Effects of smoking on tooth loss among individuals under periodontal maintenance therapy: a systematic review and meta-analysis

Os efeitos do tabagismo sobre a perda dentária em indivíduos em terapia periodontal de suporte: uma revisão sistemática e meta-análise

Los efectos del consumo de tabaco en la pérdida de dientes entre personas con una terapia de mantenimiento periodontal: un revisión sistemática y metaanálisis

Thais Ribeiral Vieira Carolina Castro Martins Renata Magalhães Cyrino Andrea Mara Oliveira Azevedo Luís Otávio Miranda Cota Fernando Oliveira Costa About the authors

Abstract:

Dental mortality has been reported by longitudinal studies on periodontal maintenance therapy (PMT), but the independent effect of smoking on tooth loss (TL), adjusted for important confounding variables, has been poorly evaluated. This systematic review aimed to assess and analyze the isolated effect of smoking TL among individuals undergoing PMT. Electronic, manual, grey literature, and recent articles (from April 2018) were searched, with no restriction regarding language; respective dates of publication were included. Epidemiological clinical studies reporting TL data among smokers undergoing PMT in comparison to nonsmoker control groups were selected. Methodological quality was assessed using the Newcastle-Ottawa Scale. Meta-analysis was performed, as well as I2 heterogeneity and sensitivity tests. Evidence quality was assessed using GRADE (Grading of Recommendations, Assessment, Development and Evaluation). Eleven papers were included in the systematic review: four case-control and seven cohort studies. Ten out of the 11 studies concluded that smoking was an important risk factor for the occurrence of TL. Meta-analysis of four of the cohort studies found that smokers had 3.24 times the chance of occurrence of TL than nonsmokers undergoing PMT (95%CI: 1.33-7.90). Overall, studies’ risk of bias was low. The quality of the scientific evidence moderately supports that smokers undergoing PMT have a greater chance of TL than nonsmokers.

Keywords:
Tooth Loss; Smoking; Periodontitis; Meta-analysis

Resumo:

A perda dentária tem sido relatada em estudos longitudinais sobre terapia periodontal de suporte (TPS), mas houve menos investigação sobre o efeito independente do tabagismo sobre a perda dentária, ajustado por importantes variáveis de confusão. Esta revisão sistemática teve como objetivo avaliar e analisar o efeito isolado do tabagismo sobre perda dentária em indivíduos em TPS. A estratégia incluiu fontes eletrônicas, busca manual, literatura cinzenta e artigos recentes (publicados a partir de abril de 2018), sem restrição quanto ao idioma; as datas de publicação foram incluídas. Foram selecionados estudos clínico-epidemiológicos com dados sobre perda dentária entre tabagistas em TPS, comparado com grupos-controle de não-tabagistas. A qualidade metodológica foi avaliada com a Escala de Newcastle-Ottawa. Foi realizada uma meta-análise, assim como, I2 testes de heterogeneidade e de sensibilidade. A qualidade das evidências foi avaliada com a escala GRADE (Grading of Recommendations, Assessment, Development, and Evaluation). Onze artigos foram incluídos na revisão sistemática, sendo quatro estudos de casos e controles e sete estudos de coorte. Dez dos 11 estudos concluíram que o tabagismo é importante fator de risco para a ocorrência de perda dentária. De acordo com a meta-análise de quatro dos estudos de coorte, os tabagistas em TPS apresentavam risco 3,24 vezes maior de ocorrência de perda dentária quando comparados aos não tabagistas (IC95%: 1,33-7,90). O risco global de viés nos estudos foi baixo. A revisão mostrou qualidade moderada das evidências científicas de que os tabagistas em TPS apresentam risco maior de perda dentária do que os não-tabagistas.

Palavras-chave:
Perda de Dente; Fumar; Periodontite; Metanálise

Resumen:

La mortalidad dental ha sido estudiada en estudios longitudinales acerca de la terapia de mantenimiento periodontal (TMP), pero el efecto independiente de fumar en la pérdida de dientes (PD), ajustado a variables de confusión importantes, se ha evaluado muy poco. Esta revisión sistemática tuvo como objetivo evaluar y analizar el efecto aislado de fumar en la PD con personas bajo TMP. Se investigó en medios electrónicos, manuales, literatura gris, y artículos recientes (desde abril 2018), sin restricciones respecto a la lengua; incluyendo sus respectivas fechas de publicación. Además, se seleccionaron estudios clínicos epidemiológicos que trabajaban sobre datos de PD entre fumadores que estaban bajo TMP, en comparación con grupos de control de no fumadores. La calidad metodológica se evaluó usando la Escala de Newcastle-Ottawa. Se realizó un metaanálisis, así como tests de heterogeneidad I2 y sensibilidad. La evidencia de calidad fue evaluada usando GRADE (Grading of Recommendations, Assessment, Development and Evaluation). Se incluyeron once trabajos en la revisión sistemática (cuatro de caso-control y siete estudios de cohortes). Diez de los once estudios concluyeron que fumar era un factor de riesgo importante para la ocurrencia de PD. Los metaanálisis de cuatro de los estudios de cohorte descubrieron que los fumadores tenían 3,24 veces más la oportunidad de sufrir PD, en comparación con los no fumadores TMP (IC95%: 1,33-7,90). En general, el riesgo de sesgo en los estudios fue bajo. La calidad de la evidencia científica respaldó moderadamente que los fumadores bajo TMP contaban con más oportunidad de PD que los no fumadores.

