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

Vieira, Thais Ribeiral; Martins, Carolina Castro; Cyrino, Renata Magalhães; Azevedo, Andrea Mara Oliveira; Cota, Luís Otávio Miranda; Costa, Fernando Oliveira

doi:10.1590/0102-311X00024918

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REVIEW • Cad. Saúde Pública 34 (9) • 2018 • https://doi.org/10.1590/0102-311X00024918 copy

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

Authorship SCIMAGO INSTITUTIONS RANKINGS

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

Study	Study design	Participants	Maintenance interventions	Smoking status	Primary outcome
Graetz et al. 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.	This longitudinal study investigated the risk of tooth loss under a nonregenerative treatment regimen and aimed to identify prognostic factors for tooth loss.	315	Nine years. Patients with chronic periodontitis who had been treated between 1982 and 1998 (according to a database) and received PMT (≥ 1 visit/year), including annual documentation of PD, as well as complete radiographic documentation at T0 and at the last documented PMT visit (T2).	Smoking status was assessed categorically as nonsmoker/ex-smoker (quit > 5 years ago) or current smoker. Statistical analyses only used smoking status at T0; note that this ignores possible changes of smoking status during SPT.	Current smokers had HR = 2.62 (95%CI: 1.34-5.14) for TL. Former smokers or individuals who never smoked had HR = 1.02 (95%CI: 0.59-1.76) for TL.
Costa et al. 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.	This 5-year study evaluated the incidence, underlying reasons and influence of risk predictors for the occurrence of TL in individuals undergoing a PMT program.	212	Five years. All individuals had undergone APT. In the PMT program, there were 96 RC individuals with maintenance intervals of 6 months, and 116 IC individuals with a maximum interval of 18 months between recalls.	This study included nonsmokers/ex-smokers and smokers (10-19 and > 19 cigarettes per day).	IC smoker individuals lost significantly more teeth. OR = 4.22 (95%CI: 2.01-8.78).
Ravald & Johanson 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.	Assessed the numbers of lost teeth and causes for TL for a time period of 11-14 years after APT (during PMT).	64	11-14 years. Individuals were submitted to PMT with 1-4 times per year maintenance intervals. Evaluated parameters were: BOP, PI, PD and bone level (measured radiographically).	Subjects were divided into 3 groups: smokers with consumption of 1-9 cigarettes/day, smokers with consumption of more than 10 cigarettes/day, and nonsmokers.	TL was significantly more prevalent among smokers than nonsmokers. Smoking contributed to explain TL with OR = 8.0 (95%CI: 1.6-39.0).
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.	Assessed disease progression longitudinally in smokers and nonsmokers with chronic periodontitis, undergoing PMT every 3-4 months.	108	3 years. Individuals undergoing PMT underwent evaluation of the following parameters: PI, BOP, PD and CAL, with 3-4 intervals months for each recall.	Smoking status was determined according to self-report, while analysis of expired carbon monoxide concentration identified and quantified this condition. A concentration ≤ 8ppm defined nonsmokers, and > 8ppm defined smokers.	No significant difference in the mean number of teeth lost between smokers and nonsmokers at baseline or after 3 years PMT (p > 0.05).
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.	Assessed reasons for TL in individuals undergoing APT and PMT.	120	Above 10 years. All subjects followed a PMT protocol: oral hygiene instructions; scaling and root planning; crown polishing; reassessment and surgical periodontal therapy, when indicated. Intervals ranged from 6-12 months.	Individuals grouped into smokers or nonsmokers; number of cigarettes smoked per day not included.	Smokers had the highest TL rates. OR = 4.76 (95%CI: 1.42-15.89).
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.	Identified risk indicators associated with TL and periodontitis in individuals undergoing PMT.	97	5-12 years. Subjects were instructed to perform their own PMT. At each first callback visit, they completed a questionnaire with a trained interviewer, to record TL reasons.	11 of the previously treated patients were current smokers, with a self-reported cumulative consumption of 0.5-56.9 packs/year.	TL due to periodontal reasons was 2.5 times higher for smokers in comparison to nonsmokers.
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.	Determined the treatment outcomes of compliant periodontal patients, which were observed for at least 8 years. All patients had been treated for moderate to advanced periodontitis and regularly received PMT.	142	8-13 years. During PMT, dental prophylaxis and/or subgingival debridement were performed when the operator found necessary. Periodontal conditions were documented annually with PD charts and IP values. 12-month recall interval.	Article mentions smokers and nonsmokers but does not describe the criteria for smoking status.	Smoking significantly associated with TL (r ² = 0.12).

