Skip to main content
Top
Published in: BMC Oral Health 1/2020

Open Access 01-12-2020 | Gingival Diseases | Research article

Association between periodontitis and all-cause and cancer mortality: retrospective elderly community cohort study

Authors: Ping-Chen Chung, Ta-Chien Chan

Published in: BMC Oral Health | Issue 1/2020

Login to get access

Abstract

Background

Periodontal infection induces inflammation, which may increase the risk of tumor-promoting effects. The aim of this study was to assess the association between periodontitis and all-cause mortality, and all-cancer and specific cancers’ mortality in a health examination cohort of the elderly in the communities.

Methods

A dataset of health examinations for the elderly with cause of death from 2005 to 2012 was obtained from the Department of Health, Taipei City Government. We enrolled 82,548 study participants with 262,035 visits. A Cox proportional hazards model and Cox frailty model were used for calculating the hazard ratios under different periodontal status by using SAS and Rstudio.

Results

Being male, elderly, having a low education level, and smoking were risk factors for mortality in this retrospective elderly community cohort study. Participants with periodontitis followed across time had significantly higher hazard ratios (HRs) for all-cause mortality and all-cancer mortality (HR = 1.092, 95% confidence interval (CI):1.038 to 1.149, HR = 1.114, 95% CI:1.032 to 1.203, respectively) in the Cox frailty models after adjusting for age, marital status, education level, sex, and smoking status. After adjusting for age and sex, the hazard ratio was 1.185 (95% CI: 1.027 to 1.368) for lung cancer mortality, and 1.340 (95% CI: 1.019 to 1.762) for prostate cancer mortality in the periodontitis group with each visit.

