows down and ultimately prevents pathological changes of this glycoprotein allow propolis to better cure wounds in patients at an increased risk of occurrence of dental and produce granulation tissue61. plaque gingivitis71. Based on a clinical trial of 25 patients, a non-alcoholic mouthwash containing 5% Brazilian green propolis proved effective in controlling plaque and gingivitis, suggesting its use in treatment and prevention The oral cavity periodontal diseases. However, a double-blinded randomized trial is needed before final clinical use in the The oral cavity represents the proximal part of the dentistry industry72. The preventative effect of propolis on digestive system and plays a role in chewing and ingestion periodontal tissues implies a slowing down of the calcium of food, as well as speech. The major components of the phosphate precipitate formation process and can therefore oral cavity are the teeth, tongue and the salivary glands. be used as ingredient in mouthwash and toothpaste, hence The mucous membrane of oral cavity has the role of limiting the accumulation of dental plaque73. protecting organs by allowing absorption and resorption Halitosis is a frequent or permanent existence of of the substances, preventing the non-physiological bad breath from the mouth, and is closely related to change of substances and stimulating the secretion of the hygiene of the oral cavity. By-products from the harmful substances from the organism62. degradation of microorganisms in the oral cavity are The most common diseases of the oral cavity one of the main causes of halitosis74. The microbes include: most commonly responsible for the onset of aching and 1. Dental caries (tooth decay) halitosis include , Porphyromonas 2. Gingivitis – inflammation of the gums endodontalis and from the bacteria of the genus 3. Periodontitis - inflammation of (tissue Eubacterium75. By measuring the content of volatile that supports the teeth) sulfur compounds in the exhaled air through the 4. Other diseases of the : angular , halometer, it was concluded that propolis significantly oral herpes, , exfoliative , reduces halitosis76. prosthetic stomatitis (denture stomatitis), aphtous Propolis has been shown to affect certain etiological ulcer, and others63. factors that lead to the development of periodontal Balk J Dent Med, Vol 23, 2019 Propolis On oral Health 5 disease. Therefore, some researchers use it as part of their device for the expansion of the palatinal suture. During therapeutic protocol in the treatment of periodontitis77. treatment, bone remodeling occurs in the area of palatinal​​ A micro-adhesive hydrophilic gel containing propolis, suturing77. Research on rats showed that propolis solution when applied to gingival pockets was also shown to helps in bone formation during treatment with orthodontic be efficacious78. Based on clinical and microbiological appliances that lead to the spread of palatinal suture. parameters, the subgingival flushing with propolis extract The results of this study showed an increased amount as an auxiliary agent in the treatment of periodontitis of osteoblastic activity in rats who received propolis in proved more effective than the conventional method of treatment and faster bone remodeling89. scraping and pollinating roots1. In restorative dentistry, propolis is used to reduce Studies have also been carried out on animals where the permeability of dentine and in direct overlapping of propolis was given per os to determine if its systemic the pulp to form reparatory dentin77. Ahangari et al.90 effect through circulation has positive action on oral have proven that propolis acts more efficiently in direct cavity health. Morphological and histological pictures overlapping of the pulp compared to products of calcium showed that oral propolis administration in rats prevents hydroxide most commonly used for this purpose. It stops 79 the loss of alveolar bone from periodontitis . the inflammatory reaction, the infection of the microbes Herpes simplex type 1 is a virus that causes skin and and the necrosis of the pulp and encourages the formation mucous lesions on the membranes of the mouth. It is one of high-quality tubular dentin by stem cell stimulation. 80 of the most common human pathogens . Propolis is used The stimulatory effect on tooth pulp is conditioned by the locally in the treatment of oral cavity lesions caused by presence of flavonoids in propolis extracts91. viruses, in studying its antiviral capabilities. As a propolis One of the aims of endodontic treatment is the mixture, it is more effective in combating viral diseases 92 81 elimination of microorganisms in the root canals of teeth . compared to its individual components separatel . The efficacy of drugs is reflected in the Enterococcus Propolis slows down changes in skin and virus growth in faecalis test that is resistant to adverse conditions and can the early stage of infection with Herpes simplex type 1 survive in the root canal system despite the use of certain and is not cytotoxic on healthy cells82. medicines93. The study has shown that it significantly Bee glue also is used in the treatment of recurrent reduces the number of cultured bacteria Enterococcus (canker sores). Although aphthous faecalis, but that it is not superior to chlorhexidine94. stomatitis is a relatively common disease whose However, due to the low level of periapical tissue and symptoms are visible in the form of aphthous ulcers protective effect on periodontal cells, propolis can be used in the mouth; the etiology of the disease has not yet in the disinfection of the root canals of the teeth95. been established which significantly complicates the Prosthetic stomatitis is a common disease in people treatment83. Propolis reduces the frequency of the disease and improves the quality of life in patients84. using dental prostheses. The etiological factors of the disease are: infection with Candida albicans, improper Dental avulsion is the traumatic displacement 96 of a tooth from its socket in the alveolar bone. In of the oral cavity and excessive use of prosthesis . surgery, propolis is used in the replantation of a broken Products based on propolis show strong anti-fungal effects permanent tooth and provides support in the healing on various types of Candida, and the most sensitive to 47 process after surgery. Maintenance of periodontal cells propolis is Candida albicans . The most commonly is one of the key factors to determine success of tooth used form of propolis for prosthetic stomatitis is as a 47 replantation. A research was carried out to determine the mouthwash or as a gel for local application. Acrylic resin medium that provides the best protection during tooth is one of the materials used to make dental prostheses. Da 98 replantation. Propolis as a transport medium showed Silva et al. showed that propolis in the form of a gel can positive results77. According to the research by Ozan adversely affect the acrylic resin in a way that makes it et al., a 10% propolis solution showed better results rough and more prone to adherence to microorganisms. compared to a 20% propolis solution, Hank’s balanced solution (HBSS) or . A new study also showed the extraordinary effectiveness of propolis in not only reducing apoptosis of periodontal cells, but also increases Potential adverse reactions of propolis metabolism and cell proliferation86. Margo-Filho and Carvalho87 have proven that locally applied propolis helps Apart from being a resinous substance with multiple to heal wounds after surgery in the oral cavity, reduces usages (as described above), propolis is also a known inflammation and also acts as an analgesic. Propolis sensitizer; as highlighted by Menniti-Ippolito et al.100 in accelerates the epithelization and formation of granulation their report. There were 18 suspected adverse reactions tissue in the area of healing​​ 88. involving propolis-based products that were reported In the case of mal-occlusion followed by narrowing between April 2002 and August 2007 to the Italian of the upper jaw, it is necessary to use an orthodontic National Surveillance System. 6 Marizela Šabanović et al. Balk J Dent Med, Vol 23, 2019

It is advised to not be used by patients with 5. Toreti VC, Sato HH, Pastore GM, Park YK. Recent progress predisposition to allergies, especially towards pollen and of propolis for its biological and chemical compositions and honey, as well as by individuals with atopy or asthma. its botanical origin. Evid Based Complement Alternat Med, 2013;2013:697390 The study concluded that healthcare practitioners and the 6. Martinotti S, Ranzato E. Propolis: a new frontier for wound general public must be made aware of the potential risk healing? Burns Trauma, 2015;22:3-9. of allergic reactions of consuming products derived from 7. Szliszka E, Kucharska AZ, Sokol-Letowska A, Mertas bees, and that a warning label should be visible on product A, Czuba ZP, Krol W. Chemical Composition and Anti- packaging. Inflammatory Effect of Ethanolic Extract of Brazilian Green In addition, a case report by Hay and Greig101,102 also Propolis on Activated J774A.1 Macrophages. Evid Based supported the antigenic property of propolis and further Complement Alternat Med, 2013:976415 8. Tosi A, Romagnoli C, Bruni A. Antrimicrobial activity suggests to consider delayed contact sensitivity reactions of some commercial extracts of propolis prepared with by propolis as a differential of oral mucosal lesions. different solvents. Phytother Res, 1996;1014:335-336. 101 Apart from the case report by Hay and Greig , 9. Umthong S, Phuwapraisirisan P, Puthong S, Chancao C. In another case report by Budimir et al.103 also noted adverse vitro antiproliferative acitvity of partially purified Trigona effects by individuals using self-prescribed propolis laeviceps propolis from Thailand on human cancer cell products. These adverse effects include oral mucositis, lines. BMC Complement Alternat Med, 2011;11:37 contact cheilitis and perioral dermatitis. However these 10. Marcucci M. Propolis: chemical composition, biological properties and therapeutic activity. Apidologie, 1995;26:83-99. case reports highlight the self-treatment with propolis- 11. Fokt H, Pereira A, Ferreira AM, Cunha A, Aguiar C. based products rather than through prescription. How do bees prevent hive ? The antimicrobial It is concluded that despite several case reports properties of propolis. Current Research, Technology and stating the adverse rections experienced by self- Education Topics in Applied Microbiology and Microbial prescribing individuals, proper patient education, Biotechnology (ed. by Mendez-Vilas A), 2010; 481-493. prescription and treatment monitoring of propolis-based 12. Choma IM, Grzelak EM. Bioautography detection in thin layer products has a bigger benefit potential. chromatography. J Chromatogr A, 2011;1218:2684-2691. 13. Burdock GA. Review of the biological properties and toxicity of bee propolis. Food and Chem Toxicol, 1998;6:347-363. 14. Park YK, Alencar SM, Aguiar CL. Botanical origin and Conclusions chemical composition of Brazilian propolis. J Agric Food Chem, 2002;50:2502-2506. With the development of modern methods of 15. Pietta PG, Gardana C, Pietta AM. Analytical methods for analysis, new knowledge about propolis activity on quality control of propolis, Fitoterapia, 2002;73:S7-S20. 16. Alencar S, Oldoni T, Castro M, Cabral I, Costa-Neto C, human health has emerged. Its mechanisms of action Cury J et al. Chemical composition and biological activity are still being investigated, which will likely lead to the of a new type of Brazilian propolis: Red propolis, J development of new products that affect the health of Ethnopharmacol, 2007;113:278-283. the oral cavity. Coupled with patient education, proper 17. Campo FM, Cuesta-Rubio O, Rosado PA. GC-MS prescription and treatment monitoring, the benefits determination of isoflavonoids in seven red Cuban propolis of propolis-based products, such as, antibacterial, samples. J Agric Food Chem, 2008;56:9927-9932. antiviral, antifungal, anti-inflammatory, antioxidant 18. Maciejewicz W. Isolation of flavonoid aglycones from propolis by column chromatography method and their and chemopreventive actions can be utilised. This may identification by GC-MS and TLC methods. J Liq significantly reduce the use of conventional treatments Chromatogr Relat Technol, 2001;24:1171-1179. and antibiotics, shifting towards the usage of propolis in 19. Shuai H, Cui-Ping Z, Kai W, George QL, Fu-Liang H. the management of oral cavity conditions. Recent Advances in the Chemical Composition of Propolis. Molecules, 2014;19:19610-19632. 20. Bogdanov S. Propolis: Composition, Health, Medicine: A Review. Bee Product Science, 2017:1-44. 21. Viuda-Martos M, Ruiz-Navajas Y, Fernandez-Lopez J, References Perez-Alvarez JA. Functional properties of honey, propolis and royal jelly. J Food Sci, 2008;73:R117-R124. 1. Coutinho A. Honeybee propolis extract in periodontal 22. Scalbert A, Johnson IT, Saltmarsh M. Polyphenols: treatment: A clinical and microbiological study of propolis antioxidants and beyond. Am J Clin Nutr, in periodontal treatment. Indian J Dent Res, 2012;23:2:294 2005;81:215S-217S. 2. Kamburoglu K, Ozen T. Analgesic effect of Anatolian 23. Almaraz-Abarca N, da Graca Campos M, Avila-Reyes JA, propolis in mice. Agri, 2011;23:47-50. Naranjo-Jimenez N, Herrera Corral J, Gonzales-Valdez LS. 3. Ghisalberti EL. Propolis – review. Bee world, 1979;60:59-84. Antioxidant activity of polyphenolic extract of monofloral 4. Vagish Kumar LS. Propolis in dentistry and oral cancer honeybee-collected pollen from mesquite (Prosopis juliflora, management. N Am J Med Sci, 2014;6:250-259. Leguminosae). J Food Compos Anal, 2007;2:119-124. Balk J Dent Med, Vol 23, 2019 Propolis On oral Health 7

24. Silva-Carvalho R, Baltazar F, Almeida-Aguiar C. Propolis: 42. Vynograd N, Vynograd I, Sosnowski Z. A comparative A Complex Natural Product with a Plethora of Biological multi-centre study of the efficacy of propolis, acyclovir Activities That Can Be Explored for Drug Development. and placebo in the treatment of genital herpes (HSV). Evid Based Complement Alternat Med, 2015;2015:1-29. Phytomedicine, 2010;7:1-6. 25. Fabris S, Bertelle M, Astafyeva O, Gregoris E, Zangrando 43. Banskota AH, Tezuka Y, Kadota S. Recent progress in R, Gambaro A, saradnici. Antioxidant properties and pharmacological research of propolis. Phytother Res, chemical composition relationship of europeans and 2001;15:561-571. Brazilians propolis. Pharmacol Pharm, 2013;4:46-51. 44. David EB, De Carvalho TB, Oliveira CM, Coradi ST, 26. Duthie GG, Gardner PT, Kyle JAM. Plant polyphenols: are Sforcin JM, Guimaraes S. Characterisation of protease they the new magic bullet? Pro Nutr Soc, 2003;62:599-603. activity in extracellular products secreted by Giardia 27. De Almeida EC, Menezes H. Anti-inflammatory activity duodenalis trophozoites treated with propolis. Nat Prod Res, of propolis extracts: a review. J Venom Anim Toxins, 26:4:370-374. 2002;8:191-212. 28. Havsteen BH. The biochemistry and medical significance of 45. Gressler LT, Da silva AS, Machado G, Dalla Rosa the flavonoids, Pharmacol Ther, 2001;96:67-202. L, Dorneles F, Gressler LT et al. Susceptibility of 29. Bankova V. Chemical diversity of propolis makes it a Trypanosoma evansi to propolis extract in vitro and in valuable source of new biologically active compounds. experimentally infected rats. Res Vet Sci, 2012;93:1314-1317. JAAS, 2009;1:23-28. 46. Tikhonov AI, Yarnich TG, Cernich VP, Zupanetz I, 30. Bankova V, Popova M, Trusheva B. Plant origin of propolis: Tichonov CA. Theory and practice of the production of Latest developments and importance for research and medical preparations on the basis of propolis (in Russian). medicinal use. In Marghitas L. A., Dezmierean D. (eds) Osnova Harkov, 1998; pp:379. Apicultura – De la stiinta la agribusiness si apiterapie. 47. Ota C, Unterkircher C, Fantinato V, Shimizu MT. Antifungal Editura Academic Pres. Cluj Napoca, 2007; 40-46. activity of propolis on different species of Candida. 31. Farooqui T, Farooqui A. Molecular Mechanism Underlying Mycoses, 2001;44:375-378. the Therapeutic Activities of Propolis: A Critical Review. 48. Ghaly MF, Ezzat SM, Sarhan MM. Use of propolis and Curr Nutr Food Sci, 2010;6:188-199. ultragriseofulvin to inhibit aflatoxigenic fungi. Folia 32. Bankova V, Christov R, Kujumgiev A, Marcucci MC, Microbiol, 1998;43:156-160. Popov S. Chemical composition and antibacterial activity 49. Da Silva SS, Da Silva Thome S, Cataneo AH, Miranda MM, of Brazilian propolis. Zeitschrift fur Naturforschung, Felipe I, De Jesus Andrade CGT et al. Brazilian propolis 1995;50:167-172. antileishmanial and immunomodulatory effects. Evid Based 33. Zwolan W, Meresta T. Bacteriostatic action of the Complement Alternat Med, 2013;2013:673058 volatile oils obtained from propolis extracts in relation to 50. Watanabe MA, Amarante MK, Conti BJ, Sforcin JM. Staphylococcus aureus. Herba Polonica, 1947;46:30-34. 34. Grange JM, Davey RW. Antibacterial properties of propolis Cytotoxic constituents of propolis inducing anti cancer (bee glue). J R Soc Med, 1990;83:159-160. effects: a review. J Pharm Pharmacol, 2011:63:1378-1386. 35. Sforcin JM, Fernandes AJr, Lopes C.A.M, Bankova 51. Chan GC, Cheung KW, Sze DM. (The immunomodulatory V, Funari SRC. Seasonal effect on Brazilian propolis and anticancer properties of propolis, Clin Rev Allergy and antibaceterial activity. J Ethnopharmacol, 2000;73:243-249. Immunol, 2013;44:262-273. 36. Mirzoeva OK, Grishanin RN, Calder PC. Antimicrobal 52. Sawicka D, Car H, Borawska MH, Niklinski J. The action of propolis and its components, the effects on growth anticancer activity of propolis. Folia Histochem Cytobiol, membrane potential, and motility of bacteria. Microbiol Res, 2012;50:25-37. 1997;152:239-246. 53. Araujo JR, Goncalves P, Martel F. Chemopreventive effect 37. Sforcin JM, Bankova V. Propolis: is there a potential of dietary polyphenols in colorectal cancer cell lines, Nutr for the development of new drugs? J Ethnopharmacol, Res, 2011;31:77-87. 2011;133:253-260. 54. Moriyasu J, Arai S, Motoda R, Kurimoto M. In vitro 38. Orsi RO, Sforcin JM, Funari SRC, Fernandes Ajr, Bankova activation of mouse macrophage by propolis extract powder. V. Synergistic effect of propolis and atibiotics on the Biother, 1994;8:364-365. Salmonella Typhi. Braz J Microbiol, 2006;37:108-112. 55. Bachiega TF, Orsatti CL, Pagliarone AC, Sforcin JM. The 39. Orsi RO, Fernandes AJr, Bankova V, Sforcin JM. The effectsof propolis and its isolated compounds on cytokine effects of Brazilian and Bulgarian propolis in vitro against production by murine macrophages. Phytother Res, Salmonella Typhi and their synergism with antibiotics acting 2012;26:1308-1313. on the ribosome. Nat Prod Res, 2012;26:430-437. 56. Orsatti CL, Missima F, Pagliarone AC, Bachiega TF, Búfalo 40. Orsi RO, Fernandes Ajr, Bankova V, Sforcin JM. Antibacterial effects of Brazilian and Bulgarian propoliis MC, Araújo JP Jr et al. Propolis immunomodulatory action and synergistic effects with antibiotics acting on the bacterial in vivo on Toll-like receptors 2 and 4 expression and on pro- DNA and folic acid. Nat Prod Res, 2012;26:344-349. inflammatory cytokines productionin mice. Phytother Res, 41. Bufalo MC, Ferreira I, Costa G, Francisco V, Liberal 2010;24:1141-1146. J, Cruz MT et al. Propolis and its constituent caffeic acid 57. Simoes LM, Gregorio LE, Da Silva Filho AA, de Souza suppress LPS-stimulated pro-inflammatoryresponse by ML, Azzolini AE, Bastos JK et al. Effect of Brazilian green blocking NF-κB and MAPK activation in macrophages. J propolis on the production of reactive oxygen species by Ethnopharmacol, 2013;149:84-92. stimulated neutrophils. J Ethnopharmacol, 2004;94:59-65. 8 Marizela Šabanović et al. Balk J Dent Med, Vol 23, 2019

58. Bufalo MC, Bordon-Graciani AP, Conti BJ, Golim MA, 76. Sterer N, Rubinstein Y. Effect of various natural medicinals Sforcin JM. The immunomodulatory effect of propolis on on salivary protein putrefaction and malodor production. receptorsexpression, cytokine production and fungicidal Quintessence Int, 2006;37:653-658. activity of human monocytes. J Pharm Pharmacol, 77. Wieckiewicz W, Miernik M, Wieckiewicz M, Morawiec 2014;66:1497-1504. T. Does propolis help to maintain oral health. Evid Based 59. Conti BJ, Bufalo MC, Golim MA, Bankova V, Sforcin Complement Alternat Med, 2013: Article ID 351062. JM. Cinnamic acid is partially involved in propolis 78. Bruschi ML, Jones DS, Panzeri H, Gremiao MPD, De immunomodulatory action on human monocytes. Evid Freitas O, Lara EHG. Semisolid systems containingpropolis Based Complement Alternat Med, 2013; Article ID 109864 for the treatment of : in vitro 60. Sforcin JM, Orsi RO, Bankova V. Effect of propolis, releasekinetics, syringeability, rheological, textural and some isolated compounds and its source plant on antibody mucoadhesive properties. J Pharm Sci, 2007;96:2074-2089. production. J Ethnopharmacol, 2005;98:301-305. 79. Toker H, Ozan F, Ozer H, Ozdemir H, Eren K, Yeler H. 61. Olczyk P, Komosinska-Vassev K, Wisowski G, Mencner A morphometric and histopathologic evaluation of the L, Stojko J, Kozma EM. Propolis modulates fibronectin effects of propolis on alveolar bone loss in experimental expression in the matrix of thermal injury. Biomed Res Int, periodontitis in rats. J Periodontol, 2008;79:1089-1094. 2014;2014:748101 80. Jamali A, Roostaee MH, Soleimanjahi H, Ghaderi pakdel F, 62. Antunović R. Bolesti usta, zuba i parodonta, Sveučilište Bamdad T. DNA vaccine-encoded glycoprotein B of HSV-1 sjever, Sveučilišni centar Varaždin, 2015;1-18 fails to protect chronic morphine-treated mice against 63. Laskaris G. Atlas oralnih bolesti, Naklada Slap. Zagreb, 2005. 64. Ikeno K, Ikeno T, Miyazawa C. Effects of propolis on dental HSV-1 challenge. Comp Immunol Microbiol Infect Dis, caries in rats. Car Res, 1991;25:347-351. 2007;30:71-80. 65. Duarte S, Rosalen PL, Hayacibara MF, Cury JA, Bowen 81. Schnitzler P, Neuner A, Nolkemper S, Zundel C, Nowack WH, Marquis RE et al. The infuence of a novel propolis on H, Sensch KH et al. Antiviral activity and mode of action mutans streptococci biofilms and caries development in rats. of propolis extracts and selected compounds. Phytother Res, Arch Oral Biol, 2006;51:15-22. 2010;24:20-28. 66. Ozan F, Sümer Z, Polat ZA, Er K, Ozan U, Deger 82. Shimizu T, Takeshita Y, Takamori Y, Hisahiro Kai, Rie O. Effect of mouthrinse containing propolis on oral Sawamura, Hiroki Yoshida et al. Efficacy of Brazilian microorganismsand human gingival fibroblasts. Eur J Dent, Propolis against Herpes Simplex Virus Type 1 Infection 2007;1:195-201. in Mice and Their Modes of Antiherpetic Efficacies. Evid 67. Steinberg D, Kaine G, Gedalia I. Antibacterial effectof propolis Based Complement Alternat Med, 2011;2011:976196 and honey on oral bacteria. Am J Dent, 1996;9:236-239. 83. Preeti L, Magesh K, Rajkumar K, Karthik R. Recurrent 68. Koo H, Gomes BP, Rosalen PL, Ambrosano GM, Park YK, aphthous stomatitis. J Oral Maxillofac Patho, 2011;15:252-256. Cury JA. In vitro antimicrobial activity of propolis and 84. Samet N, Laurent C, Susarla SM, Samet-Rubinsteen N. The Arnica montana against oral pathogens. Arch Oral Biol, effect of bee propolis on recurrent aphthous stomatitis: a 2000;45:141-148. pilot study. Clin Oral Investig, 2007;11:143-147. 69. Botushanov PI, Grigorov GI, Aleksandrov GI. Aclinical 85. Ozan F, Polat ZA, Er K, Ozan U, Deger O. Effect of study of a silicate toothpaste with extract from propolis. propolis on survival of periodontal ligament cells: new Folia Medica, 2001;43:28-30. storage media for avulsed teeth. J Endod, 2007;33:570-573. 70. Bertolini PF, Biondhi Filho O, Pomilio A, Pinheiro 86. Gjertsen AW, Stothz KA, Neiva KG, Pileggi R. Effect SL, Carvalho MS. Antimicrobial capacity of Aloe vera of propolis on proliferation and apoptosis of periodontal andpropolis dentifrice against Streptoccocus mutans ligament fibroblasts. Oral Surg Oral Med Oral Pathol Oral strains intoothbrushes: an in vitro study. J Appl Oral Sci, Radiol Endod, 2011;112:843-848. 2012;20:32-37. 87. Magro-Filho O, De Carvalho AC. Topical effect of propolis 71. Tanasiewicz M, Skucha-Nowak M, Dawiec M, Król W, Skaba in the repair of sulcoplasties by the modified Kazanjian D, Twardawa H. Influence of hygienic preparations with a 3% technique, cytological and clinical evaluation. J Nihon Univ content of ethanol extract of Brazilian propolis on the state of Sch Dent, 1994:36:102-111. the oral cavity. Adv Clin Exp Med, 2012;21:81-92. 88. Lopes-Rocha R, Miranda JL, Lima NL, Oliveira Ferreira 72. Pereira EM, Da silva JL, Silva FF, De Luca PM, Ferreira F, Aparecida Marinho S, Dornela Verli F. Effect of topical FE, Lorentz TCM. Clinical Evidence of the Efficacy of a Mouthwash Containing Propolis for the Control of Plaque propolis and dexamethasone on the healing of oral surgical and Gingivitis: A Phase II Study. Evid Based Complement wounds. WHSA, 2012;5:25-30. Alternat Med, 2011; 2011:75024 89. Altan BA, Kara IM, Nalcaci R. Ozan F, Erdogan SM, Ozkut 73. Hidaka S, Okamoto Y, Ishiyama K, Hashimoto K. Inhibition MM. Systemic propolis stimulates new bone formation of the formation of oral calcium phosphate precipitates: the at the expanded suture: a histomorphometric study. Angle possible effects of certain honeybee products. J Periodont Orthod, 2013;83:286-291. Res, 2008;43:450-458. 90. Ahangari Z, Naseri M, Jalili M, Mansouri Y, Mashhadiabbas 74. Loesche WJ. The effects of antimicrobial mouthrinses on F, Torkman A. Effect of propolis on dentin regenerationand oral malodor and their status relative to US Food and Drug the potential Role of dental pulp stem cell in guinea pig. Administration regulations. Quintessence Int, 1990;30:311-318. Cell J, 2012;13:223-228. 75. Van den Broek AM, Feenstra L, De Baat C. A review of 91. Sabir A, Tabbu CR, Agustiono P, Sosroseno W. Histological the current literature on management of halitosis. Oral Dis, analysis of rat dental pulp tissue capped with propolis. J 2008;14:30-39. Oral Sci, 2005;47:135-138. Balk J Dent Med, Vol 23, 2019 Propolis On oral Health 9

