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REVIEW ARTICLE
Correspondence
Leandro Chambrone, M.Sc. Dentistry Program, Ibirapuera University, São Paulo, SP, Brazil.
Email: leandro_chambrone@hotmail.com
Periodontology 2000. 2019;79:81–106. wileyonlinelibrary.com/journal/prd © 2019 John Wiley & Sons A/S. | 81
Published by John Wiley & Sons Ltd
82 | CHAMBRONE ET AL.
F I G U R E 2 Miller's classification of
gingival recessions; *Reprinted/adapted by
Class I Class II permission from Springer Nature Customer
Class I* Class II Service Centre GmbH: Springer Nature,
Rationale for the Surgical Treatment of
Single and Multiple Recession‐Type
Defects. In: Evidence‐Based Periodontal
and Peri‐Implant Plastic Surgery: A Clinical
Class III Class IV Roadmap from Function to Aesthetics by
Class III Class IV Leandro Chambrone, SPRINGER
INTERNATIONAL PUBLISHING
SWITZERLAND (2015)
CHAMBRONE ET AL. | 83
Laterally
positioned flaps*
Coronally
advanced flaps
Free gingival
grafts
F I G U R E 3 Examples of periodontal
plastic surgery procedures proposed for
root coverage; *Reprinted/adapted by
permission from Springer Nature Customer
Service Centre GmbH: Springer Nature,
Rationale for the Surgical Treatment of
Single and Multiple Recession‐Type
Defects. In: Evidence‐Based Periodontal
and Peri‐Implant Plastic Surgery: A Clinical Subepithelial
Roadmap from Function to Aesthetics by connective
tissue grafts*
Leandro Chambrone, SPRINGER
INTERNATIONAL PUBLISHING
SWITZERLAND (2015)
84 | CHAMBRONE ET AL.
Patient-related factors
Recession classification, depth
and width
Clinical attachment level
Width of keratinized tissue
Systemic and local conditions
(e.g. smoking, toothbrushing)
Patient’s expectation (i.e.
esthetics)
Success
Outcomes-related factors
Intervention-related factors Patient satisfaction
Type of technique Adverse effects and/or
postoperative complications
Standardized procedures
Standardized examination
Operator`s experience and skills
Mean root coverage achieved
Long-term monitoring
Scientific community,
3.2 | An Overview of periodontal plastic surgery for
clinicians and patients
root coverage: outcomes from systematic reviews
To ask
3.2.1 | The first decade of evidence‐based
periodontal plastic surgery (2002‐2012)
Since the landmark systematic review conducted by Roccuzzo et al.,
in 2002,71 more than 10 systematic reviews and meta‐analyses
To
To apply Truth exploring the effects of periodontal plastic surgery for root coverage
Obtain/retrieve
have been published in different parts of the world in the following
decade.2,3,5–7,9,11,28,32,65,66,71 and their methodology and results are
described in detail in Table 1. In its great majority, this collection of
reviews addresses the effects, clinical advantages, and adverse
To analyse effects/complications of different flap and graft procedures, associ-
To evaluate
and to adjust
ated or not with biomaterials, for the treatment of Miller Class I and
II localized or multiple recession‐type defects. For such a purpose,
FIGURE 5 Impact of evidence‐based evaluations these systematic reviews developed and incorporated specific
focused questions, inclusion and exclusion criteria, comprehensive
search strategies, quality assessment tools, and statistical models (ie,
requirements advocated by evidence‐based dentistry and periodontal
research synthesis models).
plastic surgery with clinician and patient‐related factors. Therefore,
In the broadest sense, these systematic reviews were consistent
evidence‐based periodontal plastic surgery is defined as “the system-
in their agreement on a sufficient amount of evidence for root‐cov-
atic assessment of clinically relevant scientific evidence designed to
erage procedures leading to significant recession depth reduction
explore the esthetic and functional effects of treatment of defects
and clinical attachment level gain, and thus the assessment of the
of the gingiva, alveolar mucosa, and bone, based on clinician's knowl-
outcomes of these publications represents the uppermost level of
edge and patient‐centered outcomes, such as perception of esthetic
evidence available and should be considered as the basis for clinical
conditions, functional limitations, discomfort, root sensitivity, level of
8 decision making. Despite some differences between protocols in the
sociability after surgery, and preferences” (Figure 6). Evidence‐based
reviews, it should be considered that: (a) all reviews adopted similar
periodontal plastic surgery is an important part of contemporary evi-
focused questions; (b) all reviews reported significant reduction in
dence‐based periodontology; accordingly, periodontal plastic surgery
recession depth and clinical attachment level gain, with or without a
been constantly explored and improved for use in the treatment of
significant increase in the keratinized tissue width, independently of
recession‐type defects with root‐coverage procedures.
the periodontal plastic surgery procedure; (c) outcomes from pooled
data, as reported via meta‐analyses, showed that surgical techniques
describing the use of subepithelial connective tissue grafts and coro-
nally advanced flaps (associated or not with subepithelial connective
tissue grafts or some biomaterials) were the procedures with the
Evidence-based
dentistry best outcomes (Figures 7 and 8); (d) complete root coverage was
more prevalent within subepithelial connective tissue graft proce-
dures; (e) there are insufficient data on patient‐centered outcomes
(esthetics, preferences, pain, and root sensitivity); and (f) the base of
evidence available for assessment and the criteria for conducting
Evidence-based systematic reviews were significantly improved over the last decade
Clinicians' Patient-centered
knowledge Periodontal outcomes and thus differences between systematic reviews regarding method-
plastic surgery
ology and comparisons may be evident, but they are nonsignificant
and certainly cannot decrease the value of these older reviews.
T A B L E 1 Evidence‐based periodontal plastic surgery: summary of the the first decade/‘generation’ (2002–2012) of systematic reviews appraising root coverage procedures
|
(Continues)
ET AL.
TABLE 1 (Continued)
Types of study Interventions of
and participants interest and literature Outcomes No. of Statistical P‐values
CHAMBRONE
Reference included search included Comparisons studies method Effect size Z Chi2 I2 (%) Authors’ main conclusions
ET AL.
b
Oates RCTs All periodontal plastic ΔGR GTR/ADMG vs 9 F WMD 95%CI −0.29 [−0.52, −0.06] 0.01 < 0.05 N/A “Soft tissue augmentation
et al66 Patients with surgery procedures clinical SCTC 7 F WMD 95%CIb −0.86 [−1.13, −0.58] <0.01 < 0.05 N/A procedures are effective
gingival aimed at treating GR attachment ΔGR means of obtaining root
recessions Electronic (Medline level ΔKT coverage, SCTC
and Cochrane OHG) PD techniques appear to have
and manual KT an advantage over GTR,
searching up to April PCR and there is a need for
2002 MRC further efficacy studies
limited to English PBA and for investigation of
language journals these procedures relative
to patient‐oriented
outcomes such as
esthetics, root sensitivity,
and postoperative
morbidities.”