Conclusions

The findings indicated that being male, having a low education level, and daily smoking were risk factors for mortality, and showed mixed evidence that periodontal disease is associated with all-cause, all-cancer and specific-cancer mortality including lung and prostate cancer. We suggest the importance of regular health screening in order to achieve early disease detection and lower mortality risk.
Appendix
Available only for authorised users
Literature
1.
go back to reference Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev. 2001;14(4):727–52.PubMedPubMedCentralCrossRef Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev. 2001;14(4):727–52.PubMedPubMedCentralCrossRef
3.
go back to reference Janket SJ, Baird AE, Chuang SK, Jones JA. Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003;95(5):559–69.PubMedCrossRef Janket SJ, Baird AE, Chuang SK, Jones JA. Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003;95(5):559–69.PubMedCrossRef
4.
go back to reference Kinane DF, Marshall GJ. Periodontal manifestations of systemic disease. Aust Dent J. 2001;46(1):2–12.PubMedCrossRef Kinane DF, Marshall GJ. Periodontal manifestations of systemic disease. Aust Dent J. 2001;46(1):2–12.PubMedCrossRef
5.
go back to reference Shen TC, Chang PY, Lin CL, Chen CH, Tu CY, Hsia TC, et al. Risk of periodontal diseases in patients with chronic obstructive pulmonary disease: a nationwide population-based cohort study. Medicine. 2015;94(46):e2047.PubMedPubMedCentralCrossRef Shen TC, Chang PY, Lin CL, Chen CH, Tu CY, Hsia TC, et al. Risk of periodontal diseases in patients with chronic obstructive pulmonary disease: a nationwide population-based cohort study. Medicine. 2015;94(46):e2047.PubMedPubMedCentralCrossRef
6.
go back to reference Ricardo AC, Athavale A, Chen J, Hampole H, Garside D, Marucha P, et al. Periodontal disease, chronic kidney disease and mortality: results from the third National Health and nutrition examination survey. BMC Nephrol. 2015;16:97.PubMedPubMedCentralCrossRef Ricardo AC, Athavale A, Chen J, Hampole H, Garside D, Marucha P, et al. Periodontal disease, chronic kidney disease and mortality: results from the third National Health and nutrition examination survey. BMC Nephrol. 2015;16:97.PubMedPubMedCentralCrossRef
7.
go back to reference Hujoel PP, Drangsholt M, Spiekerman C, Weiss NS. An exploration of the periodontitis-cancer association. Ann Epidemiol. 2003;13(5):312–6.PubMedCrossRef Hujoel PP, Drangsholt M, Spiekerman C, Weiss NS. An exploration of the periodontitis-cancer association. Ann Epidemiol. 2003;13(5):312–6.PubMedCrossRef
8.
go back to reference Abnet CC, Kamangar F, Islami F, Nasrollahzadeh D, Brennan P, Aghcheli K, et al. Tooth loss and lack of regular oral hygiene are associated with higher risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2008;17(11):3062–8.PubMedPubMedCentralCrossRef Abnet CC, Kamangar F, Islami F, Nasrollahzadeh D, Brennan P, Aghcheli K, et al. Tooth loss and lack of regular oral hygiene are associated with higher risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2008;17(11):3062–8.PubMedPubMedCentralCrossRef
9.
go back to reference Heikkila P, But A, Sorsa T, Haukka J. Periodontitis and cancer mortality: register-based cohort study of 68,273 adults in 10-year follow-up. Int J Cancer. 2018;142(11):2244–53.PubMedCrossRef Heikkila P, But A, Sorsa T, Haukka J. Periodontitis and cancer mortality: register-based cohort study of 68,273 adults in 10-year follow-up. Int J Cancer. 2018;142(11):2244–53.PubMedCrossRef
10.
go back to reference Michaud DS, Liu Y, Meyer M, Giovannucci E, Joshipura K. Periodontal disease, tooth loss, and cancer risk in male health professionals: a prospective cohort study. Lancet Oncol. 2008;9(6):550–8.PubMedPubMedCentralCrossRef Michaud DS, Liu Y, Meyer M, Giovannucci E, Joshipura K. Periodontal disease, tooth loss, and cancer risk in male health professionals: a prospective cohort study. Lancet Oncol. 2008;9(6):550–8.PubMedPubMedCentralCrossRef
12.
go back to reference Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436–44.CrossRefPubMed Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436–44.CrossRefPubMed
13.
go back to reference Hoare A, Soto C, Rojas-Celis V, Bravo D. Chronic inflammation as a link between periodontitis and carcinogenesis. Mediat Inflamm. 2019;2019:1029857.CrossRef Hoare A, Soto C, Rojas-Celis V, Bravo D. Chronic inflammation as a link between periodontitis and carcinogenesis. Mediat Inflamm. 2019;2019:1029857.CrossRef
