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Dose–response relationship between cigarette smoking and risk of ulcerative colitis: a nationwide population-based study

Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

Former cigarette smokers are at risk of developing ulcerative colitis (UC). However, the impact of smoking behavior on the occurrence of UC according to the amount smoked remains elusive. We aimed to determine the relationship between smoking behavior and the risk of UC development.

Methods

We conducted a retrospective population-based cohort study using the National Health Insurance Service database in South Korea. From January 2009 to December 2012, 23,235,771 individuals over 18 years of age who underwent a national health examination were enrolled and followed until 2016. All study participants were divided into the following 3 groups: nonsmokers, former smokers, and current smokers. The primary endpoint was newly developed UC.

Results

Compared with nonsmokers, the risk of UC development was significantly higher in former smokers [adjusted hazard ratio (aHR) 1.83; 95% confidence interval (CI) 1.73–1.95] but significantly lower in current smokers (aHR 0.92; 95% CI 0.87–0.98). Among current smokers, individuals who stopped smoking after the baseline evaluation had a significantly higher risk of UC development than those who continued to smoke (aHR 2.42; 95% CI 2.10–2.80). The risk of UC development among former smokers was significantly associated with smoking amount and duration. Among current smokers, however, the risk of UC development was not correlated with the cumulative lifetime smoking exposure. The preventive effect of current smoking on UC development was observed only in men (aHR 0.90; 95% CI 0.84–0.96).

Conclusions

Compared with nonsmokers, former smokers have a significantly higher risk of UC development that may be proportional to the cumulative smoking exposure.

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Abbreviations

aHR:

Adjusted hazard ratio

BMI:

Body mass index

CI:

Confidence interval

DM:

Diabetes mellitus

HR:

Hazard ratio

ICD-10:

International Classification of Disease, Tenth Revision

NHIS:

National Health Insurance Service

NHS I:

Nurses' Health Study I

NHS II:

Nurses' Health Study II

RID:

Rare intractable disease

UC:

Ulcerative colitis

References

  1. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med. 2009;361:2066–78.

    Article  CAS  Google Scholar 

  2. Ng WK, Wong SH, Ng SC. Changing epidemiological trends of inflammatory bowel disease in Asia. Intest Res. 2016;14:111–9.

    Article  Google Scholar 

  3. Zhang YZ, Li YY. Inflammatory bowel disease: pathogenesis. World J Gastroenterol. 2014;20:91–9.

    Article  Google Scholar 

  4. Ananthakrishnan AN. Epidemiology and risk factors for IBD. Nat Rev Gastroenterol Hepatol. 2015;12:205–17.

    Article  Google Scholar 

  5. Harries AD, Baird A, Rhodes J. Non-smoking: a feature of ulcerative colitis. Br Med J (Clin Res Ed). 1982;284:706.

    Article  CAS  Google Scholar 

  6. Calkins BM. A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci. 1989;34:1841–54.

    Article  CAS  Google Scholar 

  7. Higuchi LM, Khalili H, Chan AT, et al. A prospective study of cigarette smoking and the risk of inflammatory bowel disease in women. Am J Gastroenterol. 2012;107:1399–406.

    Article  Google Scholar 

  8. Lakatos PL, Vegh Z, Lovasz BD, et al. Is current smoking still an important environmental factor in inflammatory bowel diseases? Results from a population-based incident cohort. Inflamm Bowel Dis. 2013;19:1010–7.

    Article  Google Scholar 

  9. Mahid SS, Minor KS, Soto RE, et al. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006;81:1462–71.

    Article  Google Scholar 

  10. Srivasta ED, Newcombe RG, Rhodes J, et al. Smoking and ulcerative colitis: a community study. Int J Colorectal Dis. 1993;8:71–4.

    Article  CAS  Google Scholar 

  11. Song SO, Jung CH, Song YD, et al. Background and data configuration process of a nationwide population-based study using the Korean national health insurance system. Diabetes Metab J. 2014;38:395–403.

