The International Journal of Periodontics & Restorative Dentistry

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Peri-Implant Mucosal Creeping: Two Case Reports

Carlos Parra, DDS1 Periodontal plastic surgery is de- Diego Capri, DDS2 fined as any surgical procedure performed to correct or eliminate anatomical, developmental, or trau- matic deformities of the gingiva or alveolar mucosa.1 An adequate band While creeping attachment in natural teeth has been reported in the literature for of keratinized tissue around teeth tra- decades, the same phenomenon around dental implants is a new concept. This ditionally has been advocated.2 Nev- article describes two implant cases treated with free gingival autograft with follow- ertheless, when good is up at 18 and 30 months. Progressive coronal creeping of the mucosal margin was performed and inflammation is con- observed covering the implant and abutment surfaces postoperatively. This report demonstrates that mucosal creeping around implants may occur after peri-implant trolled, a very narrow or absent band plastic surgical procedures, further improving the final outcomes of therapy. of attached gingiva is still compatible Int J Periodontics Restorative Dent 2018;38:227–233. doi: 10.11607/prd.3013 with gingival health and no progres- sion of soft tissue recession.3–6 In cases of subgingival restora- tions, an adequate band of keratin- ized gingiva was found to be a factor in preventing inflammation and re- cession.7,8 In the field of implantol- ogy, the need for keratinized mucosa is controversial. While two systematic reviews have concluded that there is currently not enough evidence to determine whether an increase in ke- ratinized mucosa is beneficial for the patient,9,10 the most recent systematic reviews on the topic concluded that the absence of an adequate zone of keratinized mucosa is associated with more plaque accumulation, tis- 1Clinical Assistant Professor, Department of Periodontics, Texas A&M University College sue inflammation, mucosal recession, of Dentistry, Dallas, Texas, USA; Former Postgraduate Resident, Department of and attachment loss.11 Moreover, the , Tufts University School of Dental Medicine, Boston, Massachusetts, USA. 2Private Practice, Periodontics and Dental Implants, Bologna, Italy. presence of an adequate band of ke- ratinized mucosa has been shown to Correspondence to: Dr Carlos Parra, Texas A&M University College of Dentistry, be related to peri-implant health.12 Department of Periodontics, 3302 Gaston Avenue, Dallas, TX 75246, USA. The main indications for the treat- Fax: 214-874-4563. Email: [email protected] ment of mucosal recession around ©2018 by Quintessence Publishing Co Inc. implants are similar to the indications