14.
go back to reference Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJ, Marcenes W. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res. 2014;93(11):1045–53.PubMedPubMedCentralCrossRef Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJ, Marcenes W. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res. 2014;93(11):1045–53.PubMedPubMedCentralCrossRef
15.
go back to reference Bernabe E, Marcenes W, Hernandez CR, Bailey J, Abreu LG, Alipour V, et al. Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: a systematic analysis for the global burden of disease 2017 study. J Dent Res. 2020;99(4):362–73.PubMedCrossRef Bernabe E, Marcenes W, Hernandez CR, Bailey J, Abreu LG, Alipour V, et al. Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: a systematic analysis for the global burden of disease 2017 study. J Dent Res. 2020;99(4):362–73.PubMedCrossRef
16.
go back to reference Yu HC, Su NY, Huang JY, Lee SS, Chang YC. Trends in the prevalence of periodontitis in Taiwan from 1997 to 2013: A nationwide population-based retrospective study. Medicine. 2017;96(45):e8585–e.PubMedPubMedCentralCrossRef Yu HC, Su NY, Huang JY, Lee SS, Chang YC. Trends in the prevalence of periodontitis in Taiwan from 1997 to 2013: A nationwide population-based retrospective study. Medicine. 2017;96(45):e8585–e.PubMedPubMedCentralCrossRef
17.
go back to reference Lai H, Su CW, Yen AM, Chiu SY, Fann JC, Wu WY, et al. A prediction model for periodontal disease: Modelling and validation from a national survey of 4061 Taiwanese adults. J Clin Periodontol. 2015;42(5):413–21.PubMedCrossRef Lai H, Su CW, Yen AM, Chiu SY, Fann JC, Wu WY, et al. A prediction model for periodontal disease: Modelling and validation from a national survey of 4061 Taiwanese adults. J Clin Periodontol. 2015;42(5):413–21.PubMedCrossRef
18.
go back to reference Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J. Development of the World Health Organization (WHO) community periodontal index of treatment needs (CPITN). Int Dent J. 1982;32(3):281–91.PubMed Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J. Development of the World Health Organization (WHO) community periodontal index of treatment needs (CPITN). Int Dent J. 1982;32(3):281–91.PubMed
19.
go back to reference Visscher CM, Lobbezoo F, Schuller AA. Dental status and oral health-related quality of life. A population-based study. J Oral Rhabilitation. 2014;41(6):416–22.CrossRef Visscher CM, Lobbezoo F, Schuller AA. Dental status and oral health-related quality of life. A population-based study. J Oral Rhabilitation. 2014;41(6):416–22.CrossRef
21.
go back to reference Corbella S, Veronesi P, Galimberti V, Weinstein R, Del Fabbro M, Francetti L. Is periodontitis a risk indicator for cancer? A meta-analysis. PloS One. 2018;13(4):e0195683.PubMedPubMedCentralCrossRef Corbella S, Veronesi P, Galimberti V, Weinstein R, Del Fabbro M, Francetti L. Is periodontitis a risk indicator for cancer? A meta-analysis. PloS One. 2018;13(4):e0195683.PubMedPubMedCentralCrossRef
23.
go back to reference Heitz-Mayfield LJ, Trombelli L, Heitz F, Needleman I, Moles D. A systematic review of the effect of surgical debridement vs non-surgical debridement for the treatment of chronic periodontitis. J Clin Periodontol. 2002;29(Suppl 3):92–102 discussion 60-2.PubMedCrossRef Heitz-Mayfield LJ, Trombelli L, Heitz F, Needleman I, Moles D. A systematic review of the effect of surgical debridement vs non-surgical debridement for the treatment of chronic periodontitis. J Clin Periodontol. 2002;29(Suppl 3):92–102 discussion 60-2.PubMedCrossRef
24.
go back to reference Renvert S, Persson GR. Treatment of periodontal disease in older adults. Periodontol 2000. 2016;72(1):108–19.PubMedCrossRef Renvert S, Persson GR. Treatment of periodontal disease in older adults. Periodontol 2000. 2016;72(1):108–19.PubMedCrossRef
26.
go back to reference Cox DR. Regression models and life-tables. J R Stat Soc Ser B Methodol. 1972;34(2):187–220. Cox DR. Regression models and life-tables. J R Stat Soc Ser B Methodol. 1972;34(2):187–220.
27.
go back to reference Ripatti S, Palmgren J. Estimation of multivariate frailty models using penalized partial likelihood. Biometrics. 2000;56(4):1016–22.PubMedCrossRef Ripatti S, Palmgren J. Estimation of multivariate frailty models using penalized partial likelihood. Biometrics. 2000;56(4):1016–22.PubMedCrossRef
28.
