Evaluation of Recession DefectsTreated With Coronally AdvancedFlaps and Either Recombinant HumanPlatelet-Derived Growth Factor-BB Plusb-Tricalcium Phosphate or ConnectiveTissue: Comparison of ClinicalParameters at 5 YearsMichael K. McGuire,* E. Todd Scheyer,* and Mark B. Snyder†

Background: In a previously reported split-mouth, randomized controlled trial, Miller Class II gingivalrecession defects were treated with either a connective tissue graft (CTG) (control) or recombinant humanplatelet-derived growth factor-BB + b-tricalcium phosphate (test), both in combination with a coronallyadvanced flap (CAF). At 6 months, multiple outcome measures were examined. The purpose of thecurrent study is to examine the major efficacy parameters at 5 years.

Methods: Twenty of the original 30 patients were available for follow-up 5 years after the originalsurgery. Outcomes examined were recession depth, probing depth, clinical attachment level (CAL), heightof keratinized tissue (wKT), and percentage of root coverage. Within- and across-treatment group resultsat 6 months and 5 years were compared with original baseline values.

Results: At 5 years, all quantitative parameters for both treatment protocols showed statisticallysignificant improvements over baseline. The primary outcome parameter, change in recession depthat 5 years, demonstrated statistically significant improvements in recession over baseline, although in-tergroup comparisons favored the control group at both 6 months and 5 years. At 5 years, intergroupcomparisons also favored the test group for percentage root coverage and change in wKT, whereas nostatistically significant intergroup differences were seen for 100% root coverage and changes to CAL.

Conclusions: In the present 5-year investigation, treatment with either test or control treatments forMiller Class II recession defects appear to lead to stable, clinically effective results, although CTG + CAFresulted in greater reductions in recession, greater percentage of root coverage, and increased wKT.J Periodontol 2014;85:1361-1370.

KEY WORDS

Case-comparison studies; connective tissue; gingival recession; guided tissue regeneration;platelet-derived growth factor BB; transplants.

doi: 10.1902/jop.2014.140006

* Private practice, Houston, TX.† Private practice, Philadelphia, PA, and New York, NY.

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Achieving successful long-term clinical outcomesis the primary goal in treating the functionaland esthetic problems resulting from gingival

recession (GR). These clinical problems (e.g., chronicdentinal sensitivity, esthetic deficiencies, poor plaquecontrol) require effective surgical interventions thatresult in minimal short- and long-term sequelae. Anumber of systematic reviews have examined a rangeof therapeutic approaches to recession defects, in-cluding the coronally advanced flap (CAF) alone, CAFin combination with the subepithelial connective tis-sue graft (CTG), guided tissue regeneration (GTR),acellular dermal matrix (ADM), and enamel matrixderivative (EMD).1-12 When examining specific clini-cal parameters, alternative protocols to CAF + CTGoften appear quite effective. However, most currentreviews suggest that only CAF + CTG appears tobe consistently effective across all measured out-come parameters, especially root coverage stabilityover time.1,2,4-9,11-15

CAF + CTG, although often considered the goldstandard for root coverage treatment, has a numberof disadvantages: 1) an additional surgery to obtaindonor tissue is needed; 2) increased morbidity mayresult from the harvesting procedure; and 3) a finiteamount of autogenous donor tissue is available,restricting the number of possible treated sites perpatient visit.16,17 In addition, evidence suggests thatCAF + CTG has limited ability to regenerate missingtissues of the attachment apparatus when treatingrecession defects. Instead, most studies supporthealing through either connective tissue adaptationwith adjacent root surfaces or a long junctional epi-thelium.17-22 As a result of these disadvantages, alongwith limited ability to effect true periodontal regen-eration, alternatives to CAF +CTG continue to besought.14,23-33 Recent advances in recombinantgrowth factor technology may offer viable alterna-tives to CTG, including the potential to regeneratemissing cementum, periodontal ligament, and sup-porting alveolar bone.