Gapski RCTs of at least ADG vs CAF or SCTC ΔGR SCTC vs ADMG 4 R WMD 95%CI −0.41 [−1.33, 0.52] 0.39 < 0.05 85.6 “Differences in study design
et al39 3 mo duration Electronic (Medline ΔPD ΔGR 4 R WMD 95%CI 0.02 [−0.28, 0.24] 0.89 0.29 20.6 and lack of data precluded
Patients with and Cochrane OHG) ΔCAL ΔPD 4 R WMD 95%CI 0.52 [−0.12, 1.16] 0.11 0.02 68.3 an adequate and complete
gingival and manual ΔKT ΔKT 2 R WMD 95%CI −0.62 [−0.74, 0.51] 0.28 0.01 83.6 pooling of data for a more
recessions searching up to CAF vs ADMG 2 R WMD 95%CI 0.00 [−0.36, 0.35] 0.99 0.34 0 comprehensive analysis.
October 2004 ΔGR 2 R WMD 95%CI −0.56 [−1.33, 0.21] 0.16 0.18 45.2 Therefore, considering the
limited to English ΔPD 2 R WMD 95%CI −0.31 [−0.78, 0.15] 0.19 0.62 0 trends presented in this
language journals, ΔCAL study, there is a need for
and agreement ΔKT further randomized clinical
between the review studies of ADMG
authors calculated procedures in comparison
by k scores to common mucogingival
surgical procedures to
confirm our findings. It is
difficult to draw anything
other than tentative
conclusions from this
meta‐analysis of ADMG
for mucogingival surgery,
primarily because of the
weakness in the design
and reporting of existing
trials.”
(Continues)
|
87
88
TABLE 1 (Continued)
|
(Continues)
ET AL.
TABLE 1 (Continued)
Types of study Interventions of
and participants interest and literature Outcomes No. of Statistical P‐values
Reference included search included Comparisons studies method Effect size Z Chi2 I2 (%) Authors’ main conclusions
CHAMBRONE
without language ΔKT 4 R OR 95%CI 3.89 [1.59, 9.50] < 0.01 0.32 15.2
ET AL.
restriction, and CAF + EMD vs 2 R WMD 95%CI 0.60 [−0.52, 1.73] 0.29 < 0.01 87.1
contact with original CAF 2 R WMD 95%CI 0.28 [−0.16, 0.72] 0.22 0.55 0
authors when ΔGR 2 R WMD 95%CI 0.31 [−0.15, −0.78] 0.19 0.62 0
necessary ΔCAL 2 R OR 95%CI 4.83 [0.23, 99.88] 0.31 0.08 67.4
ΔKT 6 R WMD 95%CI −0.38 [−0.65, −0.10] < 0.01 0.10 45.6
SCRC 6 R WMD 95%CI −0.05 [−0.32, −0.22] 0.73 0.15 38.0
CAF + ADMG vs 6 R WMD 95%CI −1.18 [−1.98, −0.39] <0.01 < 0.01 91.9
CAF 6 R OR 95% CI 0.45 [0.20, 1.04] 0.06 0.20 31.9
ΔGR 4 R WMD 95%CI −0.40 [−1.07, 0.26] 0.24 < 0.01 79;4
ΔCAL 4 R WMD 95%CI −0.39 [−1.00, 0.21] 0.20 0.03 67.5
ΔKT 4 R WMD 95%CI −0.90 [−1.51, −0.28] <0.05 0.10 52.1
SCRC 4 R OR 95% CI 0.49 [0.23, 1.03] 0.06 0.61 0
CAF + GTRr vs
GAF+SCTC
ΔGR
ΔCAL
ΔKT
SCRC
CAF + ADMG vs
CAF + SCTC
ΔGR
ΔCAL
ΔKT
SCRC
Chambrone RCTs, CCTs, and ADMG, CAF, FGG, ΔGR CAF (smokers) vs. 2 R WMD 95%CI −0.09 [−0.81, 0.63] 0.81 0.04 75.0 “The results of this review
et al3 CSs of at least GTR and SCTC ΔCAL CAF 2 R WMD 95%CI 0.01 [−0.54, 0.56] 0.97 0.45 0 show that smoking may
6 mo duration Electronic (Medline, ΔKT (nonsmokers) 2 R WMD 95%CI −0.22 [−1.40, 0.97] 0.72 < 0.01 89.0 negatively influence GR
Patients with Embase, CENTRAL SCRC ΔGR 2 R RR 95%CI 0.30 [0.02, 5.78] 0.42 0.07 70.0 reduction and clinical
Miller Class I or II and Cochrane OHG) PCR ΔCAL 3 R WMD 95%CI −0.78 [−1.06, −0.51] < 0.01 0.48 0 attachment level gain,
gingival and manual MRC ΔKT 3 R WMD 95%CI −0.75 [−1.13, −0.38] <0.01 0.98 0 especially for SCTC.
recessions searching up to and Stab SCRC 2 R WMD 95%CI −0.02 [−1.05, 1.02] 0.97 0.10 63.0 Additionally, smokers may
At least 10 including June 2008 SCTC (smokers) 3 R RR 95%CI 0.24 [0.10, 0.58] <0.01 0.63 0 exhibit fewer sites with
patients per limited to English vs SCTC complete root coverage.”
group at final language journals, (nonsmokers)
examination agreement between ΔGR
Outcome measures the review authors ΔCAL
from smokers (≥ calculated by k ΔKT
10 cigarettes/day) scores, and contact SCRC
and nonsmokers, with original authors
recorded when necessary
separately
|
(Continues)
89
90
TABLE 1 (Continued)
|
(Continues)
ET AL.
CHAMBRONE
ET AL.