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© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. 228 for treatment around teeth, with the cases where peri-implant plastic sur- Presurgical Phase obvious exclusions of tooth sensitiv- gery was performed, enhancing the Oral hygiene instructions were given ity and risk of caries. Therefore, sur- quality and quantity and improving and full-mouth was gical treatment of recession around the esthetics of the soft tissues sur- performed. After reevaluation, no implants may be performed for es- rounding the implants. It confirms the clinical improvements were noted thetic reasons, to prevent further findings of Pereira-Neto et al24 and on that tooth. A free soft tissue au- recession, for cleansability of the re- adds further speculation to the bio- tograft was recommended with the construction, to establish and main- logic hypothesis regarding coro- primary goals of improving the quan- tain biologic health, and to create or nal creeping of keratinized mucosa tity and quality of peri-implant soft augment keratinized tissue.13–15 around implants. tissues and possibly achieving partial Peri-implant plastic surgery fo- peri-implant recession coverage. cuses on harmonizing peri-implant structures by means of hard and soft Case Reports Surgical Phase tissue engineering and includes en- Two carpules of 2% lidocaine hancement of bone structure and Case 1 (Xylocaine) with 1:100,000 epineph- soft tissue.16 Peri-implant plastic rine were given as maxillary left surgery also aims to create a peri- A 46-year-old man with noncontribu- buccal infiltrations and maxillary left implant keratinized mucosa and in- tory medical history was referred by greater palatine block. Bone sound- terimplant soft tissue height. his general to assess the peri- ing was performed to identify the Creeping attachment is defined implant mucosal recession and lack of subjacent bony architecture. as postoperative migration of the keratinized mucosa of the dental im- At the recipient site, a partial- in a coronal direc- plant in the position of the maxillary thickness flap preserving the un- tion over portions of a previously left first molar (Fig 1a). The patient’s derlying periosteum was performed denuded root.17 It occurs during the chief complaint was purely esthetic as described by Miller29 with two second month,18 continues for 12 due to exposure of the metal collar oblique incisions, one mesial and months after surgery, and seems not of the implant. On clinical examina- another distal, 3 mm long on the im- to follow a constant progression pat- tion, the implant presented probing plant at the site of the maxillary left tern.19,20 Nevertheless, reports have depths of 2 to 5 mm with bleeding on first molar, extending 9 mm apically. shown that creeping attachment probing, 3 mm of mucosal recession, A 6-mm bony dehiscence on the may continue to progress beyond lack of keratinized tissue, a high frenal buccal side was observed (Fig 1c). the first postoperative year.21–24 pull, and scarring from a previously At the donor site, a second Various amounts of creeping at- failed free soft tissue autograft. surgical site was created on the tu- tachment in natural teeth have been The radiographic examination berosity area. A 20 × 8-mm epithe- reported in the literature, with an av- using bitewings and periapical ra- lialized free gingival autograft of 1.5 erage ranging from 0.36 to 0.89 mm, diographs showed slight bone loss to 2 mm thick was harvested using in follow-up periods from 1 to 27 on the mesial side and up to 30% a Bard-Parker #15 blade. The donor years.18–20,22,23,25–28 Although one re- bone loss on the distal side of the wound was sutured with Vicryl 5-0 port described the coronal migra- implant (Fig 1b). (Ethicon, Johnson & Johnson) as a tion of the mucosal margin around The implant (3i Certain, 6 mm continuous suture. A periodontal implants, no measurements were diameter × 10 mm length) had been dressing (Coe-Pak, GC) was applied. mentioned other than the number of placed 9 years earlier. A free gingi- The epithelialized free gingival implant threads covered.24 val autograft was also attempted at autograft was trimmed and adapted The present case report de- that time, with suboptimal results. A over the recipient bed, covering the scribes the coronal migration of the screw-retained porcelain-fused-to- implant dehiscence. Monocryl 5-0 peri-implant mucosal margin in two metal restoration was delivered. (Ethicon, Johnson & Johnson) was

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a b Postoperative Care The patient was given 600 mg of ibuprofen (Advil, Pfizer) following the surgery and was instructed to take it every 8 hours for the first 2 days, and then as needed. The pa- tient was also instructed to rinse twice a day for 30 seconds with c d 0.12% (Peridex, 3M ESPE) starting 24 hours after the sur- gery for 14 days.

Follow-up At the 1-week follow-up, the peri- odontal dressing was gently removed, and the wound was deli- e f cately debrided with gauze soaked in Peridex. The palatal donor sutures were removed. A residual recession of 3 mm was present. At 14 days, the wound was again debrided with a gauze soaked in Peridex and the remaining sutures on the recipient area were removed. g h Recession was still present, although Fig 1 Case 1. (a) Baseline clinical photograph showing a lack of keratinized tissue, peri- it was narrower in a mesiodistal di- implant mucosal recession, and frenal pull. (b) Periapical radiograph showing mesial and mension (Fig 1e). distal implant bone levels. (c) Bed preparation. Note the implant bony dehiscence, partially A localized supragingival de- covered by the periosteum. The frenum has been dissected. (d) Graft sutured to ensure passive adaptation on the recipient bed. Note the tuberosity at the donor site. (e) Clinical bridement was performed every 2 view at 2 weeks postoperative. Note residual recession of 2.5 mm. (f) At 6 weeks postop- weeks for the first month and ev- erative, recession was reduced but still present. (g) At 3 months postoperative, recession was reduced and the implant collar was partially covered. (h) At 18 months postoperative, ery 2 months for the subsequent 6 complete implant coverage was achieved. months using an ultrasonic scaler with a plastic-coated insert (SoftTip, Denstply) and finishing with a rub- ber cup (Dentsply) on a low-speed The postoperative plaque a roll technique in a coronal direc- handpiece. After that, regular full- control regimen recommended tion, twice daily starting 14 days af- mouth debridements were per- to the patient was to use an extra ter surgery, and switching to a soft formed every 6 months. soft very gently, using toothbrush with the same technique

