ricardo de nardi fonoff vittorio moraschini.pdf · 3 ficha catalogrÁfica barboza m 829 moraschini...

UNIVERSIDADE FEDERAL FLUMINENSE

FACULDADE DE ODONTOLOGIA

USO DE MEMBRANA DE PLASMA RICO EM FIBRINA PARA O TRATAMENTO

DE RECESSÕES GENGIVAIS: UMA REVISÃO SISTEMÁTICA E META-ANÁLISE

Niterói

2015

2

UNIVERSIDADE FEDERAL FLUMINENSE

FACULDADE DE ODONTOLOGIA

USO DE MEMBRANA DE PLASMA RICO EM FIBRINA PARA O TRATAMENTO

DE RECESSÕES GENGIVAIS: UMA REVISÃO SISTEMÁTICA E META-ANÁLISE

VITTORIO MORASCHINI FILHO

Tese apresentada à Faculdade de Odontologia da Universidade Federal Fluminense, como parte dos requisitos para obtenção do título de Doutor, pelo Programa de Pós-Graduação em Odontologia. Área de Concentração: Clínica Odontológica Orientador: Profa. Dra. Eliane dos Santos Porto Barboza

Niterói

2015

3

FICHA CATALOGRÁFICA

M 829 Moraschini Filho, Vittorio O uso de membrana de plasma rico em fibrina para o tratamen- to de recessões gengivais: uma revião sistemática e meta-análise / Vittorio Moraschini Filho; orientadora: Prof.ª Eliane dos Santos Porto Barboza. – Niterói: [s.n.], 2015. xx f.:il. Inclui gráficos e tabelas. Tese (Doutorado em Odontologia)– Universidade Federal Fluminense, 2015. Bibliografia: f. x-y. 1. Retração gengival. 2. Cirurgia plástica. 3. Odontologia baseada em evidência. I. Barboza, Eliane dos Santos Porto [orien.]. II. Título. CDD 617.632

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BANCA EXAMINADORA

Profa. Dra. Eliane dos Santos Porto Barboza

Instituição: Universidade Federal Fluminense

Decisão: _________________________Assinatura: ________________________

Profa. Dra. Mônica Diuana Calasans Maia



Prof. Dr. Gustavo Oliveira dos Santos



Prof. Dr. Sergio Kahn

Instituição: Universidade Veiga de Almeida


Prof. Dr. Bernardo Oliveira de Campos

Instituição: Universidade Salgado de Oliveira


5

DEDICATÓRIA

Aos meus pais Vittorio Moraschini (in memoriam) e Angel

Aucar Moraschini (in memoriam) por todo carinho, amor,

exemplo e investimento nos meus estudos;

À minha esposa Daniela Moraschini por todo amor, carinho,

incentivo e compreensão nas horas de ausência;

Aos meus filhos Gabriella e Pedro, amores da minha vida;

As minhas irmãs Bárbara e Rebecca por serem minhas

segundas mães e meu porto seguro.

.

6

AGRADECIMENTOS

A minha orientadora Eliane dos Santos Porto Barboza por

ter acreditado em mim. Muito obrigado por todos os

ensinamentos e pela magnifica orientação não só

científica, mas para a vida;

Ao grupo de pesquisa que tenho a honra de participar e

especialmente aos colegas Diogo Luz, Diogo Moreira,

Glauco Velloso, Denise Mandarino e Telma Aguiar;

Ao amigo Gustavo Oliveira dos Santos pela parceria e

conselhos.

A coordenadora do PPGO Mônica Calasans pela

competência e por sempre se empenhar em atender as

minhas solicitações. Muito obrigado!

Enfim, a todos que direta ou indiretamente contribuíram

para a realização desse sonho!

.

7

RESUMO

Moraschini V. Uso de membrana de plasma rico em fibrina para o tratamento de

recessões gengivais: uma revisão sistemática e meta-análise [tese].

Niterói: Universidade Federal Fluminense, Faculdade de Odontologia; 2015.

O objetivo da presente revisão sistemática foi investigar à influência da

membrana de plasma rico em fibrina (PRF) nos resultados clínicos do tratamento de

recessões gengivais. Uma busca eletrônica sem restrição de datas ou idiomas em 4

banco de dados e uma busca manual em revistas regulares e na literatura cinza

foram realizadas em busca de artigos até junho de 2015. Os critérios de elegibilidade

foram estudos controlados randomizados (ECRs) e estudos controlados

prospectivos com período de acompanhamento ≥ 6 meses que compararam o

desempenho do PRF com outros biomateriais para o tratamento de recessões

gengivais classe I ou II de Miller. Para a meta-análise, o método de variância inversa

foi utilizado para o modelo de efeito fixo ou aleatório, dependendo da

heterogeneidade. As estimativas das intervenções foram expressadas em diferenças

médias em percentagem ou milímetros. Seis estudos clínicos randomizados e um

estudo clínico prospectivo foram incluídos nesse estudo. Não houve diferença

estatisticamente significativa para o recobrimento radicular e o nível de inserção

clínica entre os subgrupos analisados (P = 0.57 e P = 0.50, respectivamente). O

ganho de faixa de gengiva queratinizada foi significativamente maior (P = 0.04) no

subgrupo que utilizou o enxerto de tecido conjuntivo. Os resultados da meta-análise

sugerem que o uso da membrana de PRF não melhora os resultados clínicos do

tratamento de recessões gengivais classe I e II de Miller em relação ao recobrimento

radicular, ganho de espessura de gengiva queratinizada e nível de inserção clínica

quando comparado a outras modalidades de tratamento.