92. Byström A, Sundqvist G. Bacteriologic evaluation of 100. Hay KD, Greig DE. Propolis allergy: a cause of oral the efficacy of mechanical root canal instrumentation in mucositis with ulceration. Oral Surg Oral Med Oral Pathol, endodontic therapy. Scand J Dent Res, 1981;89:321-328. 1990;70:584-586. 93. Pardi G. Detection of Enterococcus faecalis in teeth 101. Brailo V, Boras VV, Alajbeg I, Juras V. Delayed contact with endodontic treatment failure. Acta Odontol Venez, sensitivity on the and oral mucosa due to propolis-case 2009;47:110-121 94. Kayaoglu G, Omurlu G, Akca G, Gürel M, Gençay Ö, Sorkun report. Med Oral Patol Oral Cir Bucal, 2006;11:E303-304. K et al. Antibacterial activity of Propolis versus conventional 102. Budimir V, Brailo V, Alajbeg I, Vučićević Boras V, Budimir endodontic disinfectants against Enterococcus faecalis in J. Allergic contact cheilitis and perioral dermatitis caused infected dentinal tubules. J Endod, 2011;37:376-381. by propolis: case report. Acta Dermatovenerol Croat, 95. Ramos IF, Biz MT, Paulino N, Scremin M, Della Bona 2012;20:187-190. A, Barletta FB et al. Histopathological analysis of cortycosteroid-antibiotic preparation and propolispaste Conflict of Interests: Nothing to declair. formulation as intracanal medication after pulpectomy: an in Financial Disclosure Statement: Nothing to declair. vivo study. J Appl Oral Sci, 2012;20:50-56. Human Rights Statement: None reguired. 96. Gendreau L, Loewy ZG. Epidemiology and etiology of denture stomatitis. J Prosthodont, 2011;20:251-226. Animal Rights Statement: None reguired. 97. Santos VR, Gomes RT, De Mesquita RA, De Moura MD, França EC et al. Efficacy of Brazilian propolis gel Received on March 2, 2018. for the management of denture stomatitis: a pilot study. Revised on July 11, 2018. Phytother Res, 2008;22:1544-1547. Accepted on November 2, 2018. 98. Da Silva WJ, Rached RN, Rosalen PL, Del Bel Cury AA. Effects of nystatin, fluconazole and propolis on poly(methyl Correspondence: methacrylate) resin surface. Braz Dent J, 2008;19:190-196. 99. Menniti-Ippolito F, Mazzanti G, Vitalone A, Firenzuoli F, Marizela Šabanović Santuccio C. Surveillance of suspected adverse reactions Faculty of Technology, University of Tuzla to natural health products: the case of propolis. Drug Saf, Bosnia and Herzegovina 2008;31:419-423. e-mail: [email protected]

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L BALKAN JOURNAL OF DENTAL MEDICINE A ISSN 2335-0245 IC G LO TO STOMA

How to Maintain Oral Health in Children with Respiratory Diseases –Literature Review

SUMMARY Aleksandar Sovtic1,2, Tamara Peric3, The most frequent chronic respiratory problems in childhood are Predrag Minic1,2, Dejan Markovic3 asthma and cystic fibrosis (CF). The purpose of this paper is to review 1 Department of Pulmonology, Mother and Child basic knowledge and recent advances in oral health and associated dental Health Institute of Serbia “Dr Vukan Cupic”, morbidities in children with asthma and CF. This review considered clinical Belgrade, Serbia 2 trials and systematic reviews related to oral health in children with CRD. An Faculty of Medicine, University of Belgrade, online base Medline was searched to determine relevant papers, using the Belgrade, Serbia 3 Department of Paediatric and Preventive combination of the following terms: “asthma”, “cystic fibrosis”, “caries”, Dentistry, School of Dental Medicine, University “dental erosion”, and “oral health”. Oral health problems in children with of Belgrade, Belgrade, Serbia chronic respiratory diseases (CRD) may be influenced by natural course of the disease, pharmacotherapy (inhalation therapy with bronchodilators and inhaled corticosteroids in asthmatic patients, systemic antibiotics and pancreatic enzyme replacement therapy in CF patients), medication administration technique and nutritional habits. Children with CRD may have higher prevalence of oral diseases. Patients and their parents, but also general paediatricians and pulmonologists, should be aware of importance of good oral health. Dental practitioners should be more informed about risk factors and specificities of oral health in these patients. Preventive measures, early diagnosis and effective treatment strategies in children with CRD can reduce occurrence of oral diseases and improve patient’s quality of life. Key words: Asthma, Cystic Fibrosis, Oral Health, Dental Caries, Periodontal Disease, REVIEW PAPER (RP) Dental Erosion Balk J Dent Med, 2019;10-14

Introduction Table 1. Risk factors for oral diseases in children Dental caries Gingivitis Dental erosion Acute and chronic respiratory diseases (CRD) are the • Frequent use • Dehydratation of • Frequent exposure most frequent medical problems in childhood. Prevalence of fermentable oral mucosa due to of teeth to extrinsic of CRD is increasing worldwide, why dental practitioners carbohydrates the mouthbreathing and intrinsic acids should be more aware of the specificities of oral health in • Decreased • Decreased • Decreased salivary salivary flow salivary flow and flow and pH these patients. Specificities of particular clinical problems and pH subsequent reduced in patients with CRD come from natural course of the • Increased counts concentration of disease, pharmacotherapy and nutritional risk factors that of Streptococcus secretory IgA have not favourable impact on the appearance of oral mutans and • Alteration of diseases. Risk factors associated with oral diseases in Lactobacilli immune response children are presented in Table 1. The purpose of this paper is to review basic knowledge and recent advances in oral health and Material and Methods associated dental morbidities in two most common chronic respiratory diseases in childhood - asthma and This review considered clinical trials and systematic cystic fibrosis (CF). reviews related to oral health in children with CRD. An Balk J Dent Med, Vol 23, 2019 Oral Health and Respiratory Diseases 11 online base Medline was searched to determine relevant It was speculated that mouth breathing and higher intake papers, using the combination of the following terms: of sweet drinks, which are commonly used in an attempt “asthma”, “cystic fibrosis”, “caries”, “dental erosion”, and to eliminate the bad taste of the inhaled medication or “oral health”. The last search date was March 31st 2017. to reduce the desiccating effect of mouth breathing and reduced salivary flow, may be related to worse oral health Asthma in primary dentition7,8. On the other hand, several studies Asthma is a chronic inflammatory disease, with comparable methodology showed no relationship characterised by episodes of cough, wheezing, chest between asthma and caries incidence, regardless the age tightness and difficult breathing. Its prevalence in of the participants10-16. childhood is increasing worldwide, causing hospital It has been reported that asthmatics are in a higher admissions, school and work absenteeism, decreased risk to develop dental erosions17,18. This was explained quality of life and even asthma-related death. Latest by negative influence of frequent consumption of acidic Global initiative for asthma (GINA) estimated that the soft drinks, acidity of some nebulised solutions (pH<5.5), number of people with asthma in the world may be as and possible presence of gastroesophageal reflux disease, high as 334 million. Although prevalence of asthma which show the erosive effect. On the other hand, varies widely between the countries, it is estimated that Dugmore and Rock19 showed no differences in prevalence about 14% of the world’s children were likely to have had of dental erosions between asthmatic and healthy children. asthmatic symptoms1. Besides GINA, numerous national Respiratory disorders may also be associated with asthma-reduction plans established useful diagnostic enamel developmental defects. Guergolette et al.20 criteria and different treatment modalities which resulted reported higher prevalence of enamel defects in asthmatic in proper diagnosis and decrease of asthma exacerbations. than in healthy children with demarcated diffused The cornerstones of modern therapy are inhaled opacities being the most prevalent. Since ameloblasts are bronchodilators (mostly β2 agonists) and anti- highly sensitive to the lack of oxygen, authors assumed inflammatory drugs (inhaled corticosteroids (ICS). that enamel defects are attributable to the episodes of Systemic adverse effects such as decreased growth hypoxemia during amelogenesis. velocity, adrenal suppression or osteoporosis are not Chronic therapy with ICS, oral dryness due to mouth related with chronic use of low and moderate doses of breathing, and proinflammatory cytokine release in ICS. Local adverse effects- mostly dysphonia and oral persistent asthma have been related to greater incidence diseases are associated with frequent use of inhaled of gingivitis in asthmatic patients9,21,22. Children with bronchodilators or chronic use of ICS. Proper techniques allergic asthma phenotype frequently have associated of inhalation, use of spacers with metered-dose inhalers allergic rhinitis, manifested with various degree of nasal (MDI) and good oral hygiene may decrease the incidence obstruction. Partial nasal obstruction and reduced nasal of these complications. Most of the children with asthma clearance may cause pronounced mouth breathing with have a mild disease treated intermittently with inhaled reduced salivary flow. This leads to subsequent bigger 23 22 β2 agonists. Excessive and/or prolonged use of either accumulation of . McDeera et al. showed nebulised or β2 agonists from MDI can lead to a reduced raised prevalence of dental in asthmatic children salivary flow which is essential for oral health. Alteration which can be contributed to the increased concentrations of protective role of saliva leads to increased number of salivary calcium and phosphate ions24. of cariogenic microorganisms2-4. A dry powder inhaler Asthmatic children, especially those with associated (DPI) is a device that delivers asthma medication in allergic rhinitis, may have facial dysmorhism with size of respirable particle (from 1-5μm in diameter) in increased facial height, higher palatal vaults, overjets mixture with excipients which carries the active drug. and posterior crossbites25,26. It is probably caused by Most commonly used carrier is carbohydrate - lactose difficulty breathing, preferable mouth breathing due to monohydrate. During inhalation from DPI, drug particles nasal obstruction and diminished respiratory reserve in separate from the carrier and carried into small airways in those patients with severe airway obstruction. the lungs. Larger, lactose particles, are deposited on the From the above, it is clear that attitudes about the oropharyngeal mucosa which can contribute to elevated oral health of children with asthma are not consistent. caries risk5. Some epidemiological and clinical studies showed It has been suggested that asthmatic patients may no relationship between asthma and oral diseases, have a higher risk for oral diseases, either as a result of while other studies demonstrated an increased risk for the medical condition or as adverse effects of medication. oral diseases in asthmatic patients. However, authors A higher prevalence of caries in school children6 and suggesting increased incidence of caries, gingivitis, adolescents7-9 with asthma compared with healthy candidiasis, tooth erosion, changes in the salivary children has been reported. Ersin et al.6 demonstrated flow and composition, etc. emphasized difficulties in that the duration of therapy and seriousness of the disease finding the exact reason for higher prevalence of oral had significant influence on the caries risk in asthmatics. diseases in children with asthma27-29. One of the possible 12 Aleksandar Sovtic et al. Balk J Dent Med, Vol 23, 2019 explanations for the differences between the studies may initial bacterial infection or chronic colonization of lower be the nonhomogeneity of the samples, i.e. severity of the airways in infancy and childhood (mostly Staphylococcus disease and specificity of the inhalation drugs used by the aureus), consists of chronic use of β-lactam antibiotics. subjects in diverse studies. It may also reduce cariogenic flora, i.e. Streptococcus mutans which is susceptible to β-lactams33,39,40, and Cystic Fibrosis decreases plaque pathogenicity32. Over the ages, CF is the most common autosomal-recessive disease predominant pathogen in CF lungs becomes Pseudomonas in Caucasians, with an incidence of 1:1.700-1:40.000 aeruginosa. Usual therapies are chronic treatments with newborns. It is caused by a mutation in a gene located in inhaled tobramycin or colomycin, which are not effective the long of chromosome 7, coding for the complex against Streptococcus mutans. Therefore, adolescents and protein called cystic fibrosis transmembrane regulator adults may lose protection against caries40. (CFTR). The main function of CFTR is transepithelial Increased salivary pH and higher concentration chloride transport. In case of nonfunctional ion membrane of calcium in saliva may result in increased calculus transport, secretions in the exocrine glands (including formation37. The prevalence of dental calculus formation salivary glands) become thick and dehydrated. This results was not found to be significantly different between in systemic illness with dominant obstructive, suppurative children with CF and other chronic respiratory diseases43. lung disease that leads to diffuse bronchiectasis and Children with CF may have dental maturation delay chronic respiratory insufficiency as a main cause and higher risk for development of systemic enamel of dead. In most of the cases, CF patients also have defects44. It was speculated that this was probably caused maldigestion due to exocrine pancreatic insufficiency that by metabolic and nutritional disorders and frequent leads to malnutrition which correlates to unfavourable use of antibiotics, which can have influence on teeth outcome. In the last decades, there have been numerous development42. Ferrazzano et al.42 found enamel defects improvements in early diagnosis and different treatment in 55.6% of CF patients, while they were present in 22.7% modalities, including lung transplant, with increased life of healthy persons. In addition, more severe enamel expectancy and quality of life in patients with CF30,31. defects with hypoplasia and partial loss of enamel had Therapy consists of high-calorie diet, pancreatic enzyme been noted in the CF group. Azevedo et al.45 showed no replacement therapy (PERT), fat soluble vitamins difference in occurrence of lesions on , but supplementation and medications that lead to increased enamel defects on permanent teeth were more prevalent in mucus clearance (bronchodilators, mucolytics). In CF children than in healthy controls. High prevalence of addition, patients are treated with inhaled and systemic tetracycline discolorations associated with frequent use of antibiotic therapy in order to control chronic bacterial these drugs in the past35,36 is not common nowadays. colonization in lower airways or treat exacerbation of One of less frequent indicators of current malpractice suppurative lung disease. in CF treatment is an inadequate administration of PERT, Children and adolescents with CF are thought to be which happen because of improper use of product that is at an increased risk for oral diseases. This was thought to commercially available. Exocrine pancreatic insufficiency be related to the high calorie diet with frequent in-between is clinically manifested by symptoms of maldigestion sugar-rich meals, which may contribute to the high caries (greasy stools, flatulation, abdominal pain, rectal risk32,33. In order to preserve lung function and increase prolapses) when residual pancreatic function is <10%. mucociliary clearance, inchalatory bronchodilators Mainly of porcine origin, enteric-coated microsphere are used regularly, which may reduce salivary flow34. preparations were designed to avoid inactivation by acidic However, the results of numerous studies showed that environment in the stomach. It dissolves in the duodenum children with CF have significantly lower incidence when pH becomes alkaline. In case of crushing or of caries35-40 and better gingival health32,41,42 when chewing of microspheres in the mouth, severe oral lesions compared to healthy peers. It has also been shown that may appear and, in addition, symptoms of maldigestion the incidence of dental caries in the primary dentition was persist. Irritation of the oral mucosa may be avoided by lower in children with CF in comparison with children swallowing and not chewing the medications, or mixing with other chronic respiratory diseases43. One of the them in foods46. explanations could be that CF patients probably maintain better oral hygiene to prevent spread of oral infections into the lungs33, but better oral hygiene habits were not confirmed32,40. It has also been suggested that CF patients Conclusions have significantly higher salivary pH and buffering capacity37 which may act as a compensatory mechanism Children with CRD may have higher prevalence of and contribute to the lower caries profile. It is most likely oral diseases influenced by numerous contributing factors that the chronic use of antibiotics reduces the incidence of in compare to healthy peers. Dental practitioners should caries in children with CF. Early eradication strategies of be more informed about risk factors and specificities of Balk J Dent Med, Vol 23, 2019 Oral Health and Respiratory Diseases 13 oral health in these patients. Patients and their parents 11. Meldrum AM, Thomson WM, Drummond BK, Sears MR. should be educated about importance of oral health and Is asthma a risk factor for dental caries? Finding from a possible severe general health consequences in case of cohort study. Caries Res, 2001;35:235-239. presence of oral diseases or its complications. It seems 12. Shulman JD, Taylor SE, Nunn ME. The association between that the occurrence of oral changes could be influenced by asthma and dental caries in children and adolescents: a population-based case-control study. Caries Res, improper use of inhalation and PER therapy. Therefore, 2001;35:240-246. it is important to educate children and their parents 13. Shulman JD, Nunn ME, Taylor SE, Rivera-Hidalgo F. The on the proper use of these medicines. Although strict prevalence of periodontal-related changes in adolescents clinical protocols for the prevention of oral diseases in with asthma: results of the Third Annual National Health patients with CRD have not been defined so far, it would and Nutrition Examinations Survey. Pediatr Dent, be of great importance if general paediatricians and 2003;25:279-284. pulmonologists would be aware of importance of good 14. Ferrazzano GF, Sangianantoni G, Cantile T, Amato I, Ingenito oral health suggesting regular dental examinations every A, Noschese P. Dental health in asthmatic children: a South three months. Preventive measures, early diagnosis and Italy study. J Dent Child, 2012;79:170-175. 15. Ehsani S, Moin M, Meighani G, Pourhashemi SJ, effective treatment strategies can reduce occurrence of Khayatpisheh H, Yarahmadi N. Oral health status in oral diseases and make their complications less frequent preschool asthmatic children in Iran. J Allergy Asthma which all may have significant impact on possible Immunol, 2013;12:254-261. co-morbidities and patient’s quality of life. 16. Markovic D, Peric T, Sovtic A, Minic P. Oral health in children with asthma. Srp Arh Celok Lek, 2015;143:539-544. 17. Sivasithamparam K, Young WG, Jirattanasopa V, Priest J, Khan F, Harbrow D et al. Dental erosion in asthma: A References case-control study from south east Queensland. Austr Dent J, 2002;47:298-303. 1. 2017 GINA Report, Global Strategy for Asthma 18. Al-Dlaigan YH, Shaw L, Smith AJ. Is there a relationship Management and Prevention. Available from: http:// between asthma and dental erosion? A case control study. Int ginasthma.org/2017-gina-report-global-strategy-for-asthma- J Paediatr Dent, 2002;12:189-200. management-and-prevention/ 19. Dugmore CR, Rock WP. Asthma and tooth erosion. Is there 2. Ryberg M, Moller C, Ericson T. Effect of beta an association? Int J Paediatr Dent, 2003;13:417-424. 2-adrenoceptor agonists on saliva proteins and dental caries 20. Guergolette RP, Dezan CC, Frossard WTG, Ferreira in asthmatic children. J Dent Res, 1987;66:1404-1406. FB, Cerci Neto A, Fernandes KB. Prevalence of 3. Ryberg M, Moller C, Ericson T. Saliva composition and developmental defects of enamel in children and adolescents caries development in asthmatic patients treated with with asthma. J Bras Pneumol, 2009;35:295-300. ß2-adrenoceptor agonists: a 4-year follow-up study. Scand J 21. Steinbacher DM, Glick M. The dental patient with asthma: Dent Res, 1991;99:212-218. an update and oral health considerations. J Am Dent Assoc, 4. Mazzoleni S, Stellini E, Cavalleri E. Dental caries in 2001;132:1229-1239. children undergoing treatment with short-acting β2-agonists. 22. McDerra EJ, Pollard MA, Curzon ME. The dental status Eur J Paediatr Dent, 2008;9:132-138. of asthmatic British school children. Pediatr Dent, 5. Tootla R, Toumba KJ, Duggal MS. An evaluation of the 1998;20:275-283. acidogenic potential of asthma inhalers. Arch Oral Biol, 23. Dykewicz M. Rhinitis and sinusitis. J Allergy Clin Immun, 2004;49:275-283. 2003;111:S520-529. 6. Ersin NK, Gülen F, Eronat N, Cogulu D, Demir E, Tanaç 24. Wotman S, Mercadante J, Mandel ID, Goldman RS, R et al. Oral and dental manifestations of young asthmatics Denning C. The occurrence of calculus in normal children, related to medication, severity and duration of condition. children with cystic fibrosis, and children with asthma. J Pediatr Int, 2006;48:549-554. Periodontol, 1973;44:278-280. 7. Stensson M, Wendt LK, Koch G, Oldaeus G, Birkhed D. 25. Bresolin D, Shapiro PA, Shapiro GG, Chapko MK, Dassel Oral health in preschool children with asthma. Int J Paediatr S. Mouth breathing in allergic children: its relationship to Dent. 2008;18:243-250. dentofacial development. Am J Orthod, 1983;83:334-340. 8. Stensson M, Wendt LK, Koch G, Nilsson M, Oldaeus 26. Venetikidou A. Incidence of malocclusion in asthmatic G, Birkhed D. Oral health in pre-school children with children. J Clin Pediatr Dent, 1993;17:89-94. asthma- followed from 3 to 6 years. Int J Paediatr Dent, 27. Ellepola AN, Samaranayake LP. Inhalational and topical 2010;20:165-172. steroids, and oral candidiosis: a mini review. Oral Dis, 9. Stensson M, Wendt LK, Koch G, Oldaeus G, Ramberg P, 2001;7:211-216. Birkhed D. Caries prevalence, caries-related factors and 28. Kargul B, Tanboga I, Ergeneli S, Karakoc F, Dagli E. plaque pH in adolescents with long-term asthma. Caries Inhaler medicament effects on saliva and plaque pH in Res, 2010;44:540-546. asthmatic children. J Clin Pediatr Dent, 1998;22:137-140. 10. Bjerkeborn K, Dahllöf G, Hedlin G, Lindell M, Modéer 29. Shaw L, Al-Dlaigan YH, Smith A. Childhood asthma and T. Effect of disease severity and pharmacotherapy dental erosion. J Dent Child, 2000;67:102-106. of asthma on oral health in asthmatic children. Scand J Dent 30. O’Sullivan B, Freedman S. Cystic fibrosis. Lancet, Res, 1987;95:159-164. 2009;373:1891-1904. 14 Aleksandar Sovtic et al. Balk J Dent Med, Vol 23, 2019

