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Published in: BMC Cancer 1/2024

Open Access 01-12-2024 | Lung Cancer | Research

Dental health and lung cancer risk in the Golestan Cohort Study

Authors: Yukiko Yano, Christian C. Abnet, Gholamreza Roshandel, Akua Graf, Hossein Poustchi, Masoud Khoshnia, Akram Pourshams, Farin Kamangar, Paolo Boffetta, Paul Brennan, Sanford M. Dawsey, Emily Vogtmann, Reza Malekzadeh, Arash Etemadi

Published in: BMC Cancer | Issue 1/2024

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Abstract

Background

Poor oral health has been linked to various systemic diseases, including multiple cancer types, but studies of its association with lung cancer have been inconclusive.

Methods

We examined the relationship between dental status and lung cancer incidence and mortality in the Golestan Cohort Study, a large, prospective cohort of 50,045 adults in northeastern Iran. Cox proportional hazards models were used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs) for associations between three dental health measures (i.e., number of missing teeth; the sum of decayed, missing, or filled teeth (DMFT); and toothbrushing frequency) and lung cancer incidence or mortality with adjustment for multiple potential confounders, including cigarette smoking and opium use. We created tertiles of the number of lost teeth/DMFT score in excess of the loess adjusted, age- and sex-specific predicted numbers, with subjects with the expected number of lost teeth/DMFT or fewer as the reference group.

Results

During a median follow-up of 14 years, there were 119 incident lung cancer cases and 98 lung cancer deaths. Higher DMFT scores were associated with a progressively increased risk of lung cancer (linear trend, p = 0.011). Compared with individuals with the expected DMFT score or less, the HRs were 1.27 (95% CI: 0.73, 2.22), 2.15 (95% CI: 1.34, 3.43), and 1.52 (95% CI: 0.81, 2.84) for the first to the third tertiles of DMFT, respectively. The highest tertile of tooth loss also had an increased risk of lung cancer, with a HR of 1.68 (95% CI: 1.04, 2.70) compared with subjects with the expected number of lost teeth or fewer (linear trend, p = 0.043). The results were similar for lung cancer mortality and did not change substantially when the analysis was restricted to never users of cigarettes or opium. We found no associations between toothbrushing frequency and lung cancer incidence or mortality.