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© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. 230 at 1 month after the surgery. Floss- After removal of the screw- A mucosal flap was designed ing was resumed at 1 month post- retained prosthesis, the implant buccal to the involved implant with operative. presented no mobility and was a 15C Bard-Parker blade (Aspen After the first month, the peri- considered to be osseointegrat- Surgical) to create a wide periosteal implant soft tissues displaced in a ed. However, a diagnosis of peri- recipient site. The surgical approach coronal direction throughout the implantitis could be formulated due was similar to that described in the follow-up period until complete to the combined presence of mild previous case29; two oblique inci- implant/abutment coverage was inflammation and bone loss. sions were drawn mesial and distal achieved at 18 months postopera- to the implant, being careful to in- tively (Figs 1f to 1h). The final height Presurgical Phase cise the existing keratinized mucosa of the keratinized mucosa on the im- The mandibular prosthesis was tem- with a 90-degree angle. Two verti- plant was 6 mm. porarily removed for an easier ac- cal incisions were dropped from cess to the supporting implants. The the end of the two oblique ones, five implants were carefully cleaned extending beyond the mucogingival Case 2 with Hawe carbon fiber–reinforced line. The partial-thickness flap was plastic instruments (Kerr) and 3% hy- then shortened with surgical scis- A 66-year-old woman with no aller- drogen peroxide under local anes- sors and the remaining apical por- gies and a history of a single mild thesia with 2% Xylocaine (Dentsply). tion of it was sutured down to the transient ischemic attack presented The patient was given proper oral periostium with 4-0 chromic gut su- for a first consultation. hygiene instructions. To further ad- ture (Ethicon, Johnson & Johnson). She did not smoke and was tak- dress the inflammatory condition of A 3.3-mm osseous dehiscence was ing 80 mg aspirin daily. During the the implant at the site of the man- visible, revealing three exposed im- clinical exam, her chief complaint dibular left central incisor, the de- plant threads now surrounded by a was related to her inability to prop- bridement was performed with the wide recipient periosteal bed. The erly clean one of five mandibular im- goal of reaching the bottom of the exposed implant surface was care- plants, placed 5 years earlier, due to peri-implant sulcus and local met- fully debrided using carbon fiber– discomfort on brushing. Her maxilla ronidazole 25% gel (Colgate) was reinforced plastic curettes (Kerr), was edentulous and had been re- injected into the sulcus. and a cotton pellet soaked in 3% stored with a removable denture. At reevaluation, the peri-implant was repeat- The clinical evaluation revealed probing depth ranged from 2 to edly swept against the previously that the implant in the position of 4 mm with no . cleaned machined titanium surface the mandibular left central incisor, A mild accumulation of microbial (Fig 2b). immediately placed at the time of plaque was still detected on the im- At the donor site, a 12 × 7-mm tooth extraction, presented with a plant at the site of the mandibular left epithelial and connective tissue mucosal recession of 2.5 mm and a central incisor, which presented with graft with a thickness of about 2 mm complete lack of keratinized mucosa. two buccal threads exposed (Fig 2a). was procured with a similar tech- Probing depths around the implant To improve the cleansability of this nique to that previously described. ranged from 2 to 5 mm, and there implant and to reduce discomfort The donor area was sutured with 5-0 was mild bleeding on gentle prob- during brushing, a silk (Ethicon, Johnson & Johnson) ing. The periapical radiographic ex- was suggested to the patient. (Fig 2c). The procured epithelial– amination showed bone loss down connective tissue graft was trimmed to the third thread of the implant. Surgical Phase to fit as accurately as possible on The affected implant was a Restore Local anesthesia was obtained with the recipient periosteal bed. (Lifecore Biomedical), with a 3.3 mm regional infiltration of 2 carpules of Two single interrupted coronal diameter and a length of 15 mm. 2% Xylocaine Dentsply). sutures were used to stabilize the

