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Treatment of localized gingival recessions using enamel matrix derivative as an adjunct to laterally sliding flap: 2 case reports Bahar Eren Kuru, Prof Dr, PhD, DDS1

Predictable and optimal coverage of exposed root surfaces is an important goal in periodontal plastic surgery. In this report, recession coverage was performed as laterally sliding flap technique with the adjunctive use of enamel matrix derivative (EMD). The cases of 2 female patients with on the maxillary canines are presented with 1-year follow-up observation. Initial vertical gingival recessions were 4.0 mm each, with a probing depth of 1.0 mm. The surgical procedure immediately produced a marked reduction in gingival recessions. In the course of healing, the soft tissue margin on the operated teeth showed some shrinkage in the first months. After 1 year, complete root coverage (100%) was observed, with a probing depth of 0.5 mm and 5.0-mm gain of clini- cal attachment in both cases, and there was 0.5-mm creeping tissue above the cemento- enamel junction. Within the limits of these cases, the results demonstrated the possibility of treating human buccal recessions with EMD plus laterally sliding flap, with predictable root coverage and clinical attachment gain. (Quintessence Int 2009;40:461–469)

Key words: bioengineering, enamel matrix protein derivative, gingival recession, laterally sliding flap, mucogingival surgery, root coverage

Gingival recession is the location of marginal which are involved in the formation of cemen- periodontal tissues apical to the cemento- tum during root and periodontal tissue devel- enamel junction (CEJ).1 To cover the exposed opment, have the potential to induce the root surfaces, various surgical techniques regeneration of the periodontal attachment have been proposed, including free gingi- apparatus. EMD, harvested from embryonic val/connective tissue grafting, various flap porcine teeth, has been studied extensively in designs, and guided tissue regeneration.2 animals and humans, and provided evidence Varying rates of success and predictability of tissue regeneration.10–20 Three human are obtained with these procedures.3–7 Even biopsy reports revealed that true periodontal though no single treatment can be consid- regeneration can be achieved with the topical ered superior to all others,8 regenerative application of EMD.21–23 Several clinical inves- approaches seem to be promising for obtain- tigations and case studies were undertaken ing root coverage with the formation of a to evaluate the use of EMD in the treatment of functional periodontal ligament.9 various types of periodontal defect; however, Use of enamel matrix protein derivatives the volume of published studies evaluating (EMD) is one of the tissue engineering modal- the use of EMD as an adjunct to convention- ities in regenerative periodontal treatment. It al surgical techniques in the treatment of gin- has been suggested that these proteins, gival recession is limited, and conflicting results regarding the clinical benefits have been reported.24–33 In this process, trials pre- 1Department of , Marmara University Dental senting the efficacy of combined procedures Faculty, Istanbul,Turkey. in the treatment of gingival recessions can Correspondence: Dr Bahar Eren Kuru, Marmara University add valuable information for the clinician in Dental Faculty, Department of Periodontology, Büyükciftlik sok. No: 6 Nisantası, 80200, Istanbul, Türkiye. Email: btkuru@ considering effective and predictable treat- superonline.com ment alternatives for root-surface coverage.

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Fig 1 Initial appearance of case 1. Fig 2 Initial appearance of case 2.

