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Income-related inequalities in the association of smoking with periodontitis: a cross-sectional analysis in Tokyo Metropolitan Districts

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Abstract

Objective

Socio-economic status (SES) and smoking are risk factors for periodontitis; however, their interaction has not been determined. We investigated the effect of modification of SES and smoking with periodontal conditions.

Materials and methods

Data on the social background, smoking status, and dental examination of 1033 individuals residing in the Tokyo Metropolitan District were analyzed. The outcomes were the number of remaining teeth and the proportion of teeth with probing pocket depth (PPD) ≥ 4 mm and ≥ 6 mm. Multilevel linear and Poisson regression analyses were performed after adjusting for possible confounding factors, including SES, assessed by the average income of the residential area.

Results

The mean number of remaining teeth was 24.6 ± 4.8, and the proportion of teeth with PPD ≥ 4 mm and ≥ 6 mm was 31.2 ± 28.5% and 12.2 ± 18.1%, respectively. After adjusting for confounding factors, the lowest-income population had significantly lesser teeth (coefficient: − 0.46, 95% CI − 0.89, 0.02, p = 0.039) and a higher proportion of teeth with PPD ≥ 4 mm than the highest-income population (ratio of means: 1.22, 95% CI 1.03–1.44, p = 0.013). Significant interactions were observed; income inequalities in periodontitis were significant only among current smokers.

Conclusion

Inequality in socio-economic status is associated with oral health inequalities. The adverse effects of smoking on periodontitis might be greater in the low-income population.

Clinical relevance

The low-income population, especially current smokers, had significantly more compromised oral health than the high-income population. In addition to the emphasis on smoking cessation, the promotion of universal health coverage for dental care is necessary to reduce oral health inequalities.

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References

  1. Watt RG, Heilmann A, Listl S, Peres MA (2016) London charter on oral health inequalities. J Dent Res 95:245–247. https://doi.org/10.1177/0022034515622198

    Article  Google Scholar 

  2. Kassebaum NJ, Smith AGC, Bernabe E, Fleming TD, Reynolds AE, Vos T, Murray CJL, Marcenes W, GBD 2015 Oral Health Collaborators (2017) 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 96:380–387. https://doi.org/10.1177/0022034517693566

    Article  Google Scholar 

  3. World Health Organization (2021) 74th world health assembly agenda. https://apps.who.int/gb/ebwha/pdf_files/WHA74/A74_R5-en.pdf. Accessed 10 Oct 2022

  4. Singh A, Peres MA, Watt RG (2019) The relationship between income and oral health: a critical review. J Dent Res 98:853–860. https://doi.org/10.1177/0022034519849557

    Article  Google Scholar 

  5. Petersen PE (2000) Ogawa H (2012) The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontol 60:15–39. https://doi.org/10.1111/j.1600-0757.2011.00425.x

    Article  Google Scholar 

  6. Borrell LN (2000) Crawford ND (2012) Socioeconomic position indicators and periodontitis: examining the evidence. Periodontol 58:69–83. https://doi.org/10.1111/j.1600-0757.2011.00416.x

    Article  Google Scholar 

  7. Thomson WM, Sheiham A, Spencer AJ (2012) Sociobehavioral aspects of periodontal disease. Periodontol 2000(60):54–63. https://doi.org/10.1111/j.1600-0757.2011.00405.x

    Article  Google Scholar 

  8. Buduneli N (2021) Environmental factors and periodontal microbiome. Periodontol 2000(85):112–125. https://doi.org/10.1111/prd.12355

    Article  Google Scholar 

  9. Boillot A, El Halabi B, Batty GD, Rangé H, Czernichow S, Bouchard P (2011) Education as a predictor of chronic periodontitis: a systematic review with meta-analysis population-based studies. PLoS ONE 6:e21508. https://doi.org/10.1371/journal.pone.0021508

    Article  Google Scholar 

  10. Morita I, Nakagaki H, Yoshii S, Tsuboi S, Hayashizaki J, Igo J, Mizuno K, Sheiham A (2007) Gradients in periodontal status in Japanese employed males. J Clin Periodontol 34:952–956. https://doi.org/10.1111/j.1600-051X.2007.01147.x

