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Edentulism and all–cause mortality among Brazilian older adults: 11–years follow–up

Abstract

We assessed the association between edentulism and all–cause mortality among community–dwelling older adults from São Paulo, Brazil, from 2006 to 2017. This prospective cohort study used data from the Health, Well–being and Aging Study (SABE, Portuguese acronym). Edentulism was evaluated by means of clinical oral examination and all–cause mortality data were obtained from state official records. Covariates included socioeconomic factors (age, sex, and schooling); health behavior (smoking, alcohol intake, and physical activity); dental care (prostheses use); general health (multimorbidity); and nutritional status (underweight). Kaplan–Meier survival curves were stratified by edentulism and compared using the log–rank test. Cox proportional hazards model was applied to calculate hazard ratios (HRs) for the association between edentulism and mortality after adjusting for covariates. The study sample included 1,687 participants (age, 60–102 years; edentulous: 47.2%). In the 11 years of follow–up, we analyzed 10,494 person–years and 566 deaths. In bivariate analysis, edentulous older adults were found to be at a higher risk of dying from all causes than the dentate participants (HR: 1.81; 95%CI: 1.53–2.15). After sequential adjustment for socioeconomic factors, health behavior, dental care, general health, and nutritional status, this association was attenuated, but remained significant (HR: 1.34; 95%CI: 1.10–1.63). In conclusion, edentulism is a significant predictor of all–cause mortality among older adults.

Tooth Loss; Mortality; Aged

Introduction

Edentulism is an important oral health marker in older individuals,11. Moriya S, Miura H. Oral health and general health at the early stage of ageing: a review of contemporary studies. Jpn Dent Sci Rev. 2014 Feb;50(1):15-20. https://doi.org/10.1016/j.jdsr.2013.10.002
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,22. Friedman PK, Lamster IB. Tooth loss as a predictor of shortened longevity: exploring the hypothesis. Periodontol 2000. 2016 Oct;72(1):142-52. https://doi.org/10.1111/prd.12128
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as it captures life–course cumulative effects of oral diseases.33. Ramseier CA, Anerud A, Dulac M, Lulic M, Cullinan MP, Seymour GJ, et al. Natural history of periodontitis: disease progression and tooth loss over 40 years. J Clin Periodontol. 2017 Dec;44(12):1182-91. https://doi.org/10.1111/jcpe.12782
https://doi.org/10.1111/jcpe.12782...
Prevalence of edentulism depends on the region44. Gupta A, Felton DA, Jemt T, Koka S. Rehabilitation of Edentulism and Mortality: A Systematic Review. J Prosthodont. 2019 Jun;28(5):526-35. https://doi.org/10.1111/jopr.12792
https://doi.org/10.1111/jopr.12792...
and sociodemographic characteristics of the individual,55. Peres MA, Barbato PR, Reis SC, Freitas CH, Antunes JL. Tooth loss in Brazil: analysis of the 2010 Brazilian oral health survey. Rev Saude Publica. 2013 Dec;47(3 Suppl 3):78-89. https://doi.org/10.1590/S0034-8910.2013047004226
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,66. Polzer I, Schimmel M, Müller F, Biffar R. Edentulism as part of the general health problems of elderly adults. Int Dent J. 2010 Jun;60(3):143-55. https://doi.org/10.1922/IDJ_2184Polzer13
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approximating to 10% in those aged ≥50 years worldwide77. Kassebaum NJ, Smith AG, Bernabé E, Fleming TD, Reynolds AE, Vos T, et al.; GBD 2015 Oral Health Collaborators. Global, Regional, and National Prevalence, Incidence, and Disability-Adjusted Life Years for Oral Conditions for 195 Countries, 1990-2015: A Systematic Analysis for the Global Burden of Diseases, Injuries, and Risk Factors. J Dent Res. 2017 Apr;96(4):380-7. https://doi.org/10.1177/0022034517693566
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and 54% in Brazilian adults aged 65–74 years.55. Peres MA, Barbato PR, Reis SC, Freitas CH, Antunes JL. Tooth loss in Brazil: analysis of the 2010 Brazilian oral health survey. Rev Saude Publica. 2013 Dec;47(3 Suppl 3):78-89. https://doi.org/10.1590/S0034-8910.2013047004226
https://doi.org/10.1590/S0034-8910.20130...
Edentulism is considered a disability,22. Friedman PK, Lamster IB. Tooth loss as a predictor of shortened longevity: exploring the hypothesis. Periodontol 2000. 2016 Oct;72(1):142-52. https://doi.org/10.1111/prd.12128
https://doi.org/10.1111/prd.12128...
affecting the quality of life,11. Moriya S, Miura H. Oral health and general health at the early stage of ageing: a review of contemporary studies. Jpn Dent Sci Rev. 2014 Feb;50(1):15-20. https://doi.org/10.1016/j.jdsr.2013.10.002
https://doi.org/10.1016/j.jdsr.2013.10.0...
nutritional aspects,88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
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,99. Kossioni AE. The Association of Poor Oral Health parameters with malnutrition in older adults: a review considering the potential implications for cognitive impairment. Nutrients. 2018 Nov;10(11):E1709. https://doi.org/10.3390/nu10111709
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,1010. Gupta A, Khandelwal R, Kapil U. Interrelationship between dental health status and nutritional status among elderly subjects in India. J Family Med Prim Care. 2019 Feb;8(2):477-81. https://doi.org/10.4103/jfmpc.jfmpc_353_18
https://doi.org/10.4103/jfmpc.jfmpc_353_...
and morbidity of the individual.66. Polzer I, Schimmel M, Müller F, Biffar R. Edentulism as part of the general health problems of elderly adults. Int Dent J. 2010 Jun;60(3):143-55. https://doi.org/10.1922/IDJ_2184Polzer13
https://doi.org/10.1922/IDJ_2184Polzer13...
Furthermore, several cohort studies1111. Lee HJ, Choi EK, Park JB, Han KD, Oh S. Tooth loss predicts myocardial infarction, Heart Failure, Stroke, and Death. J Dent Res. 2019 Feb;98(2):164-70. https://doi.org/10.1177/0022034518814829
https://doi.org/10.1177/0022034518814829...
,1212. Lee MS, Huang YC, Wahlqvist ML. Chewing ability in conjunction with food intake and energy status in later life affects survival in Taiwanese with the metabolic syndrome. J Am Geriatr Soc. 2010 Jun;58(6):1072-80. https://doi.org/10.1111/j.1532-5415.2010.02870.x
https://doi.org/10.1111/j.1532-5415.2010...
,1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,1414. Vogtmann E, Etemadi A, Kamangar F, Islami F, Roshandel G, Poustchi H, et al. Oral health and mortality in the Golestan Cohort Study. Int J Epidemiol. 2017 Dec;46(6):2028-35. https://doi.org/10.1093/ije/dyx056
https://doi.org/10.1093/ije/dyx056...
,1515. Furuta M, Takeuchi K, Adachi M, Kinoshita T, Eshima N, Akifusa S, et al. Tooth loss, swallowing dysfunction and mortality in Japanese older adults receiving home care services. Geriatr Gerontol Int. 2018 Jun;18(6):873-80. https://doi.org/10.1111/ggi.13271
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and recent systematic reviews44. Gupta A, Felton DA, Jemt T, Koka S. Rehabilitation of Edentulism and Mortality: A Systematic Review. J Prosthodont. 2019 Jun;28(5):526-35. https://doi.org/10.1111/jopr.12792
https://doi.org/10.1111/jopr.12792...
,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
have reported reduced survival rates among older edentulous individuals.