Conclusion

Poor dental health indicated by tooth loss or DMFT, but not lack of toothbrushing, was associated with increased lung cancer incidence and mortality in this rural Middle Eastern population.
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Literature
1.
go back to reference Peres MA, Macpherson LMD, Weyant RJ, Daly B, Venturelli R, Mathur MR, et al. Oral diseases: a global public health challenge. The Lancet. 2019;394:249–60.CrossRef Peres MA, Macpherson LMD, Weyant RJ, Daly B, Venturelli R, Mathur MR, et al. Oral diseases: a global public health challenge. The Lancet. 2019;394:249–60.CrossRef
2.
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;99:362–73.CrossRefPubMed 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;99:362–73.CrossRefPubMed
3.
go back to reference Kapila YL. Oral health’s inextricable connection to systemic health: special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontol 2000. 2021;87:11–6. Kapila YL. Oral health’s inextricable connection to systemic health: special populations bring to bear multimodal relationships and factors connecting periodontal disease to systemic diseases and conditions. Periodontol 2000. 2021;87:11–6.
4.
go back to reference Meurman JH, Bascones-Martinez A. Are oral and dental diseases linked to cancer? Oral Dis. 2011;17:779–84.CrossRefPubMed Meurman JH, Bascones-Martinez A. Are oral and dental diseases linked to cancer? Oral Dis. 2011;17:779–84.CrossRefPubMed
5.
7.
go back to reference Wu H, Zhang J, Zhou B. Toothbrushing frequency and gastric and upper aerodigestive tract cancer risk: a meta-analysis. Eur J Clin Invest. 2021;51. Wu H, Zhang J, Zhou B. Toothbrushing frequency and gastric and upper aerodigestive tract cancer risk: a meta-analysis. Eur J Clin Invest. 2021;51.
8.
go back to reference Yano Y, Abnet CC, Poustchi H, Roshandel G, Pourshams A, Islami F, et al. Oral health and risk of upper gastrointestinal cancers in a large prospective study from a high-risk region: Golestan Cohort Study. Cancer Prev Res. 2021;14:709–18.CrossRef Yano Y, Abnet CC, Poustchi H, Roshandel G, Pourshams A, Islami F, et al. Oral health and risk of upper gastrointestinal cancers in a large prospective study from a high-risk region: Golestan Cohort Study. Cancer Prev Res. 2021;14:709–18.CrossRef
9.
10.
go back to reference Nieminen M, Salaspuro M. Local acetaldehyde—An essential role in alcohol-related upper gastrointestinal tract carcinogenesis. Cancers (Basel). 2018;10:11.CrossRefPubMed Nieminen M, Salaspuro M. Local acetaldehyde—An essential role in alcohol-related upper gastrointestinal tract carcinogenesis. Cancers (Basel). 2018;10:11.CrossRefPubMed
11.
go back to reference Shapiro KB, Hotchkiss JH, Roe DA. Quantitative relationship between oral nitrate-reducing activity and the endogenous formation of N-nitrosoamino acids in humans. Food Chem Toxicol. 1991;29:751–5.CrossRefPubMed Shapiro KB, Hotchkiss JH, Roe DA. Quantitative relationship between oral nitrate-reducing activity and the endogenous formation of N-nitrosoamino acids in humans. Food Chem Toxicol. 1991;29:751–5.CrossRefPubMed
12.
go back to reference Nair J, Ohshima H, Nair UJ, Bartsch H. Endogenous formation of nitrosamines and oxidative DNA-damaging agents in tobacco users. Crit Rev Toxicol. 1996;26:149–61.CrossRefPubMed Nair J, Ohshima H, Nair UJ, Bartsch H. Endogenous formation of nitrosamines and oxidative DNA-damaging agents in tobacco users. Crit Rev Toxicol. 1996;26:149–61.CrossRefPubMed
14.
go back to reference Yoon H-S, Shu X-O, Gao Y-T, Yang G, Cai H, Shi J, et al. Tooth loss and risk of lung cancer among urban Chinese adults: a Cohort Study with meta-analysis. Cancers (Basel). 2022;14:2428.CrossRefPubMed Yoon H-S, Shu X-O, Gao Y-T, Yang G, Cai H, Shi J, et al. Tooth loss and risk of lung cancer among urban Chinese adults: a Cohort Study with meta-analysis. Cancers (Basel). 2022;14:2428.CrossRefPubMed
15.
go back to reference Chen Y, Zhu B-L, Wu C-C, Lin R-F, Zhang X. Periodontal disease and tooth loss are associated with lung cancer risk. Biomed Res Int. 2020;2020:1–12. Chen Y, Zhu B-L, Wu C-C, Lin R-F, Zhang X. Periodontal disease and tooth loss are associated with lung cancer risk. Biomed Res Int. 2020;2020:1–12.
16.