31. Ratjen. F. Recent advances in cystic fibrosis. Paediatr Respir 41. Aps JK, Van Maele GO, Martens LC. Oral hygiene habits Rev, 2008;9:144-148. and oral health in cystic fibrosis. Eur J Paediatr Dent, 32. Aps JK, Van Maele GO, Martens LC. Caries experience 2002;3:181-187. and oral cleanliness in cystic fibrosis homozygotes and 42. Ferrazzano GF, Orlando S, Sangianantoni S, Cantile T, heterozygotes. Oral Surg Oral Med Oral Pathol Oral Radiol Ingenito A. Dental and periodontal health status in children Endod, 2002;93:560-563. affected by cystic fibrosis in a southern Italian region. Eur J 33. Chi DL. Dental caries prevalence in children and Paediatr Dent, 2009;10:65-68. adolescents with cystic fibrosis: a qualitative systematic 43. Narang A, Maguire A, Nunn J, Bush A. Oral health review and recommendations for future research. Int J and related factors in cystic fibrosis and other chronic respiratory disorders. Arch Dis Child 2003; 88(8):702-707. Paediatr Dent, 2013;23:376-386. 44. Fernald GW, Roberts MW, Boat TF. Cystic fibrosis: A 34. Peker S, Kargul B, Tanboga I, Tunali-Akbay T, Yarat current review. Pediatr Dent 1990; 12:72-78. A, Karakoc F et al. Oral health and related factors in a group 45. Azevedo TD, Feijó GC, Bezerra AC. Presence of of children with cystic fibrosis in Istanbul, Turkey. Niger J Developmental Defects of Enamel in Cystic Fibrosis Clin Pract, 2015;18:56-60. Patients. J Dent Child 2006;73:159-163. 35. Jagels AE, Sweeney EA. Oral health of patients with cystic 46. Fieker A, Philpott J, Armand M. Enzyme replacement fibrosis and their siblings. J Dent Res, 1976;55:991-996. therapy for pancreatic insufficiency: present and future. Clin 36. Primosch RE. Tetracycline discoloration, enamel defects, Exp Gastroenterol 2011;4:55-73. and dental caries in patients with cystic fibrosis. Oral Surg Oral Med Oral Pathol, 1980;50:301-308. Conflict of Interests: Nothing to declair. 37. Kinirons MJ. Increased salivary buffering in association Financial Disclosure Statement: Nothing to declair. with a low caries experience in children suffering from Human Rights Statement: None reguired. cystic fibrosis. J Dent Res, 1983;62:815-817. Animal Rights Statement: None reguired. 38. Kinirons MJ. Dental health of patients suffering from cystic Received on May 17, 2018. fibrosis in Northern Ireland. Community Dent Health, Revised on July 11, 2018. 1989;6:113-120. Accepted on December 3, 2018. 39. Kinirons MJ. The effect of antibiotic therapy on the oral health of cystic fibrosis children. Int J Paediatr Dent, Correspondence: 1992;2:139-143. 40. Peker S, Mete S, Gokdemir Y, Karadag B, Kargul Tamara Peric Department of Paediatric and Preventive Dentistry B. Related factors of dental caries and molar incisor School of Dental Medicine hypomineralisation in a group of children with cystic University of Belgrade, Belgrade, Serbia fibrosis. Eur Arch Paediatr Dent, 2014;15:275-280. e-mail: [email protected]

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Change in Patients’ Self-Reported Quality of Life before and after Dental Implantation

SUMMARY Bożena Mroczek1, Małgorzata Anna Lichota1, 2 3 Background/Aim: The loss of teeth and its consequences for health, as Grzegorz Trybek , Anna Grzywacz well as the psychological discomfort it entails, have a negative impact on 1 Department of Human Sciences in Medicine of both self-reported health state and quality of life (QoL). Dental implantation the Pomeranian Medical University in Szczecin, aims to increase patients’ health and satisfaction and to improve all aspects Poland 2 of QoL. The purpose of this cross-sectional correlational study was to Department of Oral Surgery, of the Pomeranian Medical University in Szczecin, Poland compare the patients’ QoL before and after dental implantation. Material 3 Independent Laboratory of Health Promotion of and Methods: The study comprised 62 patients aged between 24 and the Pomeranian Medical University in Szczecin, 77, including 28 (45.16%) women and 34 (54.84%) men, who reported Poland to a private dental clinic in Szczecin, Poland to replace missing teeth with implants. The survey was carried out twice: prior to the treatment, when the decision to use implants had been made, and three months after implantation, during the first check-up. QoL was measured using the 36-Item Short Form Health Survey (SF-36), and sociodemographic data were collected using a questionnaire of the author. Results: There were statistically significant differences between the assessment of health and QoL before and after implantation treatment. Both the patients’ health and comfort of life improved after therapy. Conclusions: Replacement of missing teeth with dental implants brought overall improvement in patients’ QoL, social comfort, and general health. Dental implantation should be recommended in the early phase of edentulism, after tooth loss. ORIGINAL PAPER (OP) Key words: Dental Implantation, Oral Health-Related Quality of Life, Health Survey Balk J Dent Med, 2019;15-19

Introduction revealed significant relationships between QoL, overall oral status, orthodontic treatment, and treatment with The loss of teeth is a serious life event that impairs prosthetic implants3, 8. two important functions, eating and speaking, and may QoL is defined as an individual’s perception of his or be accompanied by problems such as pain and bleeding her position in life, within the cultural context and value associated with gum disease. It thus affects various system he or she lives in, and in relation to his or her 6, 9 aspects of Quality of Life (QoL). Patients experience goals, expectations, parameters, and social relations . pain and psychological discomfort1-2. Somatic diseases QoL is regarded as a dynamic construct that changes over may cause pathological changes within the oral cavity, time, and which can be affected by health problems that 5 potentially leading to partial or complete edentulism and, occur . As a vital outcome of therapy, QoL is rated among consequently, to the need to replace the missing teeth with the so-called soft effects of treatment, since it modifies the implants1, 3-5. internal and external conditions affecting the individual. QoL and general health can serve as important Researchers examining the effect of edentulism on indicators of the effects of a treatment, and should be the oral health-related quality of life (OHRQoL) have taken into account during oral diagnosis, interventions, demonstrated that patients suffering from this problem and the application of procedures5-7. Recent studies have had lower levels of QoL, higher levels of functional 16 Bożena Mroczek et al. Balk J Dent Med, Vol 23, 2019 limitation, more severe physical and psychological pain, dental implantation (this usually took place three months and more serious sleep and digestive disorders10-12. The after the treatment). purpose of prosthetic treatment is to alleviate tooth loss- The criteria for inclusion in the study were age related functional and esthetic problems, and to improve at least 18 years, committed to dental implantation, QoL. According to Levi, one factor that motivates people agreement to take part in both surveys, successfully to choose a particular method of tooth replacement is the completed implantation treatment, and attending the check-up. Each patient was examined by a using esthetic aspect13. Patients who decide to undergo dental a mirror and a probe under artificial lighting. The dentist implantation feel a difference in their own perception of assessed the patients’ needs for treatment and the oral themselves14. Dental implants are made of titanium and health status. are inserted directly into the jawbone. On account of the osseointegration and mechanical stability they offer, they Procedure serve as pillars for prosthetic filling. Bone grows up to Our study was approved by the Bioethics Committee the implant surface, meaning that the implant can function of the Pomeranian Medical University in Szczecin, as a natural tooth. Providing that hygiene principles are Poland (approval no. KB–0012/41/05/15). The patients obeyed, implants should continue to function properly. participated in the study voluntarily and gave their Implantation treatment aims to reconstruct missing informed consent. The study was conducted in accordance teeth, thus restoring the normal functioning of the with the guidelines of the Helsinki Declaration and the stomatognathic system, providing lips with support and, principles of Good Clinical Practice, as well as with consequently, restoring facial profile and improving respect for the rights and dignity of the person. appearance. Implant-based definitive dental prostheses Evaluation of oral health-related quality of life are widely applied as a highly efficient prosthetic (OHRQoL) treatment method11, 15. Some researchers maintain that the QoL related to edentulism, as well as its health, The research instruments used in this survey-based study were the 36-Item Short Form Health Survey (SF- functional, psychological, and social consequences, the 36) and a questionnaire of the author’s devising (AQ). therapy employed, and oral hygiene during implantation 10, 16-17 We obtained permission from Quality Metric, Inc. to use treatment has not yet been fully described . An the authorized Polish Version of the SF-36. The SF-36 important contributor to QoL is the overall health and oral questionnaire consists of 36 questions divided into eight hygiene status. QoL assessment is widely used in dental subscales: role physical (RP), mental health (MH),bodily medicine, since it provides information about changes in pain (BP), general health (GH), physical functioning patients’ self-perceived health and QoL level in the course (PF),vitality (V), social functioning (SF), role emotional of the pathological process and after dental treatment. (RE), and one additional question concerning health Nevertheless, as Riordain et al. ave pointed out, there change18, 19. Score on the Likert scale for each of these is still too little evidence for improvement in QoL after areas ranges from 0 to 100, with 0 denoting the worst implantation treatment4. and 100 the best possible health state. SF-36 is not time- The aim of this study was to compare the QoL of consuming to use, and its usefulness, repeatability, patients subjected to treatment before and ability to reveal changes in QoL have been and after the treatment. We assumed that this method of demonstrated20. The author’s questionnaire contained replacing missing teeth has an effect on QoL and the self- 20 simple structured questions aimed at (1) demographic reported health state. data collection (age, sex, place of residence, education, marital status, financial income), (2) selected clinical data concerning implantation treatment.

Material and Methods Statistical Analysis The normality of variables distribution was Study Design verified using the Shapiro-Wilk test. The variables This was a longitudinal clinical study with selected were characterized by arithmetic means (X), standard predictor variables. We formulated the hypothesis that, the deviations (SD), medians (M), and extremes (min–max). patients’ QoL would be considerably improved following Statistical analysis was performed using the chi-square implantation. The survey was carried out twice during test, Student’s t-test, analysis of variance (ANOVA), 2015 using the same questionnaire: once at the initial visit the correlation coefficient, and Cronbach’s alpha, in (V1), during which the doctors and patients established order to assess the reliability of the results in particular the protocol of dental implant treatment (including SF-36 domains. All tests were performed at a statistical treatment date), and then on the first check-up (V2), after significance level of α = 0.05. Balk J Dent Med, Vol 23, 2019 Quality of Life Regarding Implantation 17

Results (16 - 57.14%), and the men as good or average (22 - 64.7%), Participants 2. There was a statistically significant relationship The study comprised 62 participants, including between health assessment three months before 28 (45.2%) women and 34 (54.8%) men, aged between treatment (X= 6.78 ± 1.85) and three months after treatment (X= 8.64 ± 1.50) (Table 2), 24 and 77. The mean age of the participants was MAGE = 55.77 years, and the standard deviation (SD) was Table 2. Self-assessment of patients’ health status before and 12.01 for the entire group; MFemale = 52.61 ± 12.88 after treatment (range: 24–77), MMale = 58.38 ± 10.73 (range: 28–73). Sociodemographic data are shown in table 1. The majority Health self-assessment t-Student test of the participants had tertiary (43 - 69.35%) or secondary X SD p (18 - 29.03%) education; one person, a man (1.62%), had Before treatment 6.78 1.85 F= -7.502 no higher than vocational education. After treatment 8.64 1.50 p<0.001

Table 1. Sociodemographic data of the participants (n=62) 3. Health assessment statistically significantly depended on economic status (p= 0.04); the higher patient’s Variables n % economic status, the better health assessment, Age X ± SD 55.77±12.01 4. Patients observed positive changes in their comfort mini-max 24-77 of life, which were reflected in higher health Gender assessment (p= 0.05). Women X±SD 52.61±12.88 mini-max 24 - 77 Quality of life Men X±SD 58.38±10.73 1. The highest score was obtained for the physical mini-max 28 - 73 functioning (PF) (X= 89.68 ± 14.43), and the lowest Place of residence urban area 53 85.48 for the general health (GH) (63.87 ± 18.34) and (population): rural area 9 14.52 vitality (V) (73.63 ± 16.17) domains. Cronbach’s Economic status: very good 28 45.16 alpha was calculated for each of the SF-36 scales. good 30 48.38 For the physical functioning (PF), mental health average 4 6.45 (MH), vitality (V), bodily pain (BP), and general Employment employed 46 74.19 health (GH) domains, alpha was > 0.7, which unemployed 16 25.81 suggested high reliability of the scales; for the role Education master’s degree 43 69.35 physical (RP) and role emotional (RE) domains, secondary 18 29.03 alpha was < 0.7, vocational 1 1.61 2. The women scored higher for physical functioning (PF) than the men (p= 0.03), and the younger patients Tooth loss among the study subjects was mostly (aged up to 60 years) scored higher than those over caused by dental caries (tooth decay) (24 - 38.71%), 60 (p= 0.01), neglect of oral hygiene (19 - 30.65%), and periodontal 3. The correlation coefficient for the physical disease (20 - 32.26%). The prevailing causes among the functioning (PF) and role physical (RP) domains was women were dental caries (11 - 39.29%) and periodontal 0.718 (p< 0.001), while for the mental health (MH) disease (10 - 35.71%), and among the men, dental caries and vitality (V) domains, this was 0.756 (p< 0.001), (13 - 38.24%) and oral hygiene neglect (13 - 38.24%). 4. The lowest scores for general health (GH) were The main factor motivating the patients as a whole (50 - obtained by the patients aged between 56 and 60 80.65%) to choose implantation treatment was the esthetic years, while the highest was obtained by those aspect; the main factor motivating the women (23 - younger than 55 (p= 0.005). The lowest scores were 82.14%) was psychological comfort, and the main factor obtained by patients with vocational and secondary motivating the men (30 - 88.24%) was the esthetic aspect. education only, and the highest by those with third- level education (p< 0.001), Health assessment before and three months after 5. The largest changes in health status were reported by implantation treatment (on the check-up): patients over 60, and the smallest by patients aged up 1. The participants described their health as excellent to 55 years (p= 0.05), (3 - 4.84%) or very good (25 - 40.32%), The mean 6. Higher economic status was associated with an score was 8.77 ± 4.29. The women more often increase in the average score for the vitality (V) QoL described their health state as excellent or very good domain (p= 0.03), 18 Bożena Mroczek et al. Balk J Dent Med, Vol 23, 2019

7. City dwellers assessed their social functioning (SF) implementation, patients found their QoL to be noticeably higher than their counterparts from rural areas (p= 0.03). higher, whereas the QoL of patients with dentures was definitely lower16. Similar results, confirming the Changes in comfort of life alleviation of physical pain and psychological discomfort, 1. The majority of both the women (18 - 64.29%) and have been reported by Yoshida et al.17. We observed a the men (25 - 73.53%) felt that their eating comfort statistically significant relationship between the patients’ had considerably improved, health assessment before the treatment and three months 2. After treatment, 89.29% of the women (n= 25) and after it. We found that the assessment of patients’ 94.12% of the men (n= 32) observed that their health health changed significantly, after implantation it was status and their comfort of life significantly improved significantly higher by 2 units on average. - a total of 91.94% (n= 57), In his study, Yoshida measured chronological change 3. Both the women and the men were very satisfied in the QoL level during implantation treatment in a group with the effects of implantation treatment. The mean of 20 patients with a small number of missing teeth (less score achieved by the women was 9.14, and by the than 4 teeth), who underwent implantation treatment17. men 9.24 (total 9.19), The patients completed the shortened Japanese 4. The results concerning comfort of life before and version of the Oral Health Impact Profile (OHIP-J14) after implantation were compared. Health status after before surgery (T0), one week after surgery (T1), one dental implantation was assessed as lower by those week after interim prosthesis placement (T2), and 1 week patients whose comfort of life did not change and after definitive prosthesis placement (T3). Although assessed highest by those who did see a significant a temporary functional limitation was observed after change (p= 0.04). implant placement, overall OHRQoL improved after placement of the definitive prosthesis. What is more, implantation treatment was more effective in the unilateral free-end edentulous space. Similarly, in the study of Pavel Discussion et al., the most significant associations on the functional scale (FS) were observed with the number of front teeth The loss of teeth poses both health and esthetic replaced with implants, followed by the presence of problems. Patients can obtain satisfaction through chewing problems and marital status25. advanced implant treatment methods. Apart from the obvious esthetic advantages, dental implantation improves speaking and increases the comfort of biting and gustatory sensation, which translates into psychological and Conclusions physical well-being and a better health state1. Irrespective of age, reconstruction of missing teeth helps patients This study has demonstrated the significant effect 16, 21-23 regain their self-confidence . Polish-language of implantation, as a method of treating missing teeth, medical literature does not contain publications on the on the self-reported health state. Implantation treatment self-reported health state of implantology patients, as improved patients’ health, QoL, and comfort of life. assessed by the SF-36. Such studies can, however, be QoL as measured by the SF-36 was higher after the 5, 16, 21-23 found in the English-language literature . implantation treatment than before it. Dental implantation The mean age of the participants in our study was should be recommended in the early phase of edentulism, 56 ± 11.8 years. Hence, we can conclude that dental after tooth loss. implant treatment is appropriate for patients of all ages, and is worth recommending, considering the ease of maintaining good oral hygiene and the psychological Abbreviations comfort associated with the alleviation of digestive SF-36 - 36-Item Short Form Health Survey 24 problems . Patients’ major hesitation in deciding on AQ - Author’s Questionnaire dental implantation is related to its cost. Nevertheless, QoL - Quality of Life patients value their comfort and health, and so they often choose this treatment method, despite the cost. Our results demonstrate that the health state of our participants improved after implantation. They scored References higher in the social functioning (SF) and vitality (V) domains, and suffered less from emotional problems 1. Palma PV, Liparini Caetano P, Gonçalves Leite IC. Impact 16, 21 and limitations on their activity . Other studies have of Periodontal Diseases on Health-Related Quality of Life of compared changes in the QoL of patients with dentures Users of the Brazilian Unified Health System. Inter J Dent, and those with dental implants. Following dental 2013;2013:150357. Balk J Dent Med, Vol 23, 2019 Quality of Life Regarding Implantation 19

2. Sargoziale N, Moeintaghavi A, Shojaie H. Comparing the 18. Yoshida T, Masaki Ch, Hideki K, Misumi S, Mukaibo T, quality of life of patients requesting dental implants before Kondo Y, et al. Changes in oral health-related quality of life and after implant. Open Dent J, 2017;11:485-491. during implant treatment in partially edentulous patients: A 3. Kisely S. No mental health without oral health. Can J prospective study. J Prosthodont Res, 2016;60:258-264. Psychiatry, 2016;61:277-282. 19. Ware JE, Sherbourne CD. The MOS 36-item short-form 4. Riordain RN, Mccreary C. The use of quality of life health survey (SF-36). Med Care, 1992;30:473-483. measures in oral medicine: a review of the literature. Oral 20. Lungberg L, Johannesson M, Isacson GL, Borgquist L. Dis, 2010;16:419-430. Health-state utilities in a general population in relation to 5. Locker D, Quiñonez C. Functional and psychosocial age, gender and socioeconomic factors. Eur J Public Health, impacts of oral disorders in Canadian adults: a national 1999;9:211-217. population survey. J Can Dent Assoc, 2009;75:521. 21. Zawisza K, Tobiasz-Adamczyk B, Zapała J, Marecik T. 6. Silva CAB, Grando LJ, Luckmann Fabro SM, Ferreira de Validity and reliability of the SF-36 health questionnaire in Mello ALS. Oral health related to quality of life in patients patients with cancer of the head and neck. Polish Den Soc, with stomatological diseases. Stomatologija, 2015;17:48-53. 2009;62:751-763. 7. Bernabé E, Marcenes W. Periodontal disease and quality of 22. Heydecke G, Locker D, Awad MA, Lund JP, Feine JS. Oral life in British adults. J Clin Periodontol, 2010;37:968-972. and general health-related quality of life with conventional and implant dentures. Community Dent Oral Epidemiol, 8. Zhou W, Wang F, Monje A, Elnayef B, Huang W, Wu Y. 2003;31:161-168. Feasibility of dental implant replacement in failed sites: 23. Awad MA, Locker D, Korner-Bitensky N, Feine JS. a systematic review. Int J Oral Maxillofac Implants, Measuring the effect of intra-oral implant rehabilitation 2016;31:535-545. on health-related quality of life in a randomized controlled 9. The world oral health report 2003. World Health clinical trial. J Dent Res, 2000;79:1659-1663. Organization. Recommendations for Preventing Dental 24. Yao J, Tang H, Gao X-L, McGrath C, Mattheos N. Patients’ Diseases. expectations from dental implants: a systematic review of 10. http://www.who.int/oralhealth/publications/orh_cdoe05_ the literature. Health Qual Life Outcomes, 2014;12:153. vol33.pdf 25. Isaksson R, Becktor JP, Brown A, Laurizohn C, Isaksson S. 11. AlZarea BK. Oral health related quality of life outcomes of Oral health and oral implant status in edentulous patients partially edentulous patients treated with implant supported with implant-supported dental prostheses who are receiving single crowns or fixed partial dentures. J Clin Exp Dent, long-term nursing care. Gerodontology, 2009;26:245-249. 2017;9:e666-671. 26. Pavel K, Seydlowa M, Dostalova T, Zdenek V, Chleborad 12. Pjetursson BE, Thoma D, Jung R, Zwahlen M, Zembic A. K, Jana Z, et al. Dental implants and improvement of A systematic review of the survival and complication rates oral health-related quality of life. Community Dent Oral of implant-supported fixed dental prostheses (FDPs) after Epidemiol, 2012;40:65-70. a mean observation period of at least 5 years. Clin Oral Implants Res, 2012;23:22-38. Conflict of Interests: Nothing to declair. 13. Llewellyn CD, Warnakulasuriya S. The impact of Financial Disclosure Statement: Nothing to declair. stomatological disease on oral health-related quality of life. Human Rights Statement: All the procedures on humans were Eur J Oral Sci, 2003;111:297-304. conducted in accordance with the the Helsinki Declaration of 1975, 14. Levi A, Psoter WJ, Agar JR, Reisine ST, Taylor TD. as revised 2000, and with national ethical committee. Consent was Patient self-reported satisfaction with maxillary anterior obtained from the patient/s and approved for the current study by dental implant treatment. Int J Oral Maxillofac Implants, national ethical committee. 2003;18:113-120. Animal Rights Statement: None reguired. 15. Callan DP, Strong S. Creating the environment for implant Received on May 11, 2018. success: an interdisciplinary approach. Int J Dent Symp, Revised on July 2, 2018. 1995;3:48-51. Accepted on September 10, 2018. 16. Goodacre CJ, Bernal G, Rungcharassaeng K, Kan JY. Clinical complications with implants and implant Correspondence: prostheses. J Prosthet Dent, 2003;90:121-132. Anna Grzywacz 17. Allen, PF, McMillan AS. A longitudinal study of quality of Independent Laboratory of Health Promotion of the Pomeranian life outcomes in older adults requesting implant prostheses Medical University in Szczecin and complete removable dentures. Clin Oral Implants Res, Szczecin, Poland 2003;14:173-179. e-mail: [email protected]

10.2478/bjdm-2019-0004

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Evaluation of Permanent First Molar Tooth Loss in Young Population from North Turkey

SUMMARY Bilal Ozmen Background/Aim: Rate of missing permanent teeth in a population Faculty of Dentistry, Ondokuz Mayis University, is important for oral health indicators. The aim of this retrospective study Samsun, Turkey was to evaluate the prevalence of previously missing permanent first molar (PMF) teeth in a young population. Material and Methods: 1204 healthy patients who received panoramic radiographs were selected randomly at their first visiting to Samsun Ondokuz Mayis University Faculty of Dentistry. The patients’ age ranges were 7 to 17. Information about extracted permanent first molar teeth, missing regions, patients’ ages, and genders was recorded. The data were statistically analyzed using chi- square tests. Results: 1,204 patients, of these, 608 (51%) were female, and 596 (49%) were male. 4,816 PFM teeth were evaluated in this study, and 128 of them (2.66%) had extracted from 97 different patients. There were statistically differences between groups in terms of age and gender (p<0.05). It was observed that mandibular teeth were more frequently extracted than maxillary ones, and lower left permanent first molar teeth had more extracted than the others. Conclusions: The first permanent molar teeth could be extracted different reasons. However, these teeth should be protected by both and patients. ORIGINAL PAPER (OP) Key words: Age, Child, Permanent First Molar, Tooth Extraction Balk J Dent Med, 2019;20-23