go back to reference Therneau TM, Grambsch PM, Pankratz VS. Penalized survival models and frailty. J Comput Graph Stat. 2003;12(1):156–75.CrossRef Therneau TM, Grambsch PM, Pankratz VS. Penalized survival models and frailty. J Comput Graph Stat. 2003;12(1):156–75.CrossRef
31.
go back to reference Wickham H. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag; 2016.CrossRef Wickham H. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag; 2016.CrossRef
32.
go back to reference Tomás I, Diz P, Tobías A, Scully C, Donos N. Periodontal health status and bacteraemia from daily oral activities: systematic review/meta-analysis. J Clin Periodontol. 2012;39(3):213–28.PubMedCrossRef Tomás I, Diz P, Tobías A, Scully C, Donos N. Periodontal health status and bacteraemia from daily oral activities: systematic review/meta-analysis. J Clin Periodontol. 2012;39(3):213–28.PubMedCrossRef
33.
go back to reference Adolph M, Darnaud C, Thomas F, Pannier B, Danchin N, Batty GD, et al. Oral health in relation to all-cause mortality: the IPC cohort study. Sci Rep. 2017;7:44604.PubMedPubMedCentralCrossRef Adolph M, Darnaud C, Thomas F, Pannier B, Danchin N, Batty GD, et al. Oral health in relation to all-cause mortality: the IPC cohort study. Sci Rep. 2017;7:44604.PubMedPubMedCentralCrossRef
34.
go back to reference Bascones-Martínez A, Muñoz-Corcuera M, Meurman JH. Odontogenic infections in the etiology of infective endocarditis. Cardiovasc Hematol Disord Drug Targets. 2009;9(4):231–5.PubMedCrossRef Bascones-Martínez A, Muñoz-Corcuera M, Meurman JH. Odontogenic infections in the etiology of infective endocarditis. Cardiovasc Hematol Disord Drug Targets. 2009;9(4):231–5.PubMedCrossRef
35.
go back to reference Söder B, Yakob M, Meurman JH, Andersson LC, Söder P. The association of dental plaque with cancer mortality in Sweden. A longitudinal study. BMJ Open. 2012;2(3):e001083. Söder B, Yakob M, Meurman JH, Andersson LC, Söder P. The association of dental plaque with cancer mortality in Sweden. A longitudinal study. BMJ Open. 2012;2(3):e001083.
37.
go back to reference Hansen GM, Egeberg A, Holmstrup P, Hansen PR. Relation of periodontitis to risk of cardiovascular and all-cause mortality (from a Danish nationwide cohort study). Am J Cardiol. 2016;118(4):489–93.PubMedCrossRef Hansen GM, Egeberg A, Holmstrup P, Hansen PR. Relation of periodontitis to risk of cardiovascular and all-cause mortality (from a Danish nationwide cohort study). Am J Cardiol. 2016;118(4):489–93.PubMedCrossRef
38.
go back to reference Arora M, Weuve J, Fall K, Pedersen NL, Mucci LA. An exploration of shared genetic risk factors between periodontal disease and cancers: a prospective co-twin study. Am J Epidemiol. 2010;171(2):253–9.PubMedCrossRef Arora M, Weuve J, Fall K, Pedersen NL, Mucci LA. An exploration of shared genetic risk factors between periodontal disease and cancers: a prospective co-twin study. Am J Epidemiol. 2010;171(2):253–9.PubMedCrossRef
39.
go back to reference Hung HC, Colditz G, Joshipura KJ. The association between tooth loss and the self-reported intake of selected CVD-related nutrients and foods among US women. Community Dent Oral Epidemiol. 2005;33(3):167–73.PubMedCrossRef Hung HC, Colditz G, Joshipura KJ. The association between tooth loss and the self-reported intake of selected CVD-related nutrients and foods among US women. Community Dent Oral Epidemiol. 2005;33(3):167–73.PubMedCrossRef
40.
go back to reference Hiraki A, Matsuo K, Suzuki T, Kawase T, Tajima K. Teeth loss and risk of cancer at 14 common sites in Japanese. Cancer Epidemiol, Biomarkers Prev. 2008;17(5):1222–7.CrossRef Hiraki A, Matsuo K, Suzuki T, Kawase T, Tajima K. Teeth loss and risk of cancer at 14 common sites in Japanese. Cancer Epidemiol, Biomarkers Prev. 2008;17(5):1222–7.CrossRef
41.
go back to reference Fitzpatrick SG, Katz J. The association between periodontal disease and cancer: a review of the literature. J Dent. 2010;38(2):83–95.PubMedCrossRef Fitzpatrick SG, Katz J. The association between periodontal disease and cancer: a review of the literature. J Dent. 2010;38(2):83–95.PubMedCrossRef
42.
go back to reference Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ. Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol. 2004;159(12):1160–7.PubMedCrossRef Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ. Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol. 2004;159(12):1160–7.PubMedCrossRef
43.
go back to reference Inoue M, Iwasaki M, Otani T, Sasazuki S, Noda M, Tsugane S. Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med. 2006;166(17):1871–7.PubMedCrossRef Inoue M, Iwasaki M, Otani T, Sasazuki S, Noda M, Tsugane S. Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med. 2006;166(17):1871–7.PubMedCrossRef