go back to reference Yoon H-S, Wen W, Long J, Zheng W, Blot WJ, Cai Q. Association of oral health with lung cancer risk in a low-income population of African Americans and European Americans in the Southeastern United States. Lung Cancer. 2019;127:90–5.CrossRefPubMed Yoon H-S, Wen W, Long J, Zheng W, Blot WJ, Cai Q. Association of oral health with lung cancer risk in a low-income population of African Americans and European Americans in the Southeastern United States. Lung Cancer. 2019;127:90–5.CrossRefPubMed
17.
go back to reference Mai X, LaMonte MJ, Hovey KM, Nwizu N, Freudenheim JL, Tezal M, et al. History of periodontal disease diagnosis and lung cancer incidence in the women’s health initiative observational study. Cancer Causes Control. 2014;25:1045–53.CrossRefPubMedPubMedCentral Mai X, LaMonte MJ, Hovey KM, Nwizu N, Freudenheim JL, Tezal M, et al. History of periodontal disease diagnosis and lung cancer incidence in the women’s health initiative observational study. Cancer Causes Control. 2014;25:1045–53.CrossRefPubMedPubMedCentral
18.
go back to reference Nwizu NN, Marshall JR, Moysich K, Genco RJ, Hovey KM, Mai X, et al. Periodontal disease and incident cancer risk among postmenopausal women: results from the women’s health initiative observational cohort. Cancer Epidemiol Biomarkers Prev. 2017;26:1255–65.CrossRefPubMedPubMedCentral Nwizu NN, Marshall JR, Moysich K, Genco RJ, Hovey KM, Mai X, et al. Periodontal disease and incident cancer risk among postmenopausal women: results from the women’s health initiative observational cohort. Cancer Epidemiol Biomarkers Prev. 2017;26:1255–65.CrossRefPubMedPubMedCentral
19.
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;9:550–8.CrossRefPubMedPubMedCentral 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;9:550–8.CrossRefPubMedPubMedCentral
20.
go back to reference Michaud DS, Kelsey KT, Papathanasiou E, Genco CA, Giovannucci E. Periodontal disease and risk of all cancers among male never smokers: an updated analysis of the Health professionals follow-up study. Ann Oncol. 2016;27:941–7.CrossRefPubMedPubMedCentral Michaud DS, Kelsey KT, Papathanasiou E, Genco CA, Giovannucci E. Periodontal disease and risk of all cancers among male never smokers: an updated analysis of the Health professionals follow-up study. Ann Oncol. 2016;27:941–7.CrossRefPubMedPubMedCentral
21.
go back to reference Hujoel PP, Drangsholt M, Spiekerman C, Weiss NS. An exploration of the periodontitis–cancer association. Ann Epidemiol. 2003;13:312–6.CrossRefPubMed Hujoel PP, Drangsholt M, Spiekerman C, Weiss NS. An exploration of the periodontitis–cancer association. Ann Epidemiol. 2003;13:312–6.CrossRefPubMed
22.
go back to reference Michaud DS, Lu J, Peacock-Villada AY, Barber JR, Joshu CE, Prizment AE, et al. Periodontal disease assessed using clinical dental measurements and cancer risk in the ARIC study. JNCI: J Natl Cancer Inst. 2018;110:843–54. Michaud DS, Lu J, Peacock-Villada AY, Barber JR, Joshu CE, Prizment AE, et al. Periodontal disease assessed using clinical dental measurements and cancer risk in the ARIC study. JNCI: J Natl Cancer Inst. 2018;110:843–54.
23.
go back to reference Pourshams A, Khademi H, Malekshah AF, Islami F, Nouraei M, Sadjadi AR, et al. Cohort Profile: the Golestan Cohort Study-a prospective study of oesophageal cancer in northern Iran. Int J Epidemiol. 2010;39:52–9.CrossRefPubMed Pourshams A, Khademi H, Malekshah AF, Islami F, Nouraei M, Sadjadi AR, et al. Cohort Profile: the Golestan Cohort Study-a prospective study of oesophageal cancer in northern Iran. Int J Epidemiol. 2010;39:52–9.CrossRefPubMed
24.
go back to reference Warnakulasuriya S, Cronin-Fenton D, Jinot J, Kamangar F, Malekzadeh R, Dar NA, et al. Carcinogenicity of opium consumption. Lancet Oncol. 2020;21:1407–8.CrossRef Warnakulasuriya S, Cronin-Fenton D, Jinot J, Kamangar F, Malekzadeh R, Dar NA, et al. Carcinogenicity of opium consumption. Lancet Oncol. 2020;21:1407–8.CrossRef
25.
go back to reference Sheikh M, Shakeri R, Poustchi H, Pourshams A, Etemadi A, Islami F, et al. Opium use and subsequent incidence of cancer: results from the Golestan Cohort Study. Lancet Glob Health. 2020;8:e649–60.CrossRefPubMedPubMedCentral Sheikh M, Shakeri R, Poustchi H, Pourshams A, Etemadi A, Islami F, et al. Opium use and subsequent incidence of cancer: results from the Golestan Cohort Study. Lancet Glob Health. 2020;8:e649–60.CrossRefPubMedPubMedCentral