In a published study, McGuire et al.34 examinedgrowth factor–mediated clinical and histologic re-sults for the treatment of human Miller Class II re-cession defects treated with a composite graft ofrecombinant human platelet-derived growth factor-BB (rhPDGF-BB) and b-tricalcium phosphate (b-TCP)in conjunction with CAF. In the randomized con-trolled trial (RCT) portion of the study, 30 patientswith contralateral recession defects ‡3 mm deep and‡3 mm wide were treated with either CTG (control)or 0.3 mg/mL rhPDGF-BB + b-TCP + an absorbablecollagen wound healing dressing (test), each in com-bination with CAF. At the end of 6 months, both thetest and control treatments demonstrated significantimprovements from baseline. Statistically significant

results favoring CTG included recession depth re-duction, percent root coverage, and recession widthreduction, whereas mid-buccal probing depth re-duction (PDR) favored the growth factor–mediatedtreatment. There were no statistically significant dif-ferences detected between test and control groupsfor height of keratinized tissue (wKT), patient sat-isfaction, and esthetic results. According to theauthors, at 6-month follow-up, both test and controltreatments appeared to be viable alternative treat-ments for Miller Class II recession defects.34,35

Although 6-month follow-up durations yield valu-able outcome information, longer-term data validatingstable recession treatment clinical results over timeare desirable. Systematic reviews of GR RCTs requireat least a 6-month post-surgery follow-up and oftenextend an additional 6 months.2,3,6,8-12 Occasionally,longer RCT follow-up times extending to 2 years post-grafting are included in systematic reviews of GRtreatment. Apart from systematic reviews, a numberof individually reported studies examining a varietyof treatment protocols extend GR treatment follow-up times from 4 to 14 years, reporting a wide rangein stability of outcome measures initially reported at6 to 12 months.36-40 The purpose of the currentstudy is to examine the major patient-centered andclinical quantitative parameters initially reportedby McGuire et al. in 2009,34 ‡5 years after originaltreatment with either CTG or rhPDGF-BB + b-TCP +an absorbable collagen wound healing dressing, eachin conjunction with CAF.

MATERIALS AND METHODS

Study PopulationOf the 30 patients completing the original study,20 were available for follow-up ‡5 years after theoriginal recession-related surgery. The 40 evaluatedsites were distributed among incisors, canines, andpremolars, the majority of which (36 sites) werelocated in the maxilla. Canine sites predominated,with 28 in the maxilla and two in the mandible. Noneof the follow-up patient population (three males and17 females, aged 29 to 68 years; mean age: 52.5years) smoked. Generally, the follow-up patients werehealthy and without significant medical problems.

Patient Population Lost to Follow-UpTen of the original 30 patients were lost to follow-up.Five chose not to participate, and three could notbe located. In the remaining two, the cemento-enameljunction (CEJ) reference point was obscured byrestorations. Overall the loss to follow-up appearedunrelated to recession treatment outcomes. The studyprotocol was approved by the IntegReview institutionalreview board. Study patients gave informed writtenconsent to participate in the study.

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Summary of Original SurgeryThe surgical protocol for the test treatment was CAF +rhPDGF-BB + b-TCP‡ + an absorbable collagen woundhealing dressing,§ and that for control treatment wasCAF + CTG. Both test and control sites were surgicallytreated as described by McGuire and Scheyer41 intheir initial feasibility study, with the following excep-tion: an absorbable collagen wound healing dress-ing saturated with rhPDGF-BB was placed over thegrafted test root surfaces in place of a collagenmembrane (Figs. 1 and 2). The first surgery was

performed on the left side in allpatients, with the contralateralsurgery immediately following.For all 30 patients, postoperativeoral hygiene instructions weredesigned to minimize trauma atthe gingival margins, and follow-up continued through month 6.

Clinical Evaluation 5 YearsAfter Original SurgeryAs performed for the originalRCT 5 years earlier, the treatedsites were clinically examined,measurements were recorded,and clinical photographs taken(Fig. 3). The same examiner(Carol Waring, RDH, Perio HealthProfessionals, Houston, TX) whorecorded the original studymeasurements was still maskedand performed the follow-up5-year examinations after beingrecalibrated for measurementaccuracy and consistency. Theprimary efficacy parameter wasthe change in the depth of therecession defect. Secondary ef-ficacy parameters included thefollowing: 1) probing depth(PD); 2) clinical attachmentlevel (CAL); 3) wKT; 4) per-centage of root coverage; 5)percentage of patients with 100%root coverage; 6) root dentinhypersensitivity; 7) clinicianrating of color (compared withadjacent tissue); 8) clinicianrating of texture (compared withadjacent tissue); and 9) pa-tient satisfaction at 5 years.

At baseline, there were noobserved significant differencesbetween test and control sites.All quantitative and qualitative

outcome parameters were defined and measuredexactly as in the original 6-month study protocol.

Patient satisfaction at 5 years was assessed byresponses to the following questions: 1) How satisfiedwere you with the outcome? 2) At which site did youexperience the most discomfort? 3) If you neededtreatment again, which side would you choose, lefttreatment or right treatment?