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a b c

d e f

Fig 2 (a) Clinical view of the area after to be treated after nonsurgical therapy. Note the soft tissue recession and the complete lack of keratinized mucosa on the implant in the po- sition of the mandibular left central incisor. (b) Intraoperative view of the prepared recipient periosteal bed. (c) The palatal donor area sutured. (d) Free gingival graft sutured in posi- tion. Note the good adaptation of the graft onto the recipient periosteal bed. No attempt to completely cover the implant recession was made. (e) Uneventful healing of the area 10 days after grafting. The mucosal recession was still present. (f) At 4 months after the surgi- cal procedure, creeping of the mucosal margin was evident, with complete coverage of the previously exposed threads. (g) After 2.5 years, further creeping of the soft tissue margin was visible. The implant supported prosthesis had been removed to be cleaned. g

graft in the proper position with 4-0 Postoperative Care Follow-up chromic gut suture (Ethicon, John- The same pharmacologic regimen After 10 days, the patient presented son & Johnson), and two additional that was described for case 1 was for suture removal and deplaquing sutures, a vertical crossed sling and suggested to the second patient. Be- of the area. The early healing of the a horizontal cross, were used to fur- cause the second patient was treated area was judged to be uneventful ther immobilize the graft while gen- in Italy, the commercial names of the with excellent graft integration. In tly compressing it down onto the same drugs were different (Brufen spite of a slight residual edema of periostium (Fig 2d). A periodontal 600 mg and Curasept 0.12%). The the tissue margin, the recession was dressing (Coe-Pack, GC) was ap- patient was advised not to touch the still present at suture removal (Fig plied to the grafted area to protect wound with any home hygiene tools 2e). The patient was instructed to the wound. until further instructions. continue the use of chlorexidine and

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© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. 232 to continue refraining from brushing tachment are related to the use nective tissue attachment to the im- and flossing for the first postopera- of free gingival autografts around plant surface.32 tive month. teeth.17–23,25–29 However, it has also The two cases presented in this During the first postoperative been reported in conjunction with study were treated in a similar way month, the patient was recalled every connective tissue graft28,30 and acel- and showed creeping after the first 7 days for professional supragingival lular dermal matrix.31 month and up to 18 and 30 months hygienic maintenance of the treated To the knowledge of the pres- postoperatively. Different baseline area. After that period, the patient ent authors, only one study has anatomical and local conditions resumed her regular home hygienic described peri-implant mucosal such as the adjacent soft and hard maintenance with a soft toothbrush, creeping. One of the two cases re- tissues, the depth and width of the used with a coronal roll technique, ported in that study underwent two recession, and the buccolingual and implant floss for interimplant surgical procedures, including a position of the implant may favor cleaning. Professional recall was free gingival graft and, 3 months af- complete implant root coverage or scheduled every 2 weeks until the ter, a coronally advanced flap with a a residual recession. end of the first postsurgical trimester. connective tissue graft. The second The physiologic mechanism At each in-office appointment, car- case was treated using a free gingi- behind creeping attachment on bon fiber–reinforced plastic curettes val autograft. Both cases exhibited natural teeth has not yet been fully were used to gently clean the surgi- peri-implant mucosal creeping up elucidated. Around implants, the cal area and 3% hydrogen peroxide– to 2 years after the procedures. In observed and reported coronal mi- soaked cotton pellets were used to neither of them was complete im- gration of the peri-implant mucosal delicately brush the area. plant surface coverage obtained, margin appears even more myste- At 4 months, after free gingival and in the second case a limited rious. The present study and the grafting of the implant mucosal re- amount of keratinized mucosa was report from Pereira Neto et al24 are cession, creeping of the soft tissue noted. the first to appear in the literature. margin was evident with no remain- Matter and Cimasoni27 men- Creeping attachment seems to be ing thread exposure (Fig 2f). tioned that the factors that seem a multifactorial and unpredictable Throughout the treatment, the to have a definite influence on the phenomenon. The proliferation of patient complied with the regularly phenomenon of creeping attach- periosteum-derived connective tis- scheduled 3-month professional ment around teeth are the width of sue cells in response to surgical maintenance appointments and the recession, the position of the trauma,33 the characteristics of the reached a satisfactory level of home graft, the bone resorption, the po- donor tissue, its ability to bridge oral hygiene. sition of the tooth, and the hygiene over the implant or root surface and After 30 months, the patient of the patient. Though implants proliferate and grow once trans- presented for a recall appointment lack the vascular supply of the peri- planted, and the configuration of and further coronal growth of the odontal ligament, it appears that if the recession defect seem to be cru- mucosal margin was noticed (Fig the recipient bed is of an adequate cial in determining whether the gin- 2g). The peri-implant probing depth size and the free gingival graft is gival margin will ultimately creep in a remained at 4 mm without signs of thick enough, there is a chance for coronal direction.18 inflammation. mucosal creeping to take place. It might be speculated that Implant surface may also play a creeping attachment over natural role in the observed phenomenon. teeth might be more prevalent due Discussion While soft tissue adhesion to ma- to the favorable cellularity provided chined implant surfaces has been by the periosteum and the capac- Most of the studies available in the shown, there is evidence that some ity of the periodontal ligament to literature involving creeping at- implant surfaces may enhance con- proliferate over a denuded root sur-