44.
go back to reference Shikata K, Ninomiya T, Kiyohara Y. Diabetes mellitus and cancer risk: review of the epidemiological evidence. Cancer Sci. 2013;104(1):9–14.PubMedCrossRef Shikata K, Ninomiya T, Kiyohara Y. Diabetes mellitus and cancer risk: review of the epidemiological evidence. Cancer Sci. 2013;104(1):9–14.PubMedCrossRef
45.
go back to reference Kuriki K, Hirose K, Tajima K. Diabetes and cancer risk for all and specific sites among Japanese men and women. Eur J Cancer Prev. 2007;16(1):83–9.PubMedCrossRef Kuriki K, Hirose K, Tajima K. Diabetes and cancer risk for all and specific sites among Japanese men and women. Eur J Cancer Prev. 2007;16(1):83–9.PubMedCrossRef
46.
go back to reference Kebede TG, Holtfreter B, Kocher T, Meisel P, Dietrich T, Biffar R, et al. Association of periodontal destruction and diabetes with mortality. J Dent Res. 2017;96(1):56–63.PubMedCrossRef Kebede TG, Holtfreter B, Kocher T, Meisel P, Dietrich T, Biffar R, et al. Association of periodontal destruction and diabetes with mortality. J Dent Res. 2017;96(1):56–63.PubMedCrossRef
47.
go back to reference Grant WB. Vitamin D, periodontal disease, tooth loss, and cancer risk. Lancet Oncol. 2008;9(7):612–3.PubMedCrossRef Grant WB. Vitamin D, periodontal disease, tooth loss, and cancer risk. Lancet Oncol. 2008;9(7):612–3.PubMedCrossRef
48.
go back to reference Meyer MS, Joshipura K, Giovannucci E, Michaud DS. A review of the relationship between tooth loss, periodontal disease, and cancer. Cancer Causes Control. 2008;19(9):895–907.PubMedPubMedCentralCrossRef Meyer MS, Joshipura K, Giovannucci E, Michaud DS. A review of the relationship between tooth loss, periodontal disease, and cancer. Cancer Causes Control. 2008;19(9):895–907.PubMedPubMedCentralCrossRef
49.
go back to reference Tolonen H, Lundqvist A, Jääskeläinen T, Koskinen S, Koponen P. Reasons for non-participation and ways to enhance participation in health examination surveys—the health 2011 survey. Eur J Pub Health. 2017;27(5):909–11.CrossRef Tolonen H, Lundqvist A, Jääskeläinen T, Koskinen S, Koponen P. Reasons for non-participation and ways to enhance participation in health examination surveys—the health 2011 survey. Eur J Pub Health. 2017;27(5):909–11.CrossRef
50.
go back to reference Gaertner B, Seitz I, Fuchs J, Busch MA, Holzhausen M, Martus P, et al. Baseline participation in a health examination survey of the population 65 years and older: who is missed and why? BMC Geriatr. 2016;16:21.PubMedPubMedCentralCrossRef Gaertner B, Seitz I, Fuchs J, Busch MA, Holzhausen M, Martus P, et al. Baseline participation in a health examination survey of the population 65 years and older: who is missed and why? BMC Geriatr. 2016;16:21.PubMedPubMedCentralCrossRef
51.
go back to reference Chen BK, Yang CY. Differences in age-standardized mortality rates for avoidable deaths based on urbanization levels in Taiwan, 1971-2008. Int J Environ Res Public Health. 2014;11(2):1776–93.PubMedPubMedCentralCrossRef Chen BK, Yang CY. Differences in age-standardized mortality rates for avoidable deaths based on urbanization levels in Taiwan, 1971-2008. Int J Environ Res Public Health. 2014;11(2):1776–93.PubMedPubMedCentralCrossRef
52.
go back to reference Sazlina SG. Health screening for older people—what are the current recommendations? Malays Fam Phys. 2015;10(1):2–10. Sazlina SG. Health screening for older people—what are the current recommendations? Malays Fam Phys. 2015;10(1):2–10.
53.
go back to reference Riley P, Worthington HV, Clarkson JE, Beirne PV. Recall intervals for oral health in primary care patients. Cochrane Database Syst Rev. 2013;(12):Cd004346. Riley P, Worthington HV, Clarkson JE, Beirne PV. Recall intervals for oral health in primary care patients. Cochrane Database Syst Rev. 2013;(12):Cd004346.
54.
go back to reference Nazir MA. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci. 2017;11(2):72–80. Nazir MA. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci. 2017;11(2):72–80.
Metadata
Title
Association between periodontitis and all-cause and cancer mortality: retrospective elderly community cohort study
Authors
Ping-Chen Chung
Ta-Chien Chan
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2020
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-020-01156-w

Other articles of this Issue 1/2020

BMC Oral Health 1/2020 Go to the issue