Figure 1.A) At baseline, a maxillary canine randomized to receive test (rhPDGF-BB + b-TCP) treatment. B)Full-thickness flap elevation with divergent releasing incisions beyond the mucogingival junction. C)Intraoperative measurements after flap elevation. D) rhPDGF-BB + b-TCP placed over the root surfaceseveral millimeters apical to the CEJ. E) Collagen dressing sutured in place over the grafted root surface.F)Mucogingival flap coronally advanced to the level of the CEJ and secured with sutures. G) Six-monthfollow-up with no evidence of GR.

Figure 2.A) At baseline, the contralateral canine randomized to receive control (CTG) treatment. B) SubepithelialCTG (control) is sutured over the denuded root surface.C)Mucogingival flap coronally advanced to the levelof the CEJ and secured with sutures. D) Six-month follow-up with 0.5 mm GR.

‡ GEM 21S, Osteohealth, Shirley, NY.§ CollaTape, Integra LifeSciences, Carlsbad, CA.

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Statistical AnalysesQualitative measures, including root hypersensitiv-ity, soft tissue color (compared with adjacent tissue),and soft tissue texture (compared with adjacent tissue),were analyzed by their original categories. Specif-ically, root hypersensitivity was in four categories:1) none; 2) mild; 3) moderate; and 4) severe, indi-cating the severity of root hypersensitivity. Soft tis-sue measures compared with adjacent tissue werein three categories: 1) more red, 2) less red, and 3)equally red for soft tissue color and; 1) more firm, 2)less firm, and 3) equally firm for soft tissue texture.The Bowker test (an extension of the McNemar testfor paired measurements with >2 categories) wasused to test for changes in qualitative outcomes frombaseline to 5 years.

Within-treatment comparisons across time andbetween-treatment comparisons at each point intime were made using non-parametric tests. Likewise,all change comparisons (baseline versus 6 monthsand baseline versus 5 years) both within and be-tween treatments were made using non-parametrictests. In particular, for continuous outcomes (recessiondepth, PD, CAL, wKT, and percent root coverage),a Wilcoxon signed-rank test was used. For the bi-nary outcome of patients with 100% root coveragebetween test and control sites, Fisher exact test com-paring two binomial proportions was used. For com-paring the same sites at 6 months versus 5 yearswithin each treatment for proportion of patients with100% root coverage, McNemar test was used.

RESULTS

Five-Year Assessment of QuantitativeParametersGR depth, average percentage root coverage, andpercentage with 100% root coverage. The primary ef-ficacy endpoint of this study is change in recession

depth. At both 6 months and 5years, significant improvementscompared with baseline (timezero) were achieved for both testand control sites, with mean testreductions of 2.90 and 2.35mm (P

(time zero) were achieved for both test andcontrol sites, with mean test reductions of0.38 mm (P = 0.02) and mean controlreductions of 0.35 mm (P = 0.01) (Table1). No statistically significant differences,however, were seen at 6 months betweentest and control PDR (P = 0.94). Likewise,at 5 years no significant differences werenoted between test and control mean PDRs(P = 0.29) from baseline. However, whenexamining intragroup change at 5 yearsfrom baseline, a statistically significant in-crease in mean control PD (0.38 – 0.14mm; P = 0.02) was noted, but not in thetest group (0.15 – 0.14 mm; P = 0.38).

No significant difference in mean PDchange between test and control groupswas observed at 5 years compared with 6months (P = 0.28). However, highly sta-tistically significant intragroup increasesin PD were observed from 6 months to5 years for both test and control groups(5-year test, 0.53 – 0.11 mm, P

with 6 months, the difference again favored the controlgroup (P = 0.04). When examining intragroup wKTchange from 6 months to 5 years, a statistically sig-nificant increase occurred within the control group(P = 0.02), whereas the comparable test group com-parison remained statistically the same (P = 0.70).

Five-Year Assessment of Qualitative ParametersAt 5 years after the original grafting procedures,clinical photos were taken, and a number of quali-tative parameters were examined (Fig. 3). To avoidselection bias, images in Figure 3 represent the samegrafted sites included in the McGuire et al.34 2009publication. For each qualitative outcome param-eter (root dentin hypersensitivity, soft tissue texturecompared with adjacent sites, and color equiva-lence compared with adjacent sites), no statisticallysignificant differences between test and control siteswere seen at the end of 5 years.

Also at 5 years, patients were asked to respondto questions related to esthetic satisfaction. Of the20 test and 20 control sites, 14 sites for each wererated as ‘‘very satisfied.’’ In the test group, four siteswere rated as ‘‘satisfied,’’ one as ‘‘unsatisfied,’’ andone as ‘‘very unsatisfied.’’ In the control group, theremaining six sites were rated as ‘‘satisfied’’ with theesthetic results 5 years after the grafting procedure.As with the other qualitative parameters, the dif-ferences between the two groups failed to achievestatistical significance (P = 0.72).

