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Smoking May Affect Root CoverageOutcome: A Prospective Clinical Studyin HumansAngela Guimarães Martins,* Denise Carleto Andia,* Antonio Wilson Sallum,*Enilson A. Sallum,* Márcio Z. Casati,* and Francisco H. Nociti Jr.*†

Background: Cigarette smoking has been shown to negativelyinfluence healing following periodontal therapeutic procedures.Therefore, the aim of this study was to evaluate the impact ofsmoking on clinical outcome of root coverage following subepithe-lial connective tissue graft (CTG) surgery.

Methods: Eighteen defects were treated in 15 patients (sevensmokers and eight non-smokers) who presented canine and pre-molar Miller Class I and II recessions. CTG was performed andclinical measurements were obtained at baseline, and 30, 60, 90,and 120 days after surgery. Clinical measurements includedplaque and gingival indexes, gingival recession, probing depth,clinical attachment level, gingival thickness, and keratinized tis-sue width.

Results: Intragroup analysis showed that CTG was able to pro-mote root coverage, increase gingival thickness, and improveclinical attachment level in both groups (P <0.05). On the otherhand, intergroup analysis demonstrated that smokers presentedwith a lower percentage of root coverage (58.84% ± 13.68% versus74.73% ± 14.72%), less clinical attachment level gain (2.54 ±0.79 mm versus 2.00 ± 1.04 mm), and deeper probing depths(1.56 ± 0.53 mm versus 2.35 ± 0.67 mm) than non-smokers(P <0.05). Moreover, 4 months after CTG, smokers presentedmore keratinized tissue compared to non-smokers (3.30 ±0.86 mm versus 4.50 ± 1.16 mm) (P <0.05).

Conclusion: Within the limits of the present study, it can beconcluded that cigarette consumption may present a negativeimpact on root coverage outcome by CTG and, therefore, mayrepresent one more challenge for periodontal plastic therapy.J Periodontol 2004;75:586-591.

KEY WORDSGingival recession/surgery; grafts, connective tissue;smoking, adverse effects; tooth root/surgery.

* Department of Prosthodontics and Periodontics, Division of Periodontics, Schoolof Dentistry at Piracicaba, University of Campinas, Piracicaba, São Paulo, Brazil.

† Department of Periodontics, School of Dentistry, University of Washington, Seattle, WA.

Among the esthetic procedures inperiodontics, root coverage hasattracted the most interest. Indica-

tions for exposed root coverage areesthetic and/or cosmetic needs, as well asthe management of root hypersensitivity,shallow root caries lesions, and cervicalabrasions.1 During the 1970s, the coron-ally positioned flap,2 laterally sliding flap,3

and the combined free gingival graft pluscoronally positioned flap were the mostacceptable techniques.4 In the 1980s,subepithelial connective tissue grafts (CTG)were introduced,5,6 enhancing the pre-dictability of covering localized areas ofroot exposure. Numerous authors haveprovided variations on the technique,5,7-9

and the results of these studies confirmthat CTG is a predictable procedure forobtaining esthetic root coverage.10,11

Cigarette smoking has been shown torepresent a strong risk marker and possi-bly a true risk factor for periodontaldisease.12,13 Experimental evidence hasdemonstrated that cigarette smoking maynegatively influence the healing outcomefollowing various periodontal therapeuticprocedures. Smokers showed a signifi-cantly less favorable response comparedto non-smokers after scaling and root plan-ing,14 adjunctive antimicrobial therapy,15

modified Widman flap surgery,16 and dur-ing periodontal maintenance followingactive therapy.17 Compromised healing fol-lowing regenerative therapy in intrabony18

and in gingival-recession defects19 insmokers has also been reported. The pre-cise mechanisms by which tobacco smoke

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interferes with healing are not completely understood, dueto the fact that there are thousands of toxins in tobaccosmoke, many of which have not been identified, muchless evaluated, for their effect on periodontal healing.

To date, there is very little information on the effectof smoking on the treatment of gingival recessions byperiodontal plastic surgery. Therefore, the presentprospective clinical study was designed to investigatethe impact of smoking on treatment outcome follow-ing CTG treatment of gingival recession defects.