Study	Study design	Participants	Maintenance interventions	Smoking status	Primary outcome
Costa et al. 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.	Investigated the inﬂuence of glycemic control in the progression of periodontitis and TL during PMT.	92	5 years. Subjects were monitored at a private dental clinic. PMT was performed with 4-6 months recall intervals for all participants.	Included smokers/ex-smokers (reported having smoked > 100 cigarettes during their lifetime) and nonsmokers.	Smoking status had OR = 4.1 (95%CI: 1.98-11.6) for TL.
Costa et al. 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.	Investigated the association of periodontal risk assessment model with recurrence of periodontitis and TL during PMT.	164	Data obtained after APT were determined at baseline (T1) and compared to data obtained after 3 years of follow-up (T2). T2 was performed after 9 recall visits (RC individuals) and 4 visits (IC individuals). Periodontal clinical examinations during monitoring visits assessed: PD, CAL, furcation involvement, BOP, suppuration, radiographic evidence of bone loss (collected after T1 and T2).	Included nonsmokers/ex-smokers and smokers: 10-19 or > 19 cigarettes per day.	Smoking status had OR = 3.41 (95%CI: 1.26-11.41) for TL.
Costa et al. 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.	Evaluated and compared periodontal status, periodontitis progression, TL and influence of predictable risk variables of two PMT programs over a 12-month period.	288	Minimal follow-up time of 12 months. At each recall visit (T1, T2, T3 and T4), the following procedures were performed: interviews to determine possible changes in the variables of interest (demographic, biological, and behavioral); periodontal assessment through clinical parameters; disclosure of oral hygiene instructions using the Bass technique, interproximal brushes and dental floss; and, where appropriate, mechanical debridement, including prophylaxis, coronary polishing, and topical application of fluoride.	Included smokers/ex-smokers (reported having smoked > 100 cigarettes during their lives) and nonsmokers.	For the private group, final multivariate logistic regression models showed that smoking had OR = 3.1 (95%CI: 1.98-11.6) for TL. For the private group, OR for TL associated with smoking was not reported.
Costa et al. 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.	Determined and compared periodontal status, especially progression of periodontitis and TL, among RC and IC smokers and nonsmokers during PMT.	116	3 years. At each recall visit (T1, T2, T3 and T4), the following procedures were performed: interviews to determine possible changes in the variables of interest (demographic, biological and behavioral); periodontal assessment through clinical parameters; disclosure of oral hygiene instructions using the Bass technique, interproximal brushes and dental floss; and, where appropriate, mechanical debridement, including prophylaxis, coronary polishing, and topical application of fluoride.	Included smokers/ex-smokers (reported having smoked > 100 cigarettes during their lives) and nonsmokers.	Smokers in the IC group had OR = 7.3 (95%CI: 1.17-14.9) for TL. RC smokers presented OR = 4.2 (95%CI: 1.42-9.89) for TL.