    Article  Google Scholar 

  11. Sabbah W, Tsakos G, Sheiham A, Watt RG (2009) The role of health-related behaviors in the socioeconomic disparities in oral health. Soc Sci Med 68:298–303. https://doi.org/10.1016/j.socscimed.2008.10.030

    Article  Google Scholar 

  12. Genco RJ, Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 2000(62):59–94. https://doi.org/10.1111/j.1600-0757.2012.00457.x

    Article  Google Scholar 

  13. Sato F, Sawamura M, Ojima M, Tanaka K, Matsuo K (2013) Smoking increases risk of tooth loss: a meta-analysis of the literature. World J Meta-Anal 1(1):16–26. https://doi.org/10.13105/wjma.v1.i1.16

    Article  Google Scholar 

  14. Chaffee BW, Couch ET, Vora MV (2000) Holliday RS (2021) Oral and periodontal implications of tobacco and nicotine products. Periodontol 87:241–253. https://doi.org/10.1111/prd.12395

    Article  Google Scholar 

  15. Hajishengallis G (2000) Lamont RJ (2021) Polymicrobial communities in periodontal disease: Their quasi-organismal nature and dialogue with the host. Periodontol 86:210–230. https://doi.org/10.1111/prd.12371

    Article  Google Scholar 

  16. Souto MLS, Rovai ES, Villar CC, Braga MM, Pannuti CM (2019) Effect of smoking cessation on tooth loss: a systematic review with meta-analysis. BMC Oral Health 19:245. https://doi.org/10.1186/s12903-019-0930-2

    Article  Google Scholar 

  17. Leite FRM, Nascimento GG, Baake S, Pedersen LD, Scheutz F, López R (2019) Impact of smoking cessation on periodontitis: a systematic review and meta-analysis of prospective longitudinal observational and interventional studies. Nicotine Tob Res 21:1600–1608. https://doi.org/10.1093/ntr/nty147

    Article  Google Scholar 

  18. Aida J, Kondo K, Kondo N, Watt RG, Sheiham A, Tsakos G (2011) Income inequality, social capital and self-rated health and dental status in older Japanese. Soc Sci Med 73:1561–1568. https://doi.org/10.1016/j.socscimed.2011.09.005

    Article  Google Scholar 

  19. Nakayama Y, Mizutani K, Tsumanuma Y, Yoshino H, Aoyama N, Inagaki K, Morita M, Izumi Y, Murakami S, Yoshimura H, Matsuura T, Murakami T, Yamamoto M, Yoshinari N, Mezawa M, Ogata Y, Yoshimura A, Kono K, Maruyama K, Sato S, Sakagami R, Ito H, Numabe Y, Nikaido M, Hanioka T, Seto K, Fukuda J, Warnakulasuriya S, Nagao T (2020) A multicenter prospective cohort study on the effect of smoking cessation on periodontal therapies in Japan. J Oral Sci 63:114–118. https://doi.org/10.2334/josnusd.20-0288

    Article  Google Scholar 

  20. Poland B, Frohlich K, Haines RJ, Mykhalovskiy E, Rock M, Sparks R (2006) The social context of smoking: the next frontier in tobacco control? Tob Control 15:59–63. https://doi.org/10.1136/tc.2004.009886

    Article  Google Scholar 

  21. Barbeau EM, Krieger N, Soobader MJ (2004) Working class matters: socioeconomic disadvantage, race/ethnicity, gender, and smoking in NHIS 2000. Am J Public Health 94:269–278. https://doi.org/10.2105/ajph.94.2.269

    Article  Google Scholar 

  22. Hicks TA, Wilson SM, Thomas SP, Dennis PA, Neal JM, Calhoun PS (2018) Low income as a multiplicative risk factor for oral pain and dental problems among U.S. veteran smokers. Int J Behav Med 25:67–73. https://doi.org/10.1007/s12529-017-9660-5