Palabras-clave:
Pérdida de Diente; Fumar; Periodontitis; Metaanálisis

Introduction

Periodontal maintenance therapy (PMT) can be considered a critical factor for success in controlling periodontitis and in the long-term maintenance of teeth 11. Lee CT, Huang HY, Sun TC, Karimbux N. Impact of patient compliance on tooth loss during supportive periodontal therapy: a systematic review and meta-analysis. J Dent Res 2015; 94:777-86.. In addition, neglecting a regular PMT program has been associated with increased risk of reinfection and progression of periodontitis, as well as increased tooth loss (TL) 22. Parameter on periodontal maintenance. J Periodontol 2000; 71 Suppl 5S:849-50.,33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300..

During periodontal clinical reevaluation in PMT, it is important to analyze the biological, behavioral, and social risk variables associated with periodontal disease, especially smoking, dental plaque scores, and diabetes mellitus 44. Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000 1997; 14:9-11.,55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.,66. Schatzle M, Faddy MJ, Cullinan MP, Seymour GJ, Lang NP, Burgin W, et al. The clinical course of chronic periodontitis: V. Predictive factors in periodontal disease. J Clin Periodontol 2009; 36:365-71.. Moreover, many other factors can affect clinical outcomes during PMT: degree of compliance and adherence to the proposed recommendations, oral hygiene practice, age, smoking status, systemic diseases that can compromise the immune response, initial tooth prognosis, tooth location, residual periodontal pockets, and bleeding on probing (BOP). These factors have been cited as critical for periodontal condition stability 77. Wood WR, Greco GW, McFall WT. Tooth loss in patients with moderate periodontitis after treatment and long-term maintenance care. J Periodontol 1989; 60:516-20.,88. Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: a systematic review of observational studies. J Clin Periodontol 2010; 37:675-84..

Identification of risk variables for TL in PMT programs can help clinicians and periodontists establish the frequency of recall visits, as well as improve the adherence to maintenance programs, with greater compliance from individuals 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.. Several studies have demonstrated the effectiveness of periodontal therapy in reducing TL rates, as well as the importance of PMT compliance 1010. Chace R, Low SB. Survival characteristics of periodontally-involved teeth: a 40-year study. J Periodontol 1993; 64:701-5.,1111. Tonetti MS, Steffen P, Muller-Campanile V, Suvan J, Lang NP. Initial extractions and tooth loss during supportive care in a periodontal population seeking comprehensive care. J Clin Periodontol 2000; 27:824-31.,1212. Al-Shammari KF, Al-Khabbaz AK, Al-Ansari JM, Neiva R, Wang HL. Risk indicators for tooth loss due to periodontal disease. J Periodontol 2005; 76:1910-8.,1313. Lorentz TC, Cota LO, Cortelli JR, Vargas AM, Costa FO. Tooth loss in individuals under periodontal maintenance therapy: prospective study. Braz Oral Res 2010; 24:231-7..

Smoking is an important risk factor for periodontitis. Various studies have shown that this deleterious habit is strongly associated with increased susceptibility to periodontitis, increased periodontitis severity and progression, as well as higher TL 1414. Meinberg TA, Canarsky-Handley AM, McClenahan AK, Poulsen DD, Marx DB, Reinhardt RA. Outcomes associated with supportive periodontal therapy in smokers and nonsmokers. J Dent Hyg 2001; 75:15-9.,1515. Papantonopoulos GH. Effect of periodontal therapy in smokers and non-smokers with advanced periodontal disease: results after maintenance therapy for a minimum of 5 years. J Periodontol 2004; 75:839-43.,1616. Labriola A, Needleman I, Moles DR. Systematic review of the effect of smoking on nonsurgical periodontal therapy. Periodontol 2000 2005; 37:124-37.,1717. Heasman L, Stacey F, Preshaw PM, McCracken GI, Hepburn S, Heasman PA. The effect of smoking on periodontal treatment response: a review of clinical evidence. J Clin Periodontol 2006; 33:241-53..