Introduction prognosis, caries, orthodontic reasons and periodontal diseases7. Oral health care is part of general health, and it Early extraction of PFM teeth may cause undesirable is considered essential to an individual’s quality of rotation and mesial drifting of secondary permanent 8 life. Therefore, tooth loss is considered a public health molars . PFM teeth play an important role in balanced and normal occlusion9. Because of this, early extraction of problem1,2. Dental health programs are aimed to decrease PFM may affect whole occlusion and development of both dental plaque, tooth decay, periodontal disease and loss jaws. Additionally, asymmetry and temporomandibular of teeth3. Although many alternative practices have been joint problems may be observed8,10. For making a decision developed to protect oral health, early tooth loss is still a about extraction of PFM, dental pain, excessive material 4 big problem . loss, parental attitudes and toleration of dental treatment Permanent first molar (PFM) teeth are the first may affect indication. All conditions, in the developing developing permanent teeth in posterior region. However, dentition, should be assessed before extraction of PFM permanent first molar teeth have been characterized teeth11. as most caries-prone teeth in the mixed dentition5. In the present retrospective study was evaluated Additionally, 10-19% of PFM teeth were hypo- prevalence of missing permanent first molar teeth mineralization5,6. Consequently, PFM teeth may be lost at in young patients first admitted to Ondokuz Mayis an early age. Other reasons for PFM teeth loss were poor University, Pediatric Dentistry Clinic for examination. Balk J Dent Med, Vol 23, 2019 Permanent First Molar Tooth Loss 21

Material and Methods Table 2. The number of extracted first molar tooth Age 7 8 9 10 11 12 13 14 15 16 17 Total This study was performed in the north region of Female 0 1 0 1 3 9 11 18 16 15 5 79 Turkey (Middle Black Sea Region). Ethics approval was Male 0 1 1 3 10 1 13 5 10 5 0 49 obtained from the Ethics Committee of Medical Research Total 0 2 1 4 13 10 24 23 26 20 5 128 of Ondokuz Mayis University, Samsun, Turkey (2015/02). This study was performed in Ondokuz Mayis University, Considering the number of extracted teeth, gender, Faculty of Dentistry, and included 1,204 healthy patients age and region of jaws were all statistically significant (608 females and 596 males) who were admitted for (p<0.05). There was 49 (2.05%) extracted PFM teeth from the first time to Pediatric Dentistry Clinic for a routine dental control at first quarter of 2012. The patients’ age 38 males and 79 (3.25%) extracted PFM from 59 females ranges were 7 to 17, and they had received panoramic (p<0.05) (Figure 1). radiographs. Patients with edentulism due to a systemic disease were excluded from the study. Demographic information was recorded, including age and gender. Extracted PFM teeth, jaws, right or left side of the oral cavity were determined from panoramic radiographs. Extraction required teeth were not recorded. The data were collected retrospectively by the same physician. Statistical analyses were performed using SPSS version 22.0 (SPSS Inc., Chicago, IL, U.S.A.). All data were evaluated as frequency and percentage. Chi- square tests were used to compare relative differences in extracted PFM, gender, age and jaws. P<0.05 was accepted as statistically significant in comparisons. Figure 1. Distribution of the age and extracted PFM according to age and tooth number

Results Distribution of extracted PFM teeth according to the jaws and sides was showed in Table 3. There was In all, 1,204 patients were assessed. Of these, 608 statistical difference between the jaws but no in the sides. (51%) were females, and 596 (49%) were males (p>0.05). It was determined that 128 PFM teeth (2.66%) from a Table 3. Distribution of extracted PFM in the jaws and sides total of 4,816 had been extracted from 97 (8%) of 1,204 patients. Seventy patients had only one PFM tooth loss, Categories N (%) P value 23 patients had two, and four patients had three missing Jaw Maxilla 87 (68%) PFM teeth. No patient had four missing PFM teeth. The p<0.05 distributions by age, gender, and extracted first molar in 41 (32%) the subjects are summarized in Table 1 and Table 2. Side Right 68 (53%) p>0.05 Table 1. Distributions of patients according to age and gender Left 60 (47%) Female Male Total Extraction Extraction Extraction Age Yes* No Yes* No Yes* No 7 0 49 0 70 0 119 Discussion 8 1 64 1 64 2 128 9 0 75 1 88 1 163 For a long time, extraction of PFM has been subject 10 1 46 2 58 3 104 to debate. The extraction of PFM should be planned with 11 2 45 6 42 8 87 an orthodontist before the eruption of second and third 12 7 43 1 35 8 78 permanent molars. In recent years, orthodontists have 13 8 62 11 67 19 129 favored extraction and also have given indications for 14 12 47 4 51 16 98 extraction of PFM12,13. Pediatric dentists have to perform 15 14 61 8 43 22 104 complicated fillings that result in excessive material 16 11 53 4 38 15 91 loss in children who have dental anxiety and behavior- 17 3 4 0 2 3 6 management problems14,15. Also, these molar teeth must 59 549 38 558 97 1107 Total be kept in the mouth for preventive reasons. Sometimes, 608 596 1204 orthodontists may want to preserve these teeth because *The number of patients having at least one first molar tooth loss of orthodontic procedure13. Consequently, it is difficult 22 Bilal Ozmen Balk J Dent Med, Vol 23, 2019 to decide about PFM tooth extraction. Therefore, in the the rate of missing maxillary first molar teeth was 10%. present study, only the frequency of extracted PFM teeth Barbato and Peres20 showed that most missing teeth in was investigated. jaws were mandibular first molars. Demirbuga et al.18 Despite the researches, early tooth loss is still a big reported that rates of missing permanent first molar teeth problem, especially since the early loss of permanent first in mandibula were 2.77% (438) and 1.17% (185) teeth molars plays a key role in the asymmetry of dentition4,8,10. in maxilla. In the present study, the number of extracted Therefore, determination of the number of patients with PFM teeth in the lower arch was 87 and in the upper arch early loss of permanent first molars in the community will was 41. This situation can be explained by several factors. be beneficial. In the present study, although many cases One of them is that more nutrients remain in the lower jaw required tooth extraction etiologically, only extracted first than upper. Others are early eruption of mandibular teeth, molar teeth were investigated. In this study, the number caries, increased hypomineralization level, different effects of previously extracted permanent first molars was 128 of saliva and different anatomical structures of the teeth. (2.66%) of 4,816 PFM teeth in 97 (8%) of 1,204 patients. In the literature, there is limited information about The data were compared with previous studies16-18. early missing teeth on the left and right sides of the Alves et al.16 performed a study among 12-year- oral cavity in pediatric patients18. It was claimed that old schoolchildren from South Brazil. The researchers hand selection when tooth brushing may affect rates­ observed that tooth loss rate in 1,528 patients were 5.81%. of extraction on left or right sides of the oral cavity18. This rate was lower than in this study (8%) because they Similarly, chewing and cleaning habits and the residence included only patients who were 12 years of age. George time of food in the mouth may play important roles in et al.17 reported that rates of all missing permanent teeth ra­tes of extraction on the left or right sides of the jaws. in children and young people of 6, 12 and 15 ages were In contrast, Bhat et al.21 found no significant difference 5.7% 22% and 28.3%, respectively. These rates were between rates­ of extraction on the left and right sides higher than in this study because they had included of the oral cavity. Demirbuga et al.18 reported that right all permanent teeth. Atieh19 reported that the rate of side missing teeth numbered 302 (1.91%) and left side teeth loss in 484 patients aged 14-19 were 40.9% (198 missing teeth amount to 321 (2.03%), and they did not patients). This rate was higher than in this study because find statistical differences between the right and left sides they had included all permanent teeth. Demirbuga et al.18 of jaws. Similar to previous studies, this study’s results performed a study on 31,580 permanent first molar teeth showed that the numbers of formerly extracted PFM from 7,895 patients’ panoramic radiography, and reported teeth were 60 in the right side and 68 in the left side and that missing teeth rates from 19,488 teeth in 6-11 age showed no statistical differences. groups were 0.47% (122) and in 12-16 age groups from The ideal time for extraction of a PFM is at a 12,092 teeth were 4.14% (501). These results were very chronological age of 8-10 years11. Gill et al.23 claimed similar to the results in this study. that extraction of PFM with poor prognosis in this Several studies17,18,20 determined that gender may time interval should facilitate mesial movement of the influence tooth loss, which agrees with findings of present permanent second molar into the PFM area. Otherwise, study. Demirbuga et al.18 reported that of the 15,008 teeth extraction at a later age may result in unsatisfactory examined in the boys’ group, 1.84% (276) were missing, and inadequate space closure, condylar problems and in the girls’ group, of 16,572 teeth, 347 (2.09%) teeth and orthodontic malocclusion24. In the present study, were missing. George et al.17 determined that tooth loss according to age, the rate of missing teeth was 5.5% in rates in males (42.9%) were lower than in the females 8-10 age and 57% in 13-15 age, but the time of extraction (47.9%). Barbato and Peres20 claimed that this finding of the missing teeth was not known exactly. could be explained by the fact that females use more dental Nowadays, dental materials and treatment choices services due to their deeper health or aesthetic concerns, have rapidly evolved. Direct/indirect pulp capping, root which may lead to overtreatment. On the contrary, Bhat canal treatment, post-core, inlays/onlays, porcelain and et al.21 reported that the percentages of extracted teeth in ceramic crowns are good alternative treatments25. The males were 53.1% and in females­ were 46.9%. Jafarian results of the study showed that a large number of teeth and Etebarian7 assessed that males comprised 48.7% of had extracted between the ages of 11-16. Preventive patients, but they had more extracted teeth (56.1%) than treatments should be increased for preservation of natural females (43.9%). On the other hand, Susin et al.22 claimed dentition, especially, in females. that tooth loss was affected more by the age factor than by gender. They stated that the prevalence of tooth loss increased markedly with age from 26% to 60% in the age groups 14-19 and 25-29 years, respectively22. Conclusions Some studies stated that most missing teeth were in the mandibular20,21 . Bhat et al.21 determined that the rate In this retrospective study, mandibular first molar of missing mandibular first molar teeth was 21%, while teeth were more frequently missing than maxillary teeth, Balk J Dent Med, Vol 23, 2019 Permanent First Molar Tooth Loss 23 and females had more missing teeth than males. No 15. Jälevik B, Klingberg GA. Dental treatment, dental fear and difference existed between right and left side teeth loss. behaviour management problems in children with severe Even if PFM tooth loss is common in community, these enamel hypomineralization of their permanent first molars. Int J Paediatr Dent, 2002;12:24-32. cases are preventable. Therefore, several factors such 16. Alves LS, Susin C, Damé-Teixeira N, Maltz M. Tooth as dental education of the community, brushing habits, loss prevalence and risk indicators among 12-year- specialized dental care and conservative treatments should old schoolchildren from South Brazil. Caries Res, be improved. Further studies with different parameters 2014;48:347-352. (socio-economic status, educational status) are necessary. 17. George B, John J, Saravanan S, Arumugham IM. Prevalence of permanent tooth loss among children and adults in a suburban area of Chennai. Indian J Dent Res, 2011;22:364. 18. Demirbuga S, Tuncay O, Cantekin K, Cayabatmaz M, Dincer AN, Kilinc Hİ et al. Frequency and distribution References of early tooth loss and endodontic treatment needs of permanent first molars in a Turkish pediatric population. Eur 1. Cunha MA, Lino PA, Santos TR, Vasconcelos M, Lucas SD, J Dent, 2013;7:99-104. Abreu MH. A 15-year time-series study of tooth extraction 19. Atieh MA. Tooth loss among Saudi adolescents: social and in Brazil. Medicine (Baltimore), 2015;94:1924-1931. behavioural risk factors. Int Dent J, 2008;58:103-108. 2. Polzer I, Schimmel M, Müller F, Biffar R. Edentulism as 20. Barbato PR, Peres MA. Tooth loss and associated factors in part of the general health problems of elderly adults. Int adolescents: a Brazilian population-based oral health survey. Dent J, 2010;60:143-155. Rev Saude Publica, 2009;43:13-25. 3. Flanders RA. Effectiveness of dental health educational 21. Bhat N, Mitra R, Reddy JJ, Oza S, Patel R, Singh S. programs in schools. J Am Dent Assoc, 1987;114:239-242. Reasons and pattern of tooth mortality as perceived by 4. Caldas AF Jr. Reasons for tooth extraction in a Brazilian dental professionals in Udaipur City, Rajasthan, India. Arch population. Int Dent J, 2000;50:267-273. Oral Res, 2013;9:149-157. 5. Jälevik B, Klingberg G, Barregård L, Norén JG. The 22. Susin C, Haas AN, Opermann RV, Albandar JM. Tooth loss prevalence of demarcated opacities in permanent first in a young population from south Brazil. J Public Health molars in a group of Swedish children. Acta Odontol Scand, Dent, 2006;66:110-115. 2001;59:255-260. 23. Gill DS, Lee RT, Tredwin CJ. Treatment planning for the loss 6. Leppäniemi A, Lukinmaa PL, Alaluusua S. Nonfluoride of first permanent molars. Dent Update, 2001;28:304-308. 24. Halicioglu K, Celikoglu M, Caglaroglu M, Buyuk SK, hypomineralizations in the permanent first molars and their Akkas I, Sekerci AE. Effects of early bilateral mandibular impact on the treatment need. Caries Res, 2001;35:36-40. first molar extraction on condylar and ramal vertical 7. Jafarian M, Etebarian A. Reasons for extraction of asymmetry. Clin Oral Investi, 2013;17:1557-1561. permanent teeth in general dental practices in Tehran, Iran. 25. Sequeira-Byron P, Fedorowicz Z, Carter B, Nasser M, Med Princ Pract, 2013;22:239-244. Alrowaili EF. Single crowns versus conventional fillings for 8. Telli AE, Aytan S. Changes in the dental arch due to the restoration of root-filled teeth. Cochrane Database Syst obligatory early extraction of first permanent molars. Turk J Rev, 2015;25:CD009109. Orthod, 1989;2:138-143. 9. Andrews LF. The six keys to normal occlusion. Am J Conflict of Interests: Nothing to declair. Orthod Dentofacial Orthop, 1972;62:296-309. Financial Disclosure Statement: Nothing to declair. 10. Cağlaroğlu M, Kilic N, Erdem A. Effects of early unilateral Human Rights Statement: All the procedures on humans were first molar extraction on skeletal asymmetry. Am J Orthod conducted in accordance with the the Helsinki Declaration of 1975, Dentofacial Orthop, 2008;134:270-275. as revised 2000, and with national ethical committee. Consent was 11. Mackie IC, Blinkhorn AS, Davies HJ. The extraction of obtained from the patient/s and approved for the current study by permanent first molars during the mixed dentition period – a national ethical committee. guide to treatment planning. J Paediatr Dent, 1989;5:85-92. Animal Rights Statement: None reguired. 12. Williams JK, Gowans AJ. Hypomineralised first permanent Received on March 22, 2018. molars and the orthodontist. Eur J Paediatr Dent, Revised on May 20, 2018. 2003;4:129-132. Accepted on November 12, 2018. 13. Rahhal AA. Extraction timing of heavily destructed upper first permanent molars. OJST, 2014;4:161-168. Correspondence: 14. Koyuturk AE, Ozmen B, Tokay U, Tuloglu N, Sari ME, Bilal Ozmen Sonmez TT. Two-year follow-up of indirect posterior Ondokuz Mayis University composite restorations of permanent teeth with excessive Faculty of Dentistry material loss in pediatric patients: a clinical study. J Adhes Department of Pediatric Dentistry, Samsun, Turkey Dent, 2013;15:583-590. e-mail: [email protected]

10.2478/bjdm-2019-0005

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L BALKAN JOURNAL OF DENTAL MEDICINE A ISSN 2335-0245 IC G LO TO STOMA

A Prospective Clinical Study of the Efficacy of Hyflex CM Rotary Instruments in an Endodontics Undergraduate Program

SUMMARY Zoi-Despoina Tzima, Nikolaos Economides, Background/Aim: To investigate the incidence of procedural errors Christos Gogos, Ioannis Kolokouris with the use of a novel nickel-titanium rotary system (Hyflex CM, Coltene/ Department of Endodontology, Division Whaledent, Altstätten Switzerland), evaluate the technical quality of root of Pathology and Therapeutics of Dental canal treatments and assess a questionnaire completed by the participants Tissues and Basic Dental Sciences, School of themselves in an undergraduate dental clinic between 2014 and 2017 Dentistry, Aristotle University of Thessaloniki, Thessaloniki, Greece (Department of Endodontology, School of Dentistry, Aristotle University of Thessaloniki). Material and Methods: 118 undergraduate students in their first year of clinical practice performed a root canal treatment on a patient’s molar (maxillary/mandibular). None of the participants had previous experience in rotary instrumentation. The periapical radiographs were taken with the use of the paralleling technique for standardization and were collected and evaluated by the investigator. After the root canal treatment was performed the students completed a questionnaire in order to evaluate their training on rotary instrumentation. Results: The overall incidence of instrument separation, apical perforation, root perforation, straightening and ledges was 0.8%, 4.4%, 2.3%, 5.5% and 29% respectively on root canal level. Ledges were detected more often in mandibular mesiobuccal canals. The frequency of root canals with an ‘acceptable’ filling was 68.4%, while overfilled and underfilled canals were found to be 8.6% and 16.2% respectively. The response rate was high (94.9%), 35% of the participants encountered no difficulty in the use of rotary instrumentation and 98.2% would use it again. Conclusions: The incidence of procedural errors was considerably low and the technical quality of the filled root canals was superior to that of similar studies. The responses of the questionnaire demonstrated a positive attitude toward rotary instrumentation. Key words: Hyflex CM, Procedural Errors, Technical Quality, Undergraduate Dental Clinic, ORIGINAL PAPER (OP) Questionnaire Balk J Dent Med, 2019;24-30

Introduction procedural errors for more predictable results, have led to a rapid development of new endodontic rotary systems The advent of Ni-Ti rotary instrumentation has while formers are updated at an exponential rate. Hyflex CM rotary files (Coltene/Whaledent, improved the quality and speed of cleaning and shaping Altstätten, Switzerland) are manufactured from a procedures; simultaneously procedural errors such as novel type of Ni-Ti wire, namely Controlled Memory transportation, ledging, zipping and perforations are (CM) wire, which has undergone a unique proprietary 1,2 decreased . Despite their indisputable advantages, Ni-Ti thermomechanical processing4, that is not disclosed by instruments are still susceptible to separation3. Their the manufacturer. These instruments, as stated by the widespread use among clinicians and the need to reduce manufacturer, possess a lower percentage in weight of Balk J Dent Med, Vol 23, 2019 Efficacy of Hyflex CM Rotary Instruments 25 nickel (52.1 Ni% wt) in comparison to the vast majority K-files up to size 20. The enlargement of the root canals of commercially available Ni-Ti rotary instruments was accomplished with the following order of Hyflex (54.2-56.2 Ni% wt)5. Due to their special manufacturing instruments, 25.08, 20.04, 25.04, 20.06 and 30.04. File size process, Hyflex CM files are highly flexible6, more 40.04 taper was used only at the distal canals of mandibular resistant to cyclic fatigue6,7, they do not rebound to their molars and at the palatal canals of maxillary molars. All original shape7 and partially or fully regain their original files were used in a slow speed handpiece (CanalPro CL shape after sterilization6,8. Rotary instrumentation is an Endodontic Handpiece, Coltene/Whaledent, Altstätten, integral adjunct to endodontic practice, thus undergraduate Switzerland), at a setting and speed recommended by the programs have gradually included it in their curricula9-11. manufacturer (2.5 Ncm, 500 rpm). As an irrigant between The purpose of this prospective study that the files and after instrumentation 3% sodium hypochlorite was conducted in the Undergraduate Clinic of the (CanalPro, Coltene/Whaledent, Altstätten, Switzerland) Department of Endodontology at the Aristotle University was used. To remove smear layer 17% EDTA solution of Thessaloniki, Greece was two-fold. The primary (CanalPro, Coltene/Whaledent, Altstätten, Switzerland) objective was to investigate the frequency of root and was applied. The canals were obturated with tapered master apical perforations, ledges, straightening, separated cone (0.04) and accessory points, combined with Roeko instruments and the quality of root fillings when Seal sealer (Coltene/Whaledent, Altstätten, Switzerland) rotary instrumentation was used for the first time by using the lateral condensation technique. Each file was undergraduate students. The second objective was to used at a maximum of three times and was discarded either gain an insight on the undergraduates’ self-assessment when it did not regain its form after sterilization or when a concerning the root canal treatment and the evaluation of distortion or deformation were detected under magnifying the rotary experience based on a questionnaire. To the best loupes 3x. The incidence of each procedural error was of our knowledge, there is no published data evaluating calculated on root canal level. the efficacy of Hyflex CM rotary instruments clinically. Radiographic evaluation Specifically, this is the first prospective clinical study to assess the efficacy of Hyflex CM rotary instruments in an The periapical radiographs were taken with the ® endodontics undergraduate program and the first to use a use of digital imaging technology (DIGORA Optime questionnaire completed by the participants themselves to digital imaging plate system, Soredex Tuusula, Finland). evaluate their training on rotary instrumentation. In order for the projections to be standardized the paralleling technique was used. Superimposed canals and canal fillings, working length radiographs with incorrect estimation of the working length, missed canals, calcified Material and Methods canals, and cases of radiographs without depiction of the apices were excluded. The data were collected and Selection of cases observed by the investigator. Detection of procedural errors and evaluation of During three academic years (2014-15, 2015- the technical quality of the root fillings 16, 2016-17), a total of one hundred and eighteen undergraduate students on their first year of clinical The criteria for the detection of procedural errors practice participated in the study. None of the participants were as follows: had a previous experience in rotary instrumentation; ●● Separated instruments were diagnosed during however all of them had performed two or more root the time of the incidence and their location was canal treatments on patients with hand instruments. The determined radiographically, participants performed a root canal treatment on one ●● Ledge formation was diagnosed when the root filling molar (maxillary/ mandibular). was at least 1mm shorter than the working length and/or deviated from the original canal curvature12, Instrumentation technique ●● Apical perforation was diagnosed when the filling 13 The single-length instrumentation sequence of Hyflex material extruded through the apical foramen , CM system (Coltene/Whaledent, Altstätten, Switzerland) ●● Root perforation was diagnosed when the filling was demonstrated to each student on resin blocks by material extruded in the lateral walls of the root14, the investigator (ZDT), according to the manufacturer’s ●● Straightening was diagnosed when a deviation from recommendations. After the access cavity was prepared, the original canal curvature was evident between the the working length was determined with a radiograph and working length and the cone-fit radiograph15. in a few cases with the combination of an electronic apex The radiographic evaluation of the quality of the locator (CanalPro Apex Locator, Coltene/Whaledent, root fillings was based on the length and the density of Altstätten, Switzerland) and a radiograph. The canals the root filling and its adaptation to the canal walls. The were negotiated to the working length with stainless steel categorization of the criteria was as follows: 26 Zoi-Despoina Tzima et al. Balk J Dent Med, Vol 23, 2019

●● A length of ≤ 2m from the apex with no voids and ledges respectively. The k-values for intraexaminer (‘Acceptable’ filling) reliability were 0.88 and 0.89 for root filling’s length and ●● A length of ≤ 2m from the apex with voids presence of voids and 0.95 for ledges. Because of the ●● Overfilling with no voids near perfect agreement, the scores of one author (ZDT) ●● Overfilling with voids were used for the radiographic evaluation of the study. ●● A length of >2mm from the apex with no voids Similarly, the k-values obtained from the test-retest ●● A length of >2mm from the apex with voids.16 reliability were 0.89. Questionnaire survey Procedural errors A hand-delivered questionnaire was designed including 15 closed-ended questions concerning hand instrumentation experience, degree and reason of difficulty Separated Instruments with rotary instrumentation, familiarity with terms of rotary The overall incidence of rotary instrument separation instrumentation, preparation’s and obturation’s quality, on root canal level was 0.8%. Of the 3 separated identification of procedural errors and predisposition instruments one was located in a distal canal while the to rotary instrumentation. An external pilot survey remaining two in mesiobuccal canals of maxillary and was conducted amongst 20 undergraduate students to mandibular molars. Canal location did not have an effect evaluate the questionnaire’s reliability. The questionnaire on instrument separation (p>0.05) (Figure 1). was administered to the participants after the root canal treatment was performed and only those with all questions completed were included in the data analysis.

Ethical consideration The study was approved by the Ethical Committee of the School of Dentistry of Aristotle University of Thessaloniki, Greece (protocol no.44/24-06-2016).