    Article  Google Scholar 

  23. Hong L, Liu Y, Hottel TL, Hoff GL, Cai J (2015) Neighborhood socio-economic context and emergency department visits for dental care in a U.S. Midwestern metropolis. Public Health 129:252–257. https://doi.org/10.1016/j.puhe.2014.11.014

    Article  Google Scholar 

  24. Japanese Ministry of Internal Affairs and Communications (2019) Survey of municipal taxitation status. Retrieved from https://www.soumu.go.jp/main_sosiki/jichi_zeisei/czaisei/czaisei_seido/ichiran09_19.html, in Japanese. Accessed 10 Oct 2022

  25. Fekedulegn D, Andrew M, Violanti J, Hartley T, Charles L, Burchfiel C (2010) Comparison of statistical approaches to evaluate factors associated with metabolic syndrome. J Clin Hypertens (Greenwich) 12:365–373. https://doi.org/10.1111/j.1751-7176.2010.00264.x

    Article  Google Scholar 

  26. Buchwald S, Kocher T, Biffar R, Harb A, Holtfreter B, Meisel P (2013) Tooth loss and periodontitis by socio-economic status and inflammation in a longitudinal population-based study. J Clin Periodontol 40:203–211. https://doi.org/10.1111/jcpe.12056

    Article  Google Scholar 

  27. Schuch HS, Peres KG, Singh A, Peres MA, Do LG (2017) Socioeconomic position during life and periodontitis in adulthood: a systematic review. Community Dent Oral Epidemiol 45:201–208. https://doi.org/10.1111/cdoe.12278

    Article  Google Scholar 

  28. Haas AN, Gaio EJ, Oppermann RV, Rösing CK, Albandar JM, Susin C (2012) Pattern and rate of progression of periodontal attachment loss in an urban population of South Brazil: a 5-years population-based prospective study. J Clin Periodontol 39:1–9. https://doi.org/10.1111/j.1600-051X.2011.01818.x

    Article  Google Scholar 

  29. Poulton R, Caspi A, Milne BJ, Thomson WM, Taylor A, Sears MR, Moffitt TE (2002) Association between children’s experience of socioeconomic disadvantage and adult health: a life-course study. Lancet 360:1640–1645. https://doi.org/10.1016/s0140-6736(02)11602-3

    Article  Google Scholar 

  30. Thomson WM, Shearer DM, Broadbent JM, Foster Page LA, Poulton R (2013) The natural history of periodontal attachment loss during the third and fourth decades of life. J Clin Periodontol 40:672–680. https://doi.org/10.1111/jcpe.12108

    Article  Google Scholar 

  31. Ward E, Jemal A, Cokkinides V, Singh GK, Cardinez C, Ghafoor A, Thun M (2004) Cancer disparities by race/ethnicity and socioeconomic status. CA Cancer J Clin 54:78–93. https://doi.org/10.3322/canjclin.54.2.78

    Article  Google Scholar 

  32. Swan J, Breen N, Coates RJ, Rimer BK, Lee NC (2003) Progress in cancer screening practices in the United States: results from the 2000 National Health Interview Survey. Cancer 97:1528–1540. https://doi.org/10.1002/cncr.11208

    Article  Google Scholar 

  33. Woolfolk MW, Lang WP, Borgnakke WS, Taylor GW, Ronis DL, Nyquist LV (1999) Determining dental checkup frequency. J Am Dent Assoc 130:715–723. https://doi.org/10.14219/jada.archive.1999.0282

    Article  Google Scholar 

  34. Macleod U, Mitchell ED, Burgess C, Macdonald S, Ramirez AJ (2009) Risk factors for delayed presentation and referral of symptomatic cancer: evidence for common cancers. Br J Cancer 101(Suppl 2):S92–S101. https://doi.org/10.1038/sj.bjc.6605398

    Article  Google Scholar 

  35. Saha S, Arbelaez JJ, Cooper LA (2003) Patient-physician relationships and racial disparities in the quality of health care. Am J Public Health 93:1713–1719. https://doi.org/10.2105/ajph.93.10.1713