Investigator Versus General PractitionerFollow-Up CareOf the 20 patients, seven were followed by the in-vestigators (MKM, ETS, board-certified periodon-tists) and 13 by their referring general practitionersfrom month 7 after the initial surgery through year5. As noted in Table 3, significant differences in per-centage root coverage and 100% root coverage forboth test and control sites were seen, depending onwhether follow-up care was given by investigator orgeneral practitioner.

DISCUSSION

Standards of care in today’s clinical practice areevidence based, with the source of evidence origi-nating from a hierarchy of study types, from so-phisticated RCTs to individual case series andreports. The implied understanding is that evidencederived from well-executed trials is valid, reproducible,and capable of translating into stable, effective, long-term results. The RCTs and case series that dom-inate the periodontal and dental literature haverelatively short study durations, as highlighted bythe fact that most systematic reviews include studieswith durations from 6 to 12 months, with occasionallonger-term studies extending to >2 years.2,3,6,8-12Ta

ble

2.

PercentageRootCove

rage

6Months

5Years

P,6Months

to5Years

Changefrom

6Months

to5Years

Siteswith

100%

RootCoverage

(%)

Group

Mean–SE

SD(m

into

max)

Mean–SE

SD(m

into

max)

Mean–SE

SD(m

into

max)

Mean

Proportion

at6Months

Mean

Proportion

at5Years

P,6Months

to5Years

Control

97.90–1.47

6.59(75to

100)

89.35–4.84

21.63(33to

100)

0.13

8.55–4.65

20.78(-67to

0.0)

90

75

0.08

Test

89.85–3.57

15.95(63to

100)

74.10–8.33

37.27(0.00to

100)

0.03*

15.8

–6.03

26.97(-70to

0.0)

70

60

0.16

P,control

versus

test

0.04*

0.01*

0.41

0.24

0.50

Pva

lues

wereobtained

usingWilc

oxo

nsigned

-ranktest

forave

rageperce

ntagerootco

verageandMcN

emartest

comparingsa

mesiteswith100%

rootco

verage.

Fisher

exact

test

wasuse

dwhen

comparing

proportionbetwee

ngroups.

*Statistically

significa

nt.

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Short study durations, however, tend to minimizethe effects time may have on evidence-based ther-apies by excluding the potential impact time mayexert on long-term therapeutic effectiveness. In ad-dition to the current study, there are a number ofpublished individual studies that examine the po-tential effects time may exert on long-term resultsstemming from various approaches to root re-cession treatment.24,29,34,36,38,40,42

As in the current study, most long-term recession-related studies compare outcomes of different treat-ment protocols to CAFs in combination with CTGs(CAF + CTG).24,29,34,36,38,40,42 In a 5-year follow-upstudy, Pini-Prato et al.24 demonstrated a statisticallysignificant difference in complete root coverage be-tween sites treated with CAF + CTG (52%) and CAFalone (35%) (P = 0.02). At 6 months after surgery,no statistically significant difference had been ob-served between the two groups. Interestingly, at 5years progressive coronal migration of the gingivalmargin occurred within the CAF + CTG sites, whereasan apical shift of the gingival margin was observed inthe CAF-alone sites.

Harris,36 in a retrospective analysis of 25 patientstreated with either CTG or ADM, each with CAF, ex-amined two time points after grafting: 12.3 to 13.2weeks or 48.1 to 49.2 months. Short-term resultsrevealed no significant differences between the twotreatment types on most parameters, especially per-cent root coverage (CTG 96.6%; ADM 93.4%). Norwas a difference seen at 18.6 months.42 At 4 years,however, a statistically significant difference was seenin root coverage between ADM- and CTG-treatedsites (ADM 65.8%; CTG 97.0%).36 CTG-grafted sitesappeared stable over time, whereas ADM graftedsites exhibited significant regression at 4 years.

Two studies, Nickles et al.38 and McGuire et al.,40

with follow-up times up to 10 years demonstratesignificantly different long-term outcomes with twodifferent approaches to GR treatment. ComparingCTG to GTR, each in conjunction with CAF, Nickles

et al.38 demonstrated significant root coverage at 6months compared with baseline for both groups. By1 year, significant recession was seen in the GTR-treated sites, and at 10 years both the CTG and GTRsites exhibited significant outcome decline from the6-month time point, with the GTR sites regressingclose to baseline. In contrast, the McGuire et al.40

10-year evaluation of human recession defects treatedwith either EMD or CTG, each with a CAF, dem-onstrated statistically comparable root coverage re-sults for both treatment approaches a decade afterinitial surgical treatment (89.8% CTG, 83.3% EMD,P = 0.50). In addition, on all other study parame-ters, including increases in wKT, EMD- and CTG-treated sites at 10 years appeared comparable andstable.