MATERIALS AND METHODSPatients and Recession DefectsPatients were selected from the pool of the Universityof Campinas School of Dentistry. All the patientsrequested treatment for esthetic and/or dentin hyper-sensitivity through a root coverage procedure. None ofthe participants exhibited probing depths >3 mm orclinically appreciable gingival inflammation in the experi-mental sites. The patients were in good general healthwith no contraindications to surgical periodontal ther-apy, and were not taking any medication that couldinterfere with the final outcome of the surgery. Aninformed consent was signed by all patients accordingto the recommendations of the Ethical Committee forResearch of the University of Campinas. Fifteen patients(seven smokers and eight non-smokers, 10 womenand five men, aged 27 to 55 years [mean age 40.33 ± 6.75]) who presented at least one Miller Class I or II20

buccal gingival recession were included in this prospec-tive study. There were 18 recession defects: eight max-illary premolars, seven maxillary cuspids, and threemandibular premolars. The defects were ≥3 mm deepand 4 mm wide and presented ≥2 mm of keratinizedtissue marginal to the defect.

Patients were regarded as smokers if they smokedat least 20 cigarettes per day for at least 5 years priorto the study. Occasional and former smokers wereexcluded and, therefore, individuals who had neversmoked composed the non-smoker group.

Preoperative Treatment and RecordsPrior to surgery, patients received a complete periodontalexamination, oral hygiene instruction, and multiple scal-ing and root planing sessions. Six to 8 weeks after thecompletion of the hygienic phase (baseline), when thepatients demonstrated an acceptable oral hygiene stan-dard, the following parameters were evaluated: plaqueand gingival indexes; gingival recession (GR) measuredas the distance between the cemento-enamel junction(CEJ) and the most apical point of the gingival marginof the buccal surface of the tooth; probing depth (PD);clinical attachment level (CAL); gingival thickness (GT);and width of keratinized tissue (KT) measured from themost apical point of the gingival margin to the mucogin-gival junction. Probing depth was obtained using anautomated probe.‡ In addition, pre- and post-surgical GT

were obtained in a mid-buccal location approximately2 mm apical to the gingival margin as follows: a #15endodontic reamer was pierced, perpendicular to themucosal surface, through the soft tissue with light pres-sure until a hard surface was felt; a silicone disk stopwas placed in tight contact with the soft tissue surfaceand stabilized by a drop of an adhesive; penetrationdepth was then obtained with a digital caliper to thenearest 0.1 mm. All the clinical parameters wereobtained immediately before (baseline) and 30, 60, 90,and 120 days after surgery.

Surgical ProcedureImmediately after the baseline evaluation, the surgicalprocedure was performed. Only one operator, maskedto the smoking status of the patient, performed all surg-ical procedures. Following local anesthesia (2% lidocainewith epinephrine 1:100,000), an intracrevicular incisionand two vertical incisions (with a trapezoidal form) weremade. About 3 to 5 mm beyond the mucogingival junc-tion, the full-thickness flap was continued as a partial-thickness flap to enable coronal elongation of the flap.

After flap incisions and preparations, the papillae,mesial and distal to the recession defects, were de-epithelialized. Following flap elevation, the exposed rootsurface was gently scaled and planed with sharp curets.Donor connective tissue was obtained from the palateusing a technique previously described.6 The epithelialband of the graft was removed and only the connectivetissue was used. The tissue obtained was immediatelypositioned on the root surface, and graft stability wasachieved by two inter-proximal resorbable 4-0 sutures.§

The flap was then coronally positioned covering thegraft and sutured in position by interrupted sutures§

with special care to avoid excessive flap tension.

Postoperative CarePostoperative care consisted of a 0.12% chlorhexidinemouth rinse twice a day for 8 days without mechanicalcleaning at the surgical areas. Acetaminophen was pre-scribed for pain control. Silk ligatures were removed8 days after the surgery, and chlorhexidine 0.12% wasapplied locally over the surgical sites with a cotton swabtwice a day for 1 month. This healing phase was sup-plemented by professional plaque control every 2 weeksfor the first 2 months after surgery. After 30 days,patients re-established mechanical plaque control.