In addition to the hypothesis of the significant association between edentulism and mortality because of insufficient adjustment for proper confounders,1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1818. Iinuma T, Arai Y, Takayama M, Abe Y, Ito T, Kondo Y, et al. Association between maximum occlusal force and 3-year all-cause mortality in community-dwelling elderly people. BMC Oral Health. 2016 Sep;16(1):82. https://doi.org/10.1186/s12903-016-0283-z
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other explanations have been proposed. One explanation states that edentulism and related chewing problems predispose individuals to poor nutritional intake,88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
https://doi.org/10.14219/jada.2014.35...
and malnutrition.1010. Gupta A, Khandelwal R, Kapil U. Interrelationship between dental health status and nutritional status among elderly subjects in India. J Family Med Prim Care. 2019 Feb;8(2):477-81. https://doi.org/10.4103/jfmpc.jfmpc_353_18
https://doi.org/10.4103/jfmpc.jfmpc_353_...
Furthermore, tooth loss could carry effects from a previous low–grade chronic inflammation due to periodontal disease,33. Ramseier CA, Anerud A, Dulac M, Lulic M, Cullinan MP, Seymour GJ, et al. Natural history of periodontitis: disease progression and tooth loss over 40 years. J Clin Periodontol. 2017 Dec;44(12):1182-91. https://doi.org/10.1111/jcpe.12782
https://doi.org/10.1111/jcpe.12782...
,1919. Weintraub JA, Orleans B, Fontana M, Phillips C, Jones JA. Factors associated with becoming edentulous in the US health and retirement study. J Am Geriatr Soc. 2019 Nov;67(11):2318-24. https://doi.org/10.1111/jgs.16079;
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which, together with “inflammaging”,2020. Fülöp T, Larbi A, Witkowski JM. Human inflammaging. Gerontology. 2019;65(5):495-504. https://doi.org/10.1159/000497375
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increases the risk for arteriosclerotic diseases.1111. Lee HJ, Choi EK, Park JB, Han KD, Oh S. Tooth loss predicts myocardial infarction, Heart Failure, Stroke, and Death. J Dent Res. 2019 Feb;98(2):164-70. https://doi.org/10.1177/0022034518814829
https://doi.org/10.1177/0022034518814829...
,2121. Janket SJ, Baird AE, Jones JA, Jackson EA, Surakka M, Tao W, et al. Number of teeth, C-reactive protein, fibrinogen and cardiovascular mortality: a 15-year follow-up study in a finnish cohort. J Clin Periodontol. 2014 Feb;41(2):131-40. https://doi.org/10.1111/jcpe.12192
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,2222. Liu YH, Gao X, Mitchell DC, Wood GC, Still CD, Jensen GL. diet quality is associated with mortality in adults aged 80 years and older: a prospective study. J Am Geriatr Soc. 2019 Oct;67(10):2180-5. https://doi.org/10.1111/jgs.16089
https://doi.org/10.1111/jgs.16089...