Although TL has already been reported by longitudinal studies among individuals undergoing PMT 11. Lee CT, Huang HY, Sun TC, Karimbux N. Impact of patient compliance on tooth loss during supportive periodontal therapy: a systematic review and meta-analysis. J Dent Res 2015; 94:777-86.,77. Wood WR, Greco GW, McFall WT. Tooth loss in patients with moderate periodontitis after treatment and long-term maintenance care. J Periodontol 1989; 60:516-20.,88. Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: a systematic review of observational studies. J Clin Periodontol 2010; 37:675-84.,1818. Hirschfeld L, Wasserman B. A long-term survey of tooth loss in 600 treated periodontal patients. J Periodontol 1978; 49:225-37.,1919. Checchi L, Montevecchi M, Gatto MR, Trombelli L. Retrospective study of tooth loss in 92 treated periodontal patients. J Clin Periodontol 2002; 29:651-6.,2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.,2121. Axelsson P, Nyström B, Lindhe J. The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. Results after 30 years of maintenance. J Clin Periodontol 2004; 31:749-57.,2222. Fardal O, Johannessen AC, Linden GJ. Tooth loss during maintenance following periodontal treatment in a periodontal practice in Norway. J Clin Periodontol 2004; 31:550-5.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,2525. Carnevale G, Cairo F, Tonetti MS. Long-term effects of supportive therapy in periodontal patients treated with fibre retention osseous resective surgery. I: recurrence of pockets, bleeding on probing and tooth loss. J Clin Periodontol 2007; 34:334-41.,2626. Matuliene G, Pjetursson BE, Salvi GE, Schmidlin K, Brägger U, Zwahlen M, et al. Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol 2008; 35:685-95., the independent effect of smoking on TL, adjusted for important confounding variables (i.e. age, gender, diabetes, and socioeconomic level) in individuals undergoing PMT, has not yet been evaluated through systematic review and meta-analysis. Therefore, this paper aimed to evaluate scientific evidence of the independent effect of smoking on TL among individuals undergoing PMT.

Material and methods

This systematic review was registered in PROSPERO (n. CRD42016026083) and was conducted in agreement with the guidelines of Transparent Reporting of Systematic Reviews and Meta-Analyses (PRISMA Statement) 2727. Moher D, Liberati A, Tetzlaff J, Altman DG; Prisma Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6:e1000097..

Focal question

Our clinical question (PICO) was: “what is the effect of smoking on tooth loss, for individuals undergoing periodontal maintenance therapy?” (P = individuals undergoing PMT; I = smoking; C = nonsmoker individuals undergoing PMT; O = tooth loss).

Inclusion criteria

Epidemiological clinical studies (observational studies and clinical trials), containing data on TL among smokers and nonsmokers undergoing PMT, were included. There was no restriction regarding age, language, date of publication or follow-up period.

Exclusion criteria

Papers with absence of nonsmokers (control group), case reports or case series, letters to the editor, and literature reviews were excluded.

Search strategy

The databases included MEDLINE via PubMed (https://pubmed.gov), Web of Science (https://isiknowledge.com), Cochrane Library (https://cochrane.org/index.htm), and Scopus (https://scopus.com).

No restrictions were imposed with regard to language or year of publication. MeSH terms, keywords, and other selected terms were searched. Boolean operators (OR, AND) were used to combine searches. The following search strategy was used in MEDLINE, Web of Science, Cochrane and Scopus: ((periodontal disease [Mesh] OR periodontitis [Mesh] OR periodontitis OR maintenance periodontal therapy OR periodontal maintenance OR supportive periodontal therapy OR maintenance care OR long-term care [Mesh] OR long-term maintenance) AND (smoke [Mesh] OR smoke OR smoker* OR tobacco OR tobacco smoker*) AND (tooth loss [Mesh] OR tooth loss OR tooth mortality OR dental mortality)).

A manual and grey literature search was performed through the ISRCTN Registry (http://isrctn.com) and Clinical Trials (https://clinicaltrials.gov) databases. Manual searches in the reference lists of included articles were also performed. The reference list retrieved by the electronic databases search was organized by EndNote software, version 17.0 (https://www.endnote.com/).

Initially, 780 articles were found. After the removal of 138 duplicates, 642 articles were available for selection. The selection of articles was based on abstracts and titles and carried out independently by three trained and calibrated researchers (A.M.O.A., R.M.C., and T.R.V.). An initial reading of a 10% sample of the list was performed and the kappa agreement was of 0.84. Thus, the three researchers continued reading the remaining articles. Disagreements were resolved by discussion and consensus. After this phase, 44 studies were selected for full text analysis. This analysis was performed independently by each of the three researchers and disagreements were again resolved by discussion and consensus (Figure 1). When a study had missing data or additional information was needed, the corresponding author was contacted.