The aim of this report is to present the 1- incision around the denuded root was made year clinical follow-up results of soft tissue to remove the adjacent epithelium and con- root coverage using EMD with the lateral slid- nective tissue. The V-shaped incision was ing flap technique. beveled out on the opposite side from the donor area to permit overlap and increase vascularity for the donor tissue in this area (Fig 3). Intrasulcular incisions extended 2 DESCRIPTION OF CASES teeth distal to the recession. Vertical releas- ing incision down to the mucosa, in corre- Two female patients, 36 and 25 years of age, spondence to the line angle of the second were treated for gingival recessions that were premolar, was performed (Fig 4). creating sensitivity and esthetic problems on A full-thickness mucoperiosteal flap at the the buccal aspects of maxillary canines (Figs coronal portion, which was more of a split- 1 and 2). The patients were systemically thickness flap by partial mucosal dissection healthy, and there were no contraindications at its more apical end, was elevated to mobi- for periodontal surgery. They had no known lize the flap, ensuring passive lateral posi- drug allergies and denied use of alcohol. tioning. Partial dissection was extended far Neither were smokers. After a thorough clini- enough apically into the mucosal tissue to cal examination, the patients received permit adequate mobility of the flap. The flap plaque-control instructions and underwent was free enough to permit movement to the professional tooth cleaning on all tooth sur- recipient site, with no tension (Fig 5). By use faces. Recession depth, keratinized gingiva, of hand instruments, the exposed portion of probing depth, and clinical attachment level the roots was then planed gently to decrease were measured with a graded manual peri- the risk of removing intact periodontal fibers odontal probe to the nearest millimeter (CP from the root surfaces. The surgical area was 15 UNC, Hu-Friedy). rinsed with sterile saline, and the exposed root surfaces of all teeth were conditioned Treatment procedure for 2 minutes with ethylenediaminete- The unilaterally pedicled lateral sliding flap traacetic acid (EDTA) gel (pH 6.7) (PrefGel, technique was used in both cases to ensure Straumann). At this point, root surfaces were primary closure with the gingiva across the dis- again thoroughly rinsed with saline. EMD tal line angle of the lateral incisor. Prior to sur- gel, as Emdogain (Straumann), was then gery, the prominent convexity of the root was placed on the root surfaces (Fig 6). reduced by using diamond burs. A V-shaped

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Fig 3 Beveling out of the V-shaped incision. Fig 4 Vertical releasing incision down to the mucosa.

Fig 5 Passive lateral positioning. Fig 6 Application of EMD.

The pedicle flap was then laterally reposi- The patients received systemic antibiotic tioned to meet and overlap with the external- therapy for 2 weeks postoperatively. The reg- ly beveled-out portion of the V-shaped imen consisted of oral administration of incision at the distal line angle of the lateral doxycycline 200 mg the first day and then incisor. The flap was secured by suturing. 100 mg daily afterward. In addition, the Single suturing to the papilla regions was patients were advised to avoid hard chewing performed to pull the papilla interproximally in the surgical area and to rinse twice daily and hold the tissue tightly against the necks with a 0.2% solution of diglu- of the teeth (Fig 7). Following the lateral repo- conate for 4 weeks. After 4 weeks, gentle sitioning of the flap, the placement of a free tooth brushing was resumed in the surgical gingival graft onto the exposed bone was area. Recall appointments were scheduled performed (see Fig 7). No periodontal dress- every second week during the first 2 months ing was applied to the surgical area. After a following the surgical procedure, and the healing period of 2 weeks, the sutures were patients were recalled once a month for the removed. remaining observation period. During the 12- Postsurgical care was directed at mainte- month follow-up period, neither subgingival nance of wound stability and infection control. instrumentation nor probing of the operated

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Fig 7 Suturing and placement of a . Fig 8 Twelve-month postoperative clinical appear- ance of case 1.

Fig 9 Three-month postoperative clinical appear- Fig 10 Twelve-month postoperative clinical appear- ance of case 2. ance of case 2.

areas was performed. At 12 months, the Immediately after surgery, only case 2 cases were reevaluated and all measure- showed any recession (1.0 mm); at 3 ments repeated (Fig 8). months, recession was 0.5 mm and 1.5 mm for cases 1 and 2, respectively. Treatment outcomes In the course of healing, the soft tissue Postoperative healing was uneventful, and margin on the treated teeth showed some no complications such as allergic reactions, shrinkage in the first months (Fig 9). At the abscesses, infection, or flap dehiscence 1-year follow-up, a complete root coverage were observed. At baseline, vertical reces- was observed in both cases (100% root cov- sion in the 2 cases was 4.0 mm each, with a erage) (Figs 8 and 10) with probing depths of probing depth of 1.0 mm. The clinical attach- 0.5 mm and a total of 5.0-mm gain of clinical ment level in each case was 5.0 mm. The attachment in each case, indicating a reduc- amount of keratinized gingiva in cases 1 and tion of 0.5 mm in probing depth and 0.5 mm 2 was 2.0 mm and 0.5 mm, respectively. of creeping tissue represented as the

