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Management of Furcation-Involved Molars: Recommendation for Treatment and Regeneration

Giulio Rasperini, DDS1/Jad Majzoub, BDS2 Periodontitis is a multifactorial Lorenzo Tavelli, DDS, MS2/Enrico Limiroli, DDS1 chronic disease that affects ap- Akihiko Katayama, DDS, PhD3/Shayan Barootchi, DMD2 proximately 42% of the adults in the Roger Hill, DDS, MS2/Hom-Lay Wang, DDS, MS, PhD2 United States.1 Its progression and detrimental results on periodontal tissues have been extensively evalu- Furcation involvement (FI) is one of the most detrimental factors affecting ated.2 When this condition affects tooth survival rate over time. Several authors have used the severity of FI multi-rooted teeth exposing the fur- for assessing the prognosis of the tooth and the complexity of periodontal cation area, the treatment poses ad- disease. While many approaches have been shown to improve the prognosis ditional challenges for the clinician. of furcation-involved teeth, clinical guidelines recommending one treatment or another (based on the horizontal and vertical component of the furcation This is because the unfavorable mor- defects) have not yet been proposed. To this aim, the present article phology and restricted-access area introduces recommendations for the treatment of molars with FI and discusses that characterize furcation defects different treatment options with their potential regenerative approaches. limit not only the efficacy of nonsur- Patient-related factors, together with hard and soft-tissue conditions that gical and surgical therapies but also may affect the outcomes of periodontal regeneration, are discussed. Int J the patient’s self-performed plaque Periodontics Restorative Dent 2020;40:e137–e146. doi: 10.11607/prd.4341 control.3 Due to these limitations, the progression of the disease in the furcation area exhibits horizontal and/or vertical patterns of destruc- tion that may lead to an increased risk for tooth loss.4,5 Therefore, it is not surprising that the severity of furcation involvement (FI) has been used for assessing the prognosis of the tooth6 and the complexity of .7 In a recent meta-analysis, Nibali et al showed

1Department of Biomedical, Surgical and Dental Sciences, University of Milan, that the presence of FI increases the Foundation IRCCS Ca’ Granda Polyclinic, Milan, Italy. risk of tooth loss in molars by two- 2Department of Periodontics & Oral Medicine, University of Michigan School of , fold when maintained in supportive Ann Arbor, Michigan, USA. periodontal therapy (SPT).8 3Department of , Tokyo Dental College, Tokyo, Japan. Several surgical approaches Correspondence to: Dr Giulio Rasperini, Department of Biomedical, have been proposed for the treat- Surgical and Dental Sciences, Foundation IRCCS Ca’ Granda Polyclinic, ment of molars with FI, including Via della Commenda 12, 20122 Milan, Italy. Email: [email protected] guided tissue regeneration (GTR), bicuspidization, tunneling proce- Submitted February 15, 2019; accepted June 17, 2019. ©2020 by Quintessence Publishing Co Inc. dure, and root amputation. Car-

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Table 1 Classifications of Horizontal and erticalV Furcation Defects That Were Used in the Present Article

Horizontal component of the furcation defect13 Vertical component of the furcation defect15 A B C 1 Horizontal loss of periodontal Horizontal loss of periodontal Horizontal loss of periodontal support < 3 mm of the support < 3 mm of the support < 3 mm of the width of the tooth with width of the tooth with width of the tooth with vertical attachment/bone loss vertical attachment/bone loss vertical attachment/bone loss extending to the coronal extending to the middle extending to the apical third of the root. third of the root. third of the root. 2 Horizontal loss of periodontal Horizontal loss of periodontal Horizontal loss of periodontal support ≥ 3 mm of the support ≥ 3 mm of the support ≥ 3 mm of the width of the tooth, but not width of the tooth, but not width of the tooth, but not “through and through,” “through and through,” “through and through,” with vertical attachment/ with vertical attachment/ with vertical attachment/ bone loss extending to the bone loss extending to the bone loss extending to the coronal third of the root. middle third of the root. apical third of the root. 3 Horizontal “through and Horizontal “through and Horizontal “through and through” destruction of the through” destruction of the through” destruction of the periodontal attachment with periodontal attachment with periodontal attachment with vertical attachment/bone loss vertical attachment/bone loss vertical attachment/bone loss extending to the coronal extending to the middle extending to the apical third of the root. third of the root. third of the root. When presenting their clinical recommendation, the present authors combined the horizontal and the vertical components for describing the furcation defects (eg, A1, B3, C2).