Figure 1
Flowchart: search strategy and screening process.

Data extraction and methodological quality assessment

Data extraction followed a form in which the following information was extracted: study design, sample size, interval time, dental care protocols and procedures, smoking status, and number and/or mean of teeth lost during PMT (Tables 1 and 2, for cohort studies and case-control studies, respectively).

Table 1
Cohort studies characteristics.
Table 2
Case-control studies characteristics.

The methodological quality of the included studies was assessed via the Newcastle-Ottawa Scale (NOS), by two independent reviewers (A.M.O.A. and T.R.V.). Case-control and cohort studies were evaluated by the NOS for case-control studies and the NOS for cohort studies, respectively. Criteria was comprised of three main items: sample selection, comparability, and exposure (Tables 3 and 4).

Selection: whether the study had data on smoking status during PMT, to determine cases and/or exposed individuals.

Table 3
Quality assessment of included cohort studies based on the Newcastle-Ottawa Scale.
Table 4
Quality assessment of included case-control studies based on the Newcastle-Ottawa Scale.

Comparability: whether smoking was adjusted for two or more factors, e.g. diabetes, age, gender, or other risk variables. In this case, a maximum of two points could be assigned (one for each confounder).

Outcome of interest or Exposure: whether TL was clinically assessed using clinical examination, radiographic examination, through existing recorded data, or through self-report.

For case-control studies, the NOS scale ranges from 0 (lower methodological quality) to 9 (higher methodological quality). For cohort studies, it ranges from 0 to 10.

Meta-analysis

Comprehensive Meta-Analysis Software, version 2 (https://www.meta-analysis.com/), was used for meta-analysis. Odds ratio (OR) and 95% confidence interval (95%CI) for TL in smokers and nonsmokers were extracted as reported in the studies. I2 heterogeneity and sensitivity tests were performed 2828. Deeks JJ, Higgins JPT, Altman DG; Cochrane Statistical Methods Group. Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions. Chichester: Willey-Blackwell; 2015. p. 243-96.. For medium to moderate heterogeneity and for low heterogeneity (< 25%), the random effect (≥ 25%) and the fixed effect were used, respectively. Funnel plot analysis was not performed due to the absence of sufficient study numbers 2929. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629-34.. Instead, publication bias was analyzed qualitatively.

Quality of evidence

Two reviewers (C.C.M. and F.O.C.) evaluated evidence quality using GRADE (Grading of Recommendations, Assessment, Development and Evaluation) 3030. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008; 336:924-6.. Disagreements were resolved by discussion and consensus. GRADE evaluates evidence quality as high, moderate, low, or very low. Evidence quality assessment was performed through the GRADE PRO software (https://www.gradepro.org) (Box 1).

Box 1
Quality of evidence evaluated through GRADE (Grading of Recommendations, Assessment, Development and Evaluation).

Results

Selection of studies

Eleven papers were included in this systematic review (Figure 1): seven cohort studies 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.,99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.,2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77., and four case-control studies 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605.. The final selection included no controlled clinical trials.

Quality assessment

Results of the quality assessment are summarized in Tables 3 and 4, for case-control and cohort studies, respectively. Studies were evaluated using the NOS, with scores varying from 7 to 9 for cohort studies, and 7 to 8 for case-control studies. Among cohort studies, one did not specify TL rate of the sample 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100., while four studies adjusted smoking only for one confounding factor 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77.. Among case-control studies, TL rate of samples was not specified 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605., and only one confounding factor was adjusted 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605..

Studies description

Overall, follow-up time of individuals undergoing PMT ranged from 1 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11. to 36 years 2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.. The study sample included a minimum of 288 and a maximum of 6,431 individuals 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.. Three studies were case-control studies nested in cohort studies, including 238 individuals 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605.. Some studies 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87. evaluated the number of teeth lost and TL percentage in comparisons between regular complier (RC) and irregular complier (IC) individuals. One study 3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605. evaluated the number of teeth lost and TL percentage in individuals with diabetes and good glycemic control compared to individuals with diabetes and poor glycemic control, and to individuals without diabetes.

The 11 selected studies recruited and treated individuals at different clinics. Participants of five studies were treated in private clinics 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605. and participants of six studies were treated in university clinics 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.,2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.. One study had a mixed sample, with individuals from private and university clinics 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11..

Recall visits during PMT were performed with different time intervals, taking into consideration individuals’ degree of compliance: 3 months 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11., 4 months 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300., 4-6 months 3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605., 6 months 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8., 3-12 months 3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9., 12 months 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77., and 18 months 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8..