Statistical AnalysisIn order to test whether the experimental groups wereinitially balanced regarding all the parameters evaluated,an intergroup analysis was performed using the Studentt test (alpha = 0.05). At the end of the experimentalperiod (120 days), an intragroup analysis (paired t test;alpha = 0.05) was performed to test the hypothesis

‡ Florida Probe, Gainesville, FL.§ Vicryl, Ethicon Inc., Somerville, NJ.

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that the surgical procedure did not improve any of theindividual parameters (baseline versus day 120); sec-ondly, the Student t test (intergroup analysis) was usedto test the hypothesis that there were no differencesbetween the groups regarding the surgical outcome (atday 120, smokers versus non-smokers). Finally, to testthe hypothesis that there were no differences betweenboth groups regarding the percentage of root coverageand gingival and plaque indexes, an intergroup analysiswas carried out using the Mann Whitney test (alpha =0.05). In the present study, the 15 patients were con-sidered the unit of analysis in all of the analyses describedabove.

RESULTSBaseline dimensions of the defects were similar in bothgroups (Fig. 1). There were no statistical differencesbetween the two groups regarding extent of recession

(3.66 ± 0.67 mm and 3.73 ± 0.77 mm, fornon-smokers and smokers, respectively; P =0.85), probing depth (1.48 ± 0.69 mm and1.7 ± 0.47 mm, for non-smokers and smok-ers, respectively; P = 0.45); keratinized tis-sue width (2.70 ± 1.06 mm and 3.56 ± 1.21mm, for non-smokers and smokers, respec-tively, P = 0.12); clinical attachment level(5.14 ± 1.06 mm and 5.55 ± 0.91 mm, fornon-smokers and smokers, respectively, P= 0.39); and gingival thickness (1.14 ± 0.38mm and 1.25 ± 0.56 mm, for non-smokersand smokers, respectively, P = 0.63). In addi-tion, smokers and non-smokers presentedsimilar plaque and gingival indexes (P>0.05). Four months after surgery, intra-group analysis demonstrated that bothgroups presented a significant reduction inGR, increase in KT width and GT, and gainin CAL (P <0.05). However, KT width in

smokers and PD in non-smokers did not show any sig-nificant change (P >0.05).

Although both groups demonstrated improvementsafter surgery with respect to most of the evaluatedparameters, intergroup analysis showed that smokerspresented deeper PD (2.35 ± 0.67 mm versus 1.56 ±0.53 mm), lower percentage of root coverage (58.84%± 13.68% versus 74.73% ± 14.72%), and less CAL gainthan non-smokers (2.00 ± 1.04 mm versus 2.54 ± 0.79mm) (Figs. 1 and 2, P <0.05). Moreover, 4 monthsafter CTG surgery, smokers presented more KT com-pared to non-smokers (4.50 ± 1.16 mm versus 3.30± 0.86 mm) (P <0.05). No difference was noted regard-ing GT between both groups (1.75 ± 0.41 mm and 1.86± 0.54 mm smokers and non-smokers, respectively)(Fig. 1, P >0.05). Figures 2 through 4 illustrate CALgain, GT, and GR over time. Figure 5 illustrates typi-

Figure 1.Initial (day 0) and final (day 120) clinical conditions of smokers and non-smokers.*Intergroup analysis at 120 days, P <0.05. †Intragroup analysis, P <0.05.

Figure 2.Clinical attachment gain in both groups from day 0 to day 120.

Figure 3.Gingival thickness in both groups from day 0 to day 120.

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Figure 4.Gingival recession extension (from CEJ to most apical point of the gingival margin of the buccal surface of the tooth) in bothgroups from day 0 to day 120.

cal pre- and post-surgery cases in a non-smoker (Aand B) and smoker (C and D).

DISCUSSIONThe results of the present prospective clinical studydemonstrated that connective tissue grafts might pro-vide benefits for smokers and non-smokers, improvinggingival recession, keratinized tissue width, gingival thick-ness, and clinical attachment level. However, as previ-ously reported with respect to other periodontal therapymodalities,14-19,21 cigarette consumption significantlyaffected therapy outcome in the present investigation.Smokers presented a lower percentage of root coverage,less CAL gain, and deeper PD than non-smokers.