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amount of gingiva over the CEJ. The amount been widely used with these goals.3–5,37 of keratinized gingiva was increased in both Laterally sliding flap is one of the convention- cases, revealing a 4.0-mm and 6.5-mm kera- al surgical procedures for covering recession tinized gingiva gain, respectively. No reces- defects. It can be used when donor tissue is sion occurred on the donor teeth. available adjacent to the gingival recession, it retains the blood supply of the graft by its pedicle design, and it has advantages of ex- cellent color and texture match. However, DISCUSSION healing against the root surface following the treatment is characterized by partly epithelial This report presented the 1-year results of a and partly connective tissue attachment, unilaterally pedicled lateral sliding flap tech- while formation may rarely be nique with the adjunctive use of enamel observed.38 As gingival fibroblasts tend to matrix protein derivative bioactive material for repopulate the root surface faster than peri- the treatment of marginal tissue recession odontal ligament cells, healing will generally on 2 maxillary canines of 2 patients. The sur- not lead to the formation of a functional peri- gical procedure used in these 2 clinical odontal ligament. Furthermore, there is some cases produced complete coverage of gingi- risk of root resorption in roots directly val recession. Good clinical results were exposed to gingival fibroblasts during heal- achieved with 100% root coverage. No reces- ing.39 sion occurred on the donor teeth. Recently, attempts have been made to The 1-year follow-up demonstrated produce optimal coverage using combined changes in the degree of postoperative surgical techniques based on the principles results obtained immediately after the opera- of regenerative periodontal therapy. Regen- tion and at 3 months. The pedicle flap on the erative procedures increase the inducement exposed canine surface in the second case of cementogenesis and subsequent genera- could be repositioned only 1.0 mm beyond tion of new connective tissue attachment the CEJ at the time of surgery, and there were with functionally oriented collagen fibers, still recessions in both cases at 3 months which is desirable for the success of the root postoperatively on the recipient teeth. How- coverage. One of the treatment procedures ever, together with tissue maturation, com- to maximize the regenerative potential is the plete root coverage was obtained, with a combination of conventional pedicle flap probing depth of 0.5 mm and a total 5.0-mm designs with the use of barrier membranes gain of clinical attachment in each case, indi- according to the principles of guided tissue cating a probing depth reduction of 0.5 mm regeneration (GTR).6,7 However, in a recent and 0.5 mm of creeping tissue represented as review, Danesh-Meyer and Wikesjo40 men- the location of over the CEJ. tioned that GTR does not always provide This phenomenon had been previously additional clinical benefits over conventional observed by Matter and Cimasoni.34 In con- mucogingival techniques. The technical diffi- ventional mucogingival procedures, creeping culties of GTR are more hazardous than tissue is commonly seen, but complete cover- helpful for the clinician in controlling primary age of the residual defects is not predictable wound closure, membrane exposure, space in the long term.35,36 maintenance, and unacceptable reactions to Obtaining predictable optimal coverage of a foreign body. Because the type of healing exposed root surfaces with a sulcus exhibit- against the root surface following the treat- ing no and a depth of 2 ment is an important factor for the success of mm or less and correction of corresponding root coverage, the use of EMD may be an gingival recessions are the most important alternative treatment and of considerable goals of periodontal plastic surgery. Con- value in this process. Furthermore, it is easy ventional mucogingival surgical techniques to use clinically and represents low patient and their modifications involving pedicle soft morbidity.41 It is noteworthy that EMD obvi- tissue grafts from neighboring teeth have ates the problems of