Besides their different recall time intervals, studies also diverged in relation to dental care protocols and procedures performed during PMT. In one study 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100., dental prophylaxis and subgingival debridement were performed when the operator deemed necessary, and periodontal conditions were documented annually with probing depth (PD) and plaque index (PI) values. In another study 2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75., all subjects were instructed to perform their own PMT. At each initial return visit, they underwent a questionnaire by a trained interviewer, to record reasons for TL. In other studies 2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77., all subjects underwent the following PMT protocol: oral hygiene instructions, scaling and root planning, crown polishing, and surgical periodontal therapy (when indicated). Studies evaluated different periodontal parameters: BOP, PI, PD, and clinical attachment level (CAL) 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8., as well as PI, PD, BOP, and bone level radiographic measurements (Table 1). During the monitoring visits, complete periodontal clinical examinations, nonsurgical and surgical procedures were also performed 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11. (Table 2).

Smoking status characterization

Different definition criteria for smoking status were adopted. Some studies 3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605. classified smokers and former smokers (individuals who reported having smoked more than 100 cigarettes during their lifetime) and nonsmokers according to the criteria by Tomar & Asma 3636. Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 2000; 71:743-51.. Other studies 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77. classified nonsmokers and former smokers (individuals who smoked 10-19 cigarettes per day) and smokers (individuals who smoked more than 19 cigarettes per day) according to a previous study 3737. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev Dent 2003; 1:7-16.. In a study by Ravald & Johansson 3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9., subjects were divided into three categories: smokers who consume 1-9 cigarettes per day, smokers who consume more than 10 cigarettes per day, and nonsmokers. In a study by Leung et al. 2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75., 11.3% of the individuals were classified as current smokers, with self-reported consumption of 0.5-56.9 packets/year. In a study by Chambrone & Chambrone 2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64., individuals were classified as smokers or nonsmokers, but the number of cigarettes smoked per day was not reported. In a study by Fisher et al. 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8., smoking status was determined by self-report, while an analysis of expired carbon monoxide concentration identified and quantified the smoking status. A concentration of ≤ 8ppm (parts per million) defined nonsmokers, and a concentration of > 8ppm defined smokers, according to the criteria by Scott et al. 3838. Scott DA, Palmer RM, Stapleton JA. Validation of smoking status in clinical research into inflammatory periodontal disease. J Clin Periodontol 2001; 28:715-22.. A study by König et al. 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100. classified smokers and nonsmokers but did not describe smoking status.

Summarization of findings

Ten out of 11 selected studies in this systematic review concluded that smoking was an important factor, significantly associated with TL. Smokers had a greater chance of TL in comparison to nonsmokers [(crude OR = 8.0; 95%CI: 1.6-39.0) 3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.; (adjusted OR = 4.76; 95%CI: 1.42-15.89) 2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.; (adjusted OR = 4.1; 95%CI: 1.98-11.6) 3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605.; (adjusted OR = 3.41; 95%CI: 1.26-11.41) 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.].

TL occurrence due to periodontal reasons was 2.5 times higher in smokers than in nonsmokers 2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.. According to one study 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100., smoking was significantly associated with TL (r2 = 0.12). The same association was also observed among individuals in a private clinic, where smoking was significantly associated with TL (adjusted OR = 3.1; 95%CI: 1.98-11.6) 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11..

Smokers among IC individuals (OR = 7.3; 95%CI: 1.17-14.9) presented a greater chance of TL when compared to smokers among RC individuals (OR = 4.2; 95%CI: 1.42-9.89) 3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77.. In another study from the same research group 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8., IC smokers lost significantly more teeth (adjusted OR = 4.22; 95%CI: 2.01-8.78).

Only one study did not find a statistically significant difference in the mean number of teeth lost between smokers and nonsmokers (at baseline and after three years of PMT) (p > 0.05) 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8..

Four studies were included in the meta-analysis 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,3131. Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77. (Figure 2). There was a statistically significant association of TL and smoking habits (OR = 3.24; 95%CI: 1.33-7.90). The quality of evidence was determined to be moderate for smokers undergoing PMT and for odds of TL (Box 1).

Figure 2
Meta-analysis.

Discussion

In this systematic review and meta-analysis, smokers undergoing PMT presented a greater chance of TL when compared to nonsmokers in 10 out of 11 selected studies, and also in the meta-analysis. However, several factors seem to have impacted these findings.

Although the meta-analysis presented a relative statistical homogeneity, it was limited due to the inclusion of only four studies. Seven studies were excluded from the meta-analysis due to insufficient data for extraction.