Palavras-chave: Recessão gengival; Cirurgia plástica; Fatores de crescimento;

Odontologia baseada em evidências; Meta-análise.

8

ABSTRACT

Moraschini V. Use of Platelet-Rich Fibrin membrane in the treatment of gingival

recession: a systematic review and meta-analysis [tese].

Niterói: Universidade Federal Fluminense, Faculdade de Odontologia; 2015.

The aim of this systematic review was to evaluate the effects of platelet-rich

fibrin (PRF) membranes on the outcomes of clinical treatments in patients with

gingival recession. Articles that were published before June 2015 were electronically

searched in four databases without any date or language restrictions and manually

searched in regular journals and gray literature. The eligibility criteria comprised

randomized controlled trials (RCTs) and prospective clinical trials with follow-up

periods of 6 months or more that compared the performance of PRF with other

biomaterials in the treatment of Miller class-I or -II gingival recessions. For the meta-

analysis, the inverse variance method was used in fixed or random effect models,

which were chosen according to heterogeneity. The estimates of the intervention

effects were expressed as the mean differences in percentages or millimeters. Six

RCTs and one prospective clinical trial were included in this study. Root coverage

and clinical attachment level did not differ significantly between the analyzed

subgroups (P = 0.57 and P = 0.50, respectively). The keratinized mucosa width gain

was significantly greater (P = 0.04) in the subgroup that was treated with connective

tissue grafts. The results of the meta-analysis suggest that the use of PRF

membranes did not improve the root coverage, keratinized mucosa width, or clinical

attachment level of Miller class-I and -II gingival recessions compared to the other

treatment modalities.

Keywords: Gingival recession; plastic surgery; Growth factors; Evidence-based

dentistry; Meta-analysis.

9

1 - INTRODUÇÃO

A recessão gengival é caracterizada como a exposição da superfície da raiz

dentária pela migração da margem do tecido gengival apicalmente em relação à junção

cemento-esmalte.1,2 As recessões podem ser isoladas ou múltiplas, e normalmente estão

associadas a condições anatômicas do tecido mole, como faixa estreita de mucosa

queratinizada, trauma crônico, doença periodontal e áreas de acúmulo de biofilme, como

restaurações mal adaptadas e apinhamento dentário.1,3 Além do comprometimento

estético, as recessões gengivais podem acarretar hipersensibilidade dentinária,

dificuldade de higienização, cáries radiculares e perda de inserção periodontal.4

Inúmeras técnicas foram propostas para o tratamento das recessões unitárias ou

múltiplas, sendo a técnica de avanço coronal do retalho (ACR) associada ao enxerto de

tecido conjuntivo subepitelial (ETCS), caracterizada como o padrão ouro.5,6 As principais

desvantagens do ETCS incluem a necessidade de uma área doadora, levando muitas

vezes a dor pós-operatória e a necessidade de grande quantidade de tecido para o

tratamento de recessões múltiplas.7 Portanto, biomateriais ou enxertos alternativos vem

sendo propostos, como por exemplo os plasmas autólogos,5 matriz derivada de esmalte8

e matriz acelular dérmica.9

Recentemente, o uso de plasmas ricos em fatores de crescimento foi proposto

para cirurgia plástica periodontal.5,10,11 Alguns estudos demonstraram o potencial dos

plasmas concentrados em estimular, através de fatores de crescimento, o reparo e a

regeneração dos tecidos moles e duros e diminuir o processo inflamatório, dor e

desconforto.12,13 Importantes fatores e citocinas, tais como fator de crescimento derivado

de plaquetas, fator de transformação de crescimento beta, fator de crescimento endotelial

vascular, fator de crescimento epidérmico derivado de plaquetas, são liberados durante o

preparo dos plasmas concentrados.12 Estes fatores, que também são encontrados nos

tecidos durante o processo natural de cicatrização, são responsáveis por regular os

eventos celulares como, indução, proliferação, diferenciação, quimiotaxia e síntese de

matriz extracelular,13 acelerando a mitose e proliferação de osteoblastos, tecidos

vasculares e síntese de colágeno.14

A membrana de PRF, segunda geração de plasmas concentrados, é um

biomaterial de fácil obtenção, baixo custo e que vem apresentando bons resultados na

implantodontia e em procedimentos de cirurgia plástica periodontal.15 Diferente do seu

antecessor, o plasma rico em plaquetas (PRP), o PRF não necessita de adição de

anticoagulantes e ativadores químicos, sendo a sua elaboração mais simples e rápida.16

10

Por apresentar uma malha de fibrina com arquitetura tridimensional rica em glicoproteínas

adesivas, alguns estudos mostram que os fatores de crescimento presentes nos plasmas

são mais expressivos e concentrados. Além disso, o PRF apresenta uma liberação de

fatores de crescimento e matriz de proteínas de forma mais lenta e duradoura, fazendo

com que apresente um desempenho significativamente melhor que o seu antecessor.17-19

Outra vantagem do PRF em relação ao PRP é a possibilidade de confecção de uma

membrana densa, rica em matriz de fibrina, que apresenta consistência ideal para

manipulação e sutura, ao contrário do PRP que apresenta arquitetura em forma de um

gel.20

As decisões na área de saúde devem ser embasadas preferencialmente em

evidências científicas. O estudo controlado randomizado (ECR) consiste em um estudo

experimental em humanos, que visa o conhecimento do efeito de intervenções em saúde.