Statistical analysis Cohen’s kappa coefficient was used to calculate interobserver and intraexaminer reliability regarding ledge formation and root filling’s quality. Interobserver agreement was determined by the scores of the radiographs of 30 randomly selected cases, while intraexaminer agreement was obtained by rescoring the radiographs of 40 randomly selected cases one month after the first evaluation. The reliability of the questionnaire was measured with the test-retest model. Twenty randomly selected undergraduate students were delivered the questionnaire for a second time approximately one month after their first response and Figure 1. Example of instrument separation located in the apical the scores between the two time intervals were compared third of the distal canal on tooth #36: A) Preoperative radiograph, B) Working length radiograph, C) Cone-fit radiograph, D) Postoperative using the k-coefficient. The responses of the examiners radiograph. and participants were calculated using the Statistical Package for Social Sciences (IBM SPSS v.24, Armonk, NY, USA). Qualitative data analysis was carried out using descriptive statistics for observed values and frequencies, Ledges Chi Square test and Fisher’s Exact test. Ledges were found in 29% of the root canals (96/330). 4.5% of the ledged canals was accompanied by straightening and/or root perforation. A statistical significant correlation was found between canal type Results and the incidence of ledges (p< 0.05). Statistical significant differences were found between distobuccal Reliability and mandibular mesiobuccal, distal and mandibular mesiobuccal, maxillary mesiobuccal and mandibular The k-values for interobserver reliability were 0.87, mesiobuccal and between palatal and mandibular 0.88 and 0.87 for root filling’s length, presence of voids mesiobuccal root canals. Balk J Dent Med, Vol 23, 2019 Efficacy of Hyflex CM Rotary Instruments 27

Perforations Table 2. Percentages (%) of filled root canals according to Root perforations and apical foramen damage were classification’s criteria found to be 2.3% and 4.4% respectively. Root canal type Classification Number of root canals Percentage did not affect the incidence of root perforation (p>0.05). 0.2 mm with no voids 232 68.4 0.2 mm with voids 23 6.8 Canal Straightening Overfilling with no voids 27 8.0 Canal straightening was detected in 5.5% of the root Overfilling with voids 2 0.6 canals. No statistical significance was found between >2mm with no voids 38 11.2 the type of the root canal and the incidence of canal >2mm with voids 17 5.0 straightening (p>0.05) (Figure 2, Table 1). Total 339 100.0

Questionnaire survey

Table 3. Response details by percentage (%) and number (N) of the respondents

Type of question Responses % (N) Step-back 70.5 (79) Most used Step-down 9.8 (11) preparation Crown-down 19.6 (22) technique Other (0) Very easy 50.9 (57) Easy 41.1 (46) Degree of difficulty Moderate 7.1 (8) Hard 0.9 (1) Very hard 0.0 (0) Inexperience 58.0 (65) Protocol’s complexity 2.7 (3) Insufficient instruction 0.9 (1) Cause of difficulty Figure 2. Case of canal straightening at the mesiobuccal canal on tooth All of the above 0.9 (1) #46: A) Preoperative radiograph, B) Working length radiograph, C) None of the above 2.7 (3) Cone-fit radiograph, D) Postoperative radiograph. No difficulty 34.8 (39) Excellent 12.5 (14) Very good 56.3 (63) Preparation’s qualityGood 25.9 (29) Table 1. Incidence (%) of procedural errors Fair 4.5 (5) Poor 0.9 (1) Number of root Speed-less treatment time 70.5 (79) Type of procedural error Percentage Major advantage canals Less procedural errors 4.5 (5) of rotary Preparation’s quality 25.0 (28) Instrument separation 0.8 3 instrumentation Other 0.0 (0) Ledge formation 29.0 96 Use of rotary Yes 98.2 (110) instrumentation in Root perforation 2.3 8 No 1.8 (2) the future Apical perforation 4.4 15 Superiority of Yes 74.1 (83) rotary to hand No 25.9 (29) Canal straightening 5.5 18 instrumentation

The response rate was 94.9%. The respondents Quality of the root filling were mostly familiar with the step-back instrumentation Root filling classified as “acceptable” was observed technique (70.5%). Most participants (92%) reported that in 68.4% of the filled root canals, while 87.6% exhibited the use of rotary instrumentation varied from easy to very no voids and 75.2% were filled adequately. The frequency easy while only 0.9% described the experience as “hard”. of overfilled and underfilled canals was found to be 8.6% As the reason for the encountered difficulty-if any, the and 16.2% respectively. Root canal type did not have an majority identified their inexperience, while more than 1/3 effect on the quality of the root filling (p>0.05) (Table 2). of the participants experienced no difficulty. More than 28 Zoi-Despoina Tzima et al. Balk J Dent Med, Vol 23, 2019 half of them characterized the quality of their preparation to those of Balto et al. (2.2%)13. To a certain extent root as “very good”, while 0.9% as poor. Additionally, 70.5% perforations might have derived from the misusage of considered “speed” as the major advantage of rotary K-files when inserted in severely curved canals, followed instrumentation followed by “quality of the preparation”. by rotary instrumentation of the newly-created path. The vast majority (98.2%) was positively predisposed to The incidence of apical perforation in other studies by using rotary instrumentation in the future, while 74.1% Balto et al.13 and Khabbaz et al.14 is 10.6% and 25.7% considered rotary instrumentation superior to hand respectively, which is higher compared to ours. A loss instrumentation (Table 3). of the working length during instrumentation or canal transportation could be responsible for the incidence of apical perforations. Discussion The percentage of canals maintaining their original shape and curvature was 94.5%. It is accepted that canal deviations are minimized when rotary Ni-Ti instruments This prospective clinical study evaluated 25,26 the frequency of iatrogenic errors during rotary are used . In vitro results indicate that Hyflex CM instrumentation and obturation by undergraduate instruments produce less canal deviations compared 15,27 students in a 3-year period. Our results indicate that to other Ni-Ti rotary instruments . In our study the the overall incidence of separated rotary instruments results are relatively low, but it must be considered that is lower than those of similar clinical and case-control the use of two-dimensional radiographs to evaluate the studies. Previous studies reported instrument separation straightening of a three-dimensional structure may be by undergraduate students that ranged between 1.0 inaccurate. and 2.09% 17,18. However those results derive from The radiographic evaluation of the technical quality data consisting of all tooth types and the incidence of of root fillings showed that 68.4% of the root canals separation refers to hand and not rotary instruments. fulfilled the criteria of an “acceptable” filling. Previous Studies referring to rotary instrument separation report studies that assessed the technical quality of root fillings results between 1.33-4.44% 10,19,20. The incidence reaches performed by undergraduate students exhibited a lower 13,16,28-30 2.5% when only molars are concerned10. Nevertheless, percentage (13-55.3%) . When only molars were the root canal treatments in the latter studies were considered, the latter studies indicated results ranging performed by postgraduate students and specialists with between 6.1% and 54.6%. When each root canal was greater experience in rotary instrumentation. Mesiobuccal considered as one unit those results reached 37.6% and 16,28 canals of maxillary and mandibular first molars exhibited 46.7% . Despite the superiority of our results, it is the highest incidence of separation (0.56%). Those canals difficult to compare these studies due to the differences are narrow with great primary and apical curvatures21,22, in the categorization criteria, the tooth type selection and thus susceptible to instrument separation. The low the evaluation of each tooth as a unit or of each root canal separation rate in our study may be attributed to the individually. Moreover, the length of the root canal filling establishment of a manual glide path with a No 20 K-file. was estimated more precisely in our study, since the A direct comparison of those results is difficult to achieve radiographs were taken with the paralleling technique and since clinical studies investigating instrument fracture use the distance of the root filling from the radiographic apex different study designs and instruments. was calculated with digital measuring technology. Regarding the presence of ledges our results are The response rate on the questionnaire was high lower than those of other investigators12,13,16,23 who (94.9%), thus the results can be considered representative detected ledges in 33-51.5% of molar cases. Dentinal of the population31. This survey could be considered chips or residual debris which result in apical canal innovative since it is the first to evaluate the performance blockage can also affect the obturation length16, thus an of Hyflex CM rotary instruments after clinical use. overestimation of ledges might have occurred. It is also Rotary instrumentation was found to be superior to hand speculated that ledging was a result of inappropriate instrumentation by the majority of the participants, which usage of hand files, overusage or loss of the determined can be attributed to the fact that “speed” was suggested working length. However, due to the highly controlled to be the greatest advantage of the former. The positive conditions and the fact that the canals were rotary perception of the students about rotary techniques could instrumented, a lower percentage was expected. be related with the very low degree of difficulty. Rotary Similarly low is the frequency of this study training is not included in the preclinical courses of the regarding root perforation compared to those of similar undergraduate students and this justifies not only the lack studies that range between 2.7% and 18.8% 14,16,24. When of acquaintance with the geometrical traits and terms of only molars are considered our observations are similar rotary instruments but also the fact that the encountered Balk J Dent Med, Vol 23, 2019 Efficacy of Hyflex CM Rotary Instruments 29 difficulty was mainly related to the students’ inexperience. 8. Alfoqom Alazemi M, Bryant ST, Dummer PMH. Presumably due to their inexperience, most students were Deformation of HyFlex CM instruments and their shape not able to identify the procedural errors of their cases. recovery following heat sterilization. Int Endod J, 2015;48: 593–601. Instrument separation and ledge formation were the most 9. Shen Y, Coil JM, Haapasalo M. Defects in nickel-titanium easily recognizable errors. Those findings demonstrate instruments after clinical use. Part 3: a 4-Year retrospective the positive attitude of the undergraduate students toward study from an undergraduate clinic. J Endod, 2009; 35:193– rotary instrumentation and the necessity for rotary 196. 10. Iqbal MK, Kohli MR, Kim JS. A retrospective clinical education in preclinical training. study of incidence of root canal instrument separation in an On the basis of the results of the present study, the endodontics graduate program: a PennEndo database study. incidence of procedural errors by undergraduate students J Endod, 2006;32:1048–1052. was considerably low, despite their inexperience in 11. Arbab-Chirani R, Vulcain JM. Undergraduate teaching rotary instrumentation. The quality of the filled root and clinical use of rotary nickel-titanium endodontic canals was maintained to the highest standards. Rotary instruments: a survey of French dental schools. Int Endod J, instrumentation was followed easily and received a 2004;37:320–324. 12. Greene KJ, Krell KV. Clinical factors associated with ledged positive feedback according to the participants’ responses. canals in maxillary and mandibular molars. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 1990;70: 490–497. 13. Balto H, Al Khalifah S, Al Mugairin S, Al Deeb M, Al-Madi E. Technical quality of root fillings performed Conclusions by undergraduate students in Saudi Arabia. Int Endod J, 2010;43:292–300. The incidence of procedural errors was considerably 14. Khabbaz MG, Protogerou E, Douka E. Radiographic quality of root fillings performed by undergraduate students. Int low and the technical quality of the filled root canals Endod J, 2010;43:499–508. was superior to that of similar studies. The responses of 15. Bürklein S, Börjes L, Schäfer E. Comparison of preparation the questionnaire demonstrated a positive attitude toward of curved root canals with Hyflex CM and Revo-S rotary rotary instrumentation. nickel-titanium instruments. Int Endod J, 2014;47:470–476. 16. Eleftheriadis GI, Lambrianidis TP. Technical quality of root canal treatment and detection of iatrogenic errors in an undergraduate dental clinic. Int Endod J, 2005;38: 725–734. 17. Crump MC, Natkin E. Relationship of broken root canal References instruments to endodontic case prognosis: a clinical investigation. J Am Dent Assoc, 1970;80:1341–1347. 1. Vaudt J, Bitter K, Neumann K, Kielbassa AM. Ex vivo 18. Ungerechts C, Bårdsen A, Fristad I. Instrument fracture in study on root canal instrumentation of two rotary nickel- root canals -where, why, when and what ? A study from a titanium systems in comparison to stainless steel hand student clinic. Int Endod J, 2014;47:183–190. instruments. Int Endod J, 2009;42:22–33. 19. Tzanetakis GN, Kontakiotis EG, Maurikou DV, Marzelou 2. Taşdemir T, Aydemir H, Inan U, Unal O. Canal preparation MP. Prevalence and management of instrument fracture in with Hero 642 rotary Ni-Ti instruments compared with the postgraduate endodontic program at the Dental School stainless steel hand K-file assessed using computed of Athens: a five-year retrospective clinical study. J Endod, tomography. Int Endod J, 2005;38:402–408. 2008;34: 675–678. 3. Parashos P, Messer HH. Rotary NiTi instrument fracture and 20. Spili P, Parashos P, Messer HH. The impact of instrument its consequences. J Endod, 2006;32:1031–1043. fracture on outcome of endodontic treatment. J Endod, 4. Shen Y, Qian W, Abtin H, Gao Y, Haapasalo M. Fatigue 2005;31:845–850. testing of controlled memory wire nickel-titanium rotary 21. Lee JK, Ha BH, Choi JH, Heo SM, Perinpanayagam H. instruments. J Endod, 2011;37:997–1001. Quantitative three-dimensional analysis of root canal curvature in maxillary first molars using micro-computed 5. Zinelis S, Eliades T, Eliades G. A metallurgical tomography. J Endod, 2006;32:941–945. characterization of ten endodontic Ni-Ti instruments: 22. Kartal N, Cimilli HK. The degrees and configurations of assessing the clinical relevance of shape memory and mesial canal curvatures of mandibular first molars. J Endod, superelastic properties of Ni-Ti endodontic instruments. Int 1997;23:358-362. Endod J, 2010;43:125–134. 23. Kapalas A, Lambrianidis T. Factors associated with 6. Peters OA, Gluskin AK, Weiss RA, Han JT. An in root canal ledging during instrumentation. Endod Dent vitro assessment of the physical properties of novel Traumatol, 2000;16:229–231. Hyflex nickel-titanium rotary instruments. Int Endod J, 24. Kfir A, Rosenberg E, Zuckerman O, Tamse A, Fuss Z. 2012;45:1027–1034. Comparison of procedural errors resulting during root canal 7. Plotino G, Testarelli L, Al-Sudani D, Pongione G, Grande preparations completed by senior dental students in patients NM, Gambarini G. Fatigue resistance of rotary instruments using an ‘8-step method’ versus ‘serial step-back technique’. manufactured using different nickel-titanium alloys: a Oral Surg Oral Med Oral Pathol Oral Radiol Endod, comparative study. Odontology, 2014;102:31–35. 2004;97:745–748. 30 Zoi-Despoina Tzima et al. Balk J Dent Med, Vol 23, 2019

25. Thomson SA, Dummer PMH. Shaping ability of Profile.04 Conflict of Interests: Nothing to declair. Taper Series 29 rotary nickel-titanium instruments in Financial Disclosure Statement: Nothing to declair. simulated root canals.Part 1. Int Endod J, 1997;30:1–7. Human Rights Statement: All the procedures on humans were 26. Schäfer E, Schulz-Bongert U, Tulus G. Comparison of hand conducted in accordance with the the Helsinki Declaration of stainless steel and nickel titanium rotary instrumentation: a 1975, as revised 2000. Consent was obtained from the patient/s clinical study. J Endod, 2004;30:432–435. 27. Saber SEDM, Nagy MM, Schäfer E. Comparative and approved for the current study by national ethical committee. evaluation of the shaping ability of ProTaper Next, iRaCe Animal Rights Statement: None reguired. and Hyflex CM rotary NiTi files in severely curved root canals. Int Endod J, 2015;48:131–136. Received on January 27, 2019. 28. Barrieshi-Nusair KM, Al-Omari MA, Al-Hiyasat AS. Revised on January 28, 2019. Radiographic technical quality of root canal treatment Accepted on January 29, 2019. performed by dental students at the Dental Teaching Center in Jordan. J Dent, 2004;32:301–307. 29. Hayes SJ, Gibson M, Hammond M, Bryant ST, Dummer Correspondence PMH. An audit of root canal treatment performed by undergraduate students. Int Endod J, 2001;34:501–505. Zoi-Despoina Tzima 30. Er O, Sagsen B, Maden M, Cinar S, Kahraman Y. Department of Endodontology, Division of Pathology and Therapeutics Radiographic technical quality of root fillings performed by of Dental Tissues and Basic Dental Sciences dental students in Turkey. Int Endod J, 2006;39:867–872. School of Dentistry, Aristotle University of Thessaloniki, 31. Locker D. Response and nonresponse bias in oral health Thessaloniki, Greece surveys. J Public Health Dent, 2000;60:72–81. e-mail: [email protected]

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Efficiency of XP Endo Shaper (XPS) and Irrigation Protocol on the Quality of Cleaning the Apical Third of Root Canal: SEM Study

SUMMARY Slavoljub Živković, Background/Aim: The aim of this study was to evaluate the efficacy Milica Jovanović-Medojević, Jelena Nešković, of new rotary NiTi instrument XP- endo SHAPER (XPS) used with two Marijana Popović Bajić, Marija Živković Sandić irrigation protocols on the root canal cleaning in the apical area. Material Department of Restorative Odontology and and Methods: The research was conducted on 30 single-rooted teeth Endodontics, School of Dentistry, University of extracted for orthodontic reasons which were divided into the two groups. Belgrade, Belgrade, Serbia Instrumentation of the canals was conducted with XPS instrument and 2% solution of NaOCl was used as irrigant. Instrumentation in the first group was performed using a conventional continuous irrigation, in the second group, protocol of final irrigation was performed intermittently in 3 cycles. The SEM analysis of the apical third of the canal was performed on longitudinal root cross-section standardized photomicrography with a magnification of 2000X. Results: Results showed that a thicker smear layer was observed in the first group and with continuous irrigation protocol (2,10) in relation to the intermittent irrigation protocol in 3 cycles (1,96), but without significant differences.The walls of the root canal in the apical third of the samples of the second group were slightly cleaner (73.3%) in comparison with the teeth of the first group (64, 7%), but also without significant differences. Conclusions: The use of XPS and 2% solution of NaOCl in the root canal enables efficient cleaning of the apical third of tooth. The final irrigation protocol in three cycles improves the efficiency of the smear layer removal in the apical segment of the canal. ORIGINAL PAPER (OP) Key words: XP-endo Shaper, Smear Layer, Irrigation Protocol, Apical Third Balk J Dent Med, 2019;31-35

Introduction layer and dentin debris on the walls of the canal, and often to their accumulation in inaccessible areas of the Cleaning and shaping the root canal system is canal system4,5. In this way there is significant efficiency the most important phase in an endodontic treatment. reduction of irrigant on the residual bacteria and However, complex anatomy of a canal often prevents significant linkage material disturbance for obturation of adequate cleaning of this space using actual instruments the canal walls3,6,7. and techniques1,2. A particular problem is the irregularity In order to clean the root effectively, type and of the canal system (isthmus, ramifications, and additional quantity of the irrigant or irrigation techniques and lateral canals) or apical third of the root canal, which cannot be reached by most of the instruments, and protocol are significant. These intracanal solutions almost 30-50% of the surface of the canal walls remains provide a lubricating effect during instrumentation, have untouched1,3. an antibacterial effect, remove debris and smear layer Mechanical instrumentation with manual or from the root canal walls and from inaccessible areas of mechanical instruments leads to the formation of smear the canal system8,9,10. 32 Slavoljub Živković et al. Balk J Dent Med, Vol 23, 2019

The most frequently used endodontic irrigant is The canal instrumentation was carried out in both sodium hypochlorite (at various concentrations), primarily groups by the new NiTi rotating instrument XP-endo due to its antibacterial11 and solvent effect12, although Shaper (FKG, Dentaire, Swiss) (dimensions 30/04)21. higher concentrations can cause irritation of the periapical This instrument represents a new generation of NiTi tissue13. Exceptional and prolonged antibacterial effect of rotating instruments that, thanks to its extraordinary chlorhexidine on the large number of bacteria in the canal, superelasticity, can change its shape in the canal and thus, makes this irrigant often used in endodontic treatments8,14. reach inaccessible areas of the canal. A special production Researches has also shown that it is possible to increase technique and specific geometry of the cutting part the efficiency of the irrigant, or to achieve better ensures the cleaning and shaping of the canal with only penetration and better cleaning of the canal walls using one instrument (800 rpm). some forms of solution activation like: ultrasound15,16, a GROUP 1- In the first group, a conventional new instrument XP-endo Finisher1,17 or laser18. technique of continuous irrigation was applied. The Chemo- mechanical procedure provides a canal is filled with an irrigant (0.5 ml) and then the significantly lower number of bacteria in the canal, but XPS instrument is inserted into the canal with gentle not complete disinfection of the canal system. In addition, insertion and withdrawal placed to the working length any available set of manual or mechanical burnishing (3-5 times for 30 sec). Then the irrigant (0.5 ml) was tool results in the formation of smear layer and dentin re-inserted into the canal and usage of XPS provided the on processed canal walls2,6,8. For the success final apical preparation 8-10 times over 30 sec. The final of this endodontic treatment, it is necessary to remove this irrigation with 2% NaOCl solution was performed after layer, and the removal efficiency is significantly affected the completion of the instrumentation with another 3 ml by irrigating solutions on the basis of the chelating agent, solution for 90 sec. which effectively remove the smear layer from all areas of GROUP 2- In the second group, XPS instrumentation the canal2,19,20. was done in the same way as in the first group, but the The aim of this study was to evaluate the efficiency final irrigation was performed intermittently in 3 steps (3 of the apical third of the canal after the instrumentation times 1ml for 30 sec). of the NiTi rotating instrument XP- endo Shaper and the SEM analysis application of two final irrigation protocols using SEM analysis. After finishing the instrumentation, the crowns of all teeth were cut at the cement-enamel junction and then the roots were cut with diamond disc (without penetration into the canal) longitudinally in the vestibulo-oral direction Material and Methods and separated into two halves with sharp chisel. Obtained halves were placed on a carrier, gold-coated and analyzed by SEM (JOEL, JSM, 64660 LV, Japan). The study was conducted on 30 premolars extracted Only an apical third (region 3 mm from the for orthodontic reasons. Teeth were stored up to the instrumentation border) was analyzed, so that, experiment in a 0.2% solution of thymol, at a temperature for each sample (half of the teeth) 5 standardized of 4 °C. microphotographs were taken at 2000x magnification. SEM photographs of teeth samples (300 images) were Root Canal Instrumentation analyzed by two researchers who independently rated In all teeth the access cavity was formed and each photo. In case of disagreement, it was discussed to established initial passage with K-file #15. The working reach a consensus. The evaluation of cleaning efficiency length is determined to be 1 mm shorter than the length was based on qualitative estimation of residual smear at which the tip of the hand file appears on the apical layer in the apical segment of the canal with the criteria foramen. To prevent leakage of the solution for irrigation presented by Hülsmann et al.22: during instrumentation, a wax ball was placed at the apex of each root. Grade 1 - no smear layer, dentinal tubules open, The teeth were randomly divided into two groups Grade 2 - small amount of smear layer, several dentinal (each of 15 teeth) and the complete mechanical tubules open, instrumentation was performed by one researcher. As Grade 3 - homogeneous smear layer covers the canal an irrigant, a 2% solution of NaOCl (Cloraxid 2%, wall, small number of dentinal tubules open, Cerkamed, Poland) was used, and the canal was washed Grade 4 - the entire wall of the canal covered with smear with plastic syringes, a volume of 2 ml, and needle size layer, no open dentinal tubules, 27. A 4 ml solution for irrigation was used for each canal, Grade 5 - non-homogeneous smear layer covering the and the flushing protocol lasted 150 sec. entire wall of the canal. Balk J Dent Med, Vol 23, 2019 Permanent First Molar Tooth Loss 33

The clean wall canal included ratings 1 and 2, and the wall with the present smear layer grades 3, 4 and 5. The obtained results were processed in the SPSS 20 (IBM, CHICAGO) program. Methods of descriptive statistics and Mann Whitney test were used in statistical analysis.