TABLE 1 (Continued)
Types of study Interventions of
and participants interest and literature Outcomes No. of Statistical P‐values
Reference included search included Comparisons studies method Effect size Z Chi2 I2 (%) Authors’ main conclusions
and contact with surgical technique and any
original authors prognostic factors.”
when necessary
Chambrone RCTs of at least ADMG, CAF, EMD,
et al9 6 mo duration FGG, GTR, LPFs,
Patients with SCTC alone or in
Miller Class I or II combination with
gingival LPFs or CAF
recessions Electronic (Medline,
Embase, CENTRAL
and Cochrane OHG)
and manual
searching up to April
2011, without
language restriction,
agreement between
the review authors
calculated by k
scores, and contact
with original authors
when necessary
ADMG, acellular dermal matrix grafts; bs, associated with bone substitutes; CAF, coronally advanced flap; CCT, controlled clinical trial; CENTRAL, Cochrane Central Register of Controlled Trials; CI, confi-
dence interval; Cochrane OHG, Cochrane Oral Health Group specialist trials register; CS, case series; EMD, enamel matrix derivative protein; F, fixed‐effects meta‐analysis; FGG, free gingival graft; GR, gin-
gival recession; GTR, GTR (r, resorbable membrane; n, nonresorbable membrane); HF‐DDS, living tissue‐engineered human fibroblast‐derived dermal substitute; LPFs, laterally positioned flap; MRC, mean
root coverage; N/A, not available; OR, odd ratio; PBA, patient‐based outcomes; PCR, percentage of complete root coverage; PPS, periodontal plastic surgery; R, random‐effects meta‐analysis; RC, root condi-
tioning; RCT, randomized controlled trial; RR, risk ratio; SCRC, sites with complete root coverage; SCTG, subepithelial connective tissue graft; Stab, long‐term stability; WMD, weighted mean difference
(mm); ΔCAL, clinical attachment change; ΔGR, gingival recession change; ΔKT, keratinized tissue change; ΔPD, probing depth change.
a
Analysis performed using data extracted from the review.
b
Data extracted from the forest plots found in the review.
|
91
92 | CHAMBRONE ET AL.
treated sites showing complete root coverage within the base of evi-
dence because of aspects linked to characteristics of defects (ie,
depth, width, and classification of the recession), the amount and qual-
ity of adjacent gingival tissue, smoking habits, traumatic toothbrushing,
and the surgical procedure chosen.2,3,5–7,9,11,28,32,65,66,71,107–110
In a previous Cochrane review it was stated that better outcomes
(in terms of percentage of complete root coverage) can be accom-
plished in recession‐type defects with a baseline recession depth of
<4 mm, and also that achieving complete root coverage may be influ-
enced by the baseline position of the gingival margin.6,7,108 This view
is supported, in part, by another review included in this overview (an
individual patient data network meta‐analysis with data from 22 ran-
domized controlled trials) that appraised whether baseline recession‐,
patient‐, and procedure‐related factors could influence achievement
of complete root coverage.9 The results of this review showed that:
(a) the deeper the baseline recession depth, the smaller the chance of
achieving complete root coverage; (b) subepithelial connective tissue
grafts, matrix grafts, and enamel matrix derivative (with or without
subepithelial connective tissue graft) were superior to coronally
advanced flaps in terms of complete root coverage; and (c) trials
reporting conflicts of interest and Class I recession defects presented
a trend of better outcomes when compared with trials not reporting
conflicts of interest and Class II defects, respectively.9
In the majority of the systematic reviews, statistical methods
employing conventional pairwise meta‐analyses (ie, based on aggre-
gate data at the study level and outcomes derived from randomized
controlled trials normally comparing a new treatment with a gold
standard one) were used to supply a general estimate of the differ-
ences in the outcome measures,2,3,5–7,9,11,29,33,67,68,73,107–110 but
the calculation of weighted mean differences for some continuous
outcomes (eg, recession depth and clinical attachment level) can be
impaired by the inclusion of studies investigating gingival recession
>4 mm in depth because such trials commonly report greater out-
comes changes (ie, differences in the mean values between baseline
and follow‐up results).6,7 Likewise, other methodological factors
should be considered when pairwise meta‐analyses are used: (a)
pairwise comparisons are usually pooled using statistical methods
to supply a general estimate of the differences in the outcome
measures and thus it is not always possible to conduct direct com-
parisons when some head‐to‐head trials have not yet been per-
formed (ie, laterally positioned flaps vs subepithelial connective
tissue grafts or coronally advanced flaps + matrix grafts)112–115; (b)
F I G U R E 7 Long‐term follow‐up (72 mo) of a single recession‐ when there are more than two test treatments (eg, coronally
type defect treated with subepithelial connective tissue advanced flaps, guided tissue regeneration, and lateral pedicle
graft + coronally advanced flap51 flaps), at least six pairwise meta‐analyses have to be undertaken to
compare the differences in efficacy between pairs of treatments
reviews) also support the positive effects of treatment of recession‐ (eg, coronally advanced flaps vs coronally advanced flaps + guided
type defects by root coverage procedures. These ‘first and second tissue regeneration; coronally advanced flaps vs lateral pedicle
generation’ reviews highlighted some specific esthetical and func- flaps; and guided tissue regeneration vs lateral pedicle flaps) and
tional issues. between each of them and the gold standard (for instance, for
With respect to complete root coverage, it combines esthetics, subepithelial connective tissue grafts: coronally advanced flaps vs
and also, if necessary, can put an end to dental hypersensitivity.9 subepithelial connective tissue grafts; guided tissue regeneration vs
However, great variability can be observed in the outcomes of subepithelial connective tissue grafts; and lateral pedicle flaps vs
CHAMBRONE ET AL. | 93
subepithelial connective tissue grafts);113 and (c) they did not avoid addition, the authors concluded: (a) the hypothesis that smoking
the dilemma of combining odds ratio and risk ratio of studies decreases the expected success of root coverage is valid for
reporting dichotomous data (eg, the number of treated sites show- subepithelial connective tissue grafts; (b) at least three smokers
ing complete root coverage) that have or not have not corrected need to be treated so that one can achieve complete root cover-
for some confounders (ie, defects with different characteristics, age over nonsmokers when subepithelial connective tissue grafts
smoking, and follow‐up period).9 Therefore, the use of individual are the procedure of choice; and (c) the way in which individual
patient data meta‐analyses may surmount such constraints and studies define a subject as a smoker, and how the investigators
incorporate the information of both patients (eg, anatomy of reces- ascertain the accuracy of this classification, should be improved
sion‐type defects and systemic conditions, both at baseline) and and better described.3
procedures into a single statistical model measuring overall effi- In addition, and common to all these reviews, was the finding
cacy,116 as well as decrease the risk of including potential sources that they, in their majority, were considered to be of medium to high