Both malnutrition and chronic inflammation predict lower survival rates2323. LaMonte MJ, Genco RJ, Hovey KM, Wallace RB, Freudenheim JL, Michaud DS, et al. History of periodontitis diagnosis and edentulism as predictors of cardiovascular disease, stroke, and mortality in postmenopausal women. J Am Heart Assoc. 2017 Mar;6(4):e004518. https://doi.org/10.1161/JAHA.116.004518
https://doi.org/10.1161/JAHA.116.004518...
and have been used to adjust the relationship between oral impairments and mortality in some studies,1212. Lee MS, Huang YC, Wahlqvist ML. Chewing ability in conjunction with food intake and energy status in later life affects survival in Taiwanese with the metabolic syndrome. J Am Geriatr Soc. 2010 Jun;58(6):1072-80. https://doi.org/10.1111/j.1532-5415.2010.02870.x
https://doi.org/10.1111/j.1532-5415.2010...
,1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,2121. Janket SJ, Baird AE, Jones JA, Jackson EA, Surakka M, Tao W, et al. Number of teeth, C-reactive protein, fibrinogen and cardiovascular mortality: a 15-year follow-up study in a finnish cohort. J Clin Periodontol. 2014 Feb;41(2):131-40. https://doi.org/10.1111/jcpe.12192
https://doi.org/10.1111/jcpe.12192...
,2424. Hiratsuka T, Komiyama T, Ohi T, Tanji F, Tomata Y, Tsuji I, et al. Contribution of systemic inflammation and nutritional status to the relationship between tooth loss and mortality in a community-dwelling older Japanese population: a mediation analysis of data from the Tsurugaya project. Clin Oral Investig. 2019 Sep 4. https://doi.org/10.1007/s00784-019-03072-y
https://doi.org/10.1007/s00784-019-03072...
although evidence of this association remains unclear. Lee and colleagues1212. Lee MS, Huang YC, Wahlqvist ML. Chewing ability in conjunction with food intake and energy status in later life affects survival in Taiwanese with the metabolic syndrome. J Am Geriatr Soc. 2010 Jun;58(6):1072-80. https://doi.org/10.1111/j.1532-5415.2010.02870.x
https://doi.org/10.1111/j.1532-5415.2010...
observed that the association between chewing ability and 6–year all–cause mortality disappeared after adjusting for appetite in Taiwanese older adults. Watt and colleagues1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
found no evidence of the role of body mass index (BMI) or high–sensitive C–reactive protein (CRP) on the association between dental status and both all–cause and cardiovascular disease mortality during the 8–year follow–up period in a Scottish Health Survey. However, Hiratsuka et al.2424. Hiratsuka T, Komiyama T, Ohi T, Tanji F, Tomata Y, Tsuji I, et al. Contribution of systemic inflammation and nutritional status to the relationship between tooth loss and mortality in a community-dwelling older Japanese population: a mediation analysis of data from the Tsurugaya project. Clin Oral Investig. 2019 Sep 4. https://doi.org/10.1007/s00784-019-03072-y
https://doi.org/10.1007/s00784-019-03072...
reported a significant role of serum albumin level, not of CRP, on the association between tooth loss and all–cause mortality during the 13–year follow–up period in Japanese older adults.

Considering the accelerating aging population,2525. Lebrão ML. SABE - Saúde, bem-estar e envelhecimento: o Projeto Sabe no município de São Paulo: uma abordagem inicial. Brasília, DF: Organização Pan-Americana da Saúde; 2003. high prevalence of edentulism among older adults in Brazil,55. Peres MA, Barbato PR, Reis SC, Freitas CH, Antunes JL. Tooth loss in Brazil: analysis of the 2010 Brazilian oral health survey. Rev Saude Publica. 2013 Dec;47(3 Suppl 3):78-89. https://doi.org/10.1590/S0034-8910.2013047004226
https://doi.org/10.1590/S0034-8910.20130...
and the small number of studies evaluating the association between edentulism and mortality outside high–income countries,1414. Vogtmann E, Etemadi A, Kamangar F, Islami F, Roshandel G, Poustchi H, et al. Oral health and mortality in the Golestan Cohort Study. Int J Epidemiol. 2017 Dec;46(6):2028-35. https://doi.org/10.1093/ije/dyx056
https://doi.org/10.1093/ije/dyx056...
,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
despite its noticeable relevance,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
we performed this study. We aimed to assess the relationship between edentulism and all–cause mortality among community–dwelling older adults from São Paulo, Brazil, from 2006 to 2017.