Results A) B) Figure 2. Evaluation of cleaning quality in the apical third of the The results of the analysis of SEM photographs after canal, A) Samples of the first group where the technique of continuous the instrumentation and canal irrigation are shown in irrigation was applied (Grade 3). SEM 2000x, B) Samples of the second group where the final irrigation was performed by intermittent technique Tables 1 and 2 and in Figures 1 and 2. The analysis of the in 3 steps (Grade 2). SEM 2000x. apical thirds samples indicated mainly clear canal walls, without the smear layer in both tested groups (Figure 1). Table 2. Evaluation of cleaning quality in the apical third of the root canal

Cleaning ratings With smeared Good total layer (Grade 1,2) (Grade 3,4,5)

Continuous N 97 53 150 A) B) irrigation % 64.7% 35.3% 100% Figure 1. The representative evaluation microphotographs of the smear Group layer in the apex third of the canal Irrigation in N 110 40 150 3 steps % 73.3% 26.7% 100% Samples of the first group where the technique of N 207 93 300 continuous irrigation (grade 2) was applied. SEM 2000x, Total B) Samples of the second group where the final irrigation % 69% 31% 100% was performed by intermittent technique in 3 steps (grade 1). SEM 2000x. A slightly smear layer was registered in the first group where the instrumentation was performed using Discusion the XPS instrument and with the continual irrigation protocol (2,10) in comparison to the second group where Although there were earlier controversies, the instrumentation was performed using XPS and an today there is a generally accepted consensus among intermittent 3-step irrigation protocol (1,96), but without endodontists about the necessity of removing the smear statistically significant differences (Table 1). layer from the walls of the root canal10,11,14. This layer significantly influences the success of endodontic Table 1. Evaluation of smear layer in the apical third of the root treatment because it can contain bacteria and its presence canal can reduce the efficacy of intra canal medicaments, or reduce the adhesion of endodontic sealers to canal walls Smeared layer ratings during obturation6,7,8. N Mean SD Med Min max The possibilities of light microscopy in the debris and smear layer identification after chemo-mechanical Continuous 150 2.10 1.03 2.00 1.00 4.00 canal preparation are quite high23), but SEM analysis Group irrigation is certainly the most reliable and most popular method, Irrigation in 3 steps 150 1.96 0.98 2.00 1.00 4.00 primarily because of the possible magnification and high Total 300 2.03 1.00 2.00 1.00 4.00 image resolution5,8,18. Studies have confirmed that the smear layer from The obtained results also indicated cleaner walls the canal walls is easier to remove from the coronal in the apical third of the samples of the second group and middle third2,6,9,18, while the cleaning problem (73,3%) compared to the canal walls of the first group is particularly pronounced in the area of the apical (64,7%) (Figure 2, Table 2). third1,11,15,19,24. 34 Slavoljub Živković et al. Balk J Dent Med, Vol 23, 2019

These research were realized by an identical protocol of fresh NaOCl solution increase its cumulative efficiency (all canals were processed by one researcher), with as well as efficacy in canal cleaning quality28. one type of instrument (XPS), with the same amount A smaller amount of the smear layer in the apex part and duration of irrigation and with two final irrigation of the canal could be due to the fact that XPS due to the protocols (2% NaOCl). The obtained results indicated a specific working part of the instrument and higher speeds very efficient cleaning of the apical segment of the canal during the canal treatment, leads to considerably less and the walls mostly without a smear layer in both tested transport of the cut dentine into the apex part of the canal29. groups. A more efficient removal of the smear layer Efficient cleaning of the apical third and clean and better cleaning was observed after the intermittent walls without smear layer were also observed after the final irrigation protocol in three steps in comparison to application of the specific self-adjusting file (SAF- continuous irrigation protocol. Self Adjusting File) in the canal instrumentation. The Clean canal walls in apical third of the nearly all irrigation solution flows through the SAF file to provide a samples could be explained primarily by the simplicity of permanent freshness which is additionally activated by the canal morphology, but also by the effects of the new XPS movements of the file2. instrument, or by its specific design, at a speed of 800 rpm, What is interesting in this study is the fact that the and by the fact that it can change its shape in the canal chemo-mechanical preparation of the canal was done with during the instrumentation and thus, reach the inaccessible only one instrument and thus confirmed that the efficacy canal areas17,25. In addition, the extreme flexibility of of cleaning does not depend on the number of used the XPS and the working end with 6 cutting edges (with instruments30, but above all from the diameter of apical minimal torque) ensure efficient cleaning of all canal walls preparation1,15,24 or from type, volume, concentration, and and the apical segment. The formed dentine micro derbis irrigation protocol11,31. is easily removed due to the pronounced “turbulence” of The results of this study indicated that the apical irrigants during instrument rotation in the canal1,15,16,21. segment of the canal was clean and without a smear layer The application of XPS in the chemo- mechanical in a high percentage, although only 2% NaOCl solution canal preparation provides the necessary and sufficient was used for irrigation. These findings are inconsistent diameter of the apical preparation (30/04), which is also with the findings of the authors who suggest that the a precondition that facilitates cleaning of this part of the removal of the smear layer from the canal walls is mainly canal1,11,15. Diameter of the apical preparation formed in dependent on the usage of chelating agents6,8,19,20. this way allows the tip of the needle to easily reach the apical terminus, which also improves the efficiency of the irrigant in the removal of the smear layer2,9. One of the problems of such deep application of irrigation needles Conclusions in clinical conditions can be the conveyance of irrigant (NaOCl) into periapex, which can cause adverse effects Within the limitations of this study, it can be on periapical structures26. concluded that the chemo–mechanical instrumentation of The results comparison of various studies on root canal using XPS and 2% NaOCl solution provides the effects of cleansing the apical third is quite efficient cleaning of the apical canal segment, primarily complicated because of both, the different techniques of due to the adequate diameter of the apex preparation and instrumentation and irrigation, and different evaluation the specific effect of the new instrument during canal methods2. In this study, a 2% NaOCl solution was used as preparation. The intermittent final irrigation protocol in an irrigant with two final irrigation protocols. three cycles improves the removal of the smear layer in The largest number of researchers agree that the the apical part of the canal. quality of the cleaning of the canal system depends largely on irrigants, its quantities, irrigation techniques and the time of exposure of the canal walls to the irrigants solution1,3,9,10. The fact is that the solution for irrigation, References quantity and time of action were identical in both groups, nonetheless, better results could be obtained primarily in 1. Bao P, Shen Y, Lin J, Haapasalo M. In Vitro Efficacy of the final irrigation protocol. XP-endo Finisher with 2 Different Protocols on Biofilm An intermittent final irrigation protocol (in 3 steps) Removal from Apical Root Canals. J Endod, 2017;43:321-325. has shown somewhat better results than the conventional 2. Metzger Z, Teperovich E, Cohen R, Zary R, Paqué F, Hülsmann M. The self-adjusting file (SAF). Part 3: irrigation protocol. During the conventional protocol, the removal of debris and smear layer-A scanning electron irrigation solution is mixed with the remains of the smear microscope study. J Endod, 2010;36:697-702. layer and debris, which significantly reduces the efficiency, 3. Gulabivala K, Patel B, Evans G, Yuan Ling Ng. Effects while the fresh solution during each cycle provides better of mechanical and chemical procedures on root canal canal cleaning1,16. It has also been confirmed that 3 cycles surfaces. Endod Topics, 2005;10:103-122. Balk J Dent Med, Vol 23, 2019 Permanent First Molar Tooth Loss 35

4. Peters OA. Current challenges and concepts in 20. Khedmat S, Shokouhinejad N. Comparison of the efficacy the preparation of root canal systems: a review. J of three chelating agents in smear layer removal. J Endod, 2004;30:559-567. Endod, 2008;34:599-602. 5. Hülsmann M, Peters OA, Dummer PMH. Mechanical 21. FKG Dentaire SA. The XP Endo Shaper File Brochure. preparation of root canals: shaping goals, techniques and 22. Available at: http/www.fkg.ch/produsts/endodontics/ means. Endod Topics, 2005;10:30-76. preparatiob/XP-Endo Shaper. Accesed December 1, 2016. 6. Herrera DR, SantosZT, Tay LY, Silva EJ, Loguercio AD, 23. Hülsmann M, Rümmelin C, Schäfers F. Root canal Gomes BPFA. Efficacy of different final irrigant activation cleanliness after preparation with different endodontic protocols on smear layer removal by EDTA and citric acid. handpieces and hand instruments: a comparative SEM Microsc Res Tech, 2013;76:364-369. investigation. J Endod, 1997;23:301-306. 7. Kokkas AB, Boutsioukis ACh, Vassiliadis LP, Stavrianos 24. Lim TS, Wee TY, Choi MY, Koh WC, Sae-Lim V. Light and CK. The influence of the smear layer on dentinal tubule scanning electron microscopic evaluation of Glyde File Prep penetration depth by three different root canal sealers: an in in smear layer removal. Int Endod J, 2003;36:336-343. vitro study. J Endod, 2004;30:100-102. 25. Guerreiro-Tanomaru JM, Loiola LE, Morgental RD, 8. De Vasconcelos BC, Luna-Cruz SM, De-Deus G, de Moraes Leonardo Rde T, Tanomaru-Filho M. Efficacy of four IG, Maniglia-Ferreira C, Gurgel-Filho ED. Cleaning ability irrigation needles in cleaning the apical third of root canals. of chlorhexidine gel and sodium hypochlorite associated or Braz Dent J, 2013;24:21-24. not with EDTA as root canal irrigants: a scanning electron 26. Živković S, Nešković J, Jovanović-Medojević M, Popović- Bajić M, Živković-Sandić M. The efficacy of XPendo microscopy study. J Appl Oral Sci, 2007;15:387-391. Shaper (XPS) in the cleaning the apical third of the root 9. Gu LS, Kim JR, Ling J, Choi KK, Pashley DH, Tay canal. Serb Dent J, 2017;64:171-175. FR. Review of contemporary irrigant agitation techniques 27. Hülsmann M, Rödig T, Nordmeyer S. Complications during and devices. J Endod, 2009;35:791-804. root canal irrigation. Endod Topics, 2007;16:27-63. 10. Jaju S, Jaju PP. Newer Root Canal Irrigants in Horizon: A 28. Bronnec F, Bouillaguet S, Machtou P. Ex vivo assessment Review. Int J Dent, 2011;851359. of irrigant penetration and renewal during the cleaning and 11. Siqueira JF Jr, Rôças IN, Favieri A, Lima KC. shaping of root canals: a digital subtraction radiographic Chemomechanical reduction of the bacterial population study. Int Endod J, 2010;43:275-282. in the root canal after instrumentation and irrigation 29. Macedo RG, Verhaagen B, Wesselink PR, Versluis M, with 1%, 2.5%, and 5.25% sodium hypochlorite. J Sluis LWM. Influence of refreshment/activation cycles and Endod, 2000;26:331-334. temperature rise on the reaction rate of sodium hypochlorite 12. Zehnder M, Kosicki D, Luder H, Sener B, Waltimo T. with bovine dentine during ultrasonic activated irrigation. Tissue-dissolving capacity and antibacterial effect of Int Endod J, 2014;47:147-154. buffered and unbuffered hypochlorite solutions. Oral Surg 30. Schäfer E, Vlassis M. Comparative investigation of two Oral Med Oral Pathol Oral Radiol Endod, 2002;94:756-762. rotary nickel-titanium instruments: ProTaper versus RaCe. 13. Ercan E, Ozekinci T, Atakul F, Gül K. Antibacterial Part 2. Cleaning effectiveness and shaping ability in activity of 2% chlorhexidinegluconate and 5.25% sodium severely curved root canals of extracted teeth. Int Endod hypochlorite in infected root canal: in vivo study. J J, 2004;37:239-248. Endod, 2004;30:84-87. 31. Neves MA, Provenzano JC, Rôças IN, Siqueira JF 14. Shen Y, Qian W, Chung C, Olsen I, Haapasalo M. Jr. Clinical Antibacterial Effectiveness of Root Canal Evaluation of the effect of two chlorhexidine preparations Preparation with Reciprocating Single-instrument or on biofilm bacteria in vitro: a three-dimensional quantitative Continuously Rotating Multi-instrument Systems. J Endod, analysis. J Endod, 2009;35:981-985. 2016;42:25-29. 15. Blank-Gonçalves LM, Nabeshima CK, Martins 32. Alves FR, Almeida BM, Neves MA, Rôças IN, Siqueira JF. GH, Machado ME. Qualitative analysis of the removal Time-dependent antibacterial effects of the self-adjusting of the smear layer in the apical third of curved roots: file used with two sodium hypochlorite concentrations. J conventional irrigation versus activation systems. Endod, 2011;37:1451-1455. J Endod, 2011;37:1268-1271. 16. Haapasalo M, Wang Z, Shen Y, Curtis A, Patel P, Khakpour M. Conflict of Interests: Nothing to declair. Tissue dissolution by a novel multisonicultracleaning system Financial Disclosure Statement: Nothing to declair. and sodium hypochlorite. J Endod, 2014;40:1178-1181. Human Rights Statement: None reguired. 17. Živković S, Nešković J, Jovanović-Medojević M, Popović- Animal Rights Statement: None reguired. Bajić M, Živković-Sandić M. XP-endo Finisher: a new solution Received on April 2, 2018. for smear layer removal. Serb Dent J, 2015;62:122-129. Revised on Jun 2, 2018. 18. Ayranci LB, Arslan H, Akcay M, Capar ID, Gok T, Saygili Accepted on December 2, 2018. G. Effectiveness of laser-assisted irrigation and passive ultrasonic irrigation techniques on smear layer removal in Correspondence: middle and apical thirds. Scanning, 2016;38:121-127. Slavoljub Živković 19. Crumpton BJ, Goodell GG, McClanahan SB. Effects Department of restorative odontology and endodontics on smear layer and debris removal with varying School of Dentistry, University of Belgrade volumes of 17% REDTA after rotary instrumentation. J Belgrade, Serbia Endod, 2005;31:536-538. e-mail: [email protected]

10.2478/bjdm-2019-0007

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L BALKAN JOURNAL OF DENTAL MEDICINE A ISSN 2335-0245 IC G LO TO STOMA

Comparative Evaluation of Resistance to Cyclic Fatigue of Three Rotary Endodontic Ni-Ti Instruments

SUMMARY Lampros Intzes, Zoi-Despoina Tzima, Background/Aim: The present study examined the resistance to cyclic Christos Gogos fatigue of three different rotary Ni-Ti instruments: K3XF (Kerr, Orange, Department of Endodontology, School of CA), HyFlex CM (Coltene/Whaledent, Altstätten, Switzerland) and X7 Dentistry, Aristotle University of Thessaloniki, EdgeFile (EdgeEndo, Albuquerque, New Mexico). Material and Methods: Thessaloniki, Greece Thirty instruments (n=30) of each type were used with tip size 25 and 0.04 taper. All instruments were constrained to 600 of curvature with a of 5 mm by the use of two grooved stainless steel rods and rotated at a speed of 300 rpm and 3.0 Ncm of torque. The time until separation was recorded for each of the instruments and the number of cycles to fracture (NCF) was calculated. Statistical analysis was performed using R Programming language. Results: The X7 EdgeFile instrument showed significantly greater resistance to cyclic fatigue when compared to the HyFlex CM and the K3XF with mean NCF for each instrument 1046 ± 311, 707 ± 219 and 360 ± 96 respectively. HyFlex CM performed significantly better than K3XF. Conclusions: The X7 EdgeFile Ni-Ti file appears to be significantly more resistant to fracture, due to flexural fatigue, than the HyFlex CM and the K3XF. Key words: Cyclic Fatigue, Nickel-Titanium Rotary Instruments, K3xf, Hyflex Cm, ORIGINAL PAPER (OP) X7 Edgefile Balk J Dent Med, 2019;36-39

Introduction will result in crack propagation and failure due to cyclic flexural fatigue6. There are indisputable advantages in using nickel- Advances in the metallurgy of Ni-Ti instruments titanium (Ni-Ti) rotary instruments1, resulting in their have significantly improved the resistance to flexural 7 almost universal use among clinicians. However, fatigue . In our study three different Ni-Ti instruments during preparation, separation of these instruments can were used; K3XF (Kerr, Orange, CA), HyFlex CM (Coltene/Whaledent, Altstätten, Switzerland) and X7 occur, exacerbating the difficulty of the case. Ni-Ti file EdgeFile (EdgeEndo, Albuquerque, New Mexico). K3XF separation is mostly associated with two phenomena; files are the development of the earlier K3 files (Kerr, torsional failure and flexural fatigue of the instrument2,3. Orange, CA), maintaining the same design geometry, but Torsional failure can occur due to the relatively low now composed of R-phase heat treated Ni-Ti alloy7,8. The tensile strength of Ni-Ti alloy in comparison to stainless Ni-Ti alloy R-phase is an intermediate transformation 4 steel . In this case, the jamming of the tip of the phase with a rhombohedral crystalline structure between instrument in the root canal, while its shank continues to the austenite and martensite phases9. This crystalline rotate, will lead to fracture when the torque applied by the structure is characterized by increased flexibility and handpiece exceeds the instrument’s torsional limit5. On reduced stresses on the instrument when rotating in curved the other hand, when a Ni-Ti instrument rotates within a canals, thus enhancing cyclic fatigue resistance10. curved canal, at any moment, the inner instrument surface The EdgeFile is a relatively new rotary Ni-Ti file is subjected to compression and the outer to tension. This made of thermally treated nickel-titanium alloy, which Balk J Dent Med, Vol 23, 2019 Resistance to Cyclic Fatigue of Rotary Instruments 37 does not rebound to its original shape after sterilization. The results were analyzed with the use of the R The manufacturer claims that the EdgeFile instruments programming language. Data were analyzed for normal are mechanically compatible, therefore can be used distribution and then statistical analysis was performed interchangeably, with the files of other instrument systems with independent samples t-test. The selected level of such as Vortex, Profile (Densply-Maillefer, Ballaigues, significance was 0.05. Switzerland), Sequence (Brasseler, USA) and K3 (and K3XF in extent). Hyflex CM rotary files (Coltene/Whaledent Altstätten, Switzerland) are fabricated from an alloy subjected to special proprietary thermomechanical process resulting in more flexibility and resistance to flexural fatigue (Controlled Memory/CM wire)11,12,13. Due to their unique manufacturing process, they do not rebound to their original shape when mechanical stress is applied12. Deformed instruments partially or fully recover their original shape after sterilization14,15. The purpose of this study is to compare the resistance to cyclic fatigue between K3XF, HyFlex CM and EdgeFile (X7). The null hypothesis is that, Figure 1. The flexural fatigue testing model under continuous rotation there will be no difference in resistance to flexural fatigue between the three file systems.

Material and Methods

For this study, thirty rotary nickel-titanium instruments were used for each system (K3XF, HyFlex CM and EdgeFile X7). All instruments were of equal Figure 2. Each instrument was constrained to rotate at a 600 angle and length (25 mm), tip size 25 and a constant 0.04 taper. To 5 mm radius of curvature test the resistance to fracture of each instrument under continuous rotation, the following model (Figure 1) was constructed: Two grooved stainless steel rods with a diameter of 2 mm, were used to constrain the apical part Results of each instrument in a curvature of 600 and a radius of 5 mm (Figure 2), in accordance with previous research All instruments separated within the curved part model16. Each instrument was rotated at a constant of the file. The analysis of the data confirmed normal speed of 300 rpm and 3 Ncm of torque with the use of distribution (Shapiro-Wilk normality test). The mean an X-Smart endodontic motor handpiece (Dentsply- NCF for the K3XF, HyFlex CM and X7 EdgeFile Maillefer, Ballaigues, Switzerland). The time of rotation instruments were 360 (± 96), 707 (± 219) and 1046 (± until fracture for each instrument was recorded with the 311), respectively. The independent samples t-test showed use of a VMS-001 USB microscope (Veho, Hampshire, a statistically significant difference (p<0.05) between the UK) connected to a computer with an Ubuntu (Canonical NCF of all instruments tested, hence the null hypothesis Ltd, London, UK) Linux operating system and measured was rejected. in seconds with the use of VLC media player software (Softonic International, S.A., Barcelona, Spain). All the instruments in this study were tested at room temperature. Finally, the number of cycles to fracture (NCF) was Discussion calculated according to the mathematical formula: Number of Cycles to Fracture = Time until separation (in The ideal test model for flexural fatigue in clinical seconds) * 300 (rpm) / 60. use should be the . However, the root canal In this study, no wear was observable in the rods, and morphology would be altered after instrumentation, thus this correlated with no progressive change in the time to rendering the conditions of the study different for each fracture over the 90 tests. instrument. Testing in different canals would encounter 38 Lampros Intzes et al. Balk J Dent Med, Vol 23, 2019 the same problem. Therefore, it seems reasonable to test References Ni-Ti instruments in vitro in order to investigate resistance to flexural fatigue17. The testing rig constructed for our 1. Hülsmann M, Peters OA, Dummer PMH: Mechanical study was similar to that of Zinelis et a.l18. Alterations preparation of root canals: shaping goals, techniques and included a 60° curvature according to Pruett16 with a means. Endod Topics, 2005;10:30-76. radius of 5 mm and a higher rotational speed (300rpm). 2. Serene TP, Adams JD, Saxena A. Nickel-titanium instruments: applications in endodontics. St Louis, MO, In our model, special care was taken to ensure that the USA: Ishiyaku EuroAmerica, 1995. different instruments were constricted in exactly the 3. Sattapan B, Palamara J, Messer H. Torque during canal same position, which is not the case when a relatively instrumentation using rotary nickel-titanium files. J Endod, wide (1.2 – 2 mm) metal tube is used to simulate the 2000;26:156-160. canal19,20. In that case, the individual bending properties 4. Phillips R. Skinner’s science of dental materials. and cross section design of different files lead to differing Philadelphia: WB Saunders Co., 1991. positioning in the artificial canal. Some newer study 5. Peters OA. Current challenges and concepts in the preparation of root canal systems: a review. J Endod, models use artificial canals that follow the size and taper 21 2004;30:559-567. of the instrument at a given curvature . However, the 6. Parashos P, Messer H. Rotary NiTi instrument fracture and superiority of one laboratory study model design over its consequences. J Endod, 2006;32:1031-1043. another is relevant when attempting to extrapolate in vitro 7. Plotino G, Costanzo A, Grande NM, Petrovic R, Testarelli results to indicate potential clinical performance. K3XF L, Gambarini G. Experimental evaluation on the influence rotary Ni-Ti files are known to exhibit improved results of autoclave sterilization on the cyclic fatigue of new Nickel- when tested for flexural fatigue in comparison with its Titanium rotary instruments. J Endod, 2012;38:222-225. predecessor K37, 22. 8. Ha JH, Kim SK, Cohenca N, Kim HC. Effect of R-phase heat treatment on torsional resistance and cyclic fatigue The results of our study showed that the X7 EdgeFile fracture. J Endod, 2013;39:389-393. and Hyflex CM demonstrate greater resistance to flexural 9. Duerig TW, Bhattacharya K. The influence of the R-Phase fatigue than K3XF. Earlier research has shown that files on the superelastic behavior of NiTi. Shap Mem Superelast, made from controlled memory Ni-Ti alloy are extremely 2015;1:153-161. flexible when compared with conventional superelastic 10. Lopes HP, Gambarra-Soares T, Elias CN, Siqueira Ni-Ti files23,11. The specific mechanical properties of X7 JF Jr, Inojosa IF, Lopes WS, et al. Comparison of the EdgeFile and HyFlex CM could be a possible reason for mechanical properties of rotary instruments made of conventional Nickel-Titanium wire, M-wire, or Nickel- their superiority to K3XF. The X7 EdgeFile instrument Titanium alloy in R-phase. J Endod, 2013;39:516-520. can be deformed by light pressure, the characteristic also 11. Shen Y, Qien W, Abtin H, Gao Y, Haapasalo M. Fatigue found in Hyflex CM, which exists in a martensitic state testing of controlled memory wire nickel-titanium rotary in use24. Due to their crystalline structure, HyFlex CM instruments. J Endod, 2011;37:997-100. instruments, when deformed, partially or fully recover 12. Zhao D, Shen Y, Peng B, Haapasalo M. Micro-computed their original shape after sterilization14,15. However, X7 tomography evaluation of the preparation of mesiobuccal EdgeFile instruments do not regain their original shape root canals in maxillary first molars with Hyflex CM, Twisted when heated above 125o C. That fact has led us to assume Files, and K3 instruments. J Endod, 2013;39:385-388. 13. Plotino G, Testraelli L, Al-Sudani D, Pongione G, Grande that the X7 EdgeFile instruments exhibit a martensite/ NM, Gambarini G. Fatigue resistance of rotary instruments austensite composition, with the former constituent manufactured using different nickel-titanium alloys: a being in a greater proportion. This fact could explain the comparative study. Odontology, 2014;102:31-35. superior performance of X7 EdgeFile over HyFlex CM 14. Peters OA, Gluskin AK, Weiss RA, Han JT. An in in this study. Up to date, the specifics of the metallurgy vitro assessment of the physical properties of novel of the two aforementioned instruments remain, as yet, Hyflex nickel-titanium rotary instruments. Int Endod J, unpublished, and therefore our assumptions remain 2012;11:1027-1034. 15. Alfoqom Alazemi M, Bryant ST, Dummer PMH. unverified. Deformation of Hyflex CM instruments and their shape recovery following heat sterilization. Int Endod J, 2015;48:593-601. 16. Pruett JP, Clement DJ, Carnes DL Jr. Cyclic fatigue testing Conclusions of Nickel-Titanium endodontic instruments. J Endod, 1997;23:77-85. Under the conditions of this in vitro study, it can be 17. Plotino G, Grande NM, Cordaro M, Testarelli L, Gambarini concluded that the X7 EdgeFile Ni-Ti file is significantly G. A review of cyclic fatigue testing of Nickel-Titanium rotary instruments. J Endod, 2009;35:1469-1476. less susceptible to fracture due to flexural fatigue than the 18. Zinelis S, Darabara M, Takase T, Ogane K, Papadimitriou HyFlex CM and the K3XF. The HyFlex CM appeared GD. The effect of thermal treatment on the resistance of significantly less susceptible to fracture when compared to nickel-titanium rotary files. Oral Surg Oral Med Oral Pathol the K3XF. Oral Radiol Endod, 2007;103:843-847. Balk J Dent Med, Vol 23, 2019 Resistance to Cyclic Fatigue of Rotary Instruments 39