26.
go back to reference Etemadi A, Poustchi H, Calafat AM, Blount BC, De Jesús VR, Wang L, et al. Opiate and Tobacco Use and exposure to carcinogens and toxicants in the Golestan Cohort Study. Cancer Epidemiol Biomarkers Prev. 2020;29:650–8.CrossRefPubMedPubMedCentral Etemadi A, Poustchi H, Calafat AM, Blount BC, De Jesús VR, Wang L, et al. Opiate and Tobacco Use and exposure to carcinogens and toxicants in the Golestan Cohort Study. Cancer Epidemiol Biomarkers Prev. 2020;29:650–8.CrossRefPubMedPubMedCentral
27.
go back to reference Islami F, Kamangar F, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, Abedi-Ardekani B, et al. Socio-economic status and oesophageal cancer: results from a population-based case–control study in a high-risk area. Int J Epidemiol. 2009;38:978–88.CrossRefPubMedPubMedCentral Islami F, Kamangar F, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, Abedi-Ardekani B, et al. Socio-economic status and oesophageal cancer: results from a population-based case–control study in a high-risk area. Int J Epidemiol. 2009;38:978–88.CrossRefPubMedPubMedCentral
28.
go back to reference Abnet CC, Saadatian-Elahi M, Pourshams A, Boffetta P, Feizzadeh A, Brennan P, et al. Reliability and validity of opiate use self-report in a population at high risk for esophageal cancer in Golestan, Iran. Cancer Epidemiol Biomarkers Prev. 2004;13:1068–70.CrossRefPubMed Abnet CC, Saadatian-Elahi M, Pourshams A, Boffetta P, Feizzadeh A, Brennan P, et al. Reliability and validity of opiate use self-report in a population at high risk for esophageal cancer in Golestan, Iran. Cancer Epidemiol Biomarkers Prev. 2004;13:1068–70.CrossRefPubMed
29.
go back to reference Etemadi A, Poustchi H, Chang CM, Blount BC, Calafat AM, Wang L, et al. Urinary biomarkers of carcinogenic exposure among cigarette, waterpipe, and smokeless tobacco users and never users of tobacco in the Golestan Cohort Study. Cancer Epidemiol Biomarkers Prev. 2019;28:337–47.CrossRefPubMedPubMedCentral Etemadi A, Poustchi H, Chang CM, Blount BC, Calafat AM, Wang L, et al. Urinary biomarkers of carcinogenic exposure among cigarette, waterpipe, and smokeless tobacco users and never users of tobacco in the Golestan Cohort Study. Cancer Epidemiol Biomarkers Prev. 2019;28:337–47.CrossRefPubMedPubMedCentral
30.
go back to reference Pourshams A, Saadatian-Elahi M, Nouraie M, Malekshah AF, Rakhshani N, Salahi R, et al. Golestan cohort study of oesophageal cancer: feasibility and first results. Br J Cancer. 2005;92:176–81.CrossRefPubMed Pourshams A, Saadatian-Elahi M, Nouraie M, Malekshah AF, Rakhshani N, Salahi R, et al. Golestan cohort study of oesophageal cancer: feasibility and first results. Br J Cancer. 2005;92:176–81.CrossRefPubMed
31.
go back to reference Khademi H, Etemadi A, Kamangar F, Nouraie M, Shakeri R, Abaie B, et al. Verbal autopsy: reliability and validity estimates for causes of death in the Golestan Cohort Study in Iran. PLoS ONE. 2010;5:e11183.CrossRefPubMedPubMedCentral Khademi H, Etemadi A, Kamangar F, Nouraie M, Shakeri R, Abaie B, et al. Verbal autopsy: reliability and validity estimates for causes of death in the Golestan Cohort Study in Iran. PLoS ONE. 2010;5:e11183.CrossRefPubMedPubMedCentral
32.
go back to reference Roshandel G, Semnani S, Fazel A, Honarvar M, Taziki M, Sedaghat S, et al. Building cancer registries in a lower resource setting: the 10-year experience of Golestan, Northern Iran. Cancer Epidemiol. 2018;52:128–33.CrossRefPubMed Roshandel G, Semnani S, Fazel A, Honarvar M, Taziki M, Sedaghat S, et al. Building cancer registries in a lower resource setting: the 10-year experience of Golestan, Northern Iran. Cancer Epidemiol. 2018;52:128–33.CrossRefPubMed
33.
go back to reference Abnet CC, Qiao Y-L, Dawsey SM, Dong Z-W, Taylor PR, Mark SD. Tooth loss is associated with increased risk of total death and death from upper gastrointestinal cancer, heart disease, and stroke in a Chinese population-based cohort. Int J Epidemiol. 2005;34:467–74.CrossRefPubMed Abnet CC, Qiao Y-L, Dawsey SM, Dong Z-W, Taylor PR, Mark SD. Tooth loss is associated with increased risk of total death and death from upper gastrointestinal cancer, heart disease, and stroke in a Chinese population-based cohort. Int J Epidemiol. 2005;34:467–74.CrossRefPubMed