    Article  Google Scholar 

  36. Tonetti MS, Jepsen S, Jin L, Otomo-Corgel J (2017) Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: a call for global action. J Clin Periodontol 44:456–462. https://doi.org/10.1111/jcpe.12732

    Article  Google Scholar 

  37. Johnson GK (2000) Guthmiller JM (2007) The impact of cigarette smoking on periodontal disease and treatment. Periodontol 44:178–194. https://doi.org/10.1111/j.1600-0757.2007.00212.x

    Article  Google Scholar 

  38. Kapila YL (2000) (2021) 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 87:11–16. https://doi.org/10.1111/prd.12398

    Article  Google Scholar 

  39. Hajishengallis G (2015) Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol 15:30–44. https://doi.org/10.1038/nri3785

    Article  Google Scholar 

  40. Tomar SL, Asma S (2000) Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 71:743–751. https://doi.org/10.1902/jop.2000.71.5.743

    Article  Google Scholar 

  41. Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, Norderyd OM, Genco RJ (1994) Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 65:260–267. https://doi.org/10.1902/jop.1994.65.3.260

    Article  Google Scholar 

  42. Phelan JC, Link BG (2005) Controlling disease and creating disparities: a fundamental cause perspective. J Gerontol B Psychol Sci Soc Sci 60 Spec No 2:27–33. https://doi.org/10.1093/geronb/60.special_issue_2.s27

  43. Moore CJ, Cunningham SA (2012) Social position, psychological stress, and obesity: a systematic review. J Acad Nutr Diet 112:518–526. https://doi.org/10.1016/j.jand.2011.12.001

    Article  Google Scholar 

  44. Edwards M, Davies M, Edwards A (2009) What are the external influences on information exchange and shared decision-making in healthcare consultations: a meta-synthesis of the literature. Patient Educ Couns 75:37–52. https://doi.org/10.1016/j.pec.2008.09.025

    Article  Google Scholar 

  45. Raphael D (2002) Social justice is good for our hearts: why societal factors — not lifestyles — are major causes of heart disease in canada and elsewhere. Toronto: CSJ Foundation for Research and Education. Retrived from https://elevateni.org/app/uploads/2019/09/Social-Justice-is-Good-for-our-Hearts.pdf. Accessed 10 Oct 2022

  46. United Nations (2015) The sustainable development goals. https://www.un.org/sustainabledevelopment/development-agenda/. Accessed 10 Oct 2022

  47. Watt RG, Daly B, Allison P, Macpherson LMD, Venturelli R, Listl S, Weyant RJ, Mathur MR, Guarnizo-Herreño CC, Celeste RK, Peres MA, Kearns C, Benzian H (2019) Ending the neglect of global oral health: time for radical action. Lancet 394:261–272. https://doi.org/10.1016/s0140-6736(19)31133-x

    Article  Google Scholar 

  48. Lee JH, Yi SK, Kim SY, Kim JS, Kim HN, Jeong SH, Kim JB (2019) Factors related to the number of existing teeth among korean adults aged 55–79 years. Int J Environ Res Public Health 16:3927. https://doi.org/10.3390/ijerph16203927

    Article  Google Scholar 

  49. Nakahori N, Sekine M, Yamada M, Tatsuse T, Kido H, Suzuki M (2019) Socioeconomic status and remaining teeth in Japan: results from the Toyama dementia survey. BMC Public Health 19:691. https://doi.org/10.1186/s12889-019-7068-7

    Article  Google Scholar 

  50. Japan Gerontological Evaluation Study (2019) Research on the use of medical services and the effect of accompanying support for medical visits in needy persons. Retrieved from https://www.jages.net/project/konkyu/?action=common_download_main&upload_id=5271, in Japanese. Accessed 10 Oct 10 2022

  51. Nishioka D, Saito J, Ueno K, Kondo N (2021) Single-parenthood and health conditions among children receiving public assistance in Japan: a cohort study. BMC Pediatr 21:214. https://doi.org/10.1186/s12887-021-02682-4