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exposure. Therefore, based on the approach histologically. However, the use of EMD of tissue engineering, in the present cases, seems to be sufficient in promoting peri- this regenerative biomaterial was combined odontal regeneration. The possibility of favor- with a conventional mucogingival surgical ing the early healing of periodontal soft technique to maximize the success of soft tis- tissue wounds and obtaining new connective sue coverage. tissue attachment have already been demon- One of the most important factors in strated in animal and human studies on both achieving success in any type of mucogingi- clinical and histologic levels.11,12,21,45,46 val surgical procedure is the preservation of In a recent study, the coronally advanced an adequate blood supply. The covering pedi- flap with EMD was found histologically to cled lateral sliding flap used in these cases have all the tissues necessary for regenera- was designed to remain stable and viable, tion: new cementum, organizing periodontal and special care was taken to ensure an ade- ligament fibers, and islands of condensing quate vascularization. The pedicle provided bone. Histologic sections strongly suggest an abundant supply of blood and allowed for that EMD works in a biomimetic fashion by lateral displacement of the flap without ten- mimicking the natural process of tooth devel- sion, thereby avoiding impaired vasculariza- opment.21–23 Furthermore, it may be benefi- tion. In the literature, clinical studies using cial to use EMD with lateral sliding flap to rotational flaps revealed varying percentages avoid the risk of creating recession on the of root coverage.3,42–44 However, complete adjacent teeth. The conventional lateral slid- root coverage appears to be an infrequent ing flap design depends on transposing gin- outcome with these techniques, and less giva from the radicular surfaces of adjacent favorable treatment outcomes are obtained teeth, so there is always the potential of cre- at sites with wide recessions (> 3.0 mm). In ating recession on donor teeth because of the studies that reported data describing the the denudation of the bone plate.3,4,37 In a gingival dimensions,3,42,43 an increase in gin- previous study by the author and others eval- gival height of 2.8 to 3.2 mm was evident at uating the effect of EMD on horizontal types the follow-up examination. The percentage of of defect, no postoperative marginal bone root coverage in both of the present cases resorption was measured compared to con- was 100%, with 4.0 mm and 6.5 mm gain of ventional flap technique without EMD.19 We keratinized tissue, respectively. Although with believe that EMD may keep the marginal only 2 cases without controls, conclusions bone resorption at a minimum level. cannot be drawn regarding any possible There are limited data in the literature for additive effect of EMD, the combined treat- the use of EMD as an adjunct to mucogingi- ment approach used in the treatment of val surgery. Modica et al,24 in a study com- these 2 cases revealed a complete closure of bining coronally advanced flap with EMD the root surfaces with a high increase in ker- application for the treatment of buccal gingi- atinized tissue. val recessions, suggested that EMD did not The reductions in recession in the present seem to significantly improve the clinical out- cases paralleled the average attachment comes of gingival recession. In a correspon- gain, while the probing pocket depth ding study, Hagewald et al26 stated that with remained substantially unchanged. This the exception of keratinized tissue gain, observation would certainly have to be con- which was significantly higher in the EMD firmed by histologic analysis to be able to group, all other clinical variables were not dif- suggest that the root coverage was achieved ferent among the groups. Rasperini et al,25 through periodontal regeneration. Ethical on the other hand, studied the subepithelial considerations made it impossible to sub- connective tissue graft in the treatment of stantiate the hypothesis of periodontal regen- human gingival recessions both clinically eration with histology. The present cases and histologically and reported a successful have been reported merely to show the clini- result comparable with a periodontal barrier cal outcome of a root-coverage procedure membrane. Carnio et al,28 in a study design using EMD, not to analyze the wound healing similar to that of Rasperini et al, presented