34.
go back to reference R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2023. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2023.
35.
go back to reference Wang J, Yang X, Zou X, Zhang Y, Wang J, Wang Y. Relationship between periodontal disease and lung cancer: a systematic review and meta-analysis. J Periodontal Res. 2020;55:581–93.CrossRefPubMed Wang J, Yang X, Zou X, Zhang Y, Wang J, Wang Y. Relationship between periodontal disease and lung cancer: a systematic review and meta-analysis. J Periodontal Res. 2020;55:581–93.CrossRefPubMed
36.
go back to reference Goto Y, Wada K, Uji T, Koda S, Mizuta F, Yamakawa M, et al. Number of Teeth and all-cause and Cancer Mortality in a Japanese Community: the Takayama Study. J Epidemiol. 2020;30:213–8.CrossRefPubMedPubMedCentral Goto Y, Wada K, Uji T, Koda S, Mizuta F, Yamakawa M, et al. Number of Teeth and all-cause and Cancer Mortality in a Japanese Community: the Takayama Study. J Epidemiol. 2020;30:213–8.CrossRefPubMedPubMedCentral
37.
go back to reference Wu Z, O’Brien KM, Lawrence KG, Han Y, Weinberg CR, Sandler DP, et al. Associations of periodontal disease and tooth loss with all-cause and cause‐specific mortality in the Sister Study. J Clin Periodontol. 2021;48:1597–604.CrossRefPubMedPubMedCentral Wu Z, O’Brien KM, Lawrence KG, Han Y, Weinberg CR, Sandler DP, et al. Associations of periodontal disease and tooth loss with all-cause and cause‐specific mortality in the Sister Study. J Clin Periodontol. 2021;48:1597–604.CrossRefPubMedPubMedCentral
38.
go back to reference Sinha R, Zhao N, Goedert JJ, Byrd DA, Wan Y, Hua X, et al. Effects of processed meat and drinking water nitrate on oral and fecal microbial populations in a controlled feeding study. Environ Res. 2021;197:111084.CrossRefPubMedPubMedCentral Sinha R, Zhao N, Goedert JJ, Byrd DA, Wan Y, Hua X, et al. Effects of processed meat and drinking water nitrate on oral and fecal microbial populations in a controlled feeding study. Environ Res. 2021;197:111084.CrossRefPubMedPubMedCentral
42.
go back to reference Vogtmann E, Hua X, Yu G, Purandare V, Hullings AG, Shao D et al. The Oral Microbiome and Lung Cancer Risk: An Analysis of 3 Prospective Cohort Studies. JNCI: Journal of the National Cancer Institute. 2022;114:1501–10. Vogtmann E, Hua X, Yu G, Purandare V, Hullings AG, Shao D et al. The Oral Microbiome and Lung Cancer Risk: An Analysis of 3 Prospective Cohort Studies. JNCI: Journal of the National Cancer Institute. 2022;114:1501–10.
43.
go back to reference Shi J, Yang Y, Xie H, Wang X, Wu J, Long J, et al. Association of oral microbiota with lung cancer risk in a low-income population in the Southeastern USA. Cancer Causes Control. 2021;32:1423–32.CrossRefPubMedPubMedCentral Shi J, Yang Y, Xie H, Wang X, Wu J, Long J, et al. Association of oral microbiota with lung cancer risk in a low-income population in the Southeastern USA. Cancer Causes Control. 2021;32:1423–32.CrossRefPubMedPubMedCentral
44.
go back to reference Hosgood HD, Cai Q, Hua X, Long J, Shi J, Wan Y, et al. Variation in oral microbiome is associated with future risk of lung cancer among never-smokers. Thorax. 2021;76:256–63.CrossRefPubMed Hosgood HD, Cai Q, Hua X, Long J, Shi J, Wan Y, et al. Variation in oral microbiome is associated with future risk of lung cancer among never-smokers. Thorax. 2021;76:256–63.CrossRefPubMed
45.
go back to reference Ampomah NK, Teles F, Martin LM, Lu J, Koestler DC, Kelsey KT et al. Circulating IgG antibodies to periodontal bacteria and lung cancer risk in the CLUE cohorts. JNCI Cancer Spectr. 2023;7. Ampomah NK, Teles F, Martin LM, Lu J, Koestler DC, Kelsey KT et al. Circulating IgG antibodies to periodontal bacteria and lung cancer risk in the CLUE cohorts. JNCI Cancer Spectr. 2023;7.
Metadata
Title
Dental health and lung cancer risk in the Golestan Cohort Study
Authors
Yukiko Yano
Christian C. Abnet
Gholamreza Roshandel
Akua Graf
Hossein Poustchi
Masoud Khoshnia
Akram Pourshams
Farin Kamangar
Paolo Boffetta
Paul Brennan
Sanford M. Dawsey
Emily Vogtmann
Reza Malekzadeh
Arash Etemadi
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2024
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-024-11850-5

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