of heterogeneity and bias.105,117,118 quality (ie, they described an overall scientific quality with minor
On the one hand, evidence emerging from some of the flaws),8 which, in practical terms, indicates that the conclusions
included systematic reviews also supports that periodontal plastic about the effects of interventions may be considered as fairly cer-
surgery can effectively be applied to multiple recession tain. Nevertheless, in order to overcome eventual biases in their
defects5,108,109 and to smokers.3,107,108 On the other hand, it review processes, the complexity in interpreting results reinforces
should be taken into consideration that for multiple defects, the the premise that systematic evaluations of the literature must be
base of evidence available is still very fragile. When the systematic built on a logical and transparent methodology, with the reader of
review was performed, there were no randomized controlled trials the systematic review (patient, clinician, or researcher) being able to
available, the data retrieved for analysis was exclusively derived distinguish what has been carried out.8,89,90,105
from case series, and from then until the time when this review
was prepared, few randomized controlled trials have been pub-
3.3 | Concluding remarks from systematic reviews
lished.12,89,107,108 Regarding the effect of treatment in smokers
compared with treatment in nonsmokers, data were retrieved from The results from the set of systematic reviews on root‐coverage pro-
controlled clinical trials (because it is impossible to randomize stud- cedures included in this chapter and published over the last 18 years
ies in which only one surgical procedure is tested), and the findings indicate that:
showed that root‐coverage procedures promoted significant reduc-
tion in recession depth and in clinical attachment level gain for • Within the surgical procedures assessed, all can lead to statisti-
both groups of subjects.3 However, pooled estimates evidenced cally significant reduction of recession depth and gain in clinical
that subepithelial connective tissue grafts were less effective in attachment level when the characteristics of postsurgical reces-
smokers than in nonsmokers concerning both recession and clinical sion defects are compared with those at baseline.
attachment level reduction, while no significant differences were • Between procedures, techniques advocating the use of subepithe-
found for patients treated with coronally advanced flaps. In lial connective tissue grafts (associated with coronally advanced
94 | CHAMBRONE ET AL.
flaps alone or coronally advanced flaps + or enamel matrix deriva- imprecise conclusions for some groups of comparisons because of
tive), coronally advanced flaps (alone or in combination with acellu- the lack of information on individual patient data.
lar dermal matrix graft or enamel matrix derivative) showed a • The unique systematic review of randomized controlled trials, in
better evidence of statistically significant gains in recession depth which individual patient data of 602 recessions were pooled in
and clinical attachment level when compared with other root-cov- two sets of network meta-analyses9, as well as the 2015 Ameri-
erage procedures; however, significant improvements in the width can Academy of Periodontology Regeneration Workshop and
of keratinized tissue were directly associated with the use of 2018 Cochrane Systematic Reviews gave support to the assump-
subepithelial connective tissue grafts (Figure 7). tion that achieving complete root coverage is directly associated
• Apart from the findings related to increases of keratinized tissue with initial depth (apico-cervical length) of the gingival recession,
width, subepithelial connective tissue grafts also showed better and that surgical techniques employing subepithelial connective
outcomes in terms of complete root coverage (the main and final tissue grafts are, currently the gold standard procedures.
outcome anticipated).
• The use of root-modification agents did not increase or decrease
the rate of root coverage. 4 | SYSTEMATIC EVALUATION OF THE
• Assessment of periodontal plastic surgery procedures for the treat- ROLE AND OUTCOMES OF LATIN
ment of areas of multiple recession-type defects remains partially AMERICAN STUDIES FOR INCREASING THE
explored. The findings of the narrow base of evidence available BASE OF EVIDENCE
suggest that both subepithelial connective tissue grafts and coro-
nally advanced flaps (Figures 8 and 9) can be safely used to The role of Latin American randomized controlled trials in increasing
reestablish esthetics and decrease dental hypersensitivity. the base of knowledge concerning our understanding of periodontal
• Comparisons between procedures exploring continuous data were disease patterns and therapy has been gaining worldwide impor-
performed mainly on a pairwise basis (through obtaining weighted tance. With respect to evaluation of periodontal plastic surgery for
mean differences of the outcomes, ie, calculating final baseline treatment of recession‐type defects, some research groups have
means), and consequently such an approach precludes the direct been able to conduct and present their findings in the main interna-
comparison of more than two distinct procedures. tional and renowned periodontal journals. In addition to the profits
• As reported in a previous study,113 because the base of evidence that their results have brought to regional and worldwide research
is not always equal across all comparisons, some inconsistencies communities, they substantiate the development, growth, and con-
associated with multiple pairwise meta-analyses should be taken solidation of new high‐quality research centers. In order to assess
into consideration, such as the impossibility of making direct com- their contribution to the current base of evidence, a systematic eval-
parisons between two different procedures when head-to-head tri- uation was developed and conducted. Detailed descriptions of the
als are not available for analysis, as well as the lack of power to protocol (ie, electronic and manual searching and methodology) used
detect any significant between-treatment differences for meta-ana- to search for Latin American randomized controlled trials in the den-
lysis that include only a few studies. These aspects may lead to tal literature have been published elsewhere.2,3,5–7,9 The following
F I G U R E 9 Short‐term follow‐up
(24 mo) of multiple recession‐type defects
treated with coronally advanced flap90;
Reprinted/adapted by permission from
Springer Nature Customer Service Centre
GmbH: Springer Nature, Rationale for the
Surgical Treatment of Single and Multiple
Recession‐Type Defects. In: Evidence‐
Based Periodontal and Peri‐Implant Plastic
Surgery: A Clinical Roadmap from Function
to Aesthetics by Leandro Chambrone,
SPRINGER INTERNATIONAL PUBLISHING
SWITZERLAND (2015)
CHAMBRONE ET AL. | 95
sections provide a brief description of the specific methodological AND GTR OR “tissue NEAR regenerat* OR [(gingiva* NEAR
aspects of the present review. esthetic*) OR (gingiva* NEAR aesthetic*)] OR periodont*) AND
(“plastic surgery” OR “soft tissue graft*” OR “coronally advanced
flap*” OR “laterally positioned flap*” OR “laterally positioned
4.1 | Criteria for considering studies for this review
flap*” OR “connective tissue graft*” OR “connective tissue graft*”,
OR gingiva* NEAR transplant* OR “dermal matrix” NEAR graft*
4.1.1 | Inclusion criteria, type of participants, and
OR “enamel matrix protein”).