Methodology

Study design and participants

All data were obtained from the Brazilian Health, Well–being and Aging Study (SABE), a multicenter survey conducted in major urban centers in Latin America in 2000. However, in 2006, SABE was transformed into a cohort study performed in 5–year intervals in São Paulo, Brazil, with the representative probabilistic sample of urban older persons aged ≥ 60 years. A sample of participants aged 60–64 years were included in each new wave to keep the representativeness of that age group. In the survey, trained examiners collected data on the individual’s living conditions, socioeconomic status, anthropometric measures, general well–being, and oral health at his or her residence. Clinical oral examinations have been performed since 2006. In our study, we used data from all participants who presented complete information for the variables of interest, from 2006 to 2017. As participants were followed up for different time periods, we computed the time of contribution to the study for each participant. Of the 1,831 participants screened (1,413 interviewed in 2006 and 418 interviewed in 2010), 144 were excluded (102 from 2006 and 44 from 2010) due to loss of data. Therefore, the final sample consisted of 1,687 participants. We linked SABE data to official mortality records up to May 2017. More details on the study design, setting, and sampling are described elsewhere.88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
https://doi.org/10.14219/jada.2014.35...
,2525. Lebrão ML. SABE - Saúde, bem-estar e envelhecimento: o Projeto Sabe no município de São Paulo: uma abordagem inicial. Brasília, DF: Organização Pan-Americana da Saúde; 2003.

Ethics statement

SABE study was approved by the Ethics in Research Committee of the School of Public Health of the University of São Paulo. Written informed consent from the volunteer participants was obtained at the time of each interview.

Variables

The time to death from all causes was calculated as the years from the date of the baseline interview to: a) the date of death (for those who died during the follow–up period) or b) the date of the last location (for those who did not die during the follow–up period). For participants whose contact was lost for any reason, the time of contribution to study was defined as the participation time between two waves plus/or half the period between the last location and the next wave that he/she did not participate.

The presence of edentulism, defined as the absence of all natural teeth, was obtained through clinical oral examinations performed by trained dentists using standardized criteria.2626. World Health Organization – WHO. Oral health surveys: Basic methods. 4th ed. Geneva: World Health Organization; 1997.

To adjust for the association between edentulism and all–cause mortality, we selected relevant covariates, in accordance with recent systematic reviews,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
measured at baseline. The covariates were a) socioeconomic factors (age, 60–69; 70–79; >80 years; sex; years of schooling, 0–3; 4–7; ≥ 8; b) health behavior (current smoking status; current alcohol use [any amount of alcoholic beverages consumed weekly in the past 3 months]; physical activity [at least 150 min of moderate or vigorous activities per week2727. IPAQ Research Committee. Guidelines for Data processing and analysis of the international physical activity questionnaire (IPAQ): short and long forms. 2005 [cited 2019 Oct 21]. Available from: https://bit.ly/2skoIjp
https://bit.ly/2skoIjp...
]); c) dental care (prostheses use); d) general health (multimorbidity: self–reported ≥ 2 long–term conditions,2828. World Health Organization – WHO. Multimorbidity: technical series on safer primary care. Geneva: World Health Organization; 2016. including diabetes mellitus, hypertension, heart disease, chronic obstructive pulmonary disease, osteoporosis, stroke, and arthritis); and e) nutritional status (if the individual was underweight; i.e., BMI < 22 kg/m2).2929. Lipschitz DA. Screening for nutritional status in the elderly. Prim Care. 1994 Mar;21(1):55-67. In SABE, weight and height were measured using a portable scale (seca, Germany) and an anthropometer (Harpenden, England), respectively.

Statistical analysis

Descriptive data are expressed as proportions. Difference in the characteristics for all variables according to edentulism were evaluated using the chi-square test (Table 1).

Table 1
Baseline characteristics according to edentulism status among Brazilian older adults.

The median survival time, as the time point in which half of the participants are alive, based on the Kaplan–Meier survival curve and its 95% confidence interval (95% CI), calculated using the Greenwood exponential formula, was estimated. Survival curves stratified by edentulism status were also performed using the Kaplan–Meier method and compared using the log–rank test (Figure).

Figure
Kaplan–Meier survival curves according to edentulism among Brazilian older adults.

