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Epidemiology

Lifestyle, body mass index, diabetes, and the risk of pancreatic cancer in a nationwide population-based cohort study with 7.4 million Korean subjects

British Journal of Cancer volume 127, pages 549–557 (2022)Cite this article

Subjects

Abstract

Background

Large-scale epidemiological studies on pancreatic cancer in non-Western populations are insufficient. We investigated the risk factors for pancreatic cancer.

Methods

Using the Korean National Health Insurance database, subjects who participated in the health examination program between 2005 and 2006 were identified and followed up until 2017. Adjusted hazard ratios (HRs) for pancreatic cancer risk were estimated using a Cox proportional hazards model.

Results

During 11.5 years follow-up, 22,543 of 7,445,947 participants were newly diagnosed with pancreatic cancer. Compared with normal-weight subjects, pancreatic cancer risk was increased in those with severe obesity (BMI ≥ 28 kg/m2) (HR = 1.16; 95% CI, 1.11–1.23). Subjects with diabetes had an increased risk compared with those without diabetes (HR = 1.48; 95% CI, 1.43–1.53). Current smokers had a higher risk than never smokers (HR = 1.43; 95% CI, 1.38–1.48). Current smoking combined with diabetes increased the risk compared with never smokers without diabetes (HR = 2.13; 95% CI, 2.00–2.28). Current smoking combined with BMI ≥ 25 kg/m2 had an increased risk compared with never smokers with BMI < 23 kg/m2 (HR = 1.55; 95% CI, 1.46–1.65).

Conclusion

Smoking, obesity, and diabetes are significant risk factors for pancreatic cancer in Koreans. Lifestyle modifications for smoking and obesity would be beneficial for pancreatic cancer prevention.

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Fig. 1: Flow chart of the study population.
Fig. 2: Adjusted HRs for pancreatic cancer by BMI, smoking status, and diabetes.
Fig. 3: Adjusted HRs for pancreatic cancer showing the combined effects of risk factors for pancreatic cancer.

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Data availability

This study’s data are available from the corresponding author, upon reasonable request.

References

  1. Are C, Chowdhury S, Ahmad H, Ravipati A, Song T, Shrikandhe S, et al. Predictive global trends in the incidence and mortality of pancreatic cancer based on geographic location, socio-economic status, and demographic shift. J Surg Oncol. 2016;114:736–42.

    Article  PubMed  Google Scholar 

  2. Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371:1039–49.

    Article  CAS  PubMed  Google Scholar 

  3. Midha S, Chawla S, Garg PK. Modifiable and non-modifiable risk factors for pancreatic cancer: a review. Cancer Lett. 2016;381:269–77.

    Article  CAS  PubMed  Google Scholar 

  4. Mizrahi JD, Surana R, Valle JW, Shroff RT. Pancreatic cancer. Lancet. 2020;395:2008–20.

    Article  CAS  PubMed  Google Scholar 

  5. Iodice S, Gandini S, Maisonneuve P, Lowenfels AB. Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg. 2008;393:535–45.

    Article  PubMed  Google Scholar 

  6. Maisonneuve P, Lowenfels AB. Risk factors for pancreatic cancer: a summary review of meta-analysis studies. Int J Epidemiol. 2015;44:186–98.

    Article  PubMed  Google Scholar 

  7. Wang Y, Gou Y, Jin W, Xiao M, Fang H. Association between alcohol intake and the risk of pancreatic cancer: a dose-response meta-analysis of cohort studies. BMC Cancer. 2016;16:212.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Tramacere I, Scotti L, Jenab M, Bagnardi V, Bellocco R, Rota M, et al. Alcohol drinking and pancreatic cancer risk: a meta-analysis of the dose-risk relation. Int J Cancer. 2010;126