studies
Reference lists of any potential studies were examined (ie, by
Studies were considered for inclusion if they involved the following: manual searching) in an attempt to identify any other papers.
controlled trials conducted in Latin American universities or private addition, it should be noted that all Latin American randomized con-
practices were screened and included in this review. The full text of trolled trials found in the literature were published within the last
the included trials was obtained and their main characteristics are 18 years and their results are clearly in line with the world's base of
presented in Table 2. evidence. Their outcomes have been individually assessed and/or
Twenty‐nine papers,18,20–22,30,34,36–38,50,53,54,62,64,73–78 on 23 ran- combined into pooled estimates by most of the systematic reviews
domized controlled trials published in full, were included; therefore, available in order to assist clinicians and researchers during the clini-
Trials reported in more than one publication were grouped under cal decision‐making process. As a result, this group of studies clearly
23,37,76,119,120
one study name (ie, that of the most recent paper). contributes to improving knowledge in the treatment of recession‐
In total, 558 patients (771 defects) allocated in ten paral- type defects as they now represent an important part of the global
lel18,31,39,56,76,79,119–124 and 13 split‐mouth design trials were treated. and relevant set of information available for analysis.
One study was private practice‐based64 and 22 were based in
universities. All randomized controlled trials were conducted in the
5.1 | Concluding remarks from Latin American
same country (Brazil), except for the trial by Castellanos et al,30
randomized controlled trials
which was performed in Mexico. The majority of samples involved
localized recession‐type defects classified as Class I or II, but one Data retrieved from the 23 Latin American randomized controlled
study tested the use of periodontal plastic surgery procedures for trials on the effect of root‐coverage procedures in treatment of
Class III defects.18 Eleven studies were supported, in total or in part, recession‐type defects included in this paper indicate that:
by government agencies,18,23,38,73,121–126 and one was supported by
a commercial company.64 Finally, most of the follow‐up evaluations • Statistically significant recession reduction and clinical attachment
were after 6 months’ duration, but some lasted for up to level gain may be expected following the use of different root-
23
30 months. coverage procedures.
The procedures evaluated were: coronally advanced flaps, either • Keratinized tissue gain is directly associated with subepithelial
alone or associated with barrier/membranes or different biomaterials connective tissue graft procedures.
(ie, acellular dermal matrix grafts, xenogenic matrix grafts bone sub- • There is substantial variation in terms of mean and complete root
stitutes, or enamel matrix derivative); subepithelial connective tissue coverage between studies. The results from the included studies
grafts associated with coronally advanced flaps; and lateral pedicle indicate better outcomes for subepithelial connective tissue
flaps (Table 2). Three randomized controlled trials assessed the com- grafts.
bination of restorative procedures plus coronally advanced • The use of restorative procedures associated with root-coverage
flap54,75,76 or subepithelial connective tissue graft74 procedures in techniques in the treatment of recession-type defects associated
noncarious cervical lesions. Within and between studies, the peri- with noncarious cervical lesions seems to be an effective
odontal plastic surgery procedures tested showed statistically signifi- approach.
cant reductions in recession depth and gain in attachment level. • Despite the extensive number of publications conducted in Latin
Surgical techniques advocating the use of subepithelial connective America, almost all randomized controlled trials were performed
tissue grafts also reported better outcomes in terms of keratinized in only one country. However, it should be considered that this
tissue gain. For trials evaluating the restoration of noncarious cervi- probably did not reflect the enthusiasm and the search for
cal lesions and root‐coverage procedures, it was shown that such a knowledge of other research centers. Clinicians from several
combined approach was as safe, predictable, and effective as the as Latin American countries have been working hard to disseminate
the treatment of noncarious cervical lesions with root‐coverage pro- and clinically appraise the outcomes of their network; accord-
cedures only.54,74–76 ingly, further information will doubtless be available in the
The criteria used to assess the risk of bias (ie, methods of ran- future.
domization and allocation concealment, blinding, completeness of
the follow‐up period, selective outcome reporting, and other bias)
showed that three trials were considered to have low risk of bias. As 6 | EFFECTS OF PERIODONTAL PLASTIC
reported in Table 2, most of the trials failed to report data on one or SURGERY ON NONCARIOUS CERVICAL
more topics and accordingly were classified to be at unclear risk of LESIONS: RESULTS OF AN INDIVIDUAL
bias. Moreover, it should be taken into consideration that in two tri- PATIENT DATA META‐ANALYSIS
als74–76 evaluating noncarious cervical lesions, blindness of the EVALUATING COMPLETE ROOT COVERAGE
examiner could not be achieved because it was not feasible to hide
the type of treatment performed (that is, the examiner was able to Complete root coverage represents the final clinical outcome
identify whether the restoration was applied at the noncarious cervi- expected after treatment of recession‐type defects.2–11 As
cal lesions). On the other hand, none of the included trials showed reported in previous sections of this review, complete root cover-
evidence of reporting bias (ie, selective outcome reporting) and other age of exposed root surfaces may be influenced by the type of
sources bias, none of the trials (data not included in Table 2). In periodontal plastic surgery procedure and by the baseline recession
T A B L E 2 Characteristics of Latin American randomized controlled trials evaluating different root coverage procedures
Method of
Main outcomes random Allocation Blindness of Risk of Site (location), funding and
Study Methods Participants Interventions evaluated ization concealment examiners bias notes
CHAMBRONE
Andrade et al18 RCT, parallel design, 30 nonsmoking individuals, 16 1) EMD + CAF CAL, GRD, KTT, KTW, Adequate Unclear Unclear Unclear University‐based (Brazil) and
2 treatment groups, females, aged 22‐44, with one Miller (macrosurgery) MRC, POPain, PPD, supported by the State of São
ET AL.