Esse tipo de estudo é a ferramenta atual mais poderosa para a obtenção de evidências

para a prática clínica. Os ECRs são capazes de minimizar a influência de fatores de

confusão sobre relações da causa-efeito, por isso a sua relevância. No entanto, acima

dos ECRs, na pirâmide de evidência científica, encontram-se as revisões sistemáticas,

que são planejadas para responder a uma pergunta específica utilizando métodos

explícitos e sistemáticos para identificar, selecionar e avaliar criticamente os estudos. A

meta-análise é um método estatístico utilizado para integrar os resultados dos estudos

incluídos. Até o presente momento não há na literatura revisões sistemáticas avaliando a

utilização do PRF no tratamento de recessões gengivais. Dessa forma, esse estudo

buscou evidências científicas sobre a performance do PRF no tratamento de recessões

gengivais, embasado na hipótese de não haver diferença nos resultados clínicos quando

da utilização da membrana de PRF para o tratamento de recessões gengivais, comparado

a outros tipos de biomateriais.

Portanto, o objetivo da presente revisão sistemática e meta-análise foi investigar à

influência da membrana de PRF nos resultados clínicos no tratamento de recessões

gengivais.

11

2 - METODOLOGIA

A presente revisão sistemática foi registrada no PROSPERO (International

Prospective Register of Systematic Reviews) sob o número CRD42015026444.

A metodologia dessa revisão seguiu as recomendações do "Chrochrane Handbook for

systematic reviews of interventions".21 Com o objetivo de aumentar a qualidade e

transparência da pesquisa, as diretrizes do "PRISMA22 & AMSTAR23 checklits" foram

seguidas. Os questionamentos clínicos foram desmembrados e organizados utilizando a

estratégia "PICOS".24

Questionamento principal

Quais são os efeitos da membrana de PRF no tratamento de recessões

gengivais?

Relevância clínica

A utilização de plasmas autólogos ricos em fatores de crescimento, como o PRF,

vem crescendo a cada dia na periodontia.5 As principais características que encorajam o

uso do PRF na cirurgia plástica periodontal são a sua apresentação em forma de uma

membrana autóloga densa, a relativa facilidade de obtenção e a presença de fatores de

crescimento. Contudo, os benefícios do PRF ainda são controversos na literatura. Dessa

forma, esse estudo buscou dados científicos sobre a performance do PRF para o

tratamento de recessões gengivais, colaborando com os profissionais para a tomada de

cisão embasada em evidência científica.

Estratégia de busca

Uma busca eletrônica sem restrição de datas ou idiomas foi realizada no

PubMed/MEDLINE, Cochrane Central Register of Controlled Trials, Web of Science e

EMBASE até junho de 2015. Além disso, uma busca manual foi realizada nas seguintes

revistas regulares: Journal of Periodontology, Journal of Clinical Periodontology, Journal of

Periodontal Research e International Journal of Periodontics & Restorative Dentistry. Uma

busca na chamada "literatura cinza", na base de dados do ClinicalTrials.gov e nas

referências dos estudos incluídos ("cross referencing"), também foi realizada em busca de

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novos estudos.

Critérios de seleção

Essa revisão buscou por ECRs e estudos controlados prospectivos com período

de acompanhamento ≥ 6 meses que compararam o desempenho do PRF com outros

biomateriais em voluntários apresentando recessões gengivais classe I ou II de Miller,25

quando comparado a outros biomateriais. Os critérios de exclusão foram estudos em

animais, estudos cohort retrospectivos, estudos in vitro, série de casos, relato de casos e

revisões. Além disso, estudos em voluntários com doenças metabólicas descompensadas

ou doença periodontal ativa, foram excluídos.

Processo de seleção

O processo de pesquisa e triagem foi realizado por dois autores revisores (V.M.F

e E.P.B), primeiramente analisando títulos e resumos. Em uma segunda etapa, artigos

completos foram selecionados para leitura criteriosa e analisados segundo os critérios de

elegibilidade (inclusão/exclusão), para futura extração dos dados. Divergência entre os

revisores foram resolvidas através de criteriosa discussão. A concordância da busca entre

os dois revisores foi avaliada pelo teste estatístico Cohen's Kappa (k). Os autores dos

estudos incluídos, quando necessário, foram contatados por e-mail para esclarecimentos

de eventuais dúvidas.

Risco de viés e análise de qualidade

O risco de viés e a análise de qualidade dos estudos clínicos incluídos foi

realizada de forma independente por dois autores revisores (V.M.F e E.P.B), utilizando

uma ferramenta específica para estudos clínicos controlados ou controlados

randomizados ("Cochrane Collaboration's tool for assessing risk of bias").22 A análise de

cada estudo foi baseada em seis critérios: geração da sequência de voluntários (a

sequência de alocação foi realizada adequadamente?), randomização da sequência (a

sequência de voluntários foi randomizada adequadamente?), cegamento (os voluntários

foram cegados quanto ao tipo de intervenção?), dados não registrados (os dados não

registrados durante o estudo foram tratados adequadamente?), resultados relatados (os

resultados dos estudos estão livres de conflitos de interesse?) e outros tipos de viés (os

13

estudos estão aparentemente livre de outros tipos de risco de viés?). Os estudos que

cumpriram todos os critérios mencionados foram classificados como baixo risco de viés e

os estudos que não cumpriram um dos critérios foram classificados como risco moderado.

Quando dois ou mais critérios não foram cumpridos, os estudos foram considerados como

alto risco de viés.