Other limitations can also be pointed out, such as clinical and methodological heterogeneity among included studies. The quality of the evidence was determined to be moderate, since there was “serious” imprecision due to the wide confidence interval. Moreover, publication bias was observed 3939. Iorio A, Spencer FA, Falavigna M, Alba C, Lang E, Burnand B, et al. Use of GRADE for assessment of evidence about prognosis: rating confidence in estimates of event rates in broad categories of patients. BMJ 2015; 350:h870.. These issues can limit the validation of the findings, indicating the need for additional, more robustly designed studies, including a greater number of individuals.

There were differences in time intervals for recall visits during PMT, varying from 3 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.,3333. Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.,3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11. to 18 months 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.. In addition to the differences in reevaluation intervals, the studies also diverged in relation to maintenance protocols and periodontal procedures performed during PMT, including the evaluation of different clinical parameters. Additionally, different criteria to establish regular or irregular PMT compliance may have had a high impact on studies’ different periodontal and TL outcomes.

Regarding smoking status characterization, different criteria were considered. In some studies 33. Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.,99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.,2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.,2424. Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.,3232. Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77.,3535. Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605., individuals were grouped into smokers or nonsmokers according to self-report. Analysis of expired carbon monoxide concentration was also employed 55. Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.. One study 2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100. classified smokers and nonsmokers but did not describe its criteria for definition of smoking status. It should be noted that, even though there is a relative agreement on TL rates reported in these studies, there is also a lack of information on methodological issues, which can lead to difficulty in establishing comparisons between studies.

When evaluating study quality, the follow-up interval then adopted was considered sufficient to deal with the occurrence of TL, since eligible studies showed a great variation in the follow-up period: from a minimum of 1 year 3434. Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11. to a maximum of 36 years 2323. Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.. The mean time required for the occurrence of TL is subjected to many factors and is difficult to establish from the literature. A minimum follow-up interval of 12 months was considered adequate, and all studies fulfilled this quality requirement. However, clinical responses to periodontal treatment over time are unpredictable, involving many variables, such as periodontal diseases (and its related prognostic factors, e.g. severity of periodontal disease, degree of compliance during APT and PMT), endodontic pathologies, extensive caries lesions, gender, age, individual tooth prognosis, global prognosis, systemic conditions (e.g. diabetes, smoking), socioeconomic conditions, clinical training and operator experience, quality of dental care, and “philosophical” differences in the treatment 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8. (particularly issues related to the maintenance or extraction of periodontally compromised teeth and replacement by dental implants) 4040. McGuire MK, Nunn ME. Prognosis versus actual outcome. III. The effectiveness of clinical parameters in accurately predicting tooth survival. J Periodontol 1996; 67:666-74.,4141. Tsami A, Pepelassi E, Kodovazenitis G, Komboli M. Parameters affecting tooth loss during periodontal maintenance in a Greek population. J Am Dent Assoc 2009; 140:1100-7..

One systematic review 88. Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: a systematic review of observational studies. J Clin Periodontol 2010; 37:675-84. included 13 retrospective cohort studies that evaluated prognostic risk factors in individuals undergoing PMT. Results showed that only 6.8% of all teeth were extracted for periodontal reasons, allowing us to speculate that teeth can be preserved for as long as possible. However, other than extraction due to periodontal reasons, other reasons were also considered, such as endodontic complications, root fractures, caries lesions, prosthetic reasons (i.e. loss of crown retention), unknown reasons, or due to differences in treatment philosophies.

Another systematic review analyzed the effect of individuals’ PMT compliance on TL and investigated the potential factors affecting the association between compliance and TL. The final analysis included eight studies: seven retrospective cohort studies and one prospective cohort study 99. Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.. In the retrospective studies, it was difficult to determine clear reasons for tooth extraction, so the differentiation of the reasons underlying extractions are usually divided only into periodontal and other reasons. This fact was observed in this systematic review, as well as in the retrospective studies 1111. Tonetti MS, Steffen P, Muller-Campanile V, Suvan J, Lang NP. Initial extractions and tooth loss during supportive care in a periodontal population seeking comprehensive care. J Clin Periodontol 2000; 27:824-31.,2020. König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100..

Certain studies 11. Lee CT, Huang HY, Sun TC, Karimbux N. Impact of patient compliance on tooth loss during supportive periodontal therapy: a systematic review and meta-analysis. J Dent Res 2015; 94:777-86.,88. Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: a systematic review of observational studies. J Clin Periodontol 2010; 37:675-84. suggest a lower risk of TL in individuals with greater PMT compliance. In the present systematic review, we attempted to isolate the independent effect of smoking on TL. All possible efforts were made, employing literature electronic research, manual search, and grey literature, with no date of publication or language restrictions. Although it was not possible to generate a funnel plot, there was a predominance of studies with positive results for TL and smoking, indicating a possible publication bias. Citation bias was also identifiable, since many studies belonged to the same research group.