Cox proportional hazard models were used to estimate the risk of mortality according to the edentulism status, with the results expressed as hazard ratios (HRs) and 95% CIs (Table 2). Model 1 corresponded to the unadjusted model. Further models were sequentially adjusted by socioeconomic factors (model 2), health behaviors (model 3), dental care (model 4), general health conditions (model 5), and nutritional status (model 6). The assumption of proportional hazards was assessed using the Schoenfeld residuals and log–log plots.

Table 2
Association between edentulism and all–cause mortality among Brazilian older adults.

For all statistical procedures, a significance level of 5% was considered. All statistical analyses were performed using Stata14.0 (Stata Corp LLP, College Station, USA).

Results

In this study, we evaluated 1,687 adults aged 60–102 years, representing 10,494 person–years (maximum: 10.98–year follow–up period) with a median survival time of 10.2 years and 566 (33.6%) deaths during the follow–up period. Less than half (47.2%) the participants were edentulous, with edentulism being associated with all covariates, but not with physical activity (Table 1).

The cumulative survival rate plot demonstrated a higher mortality rate for edentulous participants than dentate participants (Figure), and this was confirmed by the log–rank test (p < 0.0001).

Edentulism was associated with shorter survival in crude and all adjusted analyses (Table 2). The unadjusted model demonstrated higher mortality risks from all causes for edentulous participants (HR: 1.81; 95%CI: 1.53–2.15) than for dentate participants (Table 2, model 1). These estimates became lower after sequential adjustment for socioeconomic factors (Table 2, model 2) and health behavior (Table 2, model 3). However, they increased after additional adjustment for dental care (Table 2, model 4) and remained stable after insertion of general health variable (Table 2, model 5). Even after further adjustment for nutritional status, the risk for death for edentulous participants was 1.34 times (95%CI: 1.10–1.63) the risk for dentate participants (Table 2, model 6). However, these estimates have been attenuated over again.

Discussion

In this prospective cohort study with a 11–year follow–up period, we demonstrated higher all–cause mortality risks among edentulous participants than dentate participants from São Paulo, Brazil. Although attenuated, this association remained significant even after adjusting for a comprehensive number of covariates,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
such as socioeconomic, health behavior, dental care, health conditions, and nutritional status.

Our findings are in line with other studies conducted in high– and upper–middle–income countries, which revealed small but significant association between tooth loss, especially edentulism, and all–cause mortality, independent of socioeconomic and health conditions.1111. Lee HJ, Choi EK, Park JB, Han KD, Oh S. Tooth loss predicts myocardial infarction, Heart Failure, Stroke, and Death. J Dent Res. 2019 Feb;98(2):164-70. https://doi.org/10.1177/0022034518814829
https://doi.org/10.1177/0022034518814829...
,1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,1414. Vogtmann E, Etemadi A, Kamangar F, Islami F, Roshandel G, Poustchi H, et al. Oral health and mortality in the Golestan Cohort Study. Int J Epidemiol. 2017 Dec;46(6):2028-35. https://doi.org/10.1093/ije/dyx056
https://doi.org/10.1093/ije/dyx056...
,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
The higher risk of dying from all causes for edentulous participants found in this study is similar to summary estimates from a recent meta–analysis.1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
In a systematic review, Koka et al.1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
suggested that the association between tooth loss and mortality may not be causal but associative. Our findings indicate that most part of the increased risk of dying among edentulous could be explained by socioeconomic factors and health behavior, which are consistent with previous study results.1212. Lee MS, Huang YC, Wahlqvist ML. Chewing ability in conjunction with food intake and energy status in later life affects survival in Taiwanese with the metabolic syndrome. J Am Geriatr Soc. 2010 Jun;58(6):1072-80. https://doi.org/10.1111/j.1532-5415.2010.02870.x
https://doi.org/10.1111/j.1532-5415.2010...
,1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
This could be because tooth loss and mortality share common risk factors such as health behavior, socioeconomic, and health conditions.511,2323. LaMonte MJ, Genco RJ, Hovey KM, Wallace RB, Freudenheim JL, Michaud DS, et al. History of periodontitis diagnosis and edentulism as predictors of cardiovascular disease, stroke, and mortality in postmenopausal women. J Am Heart Assoc. 2017 Mar;6(4):e004518. https://doi.org/10.1161/JAHA.116.004518
https://doi.org/10.1161/JAHA.116.004518...
,3030. Landmann-Szwarcwald C, Macinko J. A panorama of health inequalities in Brazil. Int J Equity Health. 2016 Nov;15(1):174. https://doi.org/10.1186/s12939-016-0462-1
https://doi.org/10.1186/s12939-016-0462-...