Extração dos dados

Os seguintes dados foram extraídos dos estudos incluídos (quando disponíveis):

autores, desenho do estudo, período de acompanhamento, número de recessões

tratadas, número de participantes, variação de idade, gênero, número de fumantes,

classificação de Miller, sítios das recessões, técnica cirúrgica, média da diferença em

percentagem antes e após o tratamento em relação ao recobrimento radicular (RR),

média da diferença em milímetros antes e após o tratamento em relação ao nível de

inserção clínica (NIC) e faixa de gengiva queratinizada (FGQ), volume de coleta

sanguínea e parâmetros de centrifugação.

Análise estatística

As variáveis contínuas (RR, NIC e FGQ) dos estudos incluídos foram analisadas

em grupos e subgrupos através de meta-análise. A estimativa dos efeitos de intervenção

foram expressas em diferenças médias (DM) em percentagem ou milímetros com um

intervalo de confiança (IC) de 95%. O método de variância inverso foi utilizado para o

modelo de efeito aleatório ou o modelo de efeito fixo. A heterogeneidade foi avaliada

através do "chi-squared" teste e o possível impacto na meta-análise foi quantificado via I2.

Valores com até 25% foram classificados como de baixa heterogeneidade e valores de 50

e 70% foram classificados como média e alta heterogeneidade, respectivamente. Quando

uma significativa heterogeneidade foi encontrada (P < 0.10), os resultados do modelo de

efeito aleatório foram validados. Quando uma baixa heterogeneidade foi verificada, o

modelo de efeito fixo foi considerado. O nível de significância estatística foi determinado

em P < 0.05.

Os dados foram analisados usando o software estatístico "Review Manager -

5.2.8, The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark,

2014".

14

O viés de publicação foi graficamente explorado através de um gráfico tipo funnel

plot. A assimetria no "funnel plot" (estudos fora da área triangular) pode indicar possível

viés de publicação.

15

3 - ARTIGO PRODUZIDO

Use of Platelet-Rich Fibrin membrane in the treatment of gingival

recession: a systematic review and meta-analysis.

Vittorio Moraschini, DDS, MSc*; Eliane dos Santos Porto Barboza, DDS, MSc, PhD*

* Department of Periodontology, School of Dentistry, Fluminense Federal University,

Niterói, Rio de Janeiro, Brazil.

Corresponding Author:

Vittorio Moraschini

Department of Periodontology, School of Dentistry, Fluminense Federal University.

Rua Mario dos Santos Braga, 30, Centro, Niterói, Rio de Janeiro, Brazil. Cep.: 24020-140.

E-mail: [email protected]

Word count: 2765 / Number of Tables: 4 / Number of Figures: 3 / Number of References:

53

Running Title: Use of PRF membrane in the treatment of gingival recession.

Summary: The use of platelet-rich fibrin membranes did not improve the root coverage,

keratinized mucosa width, or clinical attachment level of Miller class-I and -II gingival

recessions compared to the other treatment modalities.

16

Abstract

Background: The aim of this systematic review was to evaluate the effects of platelet-rich

fibrin (PRF) membranes on the outcomes of clinical treatments in patients with gingival

recession.

Methods: Articles that were published before June 2015 were electronically searched in

four databases without any date or language restrictions and manually searched in regular

journals and gray literature. The eligibility criteria comprised randomized controlled trials

(RCTs) and prospective controlled trials with follow-up periods of 6 months or more that

compared the performance of PRF with other biomaterials in the treatment of Miller class-I

or -II gingival recessions. For the meta-analysis, the inverse variance method was used in

fixed or random effect models, which were chosen according to heterogeneity. The

estimates of the intervention effects were expressed as the mean differences in

percentages or millimeters.

Results: Six RCTs and one prospective clinical trial were included in this review. Root

coverage and clinical attachment level did not differ significantly between the analyzed

subgroups (P = 0.57 and P = 0.50, respectively). The keratinized mucosa width gain was

significantly greater (P = 0.04) in the subgroup that was treated with connective tissue

grafts.

Conclusions: The results of the meta-analysis suggest that the use of PRF membranes

did not improve the root coverage, keratinized mucosa width, or clinical attachment level of

Miller class-I and -II gingival recessions compared to the other treatment modalities.

Key Words: Gingival recession; plastic surgery; Growth factors; Evidence-based dentistry;

Meta-analysis

17

Introduction

Gingival recession is characterized by the exposure of the tooth root surface due to

the migration of the apical gingival margin tissue relative to the cement enamel junction.1,2

Single or multiple recessions are usually associated with the anatomical conditions of soft

tissue (e.g., narrow band of keratinized mucosa), chronic trauma, periodontal disease, and

areas of biofilm build-up (e.g., improperly adapted dental restorations/crowding).1,3 In

addition to cosmetic problems, gingival recession can also cause tooth sensitivity, hygiene

difficulties, root caries, and periodontal insertion loss.4

Numerous techniques have been proposed for the treatment of single or multiple

recessions. However, the combination of the coronally advanced flap (CAF) and

connective tissue graft (CTG) techniques is considered the gold standard.5,6 The main

disadvantage of the CTG technique is the requirement for donor tissue, which results in

postoperative pain, and a large amount of tissue is needed to treat multiple recessions.7

Consequently, biomaterials and alternative grafts, such as autologous plasma,5 enamel

matrix derivatives,8 and acellular dermal matrices, have been proposed.9

The use of plasma that is rich in growth factors for tissue regeneration has been

proposed in periodontal plastic surgery.5,10,11 Studies have demonstrated that the growth

factors in the plasma concentrates stimulate the repair and regeneration of soft and hard

tissues and that the plasma reduces inflammation and the subsequent pain and

discomfort.12,13 Growth factors and cytokines, such as platelet-derived growth factor