nevale et al reported a 93% survival mending one treatment or another (until January 2019) was performed rate for molars with FI following root- have mostly been based upon the across the National Library of resective therapy,9 while Bowers horizontal extension of the furca- Medicine (MEDLINE by PubMed), et al achieved complete furcation tion defect and the morphology of EMBASE, the Cochrane Library, and closure in 74% of mandibular molar the tooth12 alone, while guidelines the Grey Literature, using the fol- sites with facial Class II furcations, based on the vertical component lowing keywords: “furcation involve- reporting that 68% of furcation de- of the defect and the surrounding ment,” “furcation defects,” and fects were reduced to Class I. These soft tissue components have not “guided tissue regeneration.” In results demonstrated the positive yet been proposed. Therefore, the addition, a manual search of related effect of GTR and bone graft in aim of this article is to propose rec- articles, including complete search- furcation-involved molars.10 In line ommendations for the treatment of es of The International Journal of with these results, the American molars with FI and discuss different Periodontics & Restorative Dentistry, Academy of Periodontology (AAP) treatment options with their poten- Journal of Clinical Periodontology, Regeneration Workshop on furca- tial regenerative approaches. and Journal of Periodontology were tion defects concluded that regen- performed. A decision tree for fur- eration is a viable treatment option cation management and regenera- for molars with Class II FI and that Materials and Methods tion was formulated, mainly aimed this approach should be consid- at treating the buccal furcations of ered before performing resec- To support the proposal of treat- maxillary or mandibular molars, as tive therapy or other treatments.11 ment and regeneration in FI molars, they show the most realistic and However, clinical guidelines recom- a review of all available literature promising treatment outcomes.11

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Fig 1 Decision tree for the management of a furcation-involved molar. Please see Table 1 for explanation of furcation defect classifica- tions. NSPT = nonsurgical periodontal therapy; OFD = open-flap .

Management of Furcation- tal13 or vertical attachment loss,14,15 considered the combination of the Involved Molars several classifications for furcation horizontal (grades 1, 2, and 3)13 and involvement have been proposed. vertical (subclasses A, B, and C)14,15 Based upon the evidence available While FI has been often classi- furcation components in this newly in the literature and the clinical expe- fied based on the horizontal attach- formulated decision tree (Table 1 and rience of the authors, the following ment loss, a 10-year retrospective Fig 1). The goal for treatment of FI is factors were considered for formu- study by Tonetti et al recently dem- to clean the furcation and to facilitate lating the presented decision tree: (1) onstrated that the residual periodon- patients’ .13 Bearing in furcation defects considering both tal attachment, evaluated as the loss mind that nonsurgical periodontal horizontal and vertical attachment of vertical component, is a reliable therapy (NSPT) constantly presents loss; (2) level of the interproximal predictor of survival of molars with the first step following the diagnosis bone; (3) accessibility of the area for Class II horizontal FI.15 Nibali et al of a furcation defect, the diagnosis patient oral hygiene; (4) residual at- showed that after surgical treatment of FI has to be confirmed after at tachment of the roots; and (5) tooth and SPT for at least 5 years, both the least 6 weeks following NSPT. In- anatomy (eg, root trunk length, root horizontal and vertical FI were associ- deed, a correct diagnosis is vital for length, divergence of the roots). ated with an increased risk for tooth establishing an adequate treatment Based on the severity of the horizon- loss.16 Therefore, the present authors plan.17 If the area is accessible for oral

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a b c

d e f

g h i

j k l Fig 2 (a) A 65-year-old woman presented with deep probing depths mesial to the maxillary left first premolar and first molar with Class III furcation involvement of the mesiopalatal furcation of the first molar. (b) A periapical radiograph was taken following endodontic treatment of the palatal and distal roots and extraction of the mesial root of the first molar. (c to h) Osseoresective surgery was performed around the first molar with simultaneous connective tissue graft at the buccal aspect of the first molar to mimic the presence of the mesial root. (i and j) Healing following osseous resective surgery and soft tissue augmentation with the cemented crown on the first molar. (k and l) Radiographic view 7 years later.

leading clinicians to consider peri- As recommended by the 2015 dure should be attempted for fur- odontal regeneration as the treat- AAP Regeneration Workshop,11 a cation types A2, B1, and B2 when ment of choice when indicated.21 periodontal regeneration proce- the interproximal bone is coronal to

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Fig 3 A Class B2 furcation defect was treated with a regenerative approach, including bone graft, connective tissue graft (CTG), and fibroblast growth factor (FGF-2). (a) Baseline periapical radiograph. (b) A full-thickness flap was raised and the defect degranulated. (c) Xenogeneic bone graft mixed with FGF-2 was applied in the furcation defect, and CTG harvested from the palate was sutured over it. (d) Clinical and (e) radiograph views 7 months later. Note the increased soft tissue thickness.