    Article  Google Scholar 

  12. Yun WJ, Shin MH, Kweon SS, et al. Association of smoking status, cumulative smoking, duration of smoking cessation, age of starting smoking, and depression in Korean adults. BMC Public Health. 2012;12:724.

    Article  Google Scholar 

  13. Kulak JA, LaValley S. Cigarette use and smoking beliefs among older Americans: findings from a nationally representative survey. J Addict Dis. 2018;1–9. https://doi.org/10.1080/10550887.2018.1521255

    Article  Google Scholar 

  14. Choi YJ, Lee DH, Han KD, et al. The relationship between drinking alcohol and esophageal, gastric or colorectal cancer: a nationwide population-based cohort study of South Korea. PLoS One. 2017;12:e0185778.

    Article  Google Scholar 

  15. Kim HJ, Hann HJ, Hong SN, et al. Incidence and natural course of inflammatory bowel disease in Korea, 2006–2012: a nationwide population-based study. Inflamm Bowel Dis. 2015;21:623–30.

    Article  Google Scholar 

  16. Park S, Chun J, Han K, et al. Increased end-stage renal disease risk in patients with inflammatory bowel disease: a nationwide population-based study. World J Gastroenterol. 2018;24:4798–808.

    Article  Google Scholar 

  17. Abraham N, Selby W, Lazarus R, et al. Is smoking an indirect risk factor for the development of ulcerative colitis? An age- and sex-matched case–control study. J Gastroenterol Hepatol. 2003;18:139–46.

    Article  Google Scholar 

  18. Franceschi S, Panza E, La Vecchia C, et al. Nonspecific inflammatory bowel disease and smoking. Am J Epidemiol. 1987;125:445–52.

    Article  CAS  Google Scholar 

  19. Corrao G, Tragnone A, Caprilli R, et al. Risk of inflammatory bowel disease attributable to smoking, oral contraception and breastfeeding in Italy: a nationwide case–control study. Cooperative Investigators of the Italian Group for the Study of the Colon and the Rectum (GISC). Int J Epidemiol. 1998;27:397–404.

    Article  CAS  Google Scholar 

  20. Boyko EJ, Koepsell TD, Perera DR, et al. Risk of ulcerative colitis among former and current cigarette smokers. N Engl J Med. 1987;316:707–10.

    Article  CAS  Google Scholar 

  21. Takahashi H, Matsui T, Hisabe T, et al. Second peak in the distribution of age at onset of ulcerative colitis in relation to smoking cessation. J Gastroenterol Hepatol. 2014;29:1603–8.

    Article  Google Scholar 

  22. Lindberg E, Tysk C, Andersson K, et al. Smoking and inflammatory bowel disease. A case control study. Gut. 1988;29:352–7.

    Article  CAS  Google Scholar 

  23. Ng SC, Tang W, Leong RW, et al. Environmental risk factors in inflammatory bowel disease: a population-based case–control study in Asia–Pacific. Gut. 2015;64:1063–71.

    Article  Google Scholar 

  24. Persson PG, Ahlbom A, Hellers G. Inflammatory bowel disease and tobacco smoke—a case–control study. Gut. 1990;31:1377–81.

    Article  CAS  Google Scholar 

  25. Sandler RS, Sandler DP, McDonnell CW, et al. Childhood exposure to environmental tobacco smoke and the risk of ulcerative colitis. Am J Epidemiol. 1992;135:603–8.

    Article  CAS  Google Scholar 

  26. Cosnes J, Nion-Larmurier I, Afchain P, et al. Gender differences in the response of colitis to smoking. Clin Gastroenterol Hepatol. 2004;2:41–8.

    Article  Google Scholar 

  27. Hayashi S, Hamada T, Zaidi SF, et al. Nicotine suppresses acute colitis and colonic tumorigenesis associated with chronic colitis in mice. Am J Physiol Gastrointest Liver Physiol. 2014;307:G968–G978978.