19. Anderson ME, Price JWH, Parashos P. Fracture resistance Conflict of Interests: Nothing to declair. of electropolished rotary nickel-titanium endodontic Financial Disclosure Statement: Nothing to declair. instruments. J Endod, 2007;33:1212-1216. Human Rights Statement: All the procedures on humans were 20. Ounsi HF, Salameh Z, Al-Shalan T, Ferrari M, Grandini conducted in accordance with the the Helsinki Declaration S, Pashley DH, et al. Effect of clinical use on the cyclic fatigue resistance of ProTaper nickel-titanium rotary of 1975, as revised 2000. Consent was obtained from the instruments. J Endod, 2007;33:737-741. patient/s and approved for the current study by national ethical 21. Plotino G, Grande NM, Cordaro M, Testarelli L, Gambarini committee. None reguired. G. Influence of the shape of artificial canals on the Animal Rights Statement: None reguired. fatigue resistance of NiTi rotary instruments. Int Endod J, 2010;43:69-75. 22. Perez-Higueras JJ, Arias A, Macorra JC. Cyclic fatigue Received on January 5, 2019. resistance of K3, K3XF, and Twisted File Nickel-Titanium Revised on February 20, 2019. files under continuous rotation or reciprocating motion. J Accepted on February 21, 2019. Endod, 2013;39:1585-1588. 23. Ninan E, Berzins DW. Torsion and bending properties Correspondence: of shape memory and superelastic nickel-titanium rotary instruments. J Endod, 2013;39:101-104. Lampros Intzes 24. Zhou H, Peng B, Zheng YF. An overview of the mechanical Department of Endodontology, School of Dentistry properties of nickel–titanium endodontic instruments. Endod Aristotle University of Thessaloniki, Thessaloniki, Greece Topics, 2013;29:42-54. e-mail: [email protected]

10.2478/bjdm-2019-0008

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L BALKAN JOURNAL OF DENTAL MEDICINE A ISSN 2335-0245 IC G LO TO STOMA

Modern Trends in Prosthetic Implant Rehabilitation of Patients: Case Report with 5-Year Follow-Up

SUMMARY Aleksandar Đorđević¹, Mirko Mikić², Background/Aim: Implant treatment expands extensively the Jelena Stanišić¹, Filip Đorđević¹ possibilities of prosthetic treatment, which provide benefits, bigger comfort ¹ Faculty of Medicine University of Prishtina - as well as general improvement of the patient’s life quality. In cases with Kosovska Mitrovica, Serbia no possibility of implantation, it is possible to improve conditions by using ² Medical Faculty Podgorica, Podgorica, modern methods for bone tissue repair. One of factors important for the Montenegro long-term success is proper oral hygiene, as well as raising awareness of its importance to patients. The aim of the paper is to present a patient rehabilitated with multiple implants and followed-up for a five-year period, and to point out the importance of raising patient’s awareness and motivation in order to preserve the results of the treatment. Case Report: A 31-year-old patient was admitted to the oral surgery clinic for rehabilitation of a poor oral health status. After taking history, clinical examination and additional analysis, the following treatment plan was suggested: to remove impacted upper canines and to put an implant supported by fixed prosthesis in the upper jaw, to make two implants supported by bridges laterally and one dental supported by bridge in the inter-canine sector in the lower jaw. The treatment was carried out in several stages that involved extraction of residual roots and impacted teeth, augmentation of bone defects with bone substitutes and bio-absorbable membranes, placing implant, and prosthetic rehabilitation. By verbal communication with the patient, we pointed out the importance of proper oral hygiene and regular check-ups. The five year follow-up showed the absence of factors that could adversely affect the success of the treatment, and the patient was still highly motivated to maintain proper oral hygiene. Conclusions: It is possible to achieve predictable results in complex cases by using a multiphase prosthetic treatment supported by implants. Concerning a long-term success, motivation, proper information and patient’s willingness to cooperate play an important role. CASE REPORT (CR) Key words: Dental Implants, Motivation, Quality of Life, Rehabilitation Balk J Dent Med, 2019;40-44

Introduction aspect. For many patients, prosthetic rehabilitation with implants presents a definite need and directly affects Implant treatment extensively expands possibilities quality of life, patient satisfaction and psychological state of mind3. However, in some cases, due to the of prosthetic rehabilitation, which becomes more absence of anatomical and morphological conditions acceptable to the patient, unlike conventional prosthetics (vertical and horizontal dimensions of the alveolar compensations that may be the cause of dissatisfaction, ridge and the proximity of anatomical structures such 1 causing decline in quality of life . The patients’ decision as the maxillary sinus in the maxilla and the mandibular to accept suggestion of undergoing implant treatment canal in the mandible) implant rehabilitation may be is based on several factors, primarily on expectation of carried out only by use of some additional procedures improving function and aesthetics, as well as financial that modern treatment methods ensure4. The concept of Balk J Dent Med, Vol 23, 2019 Prosthetic Implant Rehabilitation 41 guided bone regeneration, which involves the use of a inter-canine region. After presentation of the treatment bone substitutes and bio resorptive membranes, allows plan, the detailed briefing of the patient took place. vertical and horizontal bone augmentation in combination The complexity of the process and the durability of the with a different surgical approach5. Moreover, it is well multi-phase care were pointed out, as well as factors ascertained that implantation into bone substituent is that are important for the success of the therapy and possible, and that implants do not behave differently from of the possible complications. Education also included implants embedded in natural bone6. the aspect of the importance of an adequate oral care Patient’s expectations are high and, therefore, as hygiene maintenance in patients with implants. The need fixed prosthetic rehabilitation offers several advantages of coming to regular follow-ups, and responsibility of the over rehabilitation with any kind of mobile prosthetic patient in the prevention of possible complications due to appliances, it should be a treatment of choice whenever non-compliance with the proposed measures. it is possible7. However, there are several problems with implant supported fixed prosthetic appliances, especially the presence of excess cement, which is difficult to be removed, or additional difficulties in maintaining adequate oral hygiene8, especially if possibility of self-cleaning is heavy. Therefore, patient education in maintaining oral hygiene is necessary for long-term success whenever an implant supported fixed prosthetics is planned9. If patient’s cooperation and motivation is not present, a plan of rehabilitation should be focused on conventional methods10. The aim of this paper is to present a patient rehabilitated with multiple implants and followed-up for a Figure 1. Panoramic radiograph before intervention five-year period, and to point out the importance of raising patient’s awareness and motivation in preserving the results of the treatment. Preparation for Implantation Multiple extractions of all teeth in the upper jaw took place in the first phase of patient rehabilitation. In the Case Report second phase, an endodontic-surgical treatment of lower frontal teeth was done, with simultaneous extraction of Patient BG, 31 years old, came to the Clinic of remaining lower teeth. The third stage involved surgical Oral Surgery, Medical Faculty, University of Pristina extraction of upper impacted canines with augmentation with headquarters in Kosovska Mitrovica. Except wish of bone defects in order to create favourable conditions to improve his oral health from the aspect of aesthetics for the implantation (Figure 2). Bone augmentation and function, patient didn’t have any local complaint. was performed by bone substitute (Bio-Oss®) and bio- After further interviewing and examining the patient, resorptive membranes (Bio-Gide®). After a period of an extremely unfavourable oral health status and high healing extraction wounds for six months and analysis of anxiety for dental treatment was found (after completing the CBCT image, the next stage encompassed the implant- a questionnaire suggested by Humphries et al.11). Verbal prosthetic treatment. monitoring and motivational interviews have established willingness of the patient to cooperate, enabling further clinical examination and implementation of supplementary diagnostic procedures. Clinical examination revealed a lack of several teeth in the upper jaw and the advanced caries with extensive destruction of hard dental tissues at the rest of upper teeth (Figure 1), with multiple periapical lesions and the presence of both impacted upper canines. In the lower jaw, several teeth were missing or being carious. Several options of prosthetic rehabilitation were offered to the patient. One of the options was an implant- supported fixed circular bridge in the upper jaw, two implant-supported bridges in both lateral regions of the lower jaw, and one dental-supported bridge in the Figure 2. Surgical extraction of impacted canines 42 Aleksandar Đorđević et al. Balk J Dent Med, Vol 23, 2019

Surgical Aspect of Implant-Prosthetic Treatment A two-phase surgical protocol of implantation comprised implantation and covering the implant in the first phase. Three Bredent “Blue Sky” implants were installed at the right side of the maxilla in the region of teeth #13, #14, and #15, with dimensions 4.0 x 12mm, 4.0 x 12mm, and 3.5 x 12mm, while at the left side, three implants of the same dimensions were put in the region of teeth #24, #25 and #26. In the lower jaw, on the left side, we installed two implants in the region of teeth #34 and #35 (Bredent Blue Figure 4. Definitely cemented prosthetic work Sky, dimensions 3.5x12 and 4.0x10). On the right side, in the region of teeth #43 and #45, we also installed two implants (3.5x10 and 4.0x10). In the prosthetic phase, this arrangement would allow a production of two lateral Maintaining Oral Hygiene implant-supported bridges and a dentally supported bridge Measures related to the maintenance of oral hygiene in the inter-canine sector. were focused on mechanical and chemical control of After a three-month period of osseointegration dental plaque and food residues accumulation. The (meanwhile, the patient worn a mobile prosthetic device), proposed methods of mechanical control included the use a second surgical phase was carried out, which comprised of soft , less abrasive tooth paste, interdental detection of implants and setting of gingival-formers for brushes and stimulants (“soft pick”), and an interdental a period of another two weeks to form a proper gingival aids adapted for patients with implants (“Superfloss”). profile. Also, the patient was proposed to mechanically remove food residues by using water irrigation (“Water- Prosthetic Aspect of the Treatment pick” machine). For chemical control of dental plaque Firstly, a single-phase print was taken and implant accumulation, non-alcoholic (0.12% transfers placed, which were spliced to increase the chlorhexidine gluconate) were proposed, two to three stability and accuracy during the printouts (Figure 3). A times per day for a period of one month with pauses to re-registration of vertical relations was also performed avoid negative effects of the solution. due to the loss of the vertical dimension of occlusion. After that, a laboratory phase of the metal construction Follow-ups followed and after clinical testing, the laboratory phase At the follow-up six months after the submission of was finished by placing ceramics. For a period of one definitive prosthetic work, it was visible that the patient month, the patient was wearing temporarily cemented adhered to advices related to the maintenance of oral compensation in order to make any corrections that hygiene, and that the functionality and aesthetics were might reconcile to expectations of the patient concerning favourable, further motivating the patient to maintain a to colour, shape, size and other characteristics of the long-term advantageous result. prosthesis. Definitive cementation of bridges was At the follow-up after one year, the gingiva did not performed by glass-ionomer cement (Figure 4). show visual signs of inflammation. A plaque accumulation around implants was under control; clinical probing of the sulcus depth did not show noticeable resorption of bone tissue around the implants, and there was no . By checking the occlusion, it was found that the occlusion was balanced, without traumatic contacts. Panoramic radiograms did not show signs of resorption of the peri-implant bone. The patient was satisfied with the result and expressed a high degree of motivation for further maintaining oral hygiene. Five years after the treatment, everything was satisfactory (Figure 5). Further education on maintaining oral hygiene of the patient was not necessary since he adhered to everything that was proposed in the previous period. An analysis of panoramic radiogram revealed an absence of pathological bone resorption around implants Figure 3. Transfers are placed on the implants (Figure 6). Balk J Dent Med, Vol 23, 2019 Prosthetic Implant Rehabilitation 43

preserve and augment the residual alveolar ridge by bone substitutes in combination with membranes4, as bone defect was limited by bone tissue; in the case of major defects a solid non-corrosive membranes commonly made of titanium might be used to prevent deformation of the alveolar ridge15. Studies have shown that implantation into augmented bone can give predictive results as implantation into natural bone, depending on bone region and density16-18. Although several studies stressed a need for additional research, it seems that the use of bone substitutes in combination with bio-resorptive membranes can serve as an alternative to conventional protocols of implant insertion19-21. Several studies have also shown the importance of Figure 5. Clinical situation after 5 years interlinking implants with fixed prosthetic works because due to the mode of force distribution behaves as a unique functional unit22, 23. Concerning rehabilitation with implant supported fixed prostheses, in addition to fulfilling local clinical conditions needed for a long-term favourable result, a proper cooperation of the patient is absolutely necessary, as well as motivation and raising awareness of the importance of maintaining oral hygiene. Several authors state that the prevention of late complications in the form of peri-implant mucositis and periimplantitis but also the prevention of pathological resorption of peri-implant bone tissue is the matter of respecting biomechanical principles, balancing occlusal forces and maintaining adequate oral hygiene24,25. Figure 6. Panoramic radiography after 5 years The fact that cemented fixed prosthesis on implants cannot be removed during professional office maintenance, the maintenance of oral hygiene is a priority and a very Discussion important segment of preserving the health of peri-implant tissue26, 27. Therefore, more attention have been paid to the There are several factors that may be the cause patient’s education concerning dental plaque accumulation, of an unfavourable oral health status expressed in influence of pathogenic agents from bio film on peri- toothless young people, one of which being fear of pain implant tissue, complications that can arise due to failure to during dental treatment12. Therefore, obtaining patient maintain adequate oral hygiene, and the way in which the confidence at the beginning of treatment is essential13. formation of deposits can be controlled. Concerning our patient, an individual approach included primary education of the patient about the general causes of fear of dental interventions and informing him of modern methods of pain control. Applying potent local Conclusions anaesthetics allows painless oral surgery, which is an important factor in gaining confidence of the patient, It is possible to achieve predictable results in controlling fear from dental interventions, and achieving complex cases by using a multiphase prosthetic treatment further motivation for continuing therapy14. supported by implants. Concerning a long-term success, motivation, proper information and patient’s willingness A modern approach in oral implantology implies a to cooperate play an important role. multidisciplinary approach in the treatment of complex cases and teamwork. Therefore, this patient was treated from psychological, surgical and prosthetic approaches. The surgical aspect of the presented patient encompassed References some routine procedures, such as tooth apicoectomies in the lower frontal region or extraction of the impacted 1. Blomberg S, Lindquist LW. Psychological reactions to upper canines, but also some relatively modern methods, edentulousness and treatment with jawbone-anchored like the use of targeted bone regeneration protocol to bridges. Acta Psychiatr Scand, 1983;68:251-262. 44 Aleksandar Đorđević et al. Balk J Dent Med, Vol 23, 2019

2. SimensenAN, Bøe OE. Patient Knowledge and Expectations 17. Becktor JP, Isaksson S, Sennerby L. Survival analysis of Prior to Receiving Implant-Supported Restorations. Int J endosseous implants in grafted and nongrafted edentulous Oral Maxillofac Implants, 2015;30:41-47. maxillae. Int J Oral Maxillofac Implants, 2004;19:107-115. 3. Buch RS, Weibrich G, Wegener J, Wagner W. Patient 18. Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg satisfaction with dental implants. Mund Kiefer Gesichtschir, B, Thomsen P. The soft tissue barrier at implants and teeth. 2002;6:433-436. Clin Oral Implants Res, 1991;2:81-90. 4. Benic GI, Hammerle CH. Horizontal bone augmentation 19. Narayan TV, Narayan S. Longitudinal Evaluation of by means of guided bone regeneration. Periodontol, 2000 Implants Placed into Bone Regenerated by the Guided Bone 2014;66:13-40. Regeneration (GBR) Technique: A Series of 7 Patients with 5. Zitzmann NU, Scharer P, Marinello CP. Long-term results 13 Implants of at Least Months Follow-up Postloading. of implants treated with guided bone regeneration: A IJOICR, 2010;1:89-95. 5-year prospective study. Int J Oral Maxillofac Implants, 20. Esposito M, Grusovin MG, Coulthard P, Worthington HV. 2001;16:355-366. The efficacy of various bone augmentation procedures 6. Jung RE, Fenner N, Hammerle CH, Zitzmann NU. Long for dental implants: a Cochrane systematic review of term outcome of implants placed with guided bone randomized controlled clinical trials. Int J Oral Maxillofac regeneration (GBR) using resorbable and non-resorbable Implants, 2006;21:696-710. 21. Retzepi M, Donos N. Guided Bone Regeneration: biological membranes after12-14years. Clin Oral Implants Res, principle and therapeutic applications. Clin Oral Impl Res, 2013;24:1065-1073. 2010;21:567-576. 7. Jung RE, Pjetursson BE, Glauser R, Zembic A, Zwahlen 22. Taylor TD, Agar JR. Twenty years of progress in implant M, Lang NP. A systematic review of the 5-year survival and prosthodontics. J Prosthet Dent, 2002;88:89-98. complication rates of implant-supported single crowns. Clin 23. Zellin G, Gritli-Linde A, Linde A. Healing of mandibular Oral Implants Res, 2008;19:119-130. defects with different biodegradable and non-biodegradable 8. Chee W, Felton DA, Johnson PF, Sullivan DY. Cemented membranes: an experimental study in rats. Biomater, versus screw-retained implant prostheses: which is better? 1995;16:601-609. Int J Oral Maxillofac Implants, 1999;14:137-141. 24. Misch CE. Influence of biomechanics on implant 9. Augthun M, Tinschert J, Huber A. In vitro studies on the complications. Acad Dental Mater Proc, 2000;14:49-62. effect of cleaning methods on different implant surfaces. J 25. Misch CE. Screw-retained versus cement-retained implant Periodontol, 1998;69:857-864. supported prostheses. Pract Periodontics Aesthet Dent, 10. Lekholm U, Zarb GA. Patient selection and preparation. In: 1995;7:15-18. Brånemark P-I, Zarb GA, Albrektsson T (editors). Tissue 26. Serino G, Ström C. Peri-implantitis in partially edentulous integrated prostheses: osseointegration in clinical dentistry. patients: association with inadequate plaque control. Clin Chicago: Quintessence, 1985. Oral Impl Res, 2009;20:169-174. 11. Humphris GM, Dyer TA, Robinson PG. The modified dental 27. Mombelli A, Marxer M, Gaberthuel T, Grunder U, Lang anxiety scale: UK general public population norms in 2008 NP. The microbiota of osseointegrated implants in patients with further psychometrics and effects of age. BMC Oral with a history of periodontal disease. J Clin Periodontol, Health, 2009;9:20. 1995;22:124-130. 12. Djordjevic F, Stanisic J, Djordjevic A, Vlahovic Z. Pain and justification pain from dental intervention. Praxis Medica, Conflict of Interests: Nothing to declair. 2015;44:27-30. Financial Disclosure Statement: Nothing to declair. 13. Bylund CL, Peterson EB, Cameron KA. A practitioner’s Human Rights Statement: All the procedures on humans were guide to interpersonal communication theory: an overview conducted in accordance with the the Helsinki Declaration of 1975, and exploration of selected theories Patient Educ Couns, as revised 2000, and with national ethical committee. Consent was 2012;87:261-267. obtained from the patient/s and approved for the current study by 14. Ramírez-Carrasco, Butrón-Téllez Girón. Effectiveness of national ethical committee. Animal Rights Statement: None reguired. Hypnosis in Combination with Conventional Techniques of Behavior Management in Anxiety/Pain Reduction during Received on January 12, 2018. Dental Anesthetic Infiltration. Hindawi Pain Res Manage, Revised on March 2, 2018. 2017;Article ID 1434015, 5 pages. Accepted on October 12, 2018. 15. Tolstunov L. Vertical Alveolar Ridge Augmentation in Implant Dentistry: A surgical Manual. Wiley Blackwel, 2016. Correspondence: 16. Bazrafshan N, Darby I. Retrospective success and survival Aleksandar Đorđević rates of dental implants placed with simultaneous bone Department of Stomatology augmentation in partially edentulous patients. Clin Oral Faculty of Medicine University of Prishtina Impl Res, 2014;25:768-773. e-mail: [email protected]

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L BALKAN JOURNAL OF DENTAL MEDICINE A ISSN 2335-0245 IC G LO TO STOMA

Mini-Implants and Zirconium Crowns in Treating Congenitally Missing Maxillary Lateral Incisors: Case Report

SUMMARY Hend Mahmoud Mohamed Hegazi Background/Aim: A problem of congenitally missing lateral incisors Department of Removable Prosthodontics is frequently encountered in dentistry, with several available treatment Department, Cairo University, Egypt modalities, the choice depending on each case. Case Report: A young female patient with bilateral missing lateral incisors was in need for dental treatment for esthetics. She had spacing among the upper anterior teeth with class I molar relationship. Orthodontic space creation was carried out followed by two-piece mini dental implant placement. Two-stage protocol was followed. After osseointegration, implants were exposed. Healing collars were installed to allow mucosal healing. Closed tray implant level impression was taken. Zirconium crowns were chosen for optimum esthetic results. Conclusions: Mini-implants can be used successfully for restoring congenitally missing lateral incisors after space opening. Esthetic results can be enhanced using Zirconium crowns Key words: Congenitally missing lateral incisors, Mini-implants, Angled abutments, CASE REPORT (CR) Zirconium crowns Balk J Dent Med, 2019;45-49

Introduction both fixed and removable prosthesis6. They can solve problem of reduced bone width in regions with anatomical Maxillary lateral incisors are the second most limitations7. common missing teeth1. Being located in the esthetic In the following case report, a space between the zone, congenitally missing laterals represent a challenging central incisors and canines was created orthodontically to case for dentists as they affect the esthetics and general restore the maxillary lateral incisors with single zirconium appearance of the patients. There are several options crowns on two mini-implants. to treat those patients and the selection of the option depends on several factors. The space can either be closed with canine substitution for the lateral incisor2 or it can be opened for prosthetic replacement of the Case Report upper lateral incisor. Several options are available for prosthetic replacement including: resin bonded bridge, A young female patient presented to the outpatient cantilever bridge, conventional fixed partial denture, or clinic at the Faculty of dentistry, Cairo University, with single crown implant restoration3. The choice among these factors depends on occlusal relationship and other a chief complain of unpleasant appearance and spacing occlusal disharmonies, over-jet and over-bite, canine size between upper anterior teeth. A thorough examination and shape, condition of adjacent teeth, as well as patient’s was performed including extra-oral and intra-oral desire and expectations4,5. examinations as well as panoramic X-ray. The patient Mini-implants have been reported intensively in had congenitally missing upper lateral incisors bilaterally literature with a long term high success rates to support (Figures 1-4). 46 Hend Mahmoud Mohamed Hegazi Balk J Dent Med, Vol 23, 2019

Figure 2. Pre-operative occlusion - frontal view

Figure 1. Pre-operative extra-oral photos; A: Frontal view, B: Profile view

Figure 3. Occlusion. (A) Right side, (B) Left side

Figure 4. Intra-oral occlusal view. (A) Maxillary arch, (B) Mandibular arch

Treatment Planning was carefully examined. The patient had Angle’s class I molar relationship, with minor occlusal disharmonies. A Upper and lower primary impressions were taken multi-disciplinary approach combining both orthodontist to obtain a diagnostic casts. This was followed by a and prosthodontist was required to restore the esthetics face-bow (Bio-Art Equipamentos Odontológicos Ltda) and function. The chosen treatment was space creation record to mount the upper cast on a semi-adjustable by orthodontic movement of the teeth, followed by mini- articulator (Bio-Art Equipamentos Odontológicos Ltda), implant placement to support cemented zirconium crowns and a diagnostic bite to mount the lower one. Occlusion for optimum esthetics. Balk J Dent Med, Vol 23, 2019 Treatment of Missing Lateral Incisors 47

Orthodontic phase impression (Figure 7). The use of 2-piece implant system allowed for proper abutment selection for optimum It lasted for about a year and a half. Distalization of esthetic results. Angled abutments were chosen to allow the canines bilaterally was performed till a space of 6 mm for correction of the axial inclination of the implants was created to accommodate a lateral incisor in harmony dictated by the available bone. They had titanium nitride with the patient’s dentition. coated collars. Impression was sent to the lab where a master cast with tissue mimic was obtained to construct the zirconium crowns (Figures 8 and 9). First, the lab sent zirconium cores for try-in. Then, they were built Surgical phase into full crowns. Abutments were screwed to the implant at a torque of 30 N/cm. Implant protected occlusion was A cone beam computed tomography (CBCT) was assured to allow for long term success. Crowns were performed to determine the available width and height of cemented temporally to allow any further adjustments. bone for proper implant size selection. Two-piece mini After crowns installation, the patient was completely dental implants were used as there was no enough bone satisfied with the results (Figures 10 and 11). width for regular implant placement. A size 3mm x 12mm was chosen to restore left lateral incisor and 3.3mm x 12 mm for the right one. After administration of local anesthesia with 2.2 ml of Mepivicaine (Scandonest 2%, Mepivacaine HCl, USP) as a labial and palatal infiltration, a crestal incision and sulcular one were made around the central incisor and the canine using Bard Parker blade no. 15 (Hu-Friedy Mfg. Co., LLC). This was followed by a full thickness flap elevation and reflection with a sharp mucoperiosteal elevator. The implant osteotomy was created using a reduction hand piece (1:16) at a speed of 1200 rpm with Figure 5. Mucosa healed around healing collars a physio-dispenser and adequate flow of sterile saline solution. The implant was initially placed manually then continued with a ratchet till the implant flushed with the bone surface. The flap edges were repositioned and sutured. Patient was instructed to apply cold fomentation for 12 h post-surgically, take an anti-inflammatory drug (Cataflam® Novartis Pharma, S.A.E. Cairo-under license from Novartis Pharma AG., Basle, Switzeland) 3 times for 2 days, as well as broad spectrum antibiotic for 5 days and to follow the usual oral hygiene measures in combination with Chlorhexidine mouth wash (Antiseptol mouth wash; Chlohexidine gluconate, Kahira Pharmaceuticals) three to four times daily for 2 weeks. The patient was recalled Figure 6. Impression transfers after one week to remove the sutures.