The mean root coverage obtained in the present studywas 58.84% and 74.73% for smokers and non-smokers,respectively. With regard to non-smokers, the percent-age of root coverage reported here compare well withthose of others. Bouchard et al.11 suggested a mean rootcoverage of 70% to 80%, and Wennström10 reported anaverage mean root coverage of 89.3%. On the otherhand, Harris22 reported mean root coverage of 97.1%,which is higher than in the present study. Complete root

Figure 5.First upper molar in a non-smoker at baseline (A) and day 120 (B). Upper canine in a smoker at baseline (C) and day 120 (D).

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coverage was found in 35% of the non-smoker cases,which is close to that reported by Bouchard et al.11 (50%)and within the range reported by Wennström10 (20% to89%). There are no studies on the predictability of CTGfor gingival recession treatment in smokers and just a fewstudies on the impact of smoking on the treatment out-come of gingival recessions.19,23 A healing response insmokers was also reported by Trombelli and Scabbia,19

who reported a percentage of root coverage very closeto that of the present study (57% versus 58.84%, in ourstudy). Trombelli and Scabbia,19 however, treated thedefects using guided tissue regeneration. In addition,using free gingival grafts, Miller23 reported 100% corre-lation between failure to obtain root coverage and heavysmoking. Thus, these findings together indicate that cig-arette consumption should be carefully considered whileplanning periodontal plastic procedures.

It is difficult to discuss contraindications for rootcoverage procedures, since the line between indicationsand contraindications is poorly delineated. However,smoking may be a major risk factor that contributesto the failure of some mucogingival surgical proce-dures. The precise mechanisms by which tobaccosmoke interferes with healing are not completelyunderstood, mainly due to the fact that there are thou-sands of toxins in tobacco smoke and most have notbeen evaluated for their effect on periodontal healing.It seems more likely that smoking has a primarily sys-temic influence by altering the host response and/ordamaging the periodontal cells.24,25 Nicotine has alsobeen shown to affect in vitro gingival fibroblast prolif-eration and increase collagenase activity,26 and inhibitfibroblast synthesis of fibronectin and type I collagen.27

Moreover, impaired oxygen transport and metabolismcaused by carbon monoxide, as well as enzyme poi-soning by hydrogen cyanide, further reduce the oxida-tive metabolism needed for cellular repair.28

In the present study, a very interesting scenario isobserved over time (Figs. 2 through 4). Our findingsseem to support those of others suggesting that creep-ing attachment occurs when autogenous soft tissuegrafts are used. The mean change in gingival reces-sion between 1 and 4 months after surgery was 0.10mm and 0.15 mm for smokers and non-smokers,respectively. Moreover, gingival thickness achievedsoon after surgery (30 days) presents a tendency todecrease over time, with values from 2.27 to 1.75 mmand 2.23 and 1.86 mm at 30 and 120 days aftersurgery for smokers and non-smokers, respectively.Finally, both smokers and non-smokers demonstratedan increase in clinical attachment level gain from theinitial post-surgery evaluation to the final one.

Poor oral hygiene has been associated with smoking.29

In the present study, oral hygiene standards were keptsimilarly high throughout the observation period in bothsmokers and non-smokers. Therefore, the observed

differences in healing between smokers and non-smokers during the tissue maturation phase cannot beattributed to differences in supragingival plaque level.

Within the limits of the present investigation, it canbe assumed that connective tissue grafts might providebenefits for smokers and non-smokers; however, ciga-rette consumption may represent a challenge for peri-odontal plastic surgery. Future areas for investigationby our group include long-term analyses of the stabilityof the tissues.

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Lindhe J, Karring T, Lang NP, eds. Clinical Periodontol-ogy and Implant Dentistry. Copenhagen: Munksgaard;1997:569-591.

2. Bernimoulin JP, Luscher B, Muhlemann HR. Coronallyrepositioned periodontal flap. Clinical evaluation after1 year. J Clin Periodontol 1975;2:1-13.

3. Guinard EA, Caffesse RG. Treatment of localized gingivalrecessions. Part I. Lateral sliding flap. J Periodontol 1978;49:351-356.

4. Caffesse RG, Guinard EA. Treatment of localized gingi-val recessions. Part II. Coronally repositioned flap witha free gingival graft. J Periodontol 1978;49:357-361.

5. Raetzke PB. Covering localized areas of root exposureemploying the “envelope” technique. J Periodontol 1985;56:397-402.