Thus, regardless of the presence of different risk factors for TL in individuals undergoing PMT, the simple presence of smoking should be a factor to classify individuals undergoing PMT as high risk, determining a short time interval for the recall visits. Additionally, these findings can be used by public health services to create strategies for avoiding smoking initiation and promoting smoking cessation, in order to improve systemic and oral health. However, it is important to highlight the scarcity and the need for well-designed prospective cohort studies, since the GRADE evaluation considered the quality of the scientific evidence moderate.

For future studies, a methodological standardization for the following issues is imperative: (1) characterization of smoking status in terms of both frequency and dose-exposure, and (2) identification of unique dental care protocols and periodontal procedures performed during PMT. Moreover, to minimize heterogeneity, studies with larger samples and longer follow-up periods are necessary.

In conclusion, there is moderate scientific evidence that the independent effect of smoking is associated with the occurrence of TL in individuals undergoing PMT. More prospective longitudinal studies are needed to confirm these findings.

References

  • 1
    Lee CT, Huang HY, Sun TC, Karimbux N. Impact of patient compliance on tooth loss during supportive periodontal therapy: a systematic review and meta-analysis. J Dent Res 2015; 94:777-86.
  • 2
    Parameter on periodontal maintenance. J Periodontol 2000; 71 Suppl 5S:849-50.
  • 3
    Costa FO, Cota LO, Lages EJ, Lima Oliveira AP, Cortelli SC, Cortelli JR, et al. Periodontal risk assessment model in a sample of regular and irregular compliers under maintenance therapy: a 3-year prospective study. J Periodontol 2012; 83:292-300.
  • 4
    Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000 1997; 14:9-11.
  • 5
    Fisher S, Kells L, Picard JP, Gelskey SC, Singer DL, Lix L, et al. Progression of periodontal disease in a maintenance population of smokers and non-smokers: a 3-year longitudinal study. J Periodontol 2008; 79:461-8.
  • 6
    Schatzle M, Faddy MJ, Cullinan MP, Seymour GJ, Lang NP, Burgin W, et al. The clinical course of chronic periodontitis: V. Predictive factors in periodontal disease. J Clin Periodontol 2009; 36:365-71.
  • 7
    Wood WR, Greco GW, McFall WT. Tooth loss in patients with moderate periodontitis after treatment and long-term maintenance care. J Periodontol 1989; 60:516-20.
  • 8
    Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: a systematic review of observational studies. J Clin Periodontol 2010; 37:675-84.
  • 9
    Costa FO, Lages EJ, Cota LO, Lorentz TC, Soares RV, Cortelli JR. Tooth loss in individuals under periodontal maintenance therapy: 5-year prospective study. J Periodontal Res 2014; 49:121-8.
  • 10
    Chace R, Low SB. Survival characteristics of periodontally-involved teeth: a 40-year study. J Periodontol 1993; 64:701-5.
  • 11
    Tonetti MS, Steffen P, Muller-Campanile V, Suvan J, Lang NP. Initial extractions and tooth loss during supportive care in a periodontal population seeking comprehensive care. J Clin Periodontol 2000; 27:824-31.
  • 12
    Al-Shammari KF, Al-Khabbaz AK, Al-Ansari JM, Neiva R, Wang HL. Risk indicators for tooth loss due to periodontal disease. J Periodontol 2005; 76:1910-8.
  • 13
    Lorentz TC, Cota LO, Cortelli JR, Vargas AM, Costa FO. Tooth loss in individuals under periodontal maintenance therapy: prospective study. Braz Oral Res 2010; 24:231-7.
  • 14
    Meinberg TA, Canarsky-Handley AM, McClenahan AK, Poulsen DD, Marx DB, Reinhardt RA. Outcomes associated with supportive periodontal therapy in smokers and nonsmokers. J Dent Hyg 2001; 75:15-9.
  • 15
    Papantonopoulos GH. Effect of periodontal therapy in smokers and non-smokers with advanced periodontal disease: results after maintenance therapy for a minimum of 5 years. J Periodontol 2004; 75:839-43.
  • 16
    Labriola A, Needleman I, Moles DR. Systematic review of the effect of smoking on nonsurgical periodontal therapy. Periodontol 2000 2005; 37:124-37.
  • 17
    Heasman L, Stacey F, Preshaw PM, McCracken GI, Hepburn S, Heasman PA. The effect of smoking on periodontal treatment response: a review of clinical evidence. J Clin Periodontol 2006; 33:241-53.
  • 18
    Hirschfeld L, Wasserman B. A long-term survey of tooth loss in 600 treated periodontal patients. J Periodontol 1978; 49:225-37.