06 mo duration Class I or III buccal gingival recession 2) EMD + CAF SCRC/PCR Paulo Research Foundation
of at least 2 mm (microsurgery) (Automated controlled (FAPESP)
A total of 30 defects were treated (15 force periodontal probe)
per group)
Only two patients with Class III
recessions defects were included
Barros et al20 RCT, split‐mouth 14 nonsmoking individuals, 09 1) ADMG + CAF CAL, GRD, KTW, MRC, Adequate Unclear Unclear Unclear University‐based (Brazil) and
design, 2 treatment females, aged 21‐46, with at least 2 extended PPD, SCRC/PCR author contacted to provide
groups, 6 mo bilateral Miller Class I or II buccal 2) ADMG + CAF (Automated controlled further details from the trial
duration gingival recessions of at least 3 mm force periodontal probe)
A total of 32 defects were treated (16
per group)
Bittencourt RCT, split‐mouth 17 nonsmoking individuals, 11 1) Semilunar CAF ACC, CAL, GRD, GRW, Adequate Unclear Yes Unclear University‐based (Brazil),
et al22,23 design, 2 treatment females, aged 21‐52, with two 2) SCTG KTT, KTW, MRC, PPD, supported by the State of São
groups, 30 mo bilateral Miller Class I maxillary RH, SCRC/PCR Paulo Research Foundation
duration buccal gingival recessions of at least (Manual periodontal (FAPESP) and author contacted
2 mm and ≤ 4 mm probe) to provide further details from
A total of 34 defects were treated (17 the trial
per group)
Castellanos et al30 RCT, parallel design, 22 nonsmoking individuals, 13 1) EMD + CAF GRD, GRW, clinical Inadequate Unclear Unclear High University‐based (Mexico)
2 treatment groups, females, aged 28‐71, with one Miller 2) CAF attachment level,
12 mo duration Class I or II buccal gingival recessions KTW, PI, PPD, MRC
of at least 2 mm (Manual periodontal
A total of 22 defects were treated (11 probe)
per group)
da Silva et al34 RCT, split‐mouth 11 nonsmoking individuals, 5 females, 1) SCTG + CAF CAL, GRD, KTT, KTW, Adequate Unclear No High University‐based (Brazil) and
design, 2 treatment aged 18‐43, with two bilateral Miller 2) CAF MRC, SCRC/PCR author contacted to provide
groups, 6 mo Class I or II maxillary buccal gingival (Automated controlled further details from the trial
duration recessions of at least 3 mm force periodontal probe)
A total of 22 defects were treated (11
per group)
de Queiroz Cortes RCT, split‐mouth 13 nonsmoking individuals, 7 females, 1) ADMG + CAF CAL, GRD, GRW KTT, Adequate Unclear Unclear Unclear University‐based (Brazil)
et al36,37 design, 2 treatment mean age 32.8, with two bilateral 2) CAF KTW, MRC, PPD,
groups, 24 mo Miller Class I maxillary buccal gingival SCRC/PCR (Manual
duration recessions of at least 3 mm periodontal probe)
A total of 26 defects were treated (13
per group)
Felipe et al38 RCT, parallel design, 15 nonsmoking individuals, 6 females, 1) ADMG + CAF ACC, CAL, GRD, KTT, Adequate Unclear Uncleara Unclear University‐based (Brazil) and
2 treatment groups, aged 22‐54, with two bilateral Miller extended KTW, MRC,PPD, SCRC/ supported by the State of São
06 mo duration Class I or II buccal gingival recession 2) ADMG + CAF PCR (Automated Paulo Research Foundation
of at least 2 mm extended modified controlled force (FAPESP)
A total of 30 defects were treated (15 periodontal probe)
per group)
|
(Continues)
97
98
TABLE 2 (Continued)
|
Method of
Main outcomes random Allocation Blindness of Risk of Site (location), funding and
Study Methods Participants Interventions evaluated ization concealment examiners bias notes
Joly et al50 RCT, split‐mouth 10 nonsmoking individuals, 4 females, 1) ADMG + CAF (flap CAL, GRD, KTT, KTW, Adequate Unclear No High University‐based (Brazil) and
design, 2 treatment aged 24‐68, with two bilateral Miller without vertical MRC, PPD (Manual author contacted to provide
groups, 6 mo Class I or II maxillary buccal gingival incisions) probe) further details from the trial
duration recessions of at least 3 mm 2) SCTG + CAF (flap
A total of 20 defects were treated (10 without vertical
per group) incisions)
Lins et al53 RCT, parallel design, 10 nonsmoking individuals, 4 females, 1) GTR (ePTFE) + CAF CAL, GRD, KTT, KTW, Unclear Unclear Unclear Unclear University‐based (Brazil)
2 treatment groups, aged 22‐55, with 2 bilateral Miller 2) CAF MRC, PPD, SCRC/PCR,
6 mo duration Class I or II maxillary buccal gingival (Manual probe)
recessions of at least 2 mm
A total of 20 defects were treated (10
per group)
Lucchesi et al54 RCT, split‐mouth 59 nonsmoking individuals, 44 1) CAF (20 defects CAL, GRD, KTT, KTW, Adequate Unclear Yes (regarding Unclear University‐based (Brazil) and
design, 3 treatment females, aged 23‐65, with one Miller without NCCL) MRC, PPD, SCRC/PCR, restorative author contacted to provide
groups, 6 mo Class I maxillary buccal gingival 2) CAF + RMGI (20 (Manual probe) materials) further details from the trial
duration recession of at least ≥ 2 mm and defects with NCCL)
≤ 5 mm 3) CAF + RCR (19
A total of 59 defects were treated (2 defects with NCCL)
groups of 20 and one of 19 defects)
Nazareth & Cury62 RCT, split‐mouth 15 nonsmoking individuals, 6 females, 1) ABN/P‐15 + CAF CAL, GRD,KTT, KTW, Adequate Unclear Yes Unclear Practice‐based (Brazil) and
design, 2 treatment aged 22‐47, with two bilateral Miller 2) CAF MRC, PPD, SCRC/PCR, author contacted to provide
groups, 6 mo Class I maxillary buccal gingival (Manual probe) further details from the trial
duration recessions of at least 2 mm
A total of 30 defects were treated (15
per group)
Novaes et al64 RCT, split‐mouth 9 nonsmoking individuals, 7 females, 1) ADMG + CAF CAL, GRD, KTW, MRC, Unclear Unclear Unclear Unclear University‐based (Brazil) and
design, 2 treatment aged 23‐53, with at least two Miller 2) SCTG + CAF PPD, SCRC/PCR supported by Promodent Ltd.,
groups, 6 mo Class I or III buccal gingival (Automated controlled São Paulo, BR
duration recessions force periodontal probe)
A total of 30 defects were treated (15
per group)
Rossetti et al73 RCT, split‐mouth 1 1) GTR (collagen ACC, CAL, GRD, KTW, Unclear Unclear Yes Unclear University/hospital‐based (Brazil),
design, 2 treatment 2 individuals, 9 females, aged 25‐60, membrane) + TTC‐ MRC, PPD, SCRC/PCR supported by the Brazilian
groups, 18 mo with tw bilateral Miller Class I or II HCl + DFDBA (Manual probe) National Council for Scientific
duration maxillary buccal gingival recessions 2) SCTG + HCl and Technologic Development
of at least 3 mm (CNPQ) and author contacted
A total of 24 defects were treated (12 to provide further details from
per group) the trial
Santamaria RCT, split‐mouth 19 nonsmoking individuals, 10 1) CAF CAL, GRD, KTT, KTW, Adequate Unclear No High University‐based (Brazil) and
et al75,76 design, 2 treatment females, aged 24‐58, with bilateral 2) CAF + RMGI MRC, PPD, SCRC/PCR, supported by the State of São
groups, 24 mo Miller Class I maxillary buccal gingival (Manual probe) Paulo Research Foundation
duration recessions (FAPESP)
A total of 38 defects associated to
NCCL were treated (19 per group)
CHAMBRONE
(Continues)
ET AL.