a b c

d e

Discussion tal component of the defect and of furcation defects based on sys- their related vertical components, temic and local anatomical condi- This paper aimed to provide clini- Tonetti et al has shown it is pos- tions.12 Later on, several studies cal recommendations for the man- sible to achieve long-term success focused on the importance of the agement of molars with FI, as the with active periodontal treatment vertical aspect of furcation defects authors are aware that the involve- and regular SPT.15 Using a statistical and tooth survival.15,16 Therefore, the ment of the furcation area creates model, Schwendicke et al showed present authors’ decision tree was additional difficulties for the pre- that retaining molars was more cost- based on previous literature as well dictable treatment of periodontal effective than replacing them with as the clinical experience of the au- disease.5 It is not surprising to find dental implants.29 Therefore, provid- thors. Thus, it is important to note that the lower survival rate in molars ing a rationale for the treatment of that case selection, patient behavior with FI is due to the anatomy of the molars with furcation involvement in and compliance, tooth morphology, defect and the challenge it creates different scenarios is fundamental. and the characteristics of hard tis- for optimal plaque control.10 By con- Aichelmann-Reidy et al proposed sues (bone levels and root morphol- sidering the extent of the horizon- a decision tree for the treatment ogy) and soft tissues (eg, amount of

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Fig 4 A Class B2 furcation defect was treated with bone graft and amelogenins. (a) Baseline radiograph. (b) A melogenins were applied after degranulation of the defect, scaling and root planing, and root conditioning with ethylenediaminetetraacetic acid. (c) Following amelogenins application, xenogeneic bone graft (mixed with amelogenins) was also applied on the furcation defect and sutured. (d) Clinical and (e) radiographic results at 6 months.

a

b c

d e

keratinized gingiva, tissue pheno- to be mentioned that the described Conclusions type, vestibular depth) are all factors recommendations for management that should be carefully examined of furcation defects are based upon The present article provides clinical before choosing the proper treat- the clinical experience of the au- guidelines for treating furcation de- ment approach.5,30 Within the limi- thors and therefore may need to be fects based on the literature and the tations of the present article, it has confirmed in further clinical studies. authors’ clinical expertise. In par-

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Fig 5 Decision tree for the regeneration of furcation defects. FMPS = full-mouth plaque score; FMBS = full-mouth bleeding score; CEP = cervical enamel projection; RT = recession type; CTG = connective tissue graft; FGG = free gingival graft; GTR = guided tissue regeneration; ADM = acellular dermal matrix; CM = collagen membrane.

ticular, favorable and unfavorable References 3 . Chiu BM, Zee KY, Corbet EF, Holmgren conditions for periodontal regen- CJ. Periodontal implications of furca- tion entrance dimensions in Chinese eration were discussed, including . 1 Eke PI, Thornton-Evans GO, Wei L, first permanent molars. J Periodontol the importance of patient selection, Borgnakke WS, Dye BA, Genco RJ. 1991;62:308 –311. Periodontitis in US adults: National 4. Müller HP, Eger T, Lange DE. Manage- defect morphology, and the soft tis- health and nutrition examination survey ment of furcation-involved teeth. A ret- sue component. 2009–2014. J Am Dent Assoc 2018;149: rospective analysis. J Clin Periodontol 576–588. 1995;22:911–917. 2. Tonetti MS, Eickholz P, Loos BG, et al. 5. Dannewitz B, Zeidler A, Hüsing J, et al. Principles in prevention of periodontal Loss of molars in periodontally treated Acknowledgments diseases: Consensus report of Group 1 patients: Results 10 years and more af- of the 11th European Workshop on Peri- ter active periodontal therapy. J Clin odontology on effective prevention of Periodontol 2016;43:53–62. This paper was partially supported by the periodontal and peri-implant diseases. 6. McGuire MK, Nunn ME. Prognosis ver- University of Michigan Periodontal Graduate J Clin Periodontol 2015;42(suppl 16): sus actual outcome. II. The effectiveness s5 –s11. of clinical parameters in developing Student Research Fund. The authors declare an accurate prognosis. J Periodontol no conflicts of interest. 1996;67:658–665.