(PDGF), transforming growth factor-β (TGF-β), vascular endothelial growth factor (VEGF),

and platelet-derived epidermal growth factor (PD-EGF), are released during the

preparation of the plasma concentrates.12 These factors, which are also found in tissues

during the natural healing process, are responsible for regulating cellular events, such as

induction, proliferation, differentiation, chemotaxis, and extracellular matrix synthesis,13

accelerating mitosis and osteoblast proliferation, and synthesizing vascular tissue and

collagen.14

A platelet-rich fibrin (PRF) membrane is a readily available and inexpensive

biomaterial that is beneficial in implant dentistry and periodontal15 plastic surgery

procedures. In contrast to the previous biomaterial, platelet-rich plasma (PRP), the

preparation of PRF is simpler and faster because it does not require additional

anticoagulants and chemical activators.16 In addition, studies have shown that, compared

with PRP, PRF exhibits a greater expression and concentration of growth factors and

matrix proteins, which are released more slowly due to the three-dimensional architecture

of the adhesive glycoproteins in the fibrin and which results in significantly better

18

performance.17-19 Another advantage of PRF relative to PRP is that it results in a dense

fibrin-rich membrane matrix that has a consistency (gel form) that is better suited for

manipulation and suturing.20

The aim of this systematic review was to evaluate the effects of PRF on the

outcomes of the clinical treatments of patients with gingival recession.

Materials and Methods

The present systematic review was registered in PROSPERO under the number

CRD42015026444. The methodology of this study followed the recommendations of the

Cochrane Handbook for Systematic Reviews of Interventions.21 In order to increase the

quality and research transparency, the methodology adhered to the PRISMA22 and

AMSTAR23 guideline checklists. The clinical questions were organized according to the

PICOS24 strategy.

Objective

The aim of this systematic review was to evaluate the effects of the use of PRF on

the outcomes of the clinical treatments of patients with gingival recession.

Focus question

What are the effects of PRF membranes on the treatment of gingival recession?

Clinical relevance

The utilization of autologous plasma that is rich in growth factors, such as PRF, is

increasing daily in periodontics. For example, it has been used as an adjunct biomaterial in

periodontal plastic surgery.5 The main characteristics that encourage the use of PRF are

its presentation in the form of a dense autologous membrane, its relatively easy

acquisition, and its expression of growth factors. However, the benefits of PRF are still

controversial. This study searched for scientific evidence of the effects of the use of PRF

on the treatment of gingival recession.

Search strategy

Electronic searches were conducted in PubMed/MEDLINE, Cochrane Central

Register of Controlled Trials, Web of Science, and EMBASE for articles that were

published until June 2015 without restrictions on dates or language. In addition, manual

searches of the following regular journals were performed: Journal of Periodontology,

19

Journal of Clinical Periodontology, Journal of Periodontal Research, and International

Journal of Periodontics & Restorative Dentistry. Unpublished studies (gray literature) were

identified by searching the Open-GRAY database, and searches of the ClinicalTrials.gov

database and references of the included studies (cross referencing) were performed to

obtain new studies. The search strategy and the PICOS tool are presented in Table 1.

Selection criteria

This review included RCTs and prospective controlled trials with follow-up periods

of 6 months or more that compared the performances of PRF with CAF alone or in

combination with other biomaterials in patients with Miller class-I or -II gingival

recessions.25 The exclusion criteria included animal studies, retrospective cohort studies,

in vitro studies, case series, case reports, and reviews. In addition, studies of volunteers

with decompensated metabolic disorders or active periodontal disease were excluded.

Outcome measures

The primary outcome variable was the change in percentage of root coverage (RC).

The secondary outcome variables were clinical attachment level (CAL) and keratinized

mucosa width (KMW).

Screening process

The search and screening process was conducted by two of the authors (V.M.F and

E.P.B). The titles and abstracts were first analyzed, which was followed by the selection of

complete articles for careful reviewing and analysis according to the eligibility criteria for

future data extraction. Any disagreement between the reviewers was resolved through

careful discussion. The search agreement between the two reviewers was evaluated by

the Cohen's Kappa (k) test. When necessary, the authors of the examined studies were

contacted by e-mail for further clarification.

Assessments of the risk of bias and quality

The assessments of the risks of bias and quality of the clinical studies that were

included were performed independently by two authors (V.M.F and E.P.B) with the

Cochrane Collaboration's tool.26 The analysis of each study was based on the following six

criteria: sequence generation (was the allocation sequence adequately generated?),

allocation concealment (was the allocation adequately concealed?), blinding (was the

knowledge of the allocated intervention adequately prevented during the study?),

20

incomplete outcome data (were the incomplete outcome data adequately addressed?),

selective outcome reporting (were the study reports free of suggestions of selective

outcome reporting?), and other sources of bias (was the study apparently free of other

problems that could put it at a high risk of bias?). The studies that met all of the criteria

were classified to have a low risk of bias while those that did not meet a criterion were

classified as having moderate risk. When two or more criteria were not met, the studies

were considered to have a high risk of bias.

Data extraction

The following data, when available, were extracted from the included studies:

authors, study design, follow-up, number of treated recessions, number of subjects, age

range, gender, number of smokers, Miller class, site of recessions, surgical technique,

mean difference (MD) in RC between baseline and final follow-up, CAL, KMW, probing

depth, centrifugation system, volume of blood drawn, and centrifugation parameters.