    Article  Google Scholar 

  52. Nishioka D, Ueno K, Kino S, Aida J, Kondo N (2021) Sociodemographic inequities in dental care utilisation among governmental welfare recipients in Japan: a retrospective cohort study. Int J Equity Health 20:141. https://doi.org/10.1186/s12939-021-01473-8

    Article  Google Scholar 

  53. Matsuyama Y, Aida J, Takeuchi K, Tsakos G, Watt RG, Kondo K, Osaka K (2014) Inequalities of dental prosthesis use under universal healthcare insurance. Community Dent Oral Epidemiol 42:122–128. https://doi.org/10.1111/cdoe.12074

    Article  Google Scholar 

  54. Clark PI, Gautam SP, Hlaing WM, Gerson LW (1996) Response error in self-reported current smoking frequency by black and white established smokers. Ann Epidemiol 6:483–489. https://doi.org/10.1016/s1047-2797(96)00049-x

    Article  Google Scholar 

  55. Ozga JE, Bays C, Haliwa I, Felicione NJ, Ferguson SG, Dino G, Blank MD (2022) Measurement of cigarette smoking: comparisons of global self-report, returned cigarette filters, and ecological momentary assessment. Exp Clin Psychopharmacol 30:365–370. https://doi.org/10.1037/pha0000449

    Article  Google Scholar 

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Acknowledgements

The authors thank the staff of the Department of Periodontology of TMDU for their assistance with data collection. This work was supported by a Grant-in-Aid for Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (grant number 20K18497 to RM and 19K10125 to KM).

Funding

This work was supported by a Grant-in-Aid for Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (grant number 20K18497 to RM and 19K10125 to KM).

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Authors and Affiliations

  1. Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo, 113-8549, Japan

    Risako Mikami, Koji Mizutani, Takanori Matsuura, Kohei Takeda, Natsumi Saito, Yuichi Izumi & Takanori Iwata

  2. Department of Periodontology, Kanagawa Dental University, 82 Inaokacho, Yokosuka, Kanagawa, 238-8580, Japan

    Norio Aoyama

  3. Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, UCLA School of Dentistry, Los Angeles, CA, 90095-1668, USA

    Takanori Matsuura

  4. Department of Oral Surgery, Secomedic Hospital, 696-1, Toyotomicho, Funabashi, Chiba, 274-0053, Japan

    Tomonari Suda

  5. Department of Lifetime Oral Health Care Science, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo, 113-8549, Japan

    Shinichi Arakawa

  6. Oral Care and Periodontics Center, Southern Tohoku Research Institute for Neuroscience, Southern Tohoku General Hospital, Yatsuyamada, 7-115, Koriyama, Fukushima, 963-8052, Japan

    Yuichi Izumi

  7. Department of Oral Health Promotion, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo, 113-8549, Japan

    Jun Aida

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  1. Risako Mikami
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  2. Koji Mizutani
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Contributions

RM, KM, SA, YI, TI, and JA developed the concept for this study. NA, TM, TS, KT, and NS provided substantial assistance in the data collection. RM and JA performed the statistical analyses and wrote the initial draft of the manuscript. The authors reviewed the manuscript and approved its final version.

Corresponding author

Correspondence to Koji Mizutani.

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Ethical approval

This study was approved by the Research Ethics Committee of Tokyo Medical and Dental University Dental Hospital (approval number: 1085) and conducted in accordance with the Declaration of Helsinki of 1975, as revised in 2013. This study was registered at the University Hospital Medical Information Network (UMIN: http//www.umin.ac.jp/) (clinical trial number: UMIN000046582).

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Informed consent was obtained from all individual participants included in the study.

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The authors declare no competing interests.

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Mikami, R., Mizutani, K., Aoyama, N. et al. Income-related inequalities in the association of smoking with periodontitis: a cross-sectional analysis in Tokyo Metropolitan Districts. Clin Oral Invest 27, 519–528 (2023). https://doi.org/10.1007/s00784-022-04747-9

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