Furthermore, tooth loss and edentulism predict adverse health outcomes closely related to mortality.1515. Furuta M, Takeuchi K, Adachi M, Kinoshita T, Eshima N, Akifusa S, et al. Tooth loss, swallowing dysfunction and mortality in Japanese older adults receiving home care services. Geriatr Gerontol Int. 2018 Jun;18(6):873-80. https://doi.org/10.1111/ggi.13271
https://doi.org/10.1111/ggi.13271...
,1818. Iinuma T, Arai Y, Takayama M, Abe Y, Ito T, Kondo Y, et al. Association between maximum occlusal force and 3-year all-cause mortality in community-dwelling elderly people. BMC Oral Health. 2016 Sep;16(1):82. https://doi.org/10.1186/s12903-016-0283-z
https://doi.org/10.1186/s12903-016-0283-...
,3131. Matsuyama Y, Aida J, Watt RG, Tsuboya T, Koyama S, Sato Y, et al. Dental status and compression of life expectancy with disability. J Dent Res. 2017 Aug;96(9):1006-13. https://doi.org/10.1177/0022034517713166
https://doi.org/10.1177/0022034517713166...
Two main pathways have been proposed to explain this observed association.1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,1717. Peng J, Song J, Han J, Chen Z, Yin X, Zhu J, et al. The relationship between tooth loss and mortality from all causes, cardiovascular diseases, and coronary heart disease in the general population: systematic review and dose-response meta-analysis of prospective cohort studies. Biosci Rep. 2019 Jan;39(1):BSR20181773. https://doi.org/10.1042/BSR20181773
https://doi.org/10.1042/BSR20181773...
The first argues that tooth loss may carry the effects from a previous low–grade chronic infection due to periodontal disease, which, together with the chronic inflammation in aging, predisposes the individual to atherothrombogenesis occurring in coronary and cardiovascular diseases.1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,2121. Janket SJ, Baird AE, Jones JA, Jackson EA, Surakka M, Tao W, et al. Number of teeth, C-reactive protein, fibrinogen and cardiovascular mortality: a 15-year follow-up study in a finnish cohort. J Clin Periodontol. 2014 Feb;41(2):131-40. https://doi.org/10.1111/jcpe.12192
https://doi.org/10.1111/jcpe.12192...
However, few studies have reported attenuation of the association between tooth loss and mortality to a certain degree after adjusting for CRP and fibrinogen,2121. Janket SJ, Baird AE, Jones JA, Jackson EA, Surakka M, Tao W, et al. Number of teeth, C-reactive protein, fibrinogen and cardiovascular mortality: a 15-year follow-up study in a finnish cohort. J Clin Periodontol. 2014 Feb;41(2):131-40. https://doi.org/10.1111/jcpe.12192
https://doi.org/10.1111/jcpe.12192...
whereas other studies have found no significant change in the association.1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,2424. Hiratsuka T, Komiyama T, Ohi T, Tanji F, Tomata Y, Tsuji I, et al. Contribution of systemic inflammation and nutritional status to the relationship between tooth loss and mortality in a community-dwelling older Japanese population: a mediation analysis of data from the Tsurugaya project. Clin Oral Investig. 2019 Sep 4. https://doi.org/10.1007/s00784-019-03072-y
https://doi.org/10.1007/s00784-019-03072...
Among present–day Brazilian older adults, this could be partially true because their teeth were lost in early adulthood.55. Peres MA, Barbato PR, Reis SC, Freitas CH, Antunes JL. Tooth loss in Brazil: analysis of the 2010 Brazilian oral health survey. Rev Saude Publica. 2013 Dec;47(3 Suppl 3):78-89. https://doi.org/10.1590/S0034-8910.2013047004226
https://doi.org/10.1590/S0034-8910.20130...
However, poor nutritional status, that is also related to edentulism,88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
https://doi.org/10.14219/jada.2014.35...
predicts chronic inflammation and circulatory diseases3232. Gärtner S, Kraft M, Krüger J, Vogt LJ, Fiene M, Mayerle J, et al. Geriatric nutritional risk index correlates with length of hospital stay and inflammatory markers in older inpatients. Clin Nutr. 2017 Aug;36(4):1048-53. https://doi.org/10.1016/j.clnu.2016.06.019
https://doi.org/10.1016/j.clnu.2016.06.0...
and, hence, higher mortality.1111. Lee HJ, Choi EK, Park JB, Han KD, Oh S. Tooth loss predicts myocardial infarction, Heart Failure, Stroke, and Death. J Dent Res. 2019 Feb;98(2):164-70. https://doi.org/10.1177/0022034518814829
https://doi.org/10.1177/0022034518814829...
,2222. Liu YH, Gao X, Mitchell DC, Wood GC, Still CD, Jensen GL. diet quality is associated with mortality in adults aged 80 years and older: a prospective study. J Am Geriatr Soc. 2019 Oct;67(10):2180-5. https://doi.org/10.1111/jgs.16089
https://doi.org/10.1111/jgs.16089...
,3333. Yerrakalva D, Mullis R, Mant J. The associations of “fatness,” “fitness,” and physical activity with all-cause mortality in older adults: a systematic review. Obesity (Silver Spring). 2015 Oct;23(10):1944-56. https://doi.org/10.1002/oby.21181
https://doi.org/10.1002/oby.21181...