Statistical analysis

The continuous variables (RC, CAL, and KMW) of the included studies were

categorized in groups and subgroups and analyzed in a meta-analysis with statistical

software. The estimates of the intervention effects (MD) were expressed as percentages

or millimeters with 95% confidence intervals (CIs). The inverse variance method was

utilized in the random effect and fixed effect models. Heterogeneity was assessed with the

chi-squared test, and the potential impact on the meta-analysis was quantified with I2.

Values up to 25% were classified as low heterogeneity and values up to 50% or 70% were

classified as medium or high heterogeneity, respectively. When significant heterogeneity

was observed (P < 0.10), the results of the random effects model were validated. When

low heterogeneity was found, the results of the fixed effects model were considered. The

level of statistical significance was set at P < 0.05.

Publication bias was graphically explored with funnel plots. Asymmetry in the funnel

plots (studies outside the triangular area) indicated potential publication bias.

21

Results

Literature search

The initial search produced 623 titles from MEDLINE/PubMed, 66 from the

Cochrane Central Register of Controlled Trials, 51 from the Web of Science, and 64 from

EMBASE. After the first evaluation (title and abstract assessment), 804 articles were

excluded. The main reasons for exclusion were studies without abstracts, duplicates, and

follow-up periods less than 6 months. Of the 12 potential articles, five studies27-31 were

excluded after careful reading because they did not meet the inclusion criteria. The

reasons for the exclusion of potential studies are presented in Table 2. Consequently,

seven studies,5,32-37 which were published between 2009 and 2015, were included in this

systematic review. The article search and selection process is presented in Figure 1.

The k values of agreement between the two authors/reviewers for potential article

inclusion (titles and abstracts) were 0.79 and 0.85 for the selected articles, which indicated

excellent agreement.21

Study Characteristics

The characteristics of the selected studies are presented in Table 3. One controlled

clinical trial5 and six RCTs32-37 (two36,37 with a parallel design and four32-35 with a split-

mouth design) were included in this systematic review. The number of participants in the

studies ranged from 2234 to 10,37 with their ages ranging from 18 to 52 years. A total of

342 gingival recessions were treated. All of the studies dealt with single or multiple Miller

class-I or -II recessions.25 Two studies32,33 analyzed only teeth from the anterior maxillary

region. The follow-up period ranged from 65,33-36 to 1232,37 months (mean: 7.7 months). All

of the articles investigated the PRF as the test group, while the control groups used

CAF,5,35,36 CTG33,34,37, or enamel matrix derivative (EMD).32 One study33 did not report

data on the inclusion of smoking volunteers.

The PRF membrane production methodology varied among the studies. None of

the studies conducted a biomolecular analysis to quantify or qualify the components, such

as the cells, growth factors, and cytokines, of the PRF membranes.

Assessments of risk of bias and quality

The results of the quality analyses of the included studies are presented in Table 4.

None of the studies obtained the highest score in the quality analysis. Allocation

concealment and Blinding were not reported by any of the included studies. Thus, they

22

were characterized as uncertain risk biases. Despite the six studies32-37 that were RCTs,

none of the studies reported adherence to the CONSORT statement recommendations.38

Meta-analysis

In the present study, a random effects model was utilized to evaluate the RC due to

the high heterogeneity that was found between the subgroups (P < 0.00001; I2 = 92%).

The use of PRF did not differ significantly (P = 0.57) compared with CAF, CTG, and EMD,

with a MD of 3.18 (95% CI: -7.76 to 14.1) (Figure 2A). For CAL, the random effects model

was also used due to the high heterogeneity among the analyzed subgroups (P < 0.00001;

I2 = 91%). After the analysis, the subgroups did not differ significantly (P = 0.50), with a

MD of -0.16 (95% CI: -0.61 to 0.30) (Figure 2B). The random effects model was utilized (P

= 0.01; I2 = 63%) for the evaluation of an increase in KMW. Only one subgroup (PRF vs.

CTG) showed a statistically significant difference in favor of CTG (P = 0.04), with a MD of -

0.38 (95% CI: -0.74 to -0.01) (Figure 2C).

Publication Bias

The funnel plot indicated asymmetry between the subgroups when RC was

analyzed, which indicated a possible publication bias. Two studies5,35 contributed to the

asymmetry that was presented outside the triangular area of the 95% CI region (Figure 3).

Discussion

A comprehensive search for studies, including electronic databases, regular

journals, and the gray literature, was performed. In order to avoid publication bias, there

were no restrictions on language or publication date. It was necessary to contact the

authors of one study34 that was included for further clarification. Only studies with at least

6 months of follow-up were selected for this review. This period was previously reported as

sufficient for tissue stability after periodontal plastic surgery.39

In the present study, six RCTs were selected. Bias is more likely to exist in

nonrandomized studies than in RCTs.40 However, no RCT that was included in this

systematic review met all the requisites of the quality analysis that was conducted or

reported adherence to the CONSORT-statement.38 Adherence to these guidelines is

important to increase the quality and transparency of health studies.41

Only one study5 included smoking volunteers. Despite the controversy in the

literature regarding the influence of smoking on periodontal surgery healing, Kaval et al.42

demonstrated in a recent prospective clinical study high success rates for the CAF

23

surgeries for root coverage in patients who smoked. In contrast, a meta-analysis43 showed

negative results of the interaction of smoking versus periodontal plastic surgery for gingival

recession recoating. Because PRF membranes are bioactive, the adverse effects of

tobacco and its products, including reduced immune and fibroblastic function, decreased

collagen production, and vascular changes,44,45 could reduce or impair the liberation of the

growth factors and cytokines of the PRF.