TABLE 2 (Continued)
Method of
Main outcomes random Allocation Blindness of Risk of Site (location), funding and
Study Methods Participants Interventions evaluated ization concealment examiners bias notes
CHAMBRONE
Santamaria et al74 RCT, parallel design, 40 nonsmoking individuals, 19 1) SCTG CAL, GRD, KTT, KTW, Adequate Unclear No High University‐based (Brazil)
ET AL.
2 treatment groups, females, aged 19‐71, with one Miller 2) SCTG + RMGI MRC, PPD, SCRC/PCR,
06 mo duration Class I maxillary buccal gingival (Manual probe)
recession
A total of 40 defects associated to
NCCLs were treated (20 per group)
Santana et al77 RCT, parallel 36 nonsmoking individuals, 26 1) LPF CAL, GRD, KTW, MRC, Adequate Unclear Yes Unclear University‐based (Brazil)
design, 2 treatment females, mean age 34 years, with 2) CAF PPD, SCRC/PCR,
groups, 6 mo one Miller Class I maxillary buccal (Manual probe)
duration gingival recession
Santana et al78 RCT, split‐mouth 22 nonsmoking individuals, 13 1) Semilunar CAF CAL, GRD, KTW, MRC, Adequate Unclear Yes Unclear University‐based (Brazil)
design, two females, aged 18 to 47 years, with 2 2) CAF PPD, SCRC/PCR
treatment groups, bilateral maxillary Miller Class I (Manual probe)
06 mo duration buccal gingival recessions (≤5 mm)
125
Andrade et al. RCT, split‐mouth 15 nonsmoking individuals, six 1) ADMG + CAF without CAL, GRD, KTT, KTW, Adequate Unclear Yes Unclear University‐based (Brazil) and
design, 2 treatment females, aged 20 to 56 years, with vertical incisions MRC, PPD, SCRC/PCR supported by the State of São
groups, 12 mo two bilateral Miller Class I or II 2) ADMG + CAF (Automated controlled Paulo Research Foundation
duration buccal gingival recessions of at least (extended flap) force probe and (FAPESP) and Coordination for
2 mm compass) the Development of Personnel
A total of 30 defects were treated (15 in Higher Education (CAPES)
per group)
126
Ayub et al. RCT, split‐mouth 15 nonsmoking individuals, number of 1) ADMG (positioned 1 CAL, GRD, KTT, KTW, Adequate Adequate No High University‐based (Brazil) and
design, 2 treatment females not reported, aged 20 to 56 mm apical to the MRC, PPD, SCRC/PCR supported by the State of São
groups, 6 mo years, with two bilateral Miller Class cemento‐enamel (Automated controlled Paulo Research Foundation
duration I or II buccal gingival recessions of at junction) + CAF force probe and digital (FAPESP) and BioHorizons Inc
least 3 mm (extended flap) 2) caliper)
A total of 30 defects were treated (15 ADMG + CAF
per group) (extended flap)
Bittencourt et al. RCT, parallel design, 24 nonsmoking individuals, 11 1) EMD + CAF CAL, GRD, GRW, KTT, Adequate Unclear Yes Unclear University‐based (Brazil) and
121
2 treatment groups, females, aged 18‐55‐44, with two (macrosurgery) KTW, MRC, PPD, supported by the Research
06 mo duration bilaterl Miller Class I or II buccal 2) EMD + CAF SCRC/PCR (Manual Funding Agency of Bahia State
gingival recession of at least 2 mm (microsurgery) probe and digital
A total of 24 defects were treated (12 caliper)
per group)
Fernades‐Dias RCT, parallel design, 40 nonsmoking individuals, 20 1) Low‐level laser ACC, CAL, GRD, KTW, Adequate Adequte Yes Low University based (Brazil) and
et al.122/ 2 treatment groups, females, mean age 40.5 years, with therapy + SCTG + CAF KTT, MRC, PPD, RH, supported by the State of São
Santamaria 24 mo duration one maxillary Miller Class I or II 2) SCTG + CAF SCRC/PCR (Manual Paulo Research Foundation
et al.120 buccal gingival recession of at least probe and digital (FAPESP)
2 mm caliper)
A total of 40 defects were treated (20
per group) All patients completed the
6 mo evaluation, whereas 36 the
24 mo follow‐up
(Continues)
|
99
100 | CHAMBRONE ET AL.
ABN/P‐15, anorganic bone mineral/cell binding peptide; ACC, aesthetic condition change; ADMG, acellular dermal matrix graft; CAF, coronally advanced flap; CAL, clinical attachment level; DFDBA, deminer-
KTT, keratinized tissue thickness; KTW, keratinized tissue width; LPF, laterally positioned flap; MRC, mean root coverage; NCCL, noncarious cervical lesion; POPain, level of pain recorded 1 wk after sur-
gery; RCR, resin composite restoration; RCT, randomized controlled trial; RH, root hypersensitivity; RMGI, resin‐modified glass ionommer; SCRC/PCR, sites with complete root coverage/percentage of com-
alized freeze‐dried bone allograft; EMD, enamel matrix derivative; ePTFE, expanded polytetrafluorethylene; GRD, gingival recession depth; GRW, gingival recession width; GTR, guided tissue regeneration;
supported by the State of São
(FAPESP)
dietary habits (ie, erosion) can cause noncarious cervical
notes
54,74–76,127
lesions.