In the current study, the primary outcome pa-rameter is the change in recession depth at 5 yearscompared with time zero (baseline) and 6 monthsafter initial grafting surgery. Significant improve-ments from baseline were seen for both test andcontrol treatments, although statistically the reductionin recession at 5 years compared with baseline fa-vored the control group. There was, however, no sta-tistically significant difference at 5 years comparedwith the 6-month time point in GR depth changesbetween test and control sites. Although there wasa statistically significant increase in recession notedfor the test sites at 5 years compared with 6 months(0.55 – 1.00 mm), in clinical terms this differencewas quite small and would likely not be significant.

When examining percent root coverage, no sta-tistically significant intergroup comparison changewas observed from 6 months to 5 years, although ateach time point the mean percentage root coveragefavored the control group. When comparing the per-centage of sites with 100% root coverage, no sta-tistically significant differences were seen at either6 months or 5 years between test and control sites.In this study, therefore, direct recession-related pa-rameters appear relatively stable over the 5-year

follow-up period, although in absoluteterms the trend over time for both testand control sites was some loss of thegains seen at 6 months.

Of interest to both this and otherstudies are the possible long-term ef-fects that GR treatment protocols haveon keratinized tissue. In a 5-year follow-up study of CAF alone in treating 73Miller Class I and II recession defects,Zucchelli and De Sanctis37 found sta-tistically and clinically significant in-creases in wKT. At baseline, 38% of therecession sites had £1 mm wKT. At5 years, 92% of the treated teeth had

Table 3.

Percentage Root Coverage at 5 Years: RoutinePatient Follow-Up Care Rendered by Periodontists(n 5 7) Versus Referring General Dentists (n 5 13)

Mean Percentage Root

Coverage at 5 Years

Sites with 100% Root

Coverage at 5 Years (%)

Follow-Up Clinician Test Control Test Control

Periodontist 100 100 100 100

General Practitioner 60.2 83.6 38 61

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‡3 mm of KT and none had

is currently medical director of the Osteohealth di-vision of Luitpold Pharmaceuticals.

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30. Nemcovsky CE, Artzi Z, Tal H, Kozlovsky A, MosesO. A multicenter comparative study of two rootcoverage procedures: Coronally advanced flap withaddition of enamel matrix proteins and subpedicleconnective tissue graft. J Periodontol 2004;75:600-607.

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31. Spahr A, Haegewald S, Tsoulfidou F, et al. Cover-age of Miller class I and II recession defects usingenamel matrix proteins versus coronally advancedflap technique: A 2-year report. J Periodontol 2005;76:1871-1880.

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35. McGuire MK, Scheyer T, Nevins M, Schupbach P.Evaluation of human recession defects treated withcoronally advanced flaps and either purified recombi-nant human platelet-derived growth factor-BB withbeta tricalcium phosphate or connective tissue: Ahistologic and microcomputed tomographic examina-tion. Int J Periodontics Restorative Dent 2009;29:7-21.

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38. Nickles K, Ratka-Krüger P, Neukranz E, Raetzke P,Eickholz P. Ten-year results after connective tissuegrafts and guided tissue regeneration for root cover-age. J Periodontol 2010;81:827-836.

39. Pini Prato G, Rotundo R, Franceschi D, Cairo F,Cortellini P, Nieri M. Fourteen-year outcomes of coronallyadvanced flap for root coverage: Follow-up froma randomized trial. J Clin Periodontol 2011;38:715-720.

40. McGuire MK, Scheyer ET, Nunn M. Evaluation ofhuman recession defects treated with coronally ad-vanced flaps and either enamel matrix derivative orconnective tissue: Comparison of clinical parametersat 10 years. J Periodontol 2012;83:1353-1362.

41. McGuire MK, Scheyer ET. Comparison of recombi-nant human platelet-derived growth factor-BB plusbeta tricalcium phosphate and a collagen membraneto subepithelial connective tissue grafting for the treat-ment of recession defects: A case series. Int J Periodon-tics Restorative Dent 2006;26:127-133.

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Correspondence: Dr. Michael K. McGuire, 3400 S. GessnerRoad, Suite 102, Houston, TX 77063. E-mail: mkmperio@swbell.net.

Submitted January 3, 2014; accepted for publicationMarch 3, 2014.

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mailto:mkmperio@swbell.netmailto:mkmperio@swbell.net