The second pathway places edentulism and mortality at their final points and lists nutritional factors as their mediator. This is because tooth loss, edentulism, and related chewing problems affect nutritional behaviors (decrease in protein and fiber intake and increase in fat, carbohydrate, and processed food intake) and predispose individuals to malnutrition, underweight, or even overweight/obesity.88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
https://doi.org/10.14219/jada.2014.35...
Both poor nutritional status and obesity predict all– and specific–cause mortality.2222. Liu YH, Gao X, Mitchell DC, Wood GC, Still CD, Jensen GL. diet quality is associated with mortality in adults aged 80 years and older: a prospective study. J Am Geriatr Soc. 2019 Oct;67(10):2180-5. https://doi.org/10.1111/jgs.16089
https://doi.org/10.1111/jgs.16089...
,3333. Yerrakalva D, Mullis R, Mant J. The associations of “fatness,” “fitness,” and physical activity with all-cause mortality in older adults: a systematic review. Obesity (Silver Spring). 2015 Oct;23(10):1944-56. https://doi.org/10.1002/oby.21181
https://doi.org/10.1002/oby.21181...
In our study, the association between edentulism and all–cause mortality was attenuated by 12.8% after adjusting for nutritional status, but remained significant. Importantly, underweight does not entirely reflect malnutrition and, therefore, does not seize completely the nutritional pathway of the association between tooth loss and mortality.1616. Koka S, Gupta A. Association between missing tooth count and mortality: a systematic review. J Prosthodont Res. 2018 Apr;62(2):134-51. https://doi.org/10.1016/j.jpor.2017.08.003
https://doi.org/10.1016/j.jpor.2017.08.0...
,2222. Liu YH, Gao X, Mitchell DC, Wood GC, Still CD, Jensen GL. diet quality is associated with mortality in adults aged 80 years and older: a prospective study. J Am Geriatr Soc. 2019 Oct;67(10):2180-5. https://doi.org/10.1111/jgs.16089
https://doi.org/10.1111/jgs.16089...
Studies assessing the association between tooth loss and malnutrition using nutritional assessment measures other than those based on BMI have demonstrated stronger associations.99. Kossioni AE. The Association of Poor Oral Health parameters with malnutrition in older adults: a review considering the potential implications for cognitive impairment. Nutrients. 2018 Nov;10(11):E1709. https://doi.org/10.3390/nu10111709
https://doi.org/10.3390/nu10111709...
,1010. Gupta A, Khandelwal R, Kapil U. Interrelationship between dental health status and nutritional status among elderly subjects in India. J Family Med Prim Care. 2019 Feb;8(2):477-81. https://doi.org/10.4103/jfmpc.jfmpc_353_18
https://doi.org/10.4103/jfmpc.jfmpc_353_...
Similarly, the association between oral health and mortality after adjusting for nutritional factors, including serum albumin level2424. Hiratsuka T, Komiyama T, Ohi T, Tanji F, Tomata Y, Tsuji I, et al. Contribution of systemic inflammation and nutritional status to the relationship between tooth loss and mortality in a community-dwelling older Japanese population: a mediation analysis of data from the Tsurugaya project. Clin Oral Investig. 2019 Sep 4. https://doi.org/10.1007/s00784-019-03072-y
https://doi.org/10.1007/s00784-019-03072...
or nutrient intake,1212. Lee MS, Huang YC, Wahlqvist ML. Chewing ability in conjunction with food intake and energy status in later life affects survival in Taiwanese with the metabolic syndrome. J Am Geriatr Soc. 2010 Jun;58(6):1072-80. https://doi.org/10.1111/j.1532-5415.2010.02870.x
https://doi.org/10.1111/j.1532-5415.2010...
resulted in greater attenuation than in studies using BMI.1313. Watt RG, Tsakos G, de Oliveira C, Hamer M. Tooth loss and cardiovascular disease mortality risk: results from the Scottish Health Survey. PLoS One. 2012;7(2):e30797. https://doi.org/10.1371/journal.pone.0030797
https://doi.org/10.1371/journal.pone.003...
,3434. Manabe K, Tanji F, Tomata Y, Zhang S, Tsuji I. Preventive effect of oral self-care on pneumonia death among the elderly with tooth loss: the Ohsaki Cohort 2006 Study. Tohoku J Exp Med. 2019 Apr;247(4):251-7. https://doi.org/10.1620/tjem.247.251
https://doi.org/10.1620/tjem.247.251...
This could be because underweight captures only the information on body mass, but cannot qualify the loss.99. Kossioni AE. The Association of Poor Oral Health parameters with malnutrition in older adults: a review considering the potential implications for cognitive impairment. Nutrients. 2018 Nov;10(11):E1709. https://doi.org/10.3390/nu10111709
https://doi.org/10.3390/nu10111709...