Despite the possibility of restoring these defects with resin‐
Risk of
Low
Low
bias
Despite ACC being conducted by two dentists unaware of the surgical procedures performed, blinding of examiners regarding the clinical outcomes was not reported.
of the exposed root surface can prevent adequate improvement
of the esthetic condition.54 Also, because the original position of
Blindness of
examiners
Yes
Adequate
Adequate
Adequate
Adequate
random
ing for the preparation of the current review), found only three
randomized controlled trials (two randomized controlled trials con-
ACC, CAL, GRD, KTW,
SCRC/PCR (Manual
probe and digital
caliper)
material (if used), and complete root coverage. The binary depen-
dent variable was complete root coverage (yes was coded as 1
of at least 3 mm
and no was coded as 0), and the independent variables were use
Participants
per group)
2 treatment groups,
RCT, parallel design,
6 mo duration
statistically significant.
Table 3 shows the findings of the meta‐analysis performed. It
Sangiorgio et al.119/
T A B L E 3 Mixed‐effects logistic regression analysis estimating the could not have been adequately reported in the papers. Moreover, it
association between complete root coverage and receipt site should be taken into consideration that differences between the
characteristics included randomized controlled trials may occur because such trials
OR SE z P > |z| 95% CI cannot always illustrate how the study was actually conducted,
Type of PPS 0.21 0.81 −1.91 0.05 −3.15 to 0.03 rather only what has been published in the final paper(s).8 As a
procedure (SCTG) result, an evident complexity in interpreting their outcomes strength-
PPS associated with 1.41 0.83 0.41 0.67 −1.29 to 1.99 ens the condition that a randomized controlled trial has to report as
restoration (no.)
completely as possible (and in a transparent manner) the main crite-
Restorative 0.28 0.86 −1.47 0.14 −2.96 to 0.42 ria employed in the preparation of its research protocol. As such, it
material (RCR)
will provide the clinicians and experts who read it the opportunity to
95% CI, 95% confidence interval; OR, odds ratio; PPS, periodontal plastic understand and distinguish what has been achieved.8
surgery; RCR, resin composite restoration; SCTG, subepithelial connective
Accordingly, it is desirable that future randomized controlled tri-
tissue graft; SE, standard error; z, Wald z‐value.
als should present their individual patient data. It has been shown by
achieved comparable results 6 months following surgical proce- one of the included systematic reviews that meta‐analyses of indi-
dures. However, there was a trend for better outcomes (ie, com- vidual patient data can fully investigate, adjust, and assess the signif-
plete root coverage) when subepithelial connective tissue grafts icance of individual, baseline, and patient/site‐level characteristics,9
were the periodontal plastic surgery procedure of choice (odds as well as avoid some forms of publication bias (they permit pooling
ratio = 0.21, P = 0.05). of estimates using data from trials that could not be included in pair-
wise meta‐analysis), and some of the problems caused by the use of
meta‐analyses containing aggregated patient data (eg, issues that are
7 | DISCUSSION not always able to prevent bias related to randomized controlled tri-
als design). Conversely, it may also be deemed that systematic
Serious appraisal of the base of evidence for health promotion reviews on individual patient data alike conventional systematic
requires use of a structured sequence of criteria to retrieve and reviews, are also liable to bias because they depend on the amount
extract the best pool of information. The overall outcomes reported of data retrieved for analysis, the researchers who conducted the
by the available systematic reviews on periodontal plastic surgery individual randomized controlled trials (free access to their study
clearly, adequately, and positively were able to translate the signifi- data), human resources (trained review teams), costs, and time.9
cance of these procedures for daily practice, and able to enlighten It is also desirable that the research protocols for both random-
the limitations to be considered in future research. ized controlled trials and systematic reviews are registered at inter-
It is important to consider that systematic reviews are planned national databases of prospectively registered protocols (eg,
to recognize, appraise, and combine information from clinical trials to Clinicaltrials.gov, CENTRAL, or PROSPERO). Protocol registers can
provide evidence‐based responses and alternatives to clinical control for bias, offer transparency in the clinical and review pro-
8,89,90,105
research problems. Queries linked to development of the cesses, increase quality, and improve confidence that the outcomes
clinical decision‐making process, estimation of the value of treatment of these types of study are indeed derived from the best quality
modalities, and assessment of disparities in daily practice, as well as methodology available. Furthermore, PROSPERO assists in counter-
aspects evidencing the need for further research, may encourage ing publication bias by providing a permanent record of prospec-
105
researchers to write a systematic review. As a result, these issues tively registered protocols, it protects against reporting biases by
can provide important scientific bases of information for clinicians revealing any divergences between the procedures or outcome mea-
because they identify current knowledge (ie, what is known and sures reported in the final publications and those planned in the reg-
what should be studied in future randomized controlled trials).105 istered protocols, and it allows those commissioning or planning
In order to increase such a base of evidence, well‐designed ran- future studies to identify whether there are any studies already
domized controlled trials aid in assembling suitable health care deci- ongoing that address their subject of interest.9
sions, provided that such trials clearly and entirely describe their In the present overview, it could be seen that within randomized
aims, methodology (ie, inclusion criteria, study population, interven- controlled trials and systematic reviews, patient selection was based
tions, and statistical analysis), results, agreements and disagreements on esthetic and/or functional conditions, and treatment was intended
8,89,90,105
with previous studies, and conclusions. Regarding the Latin to prevent continuing development of soft (gingival recession) or hard
American randomized controlled trials included in this review, most (root abrasion or caries) tissue defects. Consequently, patients’ con-
adequately fulfilled these criteria. However, and inherent to such a cerns must be carefully assessed before any periodontal plastic sur-
study design, some limitations may be found, independently of the gery technique is planned, with meticulous attention to whether it is
location/country in which a randomized controlled trial is performed. possible to accomplish the patient's desires using the proposed treat-
Consequently, the aim of systematic overview studies (like the pre- ment modality.3,4,6–9 Moreover, recent evidence indicates that over
sent) is not just to mention the Latin American studies (or arbitrarily the last two decades improvements on surgical instruments, flap
attribute risk of bias to them), but to identify the central points that preparation and suture refelected positvely on root coverage achieved
102 | CHAMBRONE ET AL.
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