6. Langer B, Langer L. Subepithelial connective tissue grafttechnique for root coverage. J Periodontol 1985;56:715-720.

7. Nelson S. The subpedicle connective tissue graft tech-nique for root coverage. J Periodontol 1987;58:95-102.

8. Allen A. Use of supraperiosteal envelope in soft tissuegrafting for root coverage. I. Rationale and technique. IntJ Periodontics Restorative Dent 1994;14:217-227.

9. Allen A. Use of supraperiosteal envelope in soft tissuegrafting for root coverage. II. Clinical results. Int J Periodon-tics Restorative Dent 1994;14:302-315.

10. Wennström J. Mucogingival therapy. Ann Periodontol1996;1:671-701.

11. Bouchard P, Malet J, Borghetti A. Decision-making inaesthetics: Root coverage revisited. Periodontol 20002001;27:97-120.

12. Genco RJ. Current view of risk factors for periodontaldisease. J Periodontol 1996;67:1041-1049.

13. Tonetti MS. Cigarette smoking and periodontal disease:Etiology and management of disease. Ann Periodontol1998;3:88-101.

14. Grossi SG, Skrepcinski FB, DeCaro T, Zambon JJ,Cummins D, Genco RJ. Response to periodontal therapy indiabetes and smokers. J Periodontol 1996;67:1094-1102.

15. Kinane DF, Radvar M. The effect of smoking on mechan-ical and antimicrobial therapy. J Periodontol 1997;68:467-472.

16. Preber H, Bergstrom J. Effect of cigarette smoking onperiodontal healing following surgical therapy. J ClinPeriodontol 1990;17:324-328.

17. Kaldahl WB, Johnson GK, Patil KD, Kalkwarf KL. Levelsof cigarette consumption and response to periodontaltherapy. J Periodontol 1996;67:675-681.

18. Trombelli L, Kim CK, Zimmerman GJ, Wikesjö UME. Retro-spective analysis of factors related to clinical outcome ofguided tissue regeneration procedures in intrabony defects.

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J Clin Periodontol 1997;24:366-371.19. Trombelli L, Scabbia A. Healing response of gingival reces-

sion defects following guided tissue regeneration proce-dures in smokers and non-smokers. J Clin Periodontol1997;24:529-533.

20. Miller PD. A classification of marginal tissue recession.Int J Periodontics Restorative Dent 1985;5(2):8-13.

21. Scabbia A, Cho K-S, Sigurdsson TJ, Kim C-K, Trombelli L.Cigarette smoking negatively affects healing responsefollowing flap debridement surgery. J Periodontol 2001;72:43-49.

22. Harris RJ. Root coverage with connective tissue grafts: Anevaluation of short- and long-term results. J Periodontol2002;73:1054-1059.

23. Miller PD. Root coverage with free gingival graft. Factorsassociated with incomplete root coverage. J Periodontol1987;58:674-681.

24. Bennet KR, Read PC. Salivary immunoglobulin A levelsin normal subjects, tobacco smokers, and patients withminor aphthous ulceration. Oral Surg Oral Med Oral Pathol1982;53:461-465.

25. Selby C, Drost E, Brown D, Howie S, MacNee W. Inhibitionof neutrophil adherence and movement by acute cigarettesmoke exposure. Exp Lung Res 1992;18:813-827.

26. Peacock ME, Sutherland DE, Schuster GS, et al. Theeffect of nicotine on reproduction and attachment ofhuman gingival fibroblasts in vitro. J Periodontol 1993;64:658-665.

27. Tipton DA, Dabbous MK. Effects of nicotine on prolifera-tion and extracellular matrix production of human gingi-val fibroblasts in vitro. J Periodontol 1995;66:1056-1064.

28. Hanes PJ, Schuster GS, Lubas S. Binding, uptake, andrelease of nicotine by human gingival fibroblasts. J Peri-odontol 1991;62:147-152.

29. Taani DS. Association between cigarette smoking andperiodontal health. Quintessence Int 1997;28:535-539.

Correspondence: Dr. Francisco H. Nociti Jr., Av. Limeira 901,Caixa Postal: 052, CEP: 13414-903, Piracicaba, SP, Brazil.Fax: 55-19-3412-5218; e-mail: nociti@fop.unicamp.br.

Accepted for publication August 20, 2003.

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