Prosthetic phase

Implants were allowed to osseointegrate for a period of 3 months. After that, they were exposed by a crestal incision and healing collars were installed. They were left in place for 2 weeks to allow for mucosal healing (Figure 5), after which closed tray coping transfers were attached to the implants and their proper seating was verified with periapical X-rays (Figure 6). An implant level impression was made. Impression transfers were attached to fixture analogues and re-inserted into their place in the Figure 7. Impression with the transfers attached to the analogues in place 48 Hend Mahmoud Mohamed Hegazi Balk J Dent Med, Vol 23, 2019

Figure 8. Poured cast with tissue mimic Figure 9. Angled abutments (with titanium nitride coated collars) on the cast

Figure 10. Occlusion after crowns insertion (delivery). (A) Right side, (B) Left side

malocclusion. Moreover, distalization of permanent canines to their proper positions might help in alveolar ridge development in the lateral incisor region. This also would enhance the final esthetic results rather than canine substitution for the lateral incisor. Besides, having the permanent canine in place would help to obtain a stable final occlusion7. The space required for maxillary lateral incisor is about 5-7 mm5. The space created orthodontic treatment was about 6 mm bilaterally, which was sufficient for restoring lateral incisors. Since she was an adult patient, there was no problem for implant placement because growth of the maxilla was completed. CBCT was performed to determine the needed implants’ dimensions. There was deficiency in the labio- palatal dimension. This was overcome by using mini- Figure 11. Extra-oral frontal view (post-delivery) implants, which contribute the avoidance of additional surgery. Mini-implants can be supplied either as single piece or two-piece. Although single piece implants have the advantage of strength and simple Discussion restorative procedures, they provide little flexibility in abutment angulation and customization to meet the The chosen treatment plan for this patient was esthetic requirements7. Implants were placed with axial to open the space where the patient had a molar class inclination labially to avoid labial fenestration, which I relationship and had no concomitant needs to treat was corrected later on using angled abutments8. The use Balk J Dent Med, Vol 23, 2019 Treatment of Missing Lateral Incisors 49 of two-piece implants allowed for the correction of the 4. Paduano S, Cioffi I, Rongo R, Cupo A, Bucci R, Valletta axial inclination with angulated abutment. The abutments R. Orthodontic Management of Congenitally Missing had a titanium nitride coated collar giving a gold hue Maxillary Lateral Incisors: A Case Report. Case Rep Dent, which allowed for optimal esthetics. Zirconium crowns 2014;2014:1-7. 5. Kinzer GA, Kokich Jr VO. Managing congenitally missing were made to restore the lateral incisors which enhanced lateral incisors. Part III: Single-tooth implants. J Esthet the final esthetic results. Implant protected occlusion is Restor Dent, 2005;17:202-210. important to avoid un-necessary forces falling on the 6. Shatkin TE, Shatkin S, Oppenheimer BD, Oppenheimer AJ. implants predicting a long-term success. Mini dental implants for long-term fixed and removable prosthetics: a retrospective analysis of 2514 implants placed over a five-year period. Compend Contin Educ Dent, 2007;28:92-99. Conclusions 7. Jackson BJ, Slavin MR. Treatment of Congenitally Missing Maxillary Lateral Incisors: An Interdisciplinary Approach. J Oral rehabilitation of patients with congenitally Oral Implantol, 2012;39:187-192. 8. Muhamad A, Nezar W, Azzaldeen A. Managing missing lateral incisors can be achieved with orthodontic congenitally missing lateral incisors with single tooth space opening combined with implant placement to implants. Dent Oral Craniofacial Res, 2016;2:318-324. support single crowns when other conditions permit. Mini-implants can be used successfully to over-come Conflict of Interests: Nothing to declair. problem of insufficient bone. Financial Disclosure Statement: Nothing to declair. Human Rights Statement: All the procedures on humans were conducted in accordance with the the Helsinki Declaration of 1975, as revised 2000, and with national ethical committee. Consent was obtained from the patient/s and approved for the current study by References national ethical committee. Animal Rights Statement: None reguired. 1. Kokich VO, Kinzer GA. Managing Congeniatally Missing Lateral Incisors. Part I: Canine Substitution. J Esthet Restor Received on December 3, 2017. Dent, 2005;17:5-10. Revised on Macrh 2, 2018. 2. Almeida RR de, Morandini ACF, Almeida-Pedrin RR Accepted on May 2, 2018. de, Almeida MR de, Castro RCFR, Insabralde NM. A multidisciplinary treatment of congenitally missing Correspondence: maxillary lateral incisors: a 14-year follow-up case report. J Hend Mahmoud Mohamed Hegazi Appl Oral Sci, 2014;22:465-471. Department of removable prosthodontics, Faculty of dentistry, Cairo 3. Kedia N, Valiathan A. Management of Congenitally Missing University, Egypt Lateral Incisor. J Indian Orthod Soc, 2011;45:93-97. e-mail: [email protected]

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Papillon-Lefévre Syndrome: Case Report and Genetic Analysis

SUMMARY Tugcenur Uzun, Orcun Toptas Backgroung/Aim: Papillon Lefévre syndrome is a rare autosomal Department of Oral and Maxillofacial Surgery, recessive genodermatosis. The characteristic findings of the disease are Faculty of Dentistry, Abant Izzet Baysal early loss of primary and permanent teeth and palmoplantar keratoderma. University, Bolu, Turkey Notwithstanding that many etiologic factors like genetic mutations, bacterial agents, immunologic changes have been identified, the pathogenesis has not been fully understood. Although dentists play an important role in the diagnosis and treatment of Papillon Lefévre syndrome, it is appropriate to treat the disease with a multidisciplinary approach. Case Report: In this case report, the clinical, radiological and genetic examination of the patient with Papillon Lefévre syndrome who has a homozygous mutation in the CTSC gene will be presented. Conclusions: Dentists should have knowledge about treatment management of these patients. Teeth can be preserved longer with early diagnosis and appropriate treatment of the disease. CASE REPORT (CR) Key words: Papillon Lefévre, Cathepsin C, Gene Mutation Balk J Dent Med, 2019;50-53

Introduction end up with foulodor6. The lesions may appear as patches or deep fissures with different colors and appearances. The syndrome was first described by Papillon and Eyelids, cheeks, knees and labial commissure might also be 7 Lefévre in 19241. The disease is characterized by diffuse involved . The patients report that their complaints increase 8 palmoplantar keratoderma and prematurely starting in cold weather . Horizontal growth and fissure formation affecting both dentitions. It has might be seen in nails in advanced cases. an autosomal recessive inheritance pattern. The patients Vertical bone loss in first molars is seen in localized have cathepsin C(CTSC) gene mutation2. The symptoms forms of PLS as radiographic findings, while this bone loss may include all teeth in the generalized form. that may accompany are hyperhydrosis, aracnodactilia, “Floating in air” image might develop in radiography intracranial calcification, tendency to infection and mental since bone support of the teeth is completely lost in very retardation3,4. The incidence of the disease has been advanced stages8. reported to be 1 to 4 in a million. The incidence is higher Some cases are reported to have microdonti, root in societies where consanguineous marriages are common. 5 eruption and deterioration in root formation although Girls and boys are affected equally by the disease . there is no change in the form and time of tooth eruption Cutaneous lesions usually begin to appear along of primary teeth10,11. Upon eruption of primary teeth, with oral findings between 6 months to 4 years of age. an inflammatory picture begins in gingiva. Gingiva is Cutaneous lesions have been considered to develop due to hyperemic and edematous. Flow of pus from periodontal 6 the disorders of ectodermal and mesodermal components . pockets is seen. After premature loss of primary teeth, Cutaneous lesions are seen in Papillon Lefevre syndrome gingiva returns to normal. The process repeats in since CTCS gene is expressed in epithelial tissues. conjunction with the eruption of permanent teeth. The Hyperkeratosis and erythema are present in palms and patients with Papillon Lefévre syndrome usually remain soles. Keratinization may spread to the dorsum of toothless at age of 14-15. Alveolar bone resorption is and feet. Hyperkeratotic plaques developed might be observed in radiographic assessment12. Wisdom teeth are associated with hyperhidrosis of the hands and feet and may usually not affected by the disease. Balk J Dent Med, Vol 23, 2019 Papillon-Lefévre Syndrome 51

Case Report Due to constant use of the same prosthesis during growth and development period and being toothless, there A 19-year-old male patient was referred to was inadequate development of jaws in horizontal and Department of Oral and Maxillofacial Surgery of vertical planes. The vertical dimension decreased and Dentistry Faculty, Abant Izzet Baysal University to the denture face appearance occurred in the patient. The be evaluated for implant indications before prosthetic success rate and cost of implant therapy were explained rehabilitation. In the clinical examination, palmoplantar and the patient was notified that additional surgical hyperkeratosis (Figure 1), loss of all teeth except wisdom procedures may be required. Renewal of the prosthesis teeth, maxillary and mandibular growth retardation was offered to the patient as the second treatment option. were observed. Mental functions of the patient were not The patient rejected implant therapy since it has high cost affected. In the radiographic examination, resorption in and is an invasive treatment and he wanted his prosthesis the alveolar crests was detected (Figure 2). Wisdom teeth to be renewed. were not affected by the disease. In the anamnesis of the patient, it was stated that he was informed by a physician that he had a genetic disorder but no detailed examination was performed. He reported that his teeth had been Discussion extracted due to loosening at the age of 12 and started using prosthesis. He has been using the same prosthesis Although the etiology of Papillon Lefévre syndrome for seven years. No family member was affected by the is not fully understood, the syndrome has been associated disease. There was no consanguinity between the parents with cathepsin C gene mutation, various microbial agents 14 of the patient. Hematologic examination revealed no and immunologic factors . anomalies. In the genetic analysis of the patient, it was Dipeptide peptidase 1, also known as cathepsin C, confirmed that he was carrying p.Gly139Arg (c.415 is a lysosomal cysteine protease and is encoded by the G>A) mutation which was found in exon 3 of CTSC gene cathepsin C gene which is located on the 11q14.1-q14.3 homozygously. It is known that the mutation in the patient chromosome. Seventy-five different mutations related 15 causes Papillon Lefévre syndrome13. The diagnosis to the CTSC gene have been described . Among became definite as a result of clinical, hematological and the mutations, 75% are homozygous and among the genetic studies. homozygous mutations, 50% are lost mutation, 25% are meaningless mutation, 23% are frameshift mutation and 2% are other type mutations16. Mutation of c.415 G>A, seen in this presented case was defined first by Zhang et al. as heterozygous in a PLS patient with Caucasian origin13. Cases carrying homozygous c.415 G>A mutation have also been reported17,18. CTSC, CTSG and elastase functions are almost completely lost in homozygous mutations17. Cathepsin C plays an important role in the activation of cytotoxic T lymphocytes, natural killer cells, mast cells and serine proteases in neutrophils19. It also functions in collagen type I, III, IV and fibronectin degradation20. In Papillon Lefévre syndrome, as a result of the inactivation Figure 1. Palmoplantar hyperkeratosis of serine proteases in inflammatory cells due to mutations in the CTCS gene, impairment occurs in the immune system14. The periodontal disease and the tendency to infection are caused by the impairment of neutrophil, T lymphocyte and B lymphocyte functions21,22. The first immune dysfunction developing in PLS is the impairment of the cytotoxic functions of natural killer cells8. Aggregatibacter Actinomycetemcomitans, Porphyromonas gingivalis, and Prevotella intermedia are the bacteria which are present in high numbers in periodontal pockets of the patients with Papillon Lefévre syndrome and therefore they are held responsible for the pathogenesis of the Figure 2. Radiographic view shows maxillary and mandibular alveolar disease23. High levels of immunoglobulin against crest resorption Aggregatibacter Actinomycetemcomitans have been 52 Tugcenur Uzun, Orcun Toptas Balk J Dent Med, Vol 23, 2019 observed in individuals affected by the disease8. In Conclusions Papillon Lefévre syndrome, there is a decrease in the neutrophil response to Staphylococcus spp. and Dentists should have knowledge about treatment 8 Aggregatibacter Actinomycetemcomitans . Herpes management of these patients. Teeth can be preserved viruses in addition to the pathogenic bacteria including longer with early diagnosis and appropriate treatment of Aggregatibacter Actinomycetemcomitans and also the disease. impairment of the host immune response are considered to play role in periodontitis developing in patients with Papillon Lefevre syndrome24. There is no specific histopathological finding References associated with Papillon Lefevre syndrome. Hyper­ keratosis, acanthosis, hypergranulosis or psoriasiform 1. Papillon MM, Lefevre P. Twocases of symmetrically 8 hyperplasia might be seen in gingival epithelium . Intense familial palmar and plantar hyperkeratosis (Meledadisease) inflammatory infiltration in patients with PLS is observed within brother and sister combined with severe dental in the subepithelial connective tissues of the periodontal alterations in both cases (in French). Bull Soc Fr Dermatol tissues. Dominant cells of this inflammation are the Syph, 1924;31:82-84 plasma cells25. 2. Wani AA, Devkar N, Patole MS, Shouche YS. Description Dental treatment of patients with Papillon Lefevre of two new cathepsin C gene mutations in patients with is challenging for both the patient and the dentist since Papillon-Lefèvre syndrome. J Periodontol, 2006;77:233- the prognosis is poor and outcome is unpredictable. The 237. main goal of the periodontal treatment in Papillon Lefévre 3. Hattab FN, Rawashdeh MA, Yassin OM, al-Momani AS, al-Ubosi M. Papillon-Lefèvre syndrome: a review of the syndrome is to optimize oral hygiene and keep the teeth literature and report of 4 cases. J Periodontol. 1995;66:413- in the mouth as long as possible. For this purpose, oral 420. hygiene education is given, scaling and root planning 4. Sollecito TP, Sullivan KE, Pinto A, Stewart J, Korostoff is performed and oral rinse with 0.2% chlorhexidine is J. Systemic conditions associated with periodontitis recommended. Antibiotics may be used in the presence of in childhood and adolescence. A review of diagnostic active periodontitis. The most commonly used antibiotics possibilities. Med Oral Patol Oral Cir Bucal, 2005;10:142- for this purpose are erythromycin and tetracycline. There 150. are also studies reporting that amoxicillin metronidazole 5. Verma KC, Chaddha MK, Joshi RK. Papillon-Lefevre or amoxicillin clavulanic acid combinations result syndrome. Int J Dermatol, 1979;18:146-149. in success26. Some investigators defend the idea 6. Kaur B. Papillon Lefevre Syndrome: A Case Report with that cleaning the oral cavity from pathogen bacteria Review. J Dent, 2013;3:156-159 and then the tooth eruption of the permanent teeth 7. Thakare KS. Genetic Mapping in Papillon Lefevre uninfluenced from the infection increases the duration Syndrome: A Report of Two Cases. Case Rep Dentistry, 2013;Article ID 404120 of permanent teeth stay in mouth8,27. For the treatment 8. Sreeramulu B, Shyam ND, Ajay P, Suman P. Papillon- of cutaneous lesions, retinoids, salicylic acid and steroid Lefèvre syndrome: clinical presentation and management are applied. Use of retinoid was reported to increase options. J Clin Cosmet Investig Dent, 2015;7:75-81. alveolar bone height and periodontal attachment level, 9. Subramaniam P, Mathew S, Gupta K. Papillon Lefevre reduce periodontitis formation and improve cutaneous Syndrome: A Case Report. Indıan Soc Pedod Prev Dent J, 28-30 lesions . 2008;26:171-174. There are studies reporting that the use of dental 10. Baghdadi VS. Papillon-Lefévre syndrome: report of four implants result in success for prosthetic rehabilitation cases. ASDC J Dent Child, 1982;49:147-150. of PLS patients31,32. Senel et al. followed a PLS patient, 11. Fahmy MS. Papillon-Lefévre syndrome: Report of four case to whom they applied implant therapy, for 3 years and in two families with a strongtie of consanguinity. A clinical, reported successful results32. radiographic, heamatological and genetic study. J Oral Med, The role of the dentist is very important in the 1987;42:263-268. diagnosis and treatment of PLS. Duration of stay of 12. Dhanrajani PJ. Papillon-Léfevre syndrome: clinical presentation and a brief review . Oral Surg Oral Med Oral the teeth in mouth can be prolonged when the disease is Pathol Radiol Endod, 2009;108:1-7 treated appropriately. This situation is important for the 13. Zhang Y, Hart PS, Moretti AJ, Bouwsma OJ, Fisher preservation of maxillary and mandibular bone height. EM, Dudlicek L et al. Biochemical and mutational analyses Unfortunately, it was late for these treatment options of cathepsin C gene (CTSC) in three North American when the patient was admitted to us. The most appropriate families with Papillon Léfevre syndrome. Hum Mutat, treatment options were presented to the patient and the 2002;20:75. decision was left to him. He was informed about his 14. Dalgic B, Bukulmez A, Sari S. Eponym: Papillon-Léfevre disease and possible complications were explained. syndrome. Eur J Pediatr, 2011;170:689-691. Balk J Dent Med, Vol 23, 2019 Papillon-Lefévre Syndrome 53

15. Nagy N, Valyi P, Csoma Z, Sulak A, Tripolszki K, Farkas 27. Weibe C, Hakkinen L. Succesful periodontal maintenance of K et al. CTSC and Papillon–Lefevre syndrome: detection a case with Papillon-Lefevre syndrome: 12-Year follow-up of recurrent mutations in Hungarian patients, a review and review of literature. J Periodontol, 2001;72:824-830. of published variants and database update. Mol. Genet. 28. Gelmetti C, Nazzaro V, Cerri D, Fracasso L. Long- Genomic Med, 2014;2:217-228. termpreservation of permanent teeth in a patient with 16. Hamon Y. Analysis of Urinary Cathepsin C for Diagnosis Papillon-Lefèvre syndrome treated with etretinate. J Pediatr Papillon Lefevre Syndrome. Febs J, 2016;283:498-509. Dermatol, 1989;6:222-225. 17. Çağlı NA. Clinical, Genetic and biochemical findings in 29. Lee MR, Wong LC, Fischer GO. Papillon-Lefèvre syndrome two siblings with Papillon Lefevre Syndrome. J Periodontol, treated with acitretin. Australas J Dermatol, 2005;46:199- 2005;76:2322-2329. 201. 18. Tekin B. Papillon Lefevre syndrome: report of six patients 30. Sarma N, Ghosh C, Kar S, Bazmi BA. Low-dose acitretin in and identification of novel mutation. Int J Dermetol, Papillon-Lefèvre syndrome: treatment and 1-year follow-up. 2016;55:898-902. J Dermatol Ther, 2015;28:28-31. 19. Turk D, Janjic V, Stern I, Podobnik M, Lamba D, Dahl SW 31. Al Farraj, Al Dosari A. Oral rehabilitation of a case of et al. Structure of human dipeptidylpeptidase I (cathepsin Papillon-Lefevre syndrome with dental implants. Saudi Med C): exclusion domain added to an endopeptidase framework J, 2013;34:424-427. creates the machine for activation of granular serine 32. Senel FC, Altintas NY, Bagis B, Cankaya M, Pampu AA, proteases. Embo J, 2001;20:6570-6582. Satiroglu I et al. A 3-year follow-up of the rehabilitation 20. Schwartz LB. Tryptase, a mediator of human mastcells. J of Papillon-Lefèvre syndrome by dental implants. J Oral Allergy Clin Immunol, 1990;86:594-598. Maxillofac Surg, 2012;70:163-167. 21. Ryu OH, Choi SJ, Firatli E. Proteolysis of macrophage inflammatory protein-1 alpha isoforms LD78beta and Conflict of Interests: Nothing to declair. LD78alfa by neutrophil-derived serine proteas. J Biol Chem, Financial Disclosure Statement: Nothing to declair. 2005;280:17415-17421. Human Rights Statement: All the procedures on humans were 22. Liu R, Cao C, Meng H, Tang Z. Leukocyte functions in 2 conducted in accordance with the the Helsinki Declaration of 1975, cases of Papillon-Lefèvre syndrome. J Clin Periodontol, as revised 2000, and with national ethical committee. Consent was 2000;27:69-73. obtained from the patient/s and approved for the current study by 23. Albandar JM, Khattab R, Monem F, Barbuto SM, Paster BJ. national ethical committee. The subgingival microbiata of Papillon Léfevre syndrome. J Animal Rights Statement: None reguired. Periodontol, 2012;83:902-908. 24. Ishikawa I, Umeda M, Laosrisin N. Clinical, bacteriological Received on January 3, 2018. and immunological examinations and the treatment process Revised on March 8, 2018. of two Papillon Lefevre syndrome patients. J Periodontol, Accepted on April 20, 2018. 1994;65:364-371. 25. Drahanjani P. Papillon Lefevre syndrome: clinical Correspondence: presentation and a brief review. Oral Surg Oral Med Oral Tugcenur Uzun Path Oral Radiol, 2009;108:1-7. Department of Oral and Maxillofacial 26. Kellum RE. Papillon-Lefèvre syndrome in four siblings Faculty of Dentistry treated with etretinate. A nine-year evaluation. Int J Abant Izzet Baysal University, Bolu, Turkey Dermatol, 1989;28:605-608. e-mail: [email protected]

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Tri puta godišnje. - Je nastavak: Balkan Journal of Stomatology = ISSN 1107-1141 ISSN 2335-0245 = Balkan Journal of Dental Medicine COBISS.SR-ID 206352140