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face. On the other hand, on dental 4. Dorfman, HS, Kennedy JE, Bird WC. Lon- 19. Bell LA, Valluzzo TA, Garnick JJ, Pennel gitudinal evaluation of free autogenous BM. The presence of “creeping attach- implants it may be only the perios- gingival grafts. J Clin Periodontol 1980; ment” in human gingiva. J Periodontol teal stimulation effect that might 7:316–324. 1978;49:513–517. 5. Dorfman HS, Kennedy JE, Bird WC. Lon- 20. Matter J. Creeping attachment of free induce coronal migration of the gitudinal evaluation of free autogenous gingival grafts. A five-year follow-up peri-implant mucosal margin. gingival grafts: A four year report. J Peri- study. J Periodontol 1980;51:681–685. odontol 1982;53:349–352. 21. Otero-Cagide FJ, Otero-Cagide MF. 6. Wennström JL. Lack of association be- Unique creeping attachment after au- tween width of attached gingiva and togenous : Case report. development of soft tissue recession: J Can Dent Assoc 2003;69:432–435. Conclusions A 5-year longitudinal study. J Clin Peri- 22. Agudio G, Nieri M, Rotundo R, Cortellini odontol 1987;14:181–184. P, Pini Prato G. Free gingival grafts to in- 7. Ericsson I, Lindhe J. Recession in sites crease keratinized tissue: A retrospective These case reports have shown that with inadequate width of the keratinized long-term evaluation (10 to 25 years) of gingiva. An experimental study in the outcomes. J Periodontol 2008;79:587–594. mucosal creeping over implants dog. J Clin Periodontol 1984;11:95–103. 23. Agudio G, Nieri M, Rotundo R, Franceschi may occur with use a free gingi- 8. Stetler KJ, Bissada NF. Significance of D, Cortellini P, Pini Prato GP. Periodontal the width of keratinized gingiva on the conditions of sites treated with gingival- val autograft. Further randomized periodontal status of teeth with submar- augmentation surgery compared to un- controlled clinical trials using differ- ginal restorations. J Periodontol 1987;58: treated contralateral homologous sites: 696–700. A 10- to 27-year long-term study. J Peri- ent mucogingival techniques need 9. Esposito M, Grusovin MG, Maghaireh odontol 2009;80:1399–1405. to be conducted to determine the H, Coulthard P, Worthington HV. Inter- 24. Pereira Neto AR, Passoni BB, de Souza ventions for replacing missing teeth: JM Jr, et al. Creeping attachment in- prevalence and amount of creeping Management of soft tissues for dental volving dental implants: Two case re- attachment that can be expected implants. Cochrane Database Syst Rev ports with a two-year follow-up from an 2007;(3):CD006697. ongoing clinical study. Case Rep Dent on teeth and mucosal creeping on 10. Esposito M, Maghaireh H, Grusovin 2014;2014:756908. MG, Ziounas I, Worthington HV. Inter- 25. Ward VJ. A clinical assessment of the use implants. Moreover, its biologic and ventions for replacing missing teeth: of the free gingival graft for correcting physiologic mechanisms have yet to Management of soft tissues for dental localized recession associated with frenal implants. Cochrane Database Syst Rev pull. J Periodontol 1974;45:78–83. be investigated. Currently, creeping 2012;(2):CD006697. 