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4 cases with clinical and histologic signs of and also has the advantages of a single sur- successful root coverage. Berlucchi et al27 gical site, avoiding any palatal patient dis- reported good clinical results with percent- comfort, and a good color compatibility with age of root coverage comparable or superior adjacent tissue. to other techniques when EMD was com- One-year results of these 2 cases are bined with coronally advanced flap or coro- encouraging. Further controlled studies are nally advanced flap plus connective tissue needed for a proper judgment of the clinical graft for the treatment of gingival recessions. benefits of EMD used as an adjunct to later- Based on the results of a recent study by ally sliding flap. Cueva et al,30 the application of EMD to denuded root surfaces receiving coronally advanced flaps significantly increased the percentage of root coverage compared to REFERENCES coronally advanced flaps without EMD. In addition, EMD application was accompanied 1. American Academy of Periodontology. Glossary of by a significant increase in keratinized tissue Periodontal Terms, ed 4. Chicago: American Aca- demy of Periodontology, 2001:44. 6 months after surgery. 2. Wennström JL. Mucogingival therapy. Ann Perio- Nemcovsky et al,31 in another study on dontol 1996;1:671–701. treatment of gingival recession, compared 3. Guinard EA, Caffesse RG.Treatment of localized gin- the clinical efficacy of a coronally advanced gival recessions. Part III. Comparison of results flap procedure plus EMD to that of the sub- obtained with laterally sliding and coronally reposi- pedicle connective tissue graft procedure. tioned flaps. J Periodontol 1978;49:457–461. They found that the connective tissue graft 4. Caffesse RG, Guinard EA.Treatment of localized gin- procedure was superior to the coronally gival recessions.Part IV.Results after 3 years.J Perio- dontol 1980;51:167–170. positioned flap with EMD in percentage of 5. Caffesse RG, Espinel MC. Lateral sliding flap with a coverage and increase in width of kera- free gingival graft technique in the treatment of tinized tissue. They further pointed out that localized gingival recessions. Int J Periodontics the combined EMD procedure is a pre- Restorative Dent 1981;1:23–30. dictable treatment for root coverage that is 6. Tinti C, Vincenzi G, Cortellini P,Pini Prato G, Clauser relatively easy to perform and appropriate, C. Guided tissue regeneration in the treatment of especially where a substantial increase in human facial recession. A 12-case report. J Perio- dontol 1992;63:554–560. the width of keratinized tissue is not of 7. Pini Prato G,Tinti C,Vincenzi G,Magnani C,Cortellini prime importance. P, Clauser C. Guided tissue regeneration versus Differing results and comments in these mucogingival surgery in the treatment of human studies may be explained in part by the buccal gingival recession. J Periodontol 1992;63: nature of the treated lesions and in part by 919–928. the case selection, surgical technique, root 8. Roccuzzo M, Bunino M, Needleman I, Sanz M. conditioning, study designs, and evaluation Periodontal plastic surgery for treatment of local- ized gingival recessions: A systematic review. J Clin methods. However, there is no study in the Periodontol 2002;29(suppl 3):178–194. literature combining EMD with laterally slid- 9. Newman MG, McGuire MK. Evidence-based peri- ing flaps. odontal treatment. II. Predictable regeneration The results obtained either as root cover- treatment. Int J Periodontics Restorative Dent 1995; age or as an esthetic result can be consid- 15:116–127. ered positive in the present cases. Improved 10. Hammarström L. Enamel matrix, cementum devel- esthetics is one of the major indications of opment and regeneration. J Clin Periodontol 1997;24:658–668. mucogingival surgery and is a subjective 11. Hammarström L, Heijl L, Gestrelius S. Periodontal parameter, which can also be determined regeneration in a buccal dehiscence model in mon- by the patient. Our patients declared their keys after application of enamel matrix proteins. happiness and found the results enough to J Clin Periodontol 1997;24:669–677. satisfy their individual requirements. This surgical technique enabled us to cover the gingival recession with a 1-step procedure

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