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. 7 Tonetti MS, Greenwell H, Kornman KS. 16. Nibali L, Sun C, Akcalı A, Yeh YC, Tu YK, 25. Meyle J, Gonzales JR, Bödeker RH, Staging and grading of periodontitis: Donos N. The effect of horizontal and et al. A randomized clinical trial com- Framework and proposal of a new clas- vertical furcation involvement on molar paring and sification and case definition. J Peri- survival: A retrospective study. J Clin membrane treatment of buccal class odontol 2018;89(suppl 1):s159–s172. Periodontol 2018;45:373–381. II furcation involvement in mandibular 8. Nibali L, Zavattini A, Nagata K, et al. 17. Pilloni A, Rojas MA. Furcation involve- molars. Part II: Secondary outcomes. Tooth loss in molars with and without ment classification: A comprehensive J Periodontol 2004;75:1188 –1195. furcation involvement—A systematic re- review and a new system proposal. Dent 26. Momose T, Miyaji H, Kato A, et al. Col- view and meta-analysis. J Clin Periodon- J (Basel) 2018;6. pii: E34. lagen hydrogel scaffold and fibroblast tol 2016;43:156–166. 18. Al-Shammari KF, Kazor CE, Wang HL. growth factor-2 accelerate periodontal 9. Carnevale G, Pontoriero R, di Febo G. Molar root anatomy and management healing of class II furcation defects in Long-term effects of root-resective of furcation defects. J Clin Periodontol dog. Open Dent J 2016;10:347–359. therapy in furcation-involved molars. A 2001;28:730 –740. 27. Anderegg CR, Metzler DG, Nicoll BK. 10-year longitudinal study. J Clin Peri- 19. Fugazzotto PA. A comparison of the Gingiva thickness in guided tissue re- odontol 1998;25:209–214. success of root resected molars and generation and associated recession at 10. Bowers GM, Schallhorn RG, McClain molar position implants in function in a facial furcation defects. J Periodontol PK, Morrison GM, Morgan R, Reynolds private practice: Results of up to 15-plus 1995;66:397–402. MA. Factors influencing the outcome years. J Periodontol 2001;72:1113–1123. 28. de Andrade PF, de Souza SL, de Oliveira of regenerative therapy in mandibular 20. Kwok V, Caton JG. Commentary: Prog- Macedo G, et al. Acellular dermal ma- Class II furcations: Part I. J Periodontol nosis revisited: A system for assigning trix as a membrane for guided tissue 2003;74:1255–1268. periodontal prognosis. J Periodontol regeneration in the treatment of Class 11. Reddy MS, Aichelmann-Reidy ME, 2007;78:2063–2071. II furcation lesions: A histometric and Avila-Ortiz G, et al. Periodontal re- 21. Cortellini P, Buti J, Pini Prato G, Tonetti clinical study in dogs. J Periodontol generation—Furcation defects: A MS. Periodontal regeneration com- 2007;78:1288–1299. consensus report from the AAP Regen- pared with access flap surgery in human 29. Schwendicke F, Graetz C, Stolpe M, eration Workshop. J Periodontol 2015; intra-bony defects 20-year follow-up of Dörfer CE. Retaining or replacing 86(suppl 2):s131–s133. a randomized clinical trial: Tooth reten- molars with furcation involvement: A 12. Aichelmann-Reidy ME, Avila-Ortiz G, tion, periodontitis recurrence and costs. cost-effectiveness comparison of dif- Klokkevold PR, et al. Periodontal regen- J Clin Periodontol 2017;44:58–66. ferent strategies. J Clin Periodontol eration—Furcation defects: Practical 22. Cortellini P, Pini-Prato G, Tonetti M. Peri- 2014;41:1090–1097. applications from the AAP Regenera- odontal regeneration of human infrabo- 30. Trombelli L, Simonelli A, Minenna L, tion Workshop. Clin Adv Periodontics ny defects (V). Effect of oral hygiene on Rasperini G, Farina R. Effect of a con- 2015;5:30 –39. long-term stability. J Clin Periodontol nective tissue graft in combination with 13. Hamp SE, Nyman S, Lindhe J. Periodon- 1994;21:606 – 610. a single flap approach in the regenera- tal treatment of multirooted teeth. Re- 23. Zucchelli G, Tavelli L, McGuire MK, et al. tive treatment of intraosseous defects. sults after 5 years. J Clin Periodontol Autogenous soft tissue grafting for peri- J Periodontol 2017;88:348–356. 1975;2:126–135. odontal and peri-implant plastic surgi- 14. Tarnow D, Fletcher P. Classification of cal reconstruction. J Periodontol 2020; the vertical component of furcation 91:9–16. involvement. J Periodontol 1984;55: 24. Tavelli L, McGuire MK, Zucchelli G, et 283–284. al. Extracellular matrix-based scaffold 15. Tonetti MS, Christiansen AL, Cortellini technologies for periodontal and peri- P. Vertical subclassification predicts implant soft tissue regeneration J Peri- survival of molars with class II furcation odontol 2020;91:17–25. involvement during supportive peri- odontal care. J Clin Periodontol 2017; 44:1140 –1144.

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