The studies that were included in this systematic review employed different

methods for the preparation of the PRF membranes. Furthermore, no article conducted a

PRF qualification or quantification in order to analyze the levels of the growth factors,

cytokines, or other biomolecular components.18 Therefore, each study might have

obtained membranes with different PRF characteristics, which limits the data

interpretation.

In this systematic review, the effects of the use of PRF membranes were compared

with the effects of three different techniques (CAF, CAF + EMD, and CAF + CTG) on the

treatment of gingival recession. The PRF had several useful features, including low cost,

relatively simple acquisition, no requirement for tissue donation, concentration of

cytokines, immune cells, and growth factors, and suturing suitability. In addition, studies

have demonstrated its potential to reduce postoperative symptoms18,33,46 and accelerate

tissue healing18,33 through the stimulation of angiogenesis and matrix biosynthesis.47

However, their relatively rapid degradation, with the subsequent reduction in their release

of molecules,18 could interfere with the early stabilization of periodontal tissues, unlike

grafts, such as the CTG, which is considered the gold standard in the treatment of gingival

recessions.5,6,48-50

The achievement of adequate root recoating and periodontal tissue regeneration

presents the biggest challenges in periodontal plastic surgery.49 A meta-analysis showed

no statistically significant difference in RC and CAL between the analyzed subgroups (P =

0.57 and P = 0.50, respectively). This either indicated that the biomaterials did not

influence the contents analyzed or that confounding factors, such as the gingival

phenotype of the participants, recession location, number of recessions (single or

multiple), and smoking, may have influenced the results. The results of another systematic

review evaluating different surgical techniques and biomaterials for the treatment of Miller

class-I and -II indicated that treatment with or without biomaterials may lead to predictable

RC. However, the use of CTG appears to improve long-term tissue stability and the use of

CAF in conjunction with CTG appears to yield higher RC than the use of PRF.51

24

The KMW gain was significantly increased (P = 0.04) in the CTG subgroup

compared with the PRF subgroup. This can be explained by the ability of CTG that is

removed from the palate to induce greater formation of keratinized epithelium.52 However,

a recent study that compared the combination of CTG + PRF vs. CTG alone observed a

tissue thickness gain in the test group, thus demonstrating a possible benefit of the use of

PRF.53

The low number of studies that was available in the literature was the main

limitation of this systematic review. Therefore, additional studies that analyze the

performance of PRF membranes in the treatment of gingival recessions are

recommended. These studies should preferably comprise RCTs with a split-mouth design

and follow the CONSORT statement recommendations38 in order to minimize and control

the risk of bias and confounding factors. Furthermore, a standardized protocol for the

preparation of PRF membranes should be followed in combination with a biomolecular

analysis that is performed in order to qualify and quantify the biocomponents that are

present in the membranes.

Conclusions

The results of the meta-analysis suggested that the use of PRF membranes did not

improve the RC, KTW, or CAL in the treatment of Miller class-I and -II gingival recessions

compared to the other treatment modalities. For KTW, there was a positive effect of the

CTG compared to PRF. Because the treatment of gingival recessions may be influenced

by numerous clinical parameters, a greater number of clinical studies, preferably RCTs

with a split-mouth design, larger sample size, and longer follow-up period, are essential to

support this conclusion.

Footnotes

* Review Manager (version 5.2.8; The Nordic Cochrane Centre, The Cochrane

Collaboration, Copenhagen, Denmark, 2014).

Acknowledgments

The authors would like to thank Dr. Gülnihal Eren, Department of Periodontology, School

of Dentistry, Ege University, Turkey, to provided us some missing information about your

study. The authors report no conflicts of interest related to this study.

25

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30

Table 1. Systematic search strategy (PICOS strategy).

Search strategy

Population #1. (Gingival recession[MeSH] OR gingival recessions[MeSH] OR Miller

class I OR Miller class II)

Intervention #2. (Plastic surgery[MeSH] OR periodontal plastic surgery OR

mucogingival surgery OR muco-gingival surgery OR root coverage)

Comparisons #3. (Platelet-rich fibrin vs. coronally advancement flap alone or in

combination with others biomaterials)

Outcomes #4. (Root coverage OR clinical attachment level OR keratinized mucosa

width OR probing depth)

Study design

Randomized controlled trials and prospective clinical trials

Search combination #1 AND #2 AND #3 AND #4

Database search

Language

No restriction

Eletronic databases PubMed/MEDLINE, Cochrane Central Register of Controlled Trials, Web

of Science and EMBASE

31

Table 02 - Excluded studies.

Reason for rejection Authors

Furcation defect

Sambhav et al. (2014);27 Bajaj et al. (2013)28

Letter to editor

Del Corso M et al. (2009)29

Narrative review

Anilkumar et al. (2009)30

Case report

Singh and Bharti (2013)31

32

Figure 01 - Flow diagram (PRISMA format) of the screening and selection process.

Full-text articles assessed for eligibility (n = 12)

Scre

en

ing

Elig

ibili

ty

Iden

tificatio

n

Inclu

ded

MEDLINE/PubMed Records identified through

database searching (n = 623)

Cochrane (CENTRAL) Records identified through


Records excluded (n = 799)

Full-text articles excluded (n = 5)

Web of Science Records identified through

database searching (n = 51 )

EMBASE Records identified through


Studies included in quantitative synthesis

(n = 7)

Studies included in qualititative synthesis

(n = 7)

33

Table 3. Main characteristics of selected studies.