    Article  CAS  Google Scholar 

  28. Lakhan SE, Kirchgessner A. Anti-inflammatory effects of nicotine in obesity and ulcerative colitis. J Transl Med. 2011;9:129.

    Article  CAS  Google Scholar 

  29. McGilligan VE, Wallace JM, Heavey PM, et al. Hypothesis about mechanisms through which nicotine might exert its effect on the interdependence of inflammation and gut barrier function in ulcerative colitis. Inflamm Bowel Dis. 2007;13:108–15.

    Article  Google Scholar 

  30. Talhout R, Schulz T, Florek E, et al. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health. 2011;8:613–28.

    Article  Google Scholar 

  31. Capurso G, Lahner E. The interaction between smoking, alcohol and the gut microbiome. Best Pract Res Clin Gastroenterol. 2017;31:579–88.

    Article  CAS  Google Scholar 

  32. Nemoto H, Kataoka K, Ishikawa H, et al. Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig Dis Sci. 2012;57:2955–64.

    Article  Google Scholar 

  33. Lepage P, Hasler R, Spehlmann ME, et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology. 2011;141:227–36.

    Article  Google Scholar 

  34. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146:1489–99.

    Article  CAS  Google Scholar 

  35. Biedermann L, Zeitz J, Mwinyi J, et al. Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS One. 2013;8:e59260.

    Article  CAS  Google Scholar 

  36. Koliada A, Syzenko G, Moseiko V, et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17:120.

    Article  Google Scholar 

  37. Hsieh CC, Signorello LB, Lipworth L, et al. Predictors of sex hormone levels among the elderly: a study in Greece. J Clin Epidemiol. 1998;51:837–41.

    Article  CAS  Google Scholar 

  38. Klil-Drori AJ, Tascilar K, Yin H, et al. Androgen deprivation therapy and the incidence of inflammatory bowel disease in patients with prostate cancer. Am J Epidemiol. 2016;184:15–22.

    Article  Google Scholar 

  39. Khalili H, Ananthakrishnan AN, Konijeti GG, et al. Endogenous levels of circulating androgens and risk of Crohn's disease and ulcerative colitis among women: a nested case–control study from the nurses' health study cohorts. Inflamm Bowel Dis. 2015;21:1378–85.

    Article  Google Scholar 

  40. Khalili H, Higuchi LM, Ananthakrishnan AN, et al. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut. 2013;62:1153–9.

    Article  CAS  Google Scholar 

  41. Bolego C, Poli A, Paoletti R. Smoking and gender. Cardiovasc Res. 2002;53:568–76.

    Article  CAS  Google Scholar 

  42. Sheikh SZ, Hegazi RA, Kobayashi T, et al. An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol. 2011;186:5506–13.

    Article  CAS  Google Scholar 

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Authors and Affiliations

Authors

Contributions

SP, JC, and KDH: research conception and design; SP, KDH, HS, and EAK: data acquisition; SP, JC, and KDH: data analysis and interpretation; KDH: statistical analysis; SP and JC: manuscript drafting; HJL, JPI, and JSK: critical revision of the manuscript; all authors: approval of the final manuscript.

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Correspondence to Jaeyoung Chun.

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535_2019_1589_MOESM1_ESM.docx

Supplementary Fig. 1 Cumulative incidence of ulcerative colitis according to (a) smoking status at baseline and (b) changes in smoking status among current smokers at baseline. UC, ulcerative colitis (DOCX 14 kb)

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Park, S., Chun, J., Han, KD. et al. Dose–response relationship between cigarette smoking and risk of ulcerative colitis: a nationwide population-based study. J Gastroenterol 54, 881–890 (2019). https://doi.org/10.1007/s00535-019-01589-3

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  • DOI: https://doi.org/10.1007/s00535-019-01589-3

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