	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.	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.	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.	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.	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.	Costa et al. 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.	Graetz et al. 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.
Sample selection criteria ^#
1) Representativeness of the exposed cohort (subjects undergoing PMT)							
a) Truly representative of the average no. of individuals undergoing PMT (20%) in the community 
b) Partially representative of the average no. of individuals under PMT (20%) in the community 
c) Selected group of affected individuals
d) No description of the derivation of cohort
2) Selection of the nonexposed cohort							
a) Selected from the same community as the exposed group 
b) Selected from a different source
c) No description of the derivation of the nonexposed group
3) Ascertainment of exposure (smokers undergoing PMT)							
a) Secure record (pocket probing depth + bone loss + tooth loss) 
b) Clinical or radiographic exams 
c) Written self-reports or data described in the clinical records
d) No description
4) Demonstration that outcome of interest (TL) was not presented at start of study							
a) Yes 
b) No
Comparability of cohorts ^##
1) Control of confounding factors							
a) Exposure of interest (smoking) is adjusted for one confounding variable (eg.: diabetes) 
b) Exposure of interest (smoking) is adjusted for two or more factors (eg.: diabetes, gender, age, ...) 
Outcome assessment (TL) ^#
1) TL diagnostic							
a) Secure assessment using clinical and radiographic parameters 
b) Clinical examination without radiographic assessment, or only partially met the criteria (a/b)
c) Based on self-report or assessment of clinical data
2) Adequate follow-up time for the outcome (TL) to occur							
a) Yes (more than 12 months PMT) 
b) No
3) Nonresponse rate	d						c
a) Complete follow-up: all subjects accounted for 
b) Nonresponse rate ≤ 20% 
c) Nonresponse rate > 20%
d) Not described
Sum of scores ^###	7/10 (high)	8/10 (high)	8/10 (high)	9/10 (high)	8/10 (high)	9/10 (high)	9/10 (high)

	Costa et al. 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.	Costa et al. 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.	Costa et al. 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.	Costa et al. 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.
Sample selection criteria ^#
1) Adequate tooth loss diagnostic for smokers undergoing PMT (cases)?				
a) Clinical and radiographic examination 
b) Clinical examination without radiographic examination
c) Record linkage or based on self-reports
2) Representativeness and selection of smokers under PMT (cases)				
a) Cases selected from private or public clinic, random sample, sample calculation 
b) Selection biases or “a” criteria not satisfied
3) Selection of nonsmokers undergoing PMT (controls)				
a) Controls selected from private or public clinics, random sample, sample calculation 
b) Selection biases or “a” criteria not satisfied
c) No description
4) Definition of controls				
a) Nonsmokers undergoing PMT 
b) No description				
Comparability of cases and controls ^##
1) Control of confounding factors				
a) Exposure of interest (smoking) adjusted for one confounding variable (diabetes) 
b) Exposure of interest (smoking) adjusted for two or more factors (diabetes, gender, age and other variables) 
c) No description
Assessment of outcome (TL) ^#
1) Tooth loss diagnostic				
a) Secure assessment using clinical and radiographic parameters 
b Based on self-report or assessment of clinical data
c) No description
2) Same method of assessment for cases and controls				
a) Yes 
b) No
3) Nonresponse rate			c	c
a) Nonresponse rate ≤ 20%, for both groups (cases and controls) 
b) Nonresponse rate > 20%
c) Not described
Sum of scores ^###	8/9 (high)	8/9 (high)	7/9 (high)	7/9 (high)

Certainty assessment
Studies	4
Design	Observational studies
Risk of bias	Not serious *
Inconsistency	Not serious **
Indirectness	Not serious ***
Imprecision	Serious ^#
Other considerations	Publication bias strongly suspected Very strong association All plausible residual confounding factors would reduce demonstrated effect
Effect
Relative (95%CI)	OR = 3.24 (1.33-7.90)
Absolute (95%CI)	3 fewer per 1.000 (1-8 fewer)
Certainty	⨁ ⨁ ⨁ ◯ MODERATE

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[1] Correspondence F. O. Costa Faculdade de Odontologia, Universidade Federal de Minas Gerais. Av. Antônio Carlos 6627, C. P. 359, Belo Horizonte, MG 31270-091, Brasil. focperio@uol.com.br