Authors (year)

Study desing Follow-up

No. of treated recessions (per group)

No. of subjects

Age range (Mean) Gender

No. of smokers

Miller class Site of recessions

Surgical technique

Aroca et al. (2009)5 CCT 6 months

67 (G1) 67 (G2)

20

22-47 (31.7) M5 / F15

2 I and II Maxillary and mandibular

CAF + PRF (G1) CAF (G2)

Jankovic et al. (2010)32 RCT (split-mouth) 12 months

20 (G1) 20 (G2)

20

21-48 (NR) M8 / F12

0 I and II Maxillary anterior

CAF + PRF (G1) CAF + EMD (G2)

Jankovic et al. (2012)33 RCT (split-mouth) 6 months

15 (G1) 15 (G2)

15

19-47 (NR) M5 / F10

NR I and II Maxillary anterior

CAF + PRF (G1) CAF + CTG (G2)

Eren and Atilla (2013)34

RCT (split-mouth)

6 months

22 (G1) 22 (G2)

22

18-52 (33.8) M9 / F13



Padma et al. (2013)35 RCT (split-mouth) 6 months

15 (G1) 15 (G2)

15

18-35 (NR) NR

0 I and II

Maxillary and mandibular


Thamaraiselvan et al. (2015)36

RCT 6 months

10 (G1) 10 (G2)

20

21-47 (NR) M18 / F2



Tunali et al. (2015)37 RCT 12 months

22 (G1) 22 (G2)

10

25-52 (34.2) M4 / F6



34

Table 1. Continuation

Methods for PRF preparation

Authors (year)

Mean difference in RC between

baseline and final follow-up (%)

Mean difference in CAL between

baseline and final follow-up (mm)

Mean difference in KMW between baseline and final

follow-up (mm)

Mean difference in PD between

baseline and final follow-up (mm)

Volume of blood drawn

Centrifugation parameters

speed (RPM) x time (min)

Aroca et al. (2009)5 80.7 ± 14.7 (G1)

91.5 ± 11.4 (G2) 1.76 ± 1.56 (G1) 1.37 ± 0.62 (G2)

2.54 ± 0.85 (G1) 2.37 ± 0.89 (G2)

1.17 ± 0.41 (G1) 1.14 ± 0.34 (G2)

40ml 3,000 x 10

Jankovic et al. (2010)32 72.7 ± 9.55 (G1) 70.5 ± 11.7 (G2)

1.05 ± 0.45 (G1) 1.15 ± 0.65 (G2)

1.62 ± 0.28 (G1) 1.90 ± 0.81 (G2)

1.45 ± 0.51 (G1) 1.23 ± 0.65 (G2)

10ml 3,000 x 10

Jankovic et al. (2012)33

88.6 ± 10.6 (G1) 91.9 ± 15.4 (G2)

1.48 ± 0.4 (G1) 1.35 ± 0.38 (G2)

2.2 ± 0.54 (G1) 2.85 ± 0.45 (G2)

0.95 ± 0.41 (G1) 0.92 ± 0.48 (G2)

10ml 3,000 x 10


92.7 ± 13.7 (G1) 94.2 ± 12.1 (G2)

1.32 ± 0.55 (G1) 1.59 ± 0.65 (G2)

3.51 ± 1.28 (G1) 3.63 ± 1.43 (G2)

1.09 ± 0.29 (G1) 1.45 ± 0.60 (G2)

10ml NR x 12

Padma et al. (2013)35 100 ± 0.1 (G1) 68.4 ± 17.4 (G2)

1.00 ± 0.1 (G1) 2.00 ± 0.89 (G2)

5.38 ± 1.67 (G1) 4.63 ± 0.81 G2)

NR NR

10ml 3,000 x 10


74.1± 28.9 (G1) 65.0 ± 44.4 (G2)

1.20 ± 1.39 (G1) 1.70 ± 1.25 (G2)

2.70 ± 0.67 (G2) 2.80 ± 0.91 (G1)

1.00 ± 0.00 (G1) 1.00 ± 0.00 (G2)

10ml 3,000 x 10

Tunali et al. (2015)37

76.6 ± 13.2 (G1) 77.3 ± 17.4 (G2)

2.33 ± 0.90 (G1) 2.16 ± 0.79 (G2)

2.86 ± 0.69 (G1) 3.03 ± 0.74 (G2)

1.18 ± 0.33 (G1) 1.18 ± 0.35 (G2)

10ml 2,700 x 12

NR= not reported; G1= test group; G2= control group; M= male; F= female.

35

Table 4. Risk of bias and quality assessment of included studies.

Authors (year) Adequate sequence generation

Allocation concealment

Blinding

Incomplete outcome

data addressed

Selective outcome reporting

Free of other

soucers of bias

Estimated potencial risk of

bias

Aroca et al. (2009)5

Yes Unclear Unclear Yes Yes Yes Moderate




Yes Unclear Unclear No Yes Yes High



Padma et al. (2013)35




Tunali et al. (2015)37


36

Figure 2. Forest plot for the events root coverage (A); clinical attachment level (B), and keratinized mucosa width (C).

A

39

Figure 3. Funnel plot for the studies reporting the outcome root coverage.

40

4 - CONCLUSÕES

Os resultados da meta-análise sugerem que o uso da membrana de PRF

não apresenta melhores resultados para o tratamento de recessões gengivais classe

I e II de Miller em relação ao RR, NIC e FGQ quando comparado às outras

modalidades de tratamento. Em relação a FGQ, houve um efeito positivo do ETCS

quando comparado ao PRF. Como os tratamentos das recessões gengivais podem

ser influenciados por inúmeros parâmetros clínicos, um maior número de estudos,

de preferência ECRs com desenho de boca dividida, com um maior número de

amostras e um maior período de acompanhamento, são fundamentais para dar

suporte a essa conclusão.

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