The strengths of this study must be highlighted. To the best of our knowledge, this was the first study to assess the relationship between dental status and mortality in an unequal western upper–middle income country. This population–based study was conducted on a large representative probabilistic sample of community–dwelling older adults living in São Paulo, the largest Brazilian city that represents significative sociodemographic variety of that country.2525. Lebrão ML. SABE - Saúde, bem-estar e envelhecimento: o Projeto Sabe no município de São Paulo: uma abordagem inicial. Brasília, DF: Organização Pan-Americana da Saúde; 2003. However, there are some limitations. First, the use of a summary measure of poor nutritional status was based on BMI, which has been shown to be an useful and reliable tool in large surveys.3636. Nascimento-Souza MA, Lima-Costa MF, Peixoto SV. “A body shape index” and its association with arterial hypertension and diabetes mellitus among Brazilian older adults: National Health Survey (2013). Cad Saude Publica. 2019 Aug;35(8):e00175318. https://doi.org/10.1590/0102-311x00175318
https://doi.org/10.1590/0102-311x0017531...
Second, the Lipschitz nutritional status classification limits comparison of our results with those from other studies, although this cut–off has been validated and indicated for older adults.2929. Lipschitz DA. Screening for nutritional status in the elderly. Prim Care. 1994 Mar;21(1):55-67. Finally, edentulism and nutritional status were measured at baseline. However, reverse causality hypothesis can be ruled out because edentulism occurred several years before the occurrence of weight loss among Brazilian older adults.55. Peres MA, Barbato PR, Reis SC, Freitas CH, Antunes JL. Tooth loss in Brazil: analysis of the 2010 Brazilian oral health survey. Rev Saude Publica. 2013 Dec;47(3 Suppl 3):78-89. https://doi.org/10.1590/S0034-8910.2013047004226
https://doi.org/10.1590/S0034-8910.20130...

The results of this study highlight the importance of preventing tooth loss throughout life to avoid edentulism and the related adverse health outcomes.11. Moriya S, Miura H. Oral health and general health at the early stage of ageing: a review of contemporary studies. Jpn Dent Sci Rev. 2014 Feb;50(1):15-20. https://doi.org/10.1016/j.jdsr.2013.10.002
https://doi.org/10.1016/j.jdsr.2013.10.0...
,66. Polzer I, Schimmel M, Müller F, Biffar R. Edentulism as part of the general health problems of elderly adults. Int Dent J. 2010 Jun;60(3):143-55. https://doi.org/10.1922/IDJ_2184Polzer13
https://doi.org/10.1922/IDJ_2184Polzer13...
,88. de Andrade FB, Lebrão ML, de Oliveira Duarte YA, Santos JL. Oral health and changes in weight and waist circumference among community-dwelling older adults in Brazil. J Am Dent Assoc. 2014 Jul;145(7):731-6. https://doi.org/10.14219/jada.2014.35
https://doi.org/10.14219/jada.2014.35...
Furthermore, it is necessary to evaluate how prosthetic dental rehabilitation affects the relationship between edentulism and mortality considering its already known beneficial effects on quality of life3535. Heydecke G, Locker D, Awad MA, Lund JP, Feine JS. Oral and general health-related quality of life with conventional and implant dentures. Community Dent Oral Epidemiol. 2003 Jun;31(3):161-8. https://doi.org/10.1034/j.1600-0528.2003.00029.x
https://doi.org/10.1034/j.1600-0528.2003...
, general health,66. Polzer I, Schimmel M, Müller F, Biffar R. Edentulism as part of the general health problems of elderly adults. Int Dent J. 2010 Jun;60(3):143-55. https://doi.org/10.1922/IDJ_2184Polzer13
https://doi.org/10.1922/IDJ_2184Polzer13...
and survival.44. Gupta A, Felton DA, Jemt T, Koka S. Rehabilitation of Edentulism and Mortality: A Systematic Review. J Prosthodont. 2019 Jun;28(5):526-35. https://doi.org/10.1111/jopr.12792
https://doi.org/10.1111/jopr.12792...

Conclusions

Edentulism is a significant predictor of all-cause mortality, independently of socioeconomic factors, health behavior, and health status among Brazilian older adults. This association remains significant, although attenuated, even after additional adjustment for underweight. Further studies should investigate the effect of other nutritional assessment measures and the role of inflammatory markers and health conditions on this association, considering the most recent causal mediation approaches available.

Acknowledgements

SABE study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (Fapesp). EJP Oliveira received a doctoral scholarship from Coordenação de Aperfeicoamento de Pessoal de Nível Superior (Capes).

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Publication Dates

  • Publication in this collection
    19 June 2020
  • Date of issue
    2020

History

  • Received
    12 Nov 2019
  • Accepted
    23 Mar 2020
  • Reviewed
    15 Apr 2020
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