26. Fagan F. Clinical comparison of the free attachment around teeth and muco- 11. Lin GH, Chan HL, Wang HL. The signifi- soft tissue autograft and partial thick- cance of keratinized mucosa on implant ness apically positioned flap—Preop- sal creeping around implants are an health: A systematic review. J Periodontol erative gingival or mucosal margins. unpredictable and not fully under- 2013;84:1755–1767. J Periodontol 1975;46:586–595. 12. Brito C, Tenenbaum HC, Wong BK, 27. Matter J, Cimasoni G. Creeping attach- stood phenomenon. Schmitt C, Nogueira-Filho G. Is keratin- ment after free gingival grafts. J Peri- ized mucosa indispensable to maintain odontol 1976;47:574–579. peri-implant health? A systematic review 28. Harris RJ. Creeping attachment asso- of the literature. J Biomed Mater Res B ciated with the connective tissue with Appl Biomater 2014;102:643–650. partial-thickness double pedicle graft. Acknowledgments 13. Thoma DS, Buranawat B, Hämmerle J Periodontol 1997;68:890–899. CH, Held U, Jung RE. Efficacy of soft 29. Miller PD Jr. Root coverage using a free tissue augmentation around dental im- soft tissue autograft following citric The authors reported no conflicts of interest plants and in partially edentulous areas: acid application. Part 1: Technique. Int related to this study. A systematic review. J Clin Periodontol J Periodontics Restorative Dent 1982;2: 2014;41(Suppl 15):S77–S91. 65–70. 14. Chambrone L, Tatakis DN. Periodontal 30. Nelson SW. The subpedicle connective soft tissue root coverage procedures: A tissue graft. A bilaminar reconstructive systematic review from the AAP Regen- procedure for the coverage of denuded References eration Workshop. J Periodontol 2015;86 root surfaces. J Periodontol 1987;58: (2 Suppl):S8–S51. 95–102. 15. Zucchelli G, Mounssif I. Periodontal plas- 31. Papageorgakopoulos G, Greenwell H, . 1 Miller PD Jr. Regenerative and recon- tic surgery. Periodontol 2000 2015;68: Hill M, Vidal R, Scheetz JP. Root cover- structive periodontal plastic surgery: Mu- 333–368. age using acellular dermal matrix and cogingival surgery. Dent Clin North Am 16. Palacci P, Nowzari H. Soft tissue enhance- comparing a coronally positioned tunnel 1988;32:287–306. ment around dental implants. Periodon- to a coronally positioned flap approach. 2. Lang NP, Löe H. The relationship between tol 2000 2008;47:113–132. J Periodontol 2008;79:1022–1030. the width of keratinized gingiva and 17. Goldman HM, Schluger S, Fox L, Cohen 32. Nevins M, Nevins ML, Camelo M, Boye- gingival health. J Periodontol 1972;43: DW. Periodontal Therapy, ed 3. St. Louis: sen JL, Kim DM. Human histologic evi- 623–627. Mosby, 1964. dence of a connective tissue attachment 3. Miyasato M, Crigger M, Egelberg J. Gin- 18. Borghetti A, Gardella JP. Thick gingival au- to a . Int J Periodontics Re- gival condition in areas of minimal and tograft for the coverage of gingival reces- storative Dent 2008;28:111–121. appreciable width of keratinized gingiva. sion: A clinical evaluation. Int J Periodontics 33. Goldman HM, Smukler H. Controlled J Clin Periodontol 1977;4:200–209. Restorative Dent 1990;10:216–229. surgical stimulation of periosteum. J Peri- odontol 1978;49:518–522.

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