  • 19
    Checchi L, Montevecchi M, Gatto MR, Trombelli L. Retrospective study of tooth loss in 92 treated periodontal patients. J Clin Periodontol 2002; 29:651-6.
  • 20
    König J, Plagmann HC, Rühling A, Kocher T. Tooth loss and pocket probing depths in compliant periodontally treated patients: a retrospective analysis. J Clin Periodontol 2002; 29:1092-100.
  • 21
    Axelsson P, Nyström B, Lindhe J. The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. Results after 30 years of maintenance. J Clin Periodontol 2004; 31:749-57.
  • 22
    Fardal O, Johannessen AC, Linden GJ. Tooth loss during maintenance following periodontal treatment in a periodontal practice in Norway. J Clin Periodontol 2004; 31:550-5.
  • 23
    Chambrone LA, Chambrone L. Tooth loss in well-maintained patients with chronic periodontitis during long-term supportive therapy in Brazil. J Clin Periodontol 2006; 33:759-64.
  • 24
    Leung WK, Ng DK, Jin L, Corbet EF. Tooth loss in treated periodontitis patients responsible for their supportive care arrangements. J Clin Periodontol 2006; 33:265-75.
  • 25
    Carnevale G, Cairo F, Tonetti MS. Long-term effects of supportive therapy in periodontal patients treated with fibre retention osseous resective surgery. I: recurrence of pockets, bleeding on probing and tooth loss. J Clin Periodontol 2007; 34:334-41.
  • 26
    Matuliene G, Pjetursson BE, Salvi GE, Schmidlin K, Brägger U, Zwahlen M, et al. Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol 2008; 35:685-95.
  • 27
    Moher D, Liberati A, Tetzlaff J, Altman DG; Prisma Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6:e1000097.
  • 28
    Deeks JJ, Higgins JPT, Altman DG; Cochrane Statistical Methods Group. Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions. Chichester: Willey-Blackwell; 2015. p. 243-96.
  • 29
    Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629-34.
  • 30
    Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008; 336:924-6.
  • 31
    Ravald N, Johansson CS. Tooth loss in periodontally treated patients: a long-term study of periodontal disease and root caries. J Clin Periodontol 2012; 39:73-9.
  • 32
    Graetz C, Plaumann A, Schlattmann P, Kahl M, Springer C, Sälzer S, et al. Long-term tooth retention in chronic periodontitis - results after 18 years of a conservative periodontal treatment regimen in a university setting. J Clin Periodontol 2017; 44:169-77.
  • 33
    Costa FO, Miranda Cota LO, Pereira Lages EJ, Medeiros Lorentz TC, Soares Dutra Oliveira AM, Dutra Oliveira PA, et al. Progression of periodontitis in a sample of regular and irregular compliers under maintenance therapy: a 3-year follow-up study. J Periodontol 2011; 82:1279-87.
  • 34
    Costa FO, Santuchi CC, Lages EJ, Cota LO, Cortelli SC, Cortelli JR, et al. Prospective study in periodontal maintenance therapy: comparative analysis between academic and private practices. J Periodontol 2012; 83:301-11.
  • 35
    Costa FO, Miranda Cota LO, Pereira Lages EJ, Soares Dutra Oliveira AM, Dutra Oliveira PA, Cyrino RM, et al. Progression of periodontitis and tooth loss associated with glycemic control in individuals undergoing periodontal maintenance therapy: a 5-year follow-up study. J Periodontol 2013; 84:595-605.
  • 36
    Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 2000; 71:743-51.
  • 37
    Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev Dent 2003; 1:7-16.
  • 38
    Scott DA, Palmer RM, Stapleton JA. Validation of smoking status in clinical research into inflammatory periodontal disease. J Clin Periodontol 2001; 28:715-22.
  • 39
    Iorio A, Spencer FA, Falavigna M, Alba C, Lang E, Burnand B, et al. Use of GRADE for assessment of evidence about prognosis: rating confidence in estimates of event rates in broad categories of patients. BMJ 2015; 350:h870.
  • 40
    McGuire MK, Nunn ME. Prognosis versus actual outcome. III. The effectiveness of clinical parameters in accurately predicting tooth survival. J Periodontol 1996; 67:666-74.
  • 41
    Tsami A, Pepelassi E, Kodovazenitis G, Komboli M. Parameters affecting tooth loss during periodontal maintenance in a Greek population. J Am Dent Assoc 2009; 140:1100-7.

Publication Dates

  • Publication in this collection
    21 Sept 2018
  • Date of issue
    2018

History

  • Received
    08 Feb 2018
  • Reviewed
    25 May 2018
  • Accepted
    06 July 2018
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