The influence of tobacco smoking on the outcomes achieved by root- coverage procedures

7/24/2019 The influence of tobacco smoking on the outcomes achieved by rootcoverage procedures

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294 JADA, Vol. 140 http://jada.ada.org March 2009

F

requently, the oral expo-sure of the root surface dueto a displacement of thegingival margin apical tothe cementoenamel junc-

tion (that is, gingival recession)

leads to tactile and thermal dentalhypersensitivity, root abrasion anddeterioration in the smiles esthetics.1

In such conditions, periodontal treat-ment itself is designed to stop theprogression of recession and to re-establish a condition of health, func-tion and esthetics through the use ofclinically predictable procedures.

With respect to the coverage ofdenuded root surfaces, researchersin several trials have described

attempts to treat recession-typedefects through the use of diversesurgical techniques such as later-ally repositioned flaps,2-4 coronallyadvanced flaps,5,6 free gingivalgrafts,7,8 subepithelial connective-tissue grafts,1,9-13 acellular dermalmatrix allografts14,15 and guidedtissue regeneration.16-19 These perio-dontal plastic surgery proceduresare indicated1-19 for the treatment ofMiller20 Class I and Class II reces-sions. Additionally, investigators in

systematic reviews evaluating dif-ferent periodontal plastic surgeryprocedures have demonstrated thatsuch techniques are effective inreducing the extent of exposed rootsurface, with a concomitant gain inclinical attachment level (CAL)21-24

and in the width of keratinizedtissue (KT).21,22 On the other hand, it

Dr. Leandro Chambrone is a didactic trainer, Division of Periodontics, Department of Stomatology,

School of Dentistry, University of So Paulo, Av. Prof. Lineu Prestes, 2227 Cidade Universitria, 05508-

000, So Paulo SP, Brazil, e-mail [email protected]. Address reprint requests to Dr. Chambrone.

Dr. Daniela Chambrone is an assistant professor, Discipline of Periodontics, Faculty of Dentistry,

Methodist University of So Paulo, So Bernardo do Campo, Brazil.

Dr. Pustiglioni is a professor and chair, Division of Periodontics, Department of Stomatology, School of

Dentistry, University of Sao Paulo, So Paulo, Brazil.

Dr. Luiz Armando Chambrone is a professor and chair, Discipline of Periodontics, Faculty of Dentistry,

Methodist University of So Paulo, So Bernardo do Campo, Brazil.

Dr. Lima is an associate professor, Division of Periodontics, Department of Stomatology, School of

Dentistry, University of So Paulo, So Paulo, Brazil.

The influence of tobacco smokingon the outcomes achieved by root-

coverage proceduresA systematic reviewLeandro Chambrone, MSD, DDS; Daniela Chambrone, PhD, MSD, DDS; Francisco E. Pustiglioni,PhD, MSD, DDS; Luiz Armando Chambrone, PhD, MSD, DDS; Luiz A. Lima, PhD, MSD, DDS

Background. The authors conducted a system-

atic review to evaluate the effect of smoking on the

clinical outcomes achieved by periodontal plastic

surgery procedures in the treatment of recession-type defects.

Types of Studies Reviewed. The authors per-

formed an electronic search on MEDLINE, EMBASE and the Cochrane

Central Register of Controlled Trials (CENTRAL) for randomized con-

trolled clinical trials, controlled clinical trials and case series that

involved at least six months follow-up. They looked for studies published

through June 2008 that compared the outcome measures achieved by

smokers and nonsmokers after they underwent periodontal plastic

surgery procedures for treatment of gingival recession.

Results. From a total of 632 references, the authors considered seven

studies to be relevant. The meta-analysis indicated a statistically signifi-

cant greater reduction in gingival recession (P < .001) and gain in clinical

attachment level (P < .001) for nonsmokers when compared with smokerswhose gingival recession was treated with subepithelial connective-tissue

grafts. Additionally, nonsmokers exhibited significantly more sites with

complete root coverage than did smokers (P = .001). For coronally

advanced flaps, differences between the groups were not significant.

Clinical Implications. The results of this review show that smoking

may negatively influence gingival recession reduction and clinical attach-

ment level gain. Additionally, smokers may exhibit fewer sites with com-

plete root coverage.

Key Words. Gingival recession; gingival recession/surgery; root cov-

erage; systematic review; smoking.

JADA 2009;140(3):294-306.

ABSTRACT

ARTICLE

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Copyright 2009 American Dental Association. All rights reserved. Reprinted by permission.


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JADA, Vol. 140 http://jada.ada.org March 2009 295

is difficult to predict accurately an individualtooths clinical response to treatment over time,especially if the patient is exposed to one or morerisk factors known to influence host response.25,26

With respect to tobacco smoking, evidence isbuilding that smoking may negatively affect the

results achieved through periodontal plasticsurgery procedures. Tobacco smoking is a recog-nized risk factor that affects the oral environmentand ecology, vascularization of the gingival tis-sues, immune and inflammatory responses andthe healing potential of the periodontal connec-tive tissues.27 Smokers are two to eight timesmore susceptible to periodontal disease than arenonsmokers.28 Moreover, researchers have identi-fied tobacco smoking as producing a negativeeffect on periodontal therapy, nonsurgical andsurgical alike.29-31 Moreover, smokers are moresusceptible to needing periodontally related tooth

extractions during maintenance care after under-going periodontal treatment.25,26

Even though previous systematic reviews21-24

provided some information of interest aboutsmoking, the majority of trials included in thesereviews did not include smokers, and the authorsof these reviews did not delineate inclusion cri-teria in such a way as to warrant inclusion of allstudies that have estimated the impact ofsmoking on clinical outcome measures.21-24 Todate, to our knowledge, no investigators havedesigned a systematic review that compares the

effect of treatment of gingival recession insmokers and nonsmokers. Therefore, our objectivein performing a systematic review was to eval-uate the effect of tobacco smoking on clinical out-comes achieved by periodontal plastic surgeryprocedures in the treatment of recession-typedefects. The research question on which wefocused for this systematic review was Doestobacco smoking influence the outcome measuresachieved by root-coverage procedures?

MATERIALS AND METHODS

Study selection, inclusion criteria and types

of interventions. We undertook a systematicreview of randomized controlled clinical trials,controlled clinical trials and case series with afollow-up period of at least six months. Owing tothe limited number of randomized controlled clin-ical trials available in previous reviewsthat is,trials comparing data from smokers and non-smokers21-24as well as the impossibility of ran-domization in studies in which only one surgical

procedure was tested, we included all levels ofevidence in the review. We considered studies forinclusion if they involved the following:

drecession areas selected for treatment classi-fied as Miller20 Class I or II that were treated sur-gically by means of periodontal plastic surgery

procedures (such as acellular dermal matrixallografts, coronally advanced flaps, free gingivalgrafts, guided tissue regeneration and subepithe-lial connective-tissue grafts);

doutcome measures from smokers and non-smokers, recorded separately;

dsubjects 18 years or older.In addition, we considered subjects to be

smokers if they smoked 10 cigarettes or more perday at the time of the baseline examination.

Outcome measures. Outcome measures werereported in terms of changes from baseline toeach follow-up period. The following outcome

measures were reported:dchange in gingival recession (GR);

dchange in CAL;

dchange in KT;

dpercentage of sites exhibiting complete rootcoverage;dmean root coverage.

Search strategy. To streamline the identifica-tion of studies included in or considered for thisreview, we developed detailed search strategiesfor each database we searched that were based onthe strategy described below for searching the

Cochrane Central Register of Controlled Trials(CENTRAL). We adopted a similar searchstrategy as reported by a recent Cochrane reviewregarding the effectiveness of different root-coverage procedures in the treatment ofrecession-type defects.22 We searched databasesfor articles published through June 2008,including papers and abstracts published inEnglish-language journals. We searched MEDLINE,EMBASE, CENTRAL and the Cochrane OralHealth Groups Specialized Register databases.The search strategy we applied was as follows:(gingival recession OR ((recession NEAR gingiva*)

ABBREVIATION KEY. CAF: Coronally advanced flap.CAL: Clinical attachment level. CENTRAL: CochraneCentral Register of Controlled Trials. GR: Gingivalrecession. KT: Keratinized tissue. MRC: Mean rootcoverage. NR: Not reported. PCRC: Percentage of com-plete root coverage. SCRC: Sites exhibiting completeroot coverage. SCTG: Subepithelial connective-tissuegraft.



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OR (recession NEAR defect*) OR recession-typedefect*) OR ((exposure NEAR root*) OR (exposedNEAR root*)) OR (gingiva* NEAR defect*), ORdenude* NEAR root surface* AND GUIDEDTISSUE REGENERATION OR tissue NEARregenerat* OR ((gingiva* NEAR esthetic*) OR

(gingiva* NEAR aesthetic*)) OR periodont*) AND(plastic surgery OR soft tissue graft* ORcoronally advanced flap* OR laterally posi-tioned flap* OR laterally-positioned flap* ORconnective tissue graft* OR connective-tissuegraft*, OR gingiva* NEAR transplant* ORdermal matrix NEAR graft* OR enamel matrixprotein). We conducted hand searching in severalpublications: Journal of Periodontology, Journal ofClinical Periodontology and International Journalof Periodontics and Restorative Dentistry.

Validity assessment and data extraction.Two reviewers (L.C. and D.C.) independently

screened titles, abstracts and full texts of thesearch results. They obtained full reports for allstudies appearing to meet the inclusion criteria orin instances in which there was insufficient infor-mation from the title, key words and abstract tomake a clear decision. The reviewers assessedagreement between them by means of calculating scores. They resolved disagreement regardinginclusion by discussing the issue with anotherreviewer (L.A.C.). They contacted authors whennecessary for clarification of data or to obtainmissing data. They excluded data in cases in

which they did not reach agreement.The reviewers extracted data regarding the fol-lowing issues:

dcitation, publication status and year ofpublication;

dlocation of trial;

dstudy design (randomized controlled clinicaltrial, controlled clinical trial and case series);dcharacteristics of participants;

dcharacteristics of interventions;

dmethodological quality of trials.Quality assessment. The two reviewers (L.C.

and D.C.) assessed the methodological quality of

the included studies by focusing on the followingissues: method of randomization and allocationconcealment (exclusively for randomized trials),blindness of examiners and completeness of thefollow-up period.

Data synthesis. We collated data into evi-dence tables and grouped them according to typeof intervention and type of study. We performed adescriptive summary to determine the quantity of

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data, checking further for variations in terms ofstudy characteristics and results. In cases in whicha trials original design did not explore differencesbetween smokers and nonsmokers, yet the studysresults included individual patient data (baselineand final measurements), we used the nonpara-

metric Mann-Whitney Utest to evaluate thestudys outcomes according to smoking status.

We used random-effects meta-analysesthroughout. For continuous data, we expressedpooled outcomes as weighted mean differenceswith their associated 95 percent confidenceinterval (CIs). For dichotomous data, these werepredominantly pooled risk ratios and associated95 percent CIs. We calculated risk difference andnumber needed to treat for sites exhibiting com-plete root coverage for which the studys resultsreached a level ofP < .05. We assessed statisticalheterogeneity by calculating 2. We performed

analyses using Review Manager (RevMan) statis-tical analysis software (Version 5.0, The NordicCochrane Centre, The Cochrane Collboration,Copenhagen, Denmark). We conducted varianceimputation methods to estimate appropriate vari-ance estimates in cases in which a trial did notinclude the appropriate standard deviation of thedifferences.32,33 During the conduction of meta-analysis, we pooled data from trials reportingresults from different periods of follow-upaccording to the longest follow-up period. Addi-tionally, we assessed the significance of discrepan-

cies in the estimates of the treatment effects fromthe different trials by means of the Cochran Q testfor heterogeneity and the I2 statistic.

RESULTS

Results of the search. Our initial searchresulted in the identification of 632 articles. Sub-sequently, we excluded 535 of them on the basisof title and abstract and screened the full text of97 studies that we considered to be potentiallyrelevant for this review. Of these, we excluded 87articles during full-text screening because theydid not provide individual patient data (which

would allow for the extraction of data from bothgroups separately) or comparisons betweensmokers and nonsmokers5,13-16,18,34-114; in addition,we excluded two articles because they involved afollow-up period of less than six months115,116 andone article because we considered it a duplicatereport.117 The scores between examiners were> 0.75, indicating a good level of agreement.

By the end of the search phase, we considered



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TABLE 1

Characteristics of included studies.STUDY METHODS SUBJECTS INTERVENTIONS

AND NO. OFPATIENTS

TREATED PERGROUP

OUTCOMES SITE AND FUNDING

Andia andColleagues118

(2008)

Controlled clinicaltrial, parallel design,one treatmentgroup, 24 monthsduration

22 subjects, aged 27-55years, with at least oneMiller Class I or IIbuccal gingival reces-sion of at least 3 mil-limeters; no subjectwas excluded from thestudy

Subepithelial connec-tive-tissue graft(SCTG) 11 nonsmokers 11 smokers ( 20cigarettes per dayfor a minimum offive years)

Change in gingivalrecession (GR)Change in clinicalattachment level (CAL)Sites with completeroot coveragePercentage of completeroot coverageMean root coverage(as determined viaautomated controlledforce probe)

University-based andsupported by theNational Council forScientific and Tech-nological Develop-ment, Brazil

Erley andColleagues119

(2006)

Controlled clinicaltrial, parallel design,one treatmentgroup, six monthsduration

17 subjects, onefemale, aged 27-45years, with at least oneMiller Class I or IIbuccal gingival reces-

sion of at least 2 mm(22 recession defects);no subject wasexcluded from thestudy

SCTG Nine nonsmokers,10 sites Eight smokers, 12sites 10 cigarettes

per day (as verifiedby a salivary cotininetest)

Change in GRChange in CALChange in keratinizedtissue (KT)Sites with complete

root coveragePercentage of completeroot coverageMean root coverage (asdetermined via manualprobe)

Hospital-based andfunded by ClinicalInvestigation Depart-ment, Fort Gordon,Army Dental Corps,

and the Fort GordonDental Activity, FortGordon, Ga.

Pini Prato andColleagues6

(2005)

Case series, onetreatment group, sixmonths duration

60 subjects, with oneMiller Class I buccalgingival recession of atleast 2 mm (individualpatient data availablefor analysis); no sub-

ject was excluded fromthe study

Coronally advancedflap (CAF) 49 nonsmokers 11 smokers ( 10cigarettes per day)

Change in GRChange in CALChange in KTSites with completeroot coveragePercentage of completeroot coverageMean root coverage (asdetermined via manualprobe)

Practice-based

Silva andColleagues121

(2007)

Controlled clinicaltrial, parallel design,one treatmentgroup, 24 monthsduration (exami-nations at six, 12and 24 months afterprocedure)

20 subjects, ninefemale, aged 22-53years, with one havingMiller Class I buccalgingival recession (2 to3 mm in depth); nosubject was excludedfrom the study

CAF 10 nonsmokers 10 smokers ( 10cigarettes per dayfor a minimum offive years)

Change in GRChange in CALChange in KTSites with completeroot coveragePercentage of completeroot coverageMean root coverage (asdetermined via auto-mated controlled forceprobe)

University-based

Souza andColleagues122

(2008)

Controlled clinicaltrial, parallel design,one treatmentgroup, six monthsduration

30 subjects, 10female, aged 24-47years, with one MillerClass I or II buccal gin-gival recession of atleast 3 mm; no subjectwas excluded from thestudy

SCTG 15 nonsmokers 15 smokers ( 10cigarettes per dayfor a minimum offive years)

Change in GRChange in CALChange in KTSites with completeroot coveragePercentage of completeroot coverageMean root coverage (asdetermined via auto-

mated controlled forceprobe and manualprobe)

University-based andsupported by theNational Council forScientific and Tech-nological Develop-ment, Brazil

Trombelli andScabbia19

(1997)

Case series, paralleldesign, one treat-ment group, sixmonths duration

22 subjects, 12female, aged 23-57years, with one MillerClass I or II buccal gin-gival recession of atleast 4 mm; no subjectwas excluded from thestudy

Guided tissue regen-eration nonre-sorbable membrane 13 nonsmokers Nine smokers ( 10cigarettes per day)

Change in GRChange in CALChange in KTMean root coverage (asdetermined via manualprobe)

Practice-based



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seven articles eligible; their data are the basis ofthis review (Table 1).6,19, 118-122 However, data fromone study were reported in two articles accordingto the follow-up period (short term and longterm).120,121 Therefore, we cited the article with theshorter follow-up period120 and the articledescribing the longer follow-up period under the

one study name.121

Figure 1 is a flow chart ofstudies assessed and excluded at various stages ofthe review.

Characteristics of the included studies. Ofthe six included studies, we categorized four ascontrolled clinical trials118,119,121,122 and two as caseseries.6,19 Four trials had been conducted at uni-versity dental clinics.118,119,121,122 Three studies hadbeen performed in Brazil,118,121,122 two in Italy6,19

and one in the UnitedStates.119 In total,64 smokers and 107 non-smokers received treatmentand three types of perio-dontal plastic surgery pro-

cedures were evaluated(coronally advanced flaps,guided tissue regenerationand subepithelialconnective-tissue grafts).

Quality assessment ofincluded studies. Exam-iner blinding was evident inthree trials,119,121,122 while inthe remaining articles itwas unclear or not stated.

Also, we noted a clearaccounting of participants in

all studies (Table 1).Outcomes measures.

Researchers observedchanges in GR depth, CALand KT during the course ofeach study. Most of theinvestigators reported a sta-tistically significant reduc-tion in initial recessionmeans, with a concomitantgain in CAL19,118,119,121,122 andKT19,119,122 for smokers and

nonsmokers.With respect to inter-group comparisons (smokersversus nonsmokers), re-searchers in five trialsreported statistically signifi-

cant superior recession reduction19,118,119,121,122 andCAL gain for nonsmokers118,121,122 when comparedwith smokers (Table 2).

In one study designed to evaluate the postsur-gical position of the gingival margin, examiningthe individual patient data from 11 smokers and49 nonsmokers allowed us to perform intergroup

comparisons.6

Within groups, we found statisti-cally significant changes from baseline to the six-month evaluation for GR, CAL and KT. Between-groups analyses by Mann-Whitney Utest showedno statistically significant differences in the meanpostoperative recession depth (P = .75), CAL(P = .90) and width of KT (P = .10).6

In addition, we performed two sets of interstudycomparisonsa total of eight meta-analyses, four

Potentially relevant articles identifiedand screened for retrieval from CENTRAL,

MEDLINE and EMBASE (n = 631)and hand searching (n = 1)

Articles excluded on basis of titleand abstract (n = 535)

Full-text articles screened to identify potentiallyrelevant studies for review (n = 97)

Excluded articles that did not fulfillinclusion criteria (n = 90)

Articles initially included in the review (n = 7)BUT

one controlled clinical trial was reportedin two articles

SOin total, 6 articles included in review

Articles included in meta-analyses (n = 5)

Articles not included in meta-analyses(n = 1)

Figure 1. Flow chart of manuscripts screened through the review process. CENTRAL: CochraneCentral Register of Controlled Trials.



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comparing outcomes for subepithelial connective-tissue graft procedures and four comparing out-comes for coronally advanced flapsfor changesin GR, CAL and KT and for the number of sites

exhibiting complete root coverage (Table 3). Forsubepithelial connective-tissue grafts, the resultsindicated a statistically significant greater reduc-tion in GR, with the weighted mean difference0.78 mm (95 percent CI, 1.06 to 0.51) (Figure2) and significant CAL gain, with the weightedmean difference 0.75 mm (95 percent CI, 1.13 to0.38) (Figure 3, page 301) for nonsmokers, whencompared with smokers, whereas the width of KT

differences between smokers and nonsmokers wasnot significant (P = .97). For coronally advancedflaps, we found that the differences in GR reduc-tion and gains in CAL and KT between smokers

and nonsmokers were not significant.Complete root coverage and mean root

coverage. The percentages of complete root cov-erage and mean root coverage showed markedvariation. Subepithelial connective-tissue graftsresulted in 27.0 to 80.0 percent complete root cov-erage for nonsmokers and 0 to 25.0 percent forsmokers. Similarly, coronally advanced flapsresulted in 20.0 to 55.1 percent complete root cov-

TABLE 2

Outcome measures from included studies.

STUDY ANDSUBJECTS,ACCORDING TOSMOKING STATUS

INTERVENTIONTYPE AND

FOLLOW-UPPERIOD

OUTCOME MEASURE

Change inRecession

Depth

(mean SD)(mm*)

Change inClinical Attach-

ment Level

(mean SD)(mm)

Change inKeratinized

Tissue

(mean SD)(mm)

SCRC

(n/N)PCRC

(%)MRC

(%)

Andia andColleagues118

(2008)

Subepithelialconnective-tissuegraft (SCTG)

Nonsmokers 24 months 2.80 + 0.56# 2.40 + 0.81# NR** 3/11 27.0 77.8

Smokers 24 months 1.80 + 0.50 1.60 + 0.81 NR 0/11 0 50.0

Erley andColleagues119 (2006)

SCTG

Nonsmokers 6 months 3.00 + 0.42# 3.43 + 0.50 2.80 + 1.48 8/10 80.0 98.3

Smokers 6 months 2.33 + 0.92 2.69 + 0.82 2.08 + 1.44 3/12 25.0 82.3

Pini Prato andColleagues6 (2005)

Coronally advancedflap (CAF)

Nonsmokers 6 months 2.81 + 1.02 3.62 + 3.30 0.44 + 0.62 27/49 55.1 89.8

Smokers 6 months 3.13 + 0.92 3.18 + 1.15 0.09 + 0.53 6/11 54.5 89.6

Silva andColleagues121 (2007)

CAF


12 months 2.20 + 0.48# 2.16 + 0.55 0.02 + 0.55 4/10 40.0 85.4

24 months 2.04 + 0.47# 1.98 + 0.58 0.14 + 0.58 2/10 20.0 78.7

Smokers 6 months 1.90 + 0.45 2.44 + 0.82 0.72 + 0.98 0/10 0 69.3

12 months 1.64 + 0.51 2.22 + 0.81# 0.76 + 0.98 0/10 0 60.6

24 months 1.46 + 0.50 2.02 + 0.82# 0.88 + 0.98 0/10 0 53.9

Souza andColleagues122 (2008)

SCTG

Nonsmokers 6 months 2.63 + 0.92# 2.15 + 1.08# 0.95 + 0.77 8/15 53.3 83.3

Smokers 6 months 1.99 + 0.68 1.44 +1.08 1.33 + 0.50 1/15 6.7 58.0

Trombelli andScabbia (1997)19

Guided tissueregeneration


Smokers 6 months 2.50 + 1.20 2.70 + 1.40 1.20 + 0.80 1/9 11.1 57.0

* mm: Millimeters. SCRC: Sites exhibiting complete root coverage. PCRC: Percentage of complete root coverage. MRC: Mean root coverage. Significant difference within group.# Significant difference between groups.

** NR: Not reported.



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erage for nonsmokers and 0 to 54.5 percent forsmokers (Table 2). For guided tissue regenera-tion, complete root coverage was 38.5 percent fornonsmokers and 11.1 percent for smokers.

Between smokers and nonsmokers who receivedsubepithelial connective-tissue grafts, non-smokers achieved more complete root coverage.They showed a significant difference in thenumber of sites with complete root coverage whencompared with smokers (risk ratio, 0.24; 95 per-cent CI, 0.10 to 0.58) in the two arms of the trials(Figure 4). Moreover, we observed little evidenceof heterogeneity (2 for heterogeneity = 0.92,

df= 2,P = .63, I2 = 0 percent). In addition, we cal-culated the risk difference (that is, the differencebetween the proportions of subjects exhibitingcomplete root coverage in the two groups) and

number needed to treat for this comparison; theresults were 0.41 (95 percent CI, 0.59 to 0.24;

P < .001) and 3.00, respectively.

DISCUSSION

In this review, we explored the literatureregarding the potential effect of smoking on theresults achieved by periodontal plastic surgeryprocedures, with the aim of evaluating differences

Figure 2. Forest plot of random effects meta-analysis evaluating the difference in gingival recession change between smokers andnonsmokers after treatment with subepithelial connective-tissue graft. IV: Inverse variance. CI: Confidence interval. : Kendall tau. z: z test.

TABLE 3

Summary of meta-analyses.

TREATMENTCOMPARED

STUDY OUTCOME STATISTICALMETHOD

EFFECT SIZEIN mm*(95% CI)

PVALUE HETEROGENEITY I2

(%)2 PValue

Coronally

AdvancedFlap

Pini Prato and

colleagues6

(2005), Silvaand

colleagues 121

(2007)

Change in gingival

recession

WMD 95% CI 0.09 (0.81 to 0.63) .81 4.02 .04 75

Change in clinicalattachment level

WMD 95% CI 0.01 (0.54 to 0.56) .97 0.58 .45 0

Change inkeratinized tissue

WMD 95% CI 0.22 (1.40 to 0.97) .72 9.11 .003 89

Sites with completeroot coverage

RR 95 % CI 0.30 (0.02 to 5.78) .42 3.31 .07 70

SubepithelialConnective-Tissue Graft

Andia andcolleagues118

(2008),Erley and

colleagues119

(2006),Souza and

colleagues122

(2008)

Change in gingivalrecession

WMD 95% CI 0.78 (1.06 to 0.51) < .000 1.48 .48 0

Change in clinicalattachment level

WMD 95% CI 0.75 (1.13 to 0.38) < .000 0.03 .98 0

Change inkeratinized tissue

WMD 95% CI 0.02 (1.05 to 1.02) .97 2.70 .10 63

Sites with complete

root coverage

RR 95% CI 0.24 (0.10 to 0.58) .001 0.92 .63 0

* mm: Millimeters. CI: Confidence interval. WMD: Weighted mean difference. RR: Risk ratio. Comparison made with two studies (data from Andia and colleagues118 2008 study were not available).



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in clinical outcomes. Six trials fulfilled the pro-

posed inclusion criteria, providing data frompatients treated with coronally advanced flaps,guided tissue regeneration and subepithelialconnective-tissue grafts. When we accumulatedevidence from individual studies, the pooled datasuggested that tobacco smoking affects rootcoverage.19,118,119,121,122 Likewise, the results of ourmeta-analyses showed that the use of subepithe-lial connective-tissue grafts was less effective insmokers than in nonsmokers in reducing theextent of exposed root surface and in improvingthe CAL. These findings may support the hypoth-esis that smoking decreases the expected success

of periodontal plastic surgery procedures.On the other hand, we should discuss some

inherent limitations of our review. We found nostatistically significant differences betweensmokers and nonsmokers when investigatorsused coronally advanced flap procedures. Despitethis fact, we should note that there remains causefor concern that smoking can affect root-coverageoutcomes, because only two studies in which

investigators used this procedure were available

for analysis, and one of these trials (a two-yearcontrolled clinical trial) showed that smokerslong-term healing response was indeed affectedby their tobacco use.121 Within-study comparisonsrevealed that recession reduction, clinical attach-ment gain, mean root coverage and the number ofsites exhibiting complete root coverage were lessevident in smokers.121 Furthermore, we shouldnote that we also found differences in the appliedmethodology in each trial (that is, inclusioncriteria, variability between surgical procedures,examiner blinding and follow-up period).

With respect to the study protocol, an impor-

tant issue we evaluated in trials reporting resultsfrom smokers was how the individual studiesdefined a subject as a smoker, and how the inves-tigators ascertained the accuracy of this classifi-cation. Erley and colleagues119 reported that theyclassified subjects as smokers if they reportedusing 10 or more cigarettes per day, which theresearchers later verified by means of a salivarycotinine sample (negative, 0 to 10 nanograms per

Figure 3. Forest plot of random effects meta-analysis evaluating the difference in clinical attachment level change between smokers andnonsmokers after treatment with subepithelial connective-tissue graft. IV: Inverse variance. CI: Confidence interval. : Kendall tau. z: z test.

Figure 4. Forest plot of random effects meta-analysis evaluating the difference in the number of sites exhibiting complete root coveragebetween smokers and nonsmokers after treatment with subepithelial connective-tissue graft. IV: Inverse variance. CI: Confidence interval.: Kendall tau. z: z test.



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milliliter; low, 10 to 20 ng/mL; medium, 20 to 40ng/mL; high, more than 40 ng/mL). Theresearchers used these cotinine levels to confirmthe subjects self-reported smoking history. Thisstudys results showed that the percentage of meanroot coverage at six months varied according to the

level of cotinine (84.2 percent for 10- to 40-ng/mLlevels and 76.6 percent for levels > 40 ng/mL), andthat higher levels of cotinine were negatively asso-ciated with the mean root coverage (r = 0.97).119 Inthe remaining trials,6,19,118, 121,122 the investigatorsconsidered subjects to be smokers if they reportedthe use of at least 10 cigarettes per day at the timeof the initial examination, but these authors con-ducted no cotinine tests. Additionally, we excludedthe results from one further study comparing theoutcomes for smokers and nonsmokers treatedwith acellular dermal matrix grafts because theinvestigators did not report how they had defined

patients as smokers.63

Palmer and colleagues27 and Johnson and Guth-miller28 observed that tobacco smoking demon-strated a long-term effect that harms the vascu-larization of a persons periodontal tissues ratherthan a simple vasoconstrictive effect that follows asmoking event. Alterations consist of chronicreductions in gingival blood flow, vascularity, gin-gival crevicular fluid levels and oxygen saturationof hemoglobin; suppression of neutrophil func-tions; negative effects on cytokines and growthfactor production; inhibition of fibroblast growth;

inhibition of collagen production by gingivalfibroblasts; and less attachment of periodontal lig-ament fibroblasts to root surfaces.27,28 The combi-nation of such effects may have affected thehealing response of smokers, especially thosetreated with subepithelial connective-tissue grafts.

As previously noted, having observed an adequateblood supply is critical for revascularization ofconnective-tissue grafts.1,10-13,119

Moreover, the success of a periodontal plasticsurgery procedure usually is associated with there-establishment of the gingival wall over previ-ously exposed root surfaces, with a concomitant

improvement in CAL and esthetics and a decreasein dental hypersensitivity. In the studies weincluded in this review, both smokers and non-smokers demonstrated improvement in GR depth,CAL and KT; however, nonsmokers exhibitedgreater improvement than smokers in all of thesemeasures. Authors of all studies we includedreported statistically significant changes in therecorded outcome measures from baseline to the

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most recent follow-up evaluations (Table 2).Besides, not all periodontal plastic surgery pro-cedures may result in an identical range of rootcoverage. Previous reviews have indicated thatsubepithelial connective-tissue grafts produceresults that are better in terms of mean and com-

plete root coverage than those of other tech-niques.21-24 In spite of the limited number ofstudies included in this systematic review, wefound a similar tendency for both outcomesamong smokers.

With respect to mean root coverage and com-plete root coverage, we found a marked variationin results (Table 2), as well as a statistically sig-nificant greater chance of achieving complete rootcoverage with subepithelial connective-tissuegrafts, in nonsmokers when compared withsmokers. Differences between techniques, the oper-ators level of experience, recession localization

and gingival anatomy8,123 may be linked to thegreat variability of results we observed betweenthe included studies. Some of these conditionsmay cause the patients wound to reopen duringhealing.123Additionally, we calculated the numberneeded to treat to determine how many smokerswould need to be treated with subepithelial con-nective-tissue graft procedures to result in onemore patients achieving complete root coveragethan would have done so in the nonsmokersgroup. The number needed to treat for smokers toobtain one more site exhibiting complete root

coverage than nonsmokers was three (that is,three patients who smoke need to be treated sothat one can achieve this benefit over nonsmokingpatients).

As previously mentioned, investigators in onestudy reported their data in two articlesaccording to the follow-up period (short term andlong term).120,121 They found that mean root cov-erage and complete root coverage decreasedacross time, both in smokers and in non-smokers.120,121 Nonetheless, this recurrence of GRseemed to be more evident among smokers. Thus,this evidenceregarding both the mean root cov-

erage and the number of sites exhibiting completeroot coverageprovides compelling support forthe concept that behavioral, environmental andindividual factors may be associated with therecurrence of GR. Consequently, researchersshould evaluate the possible causes of the reces-sion, as well as whether these undesirablechanges in root-coverage outcomes will lead todeterioration in the patients oral esthetic status



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and functional conditions over time. Mechanismsof host response in the periodontal tissues arecomplex and involve numerous systems of inter-actions.124Although lifestyle change (in this case,smoking cessation) cannot reverse the effects ofsmoking immediately, it may improve wound

healing conditions in the future.In light of this discussion, it seems reasonable

that patients should be encouraged to quitsmoking. It has been advocated that smoking ces-sation in the time surrounding the immediatesurgical procedure may be beneficial.28,40,41,119

While there are several examples of the use ofperiodontal plastic surgery procedures to coverexposed root surfaces, studies regarding theeffects of smoking on the outcomes of such pro-cedures are particularly important. Otherresearchers have recognized that smokersespecially so-called heavy smokers (patients who

smoke 20 or more cigarettes per day) have moreGR than do nonsmokers.28,125 Heavy smokersexpose themselves to tobacco products (nicotineand tar) many times per day.27As tobaccosmokers experience widespread negative systemiceffects of their tobacco use, this long-term expo-sure will affect the oral cavity as well. Clearly,identification of the specific factors associatedwith the healing process in smokers is an area inwhich much more research is needed.

CONCLUSIONS

In our systematic review of the limited informa-tion available, we found that the treatment ofrecession-type defects by means of periodontalplastic surgery procedures led to statistically sig-nificant improvements in GR and CAL for bothsmokers and nonsmokers.

Our meta-analysis showed that subepithelialconnective-tissue grafts provide significantlymore root coverage and clinical attachment gainfor nonsmokers than for smokers. However, coro-nally advanced flaps produced similar outcomesfor smokers and nonsmokers in terms of changesin GR, CAL and width of KTs.

There was a noticeable variation in the percent-ages of mean root coverage and complete root cov-erage between studies and procedures. Smokerswho received subepithelial connective-tissue graftsfor treatment of GR had fewer sites exhibitingcomplete root coverage than did nonsmokers.Overall, nonsmokers had the best outcomes.

Implications for research. Further compari-sons between smokers and nonsmokers (in the

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form of controlled clinical trials) are necessary tocorroborate our findings of the effects of tobaccosmoking on periodontal plastic surgery procedures.Randomized controlled clinical trials performedwith smokers are needed to evaluate periodontalplastic surgery procedures and to determine which

techniques provide the best results. Researchersshould evaluate differences between light andheavy smokers in these trials.

In future trials, researchers should includebaseline and final measurements of individualdefects (GR, CAL, KT and GR width) andpatient-based outcomes (esthetics and dentalhypersensitivity).

Implications for practice. Patients whosmoke should be encouraged to quit before under-going any periodontal plastic surgery procedure,with the goal of improving the expected outcomesas well as their overall health. However, if

patients cannot achieve this, clinicians shouldencourage them to consider, at the least, reducingthe number of cigarettes smoked per day oravoiding smoking completely during the earlyphase of healing.

Disclosure. None of the authors reported any disclosures.

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The influence of tobacco smoking on the outcomes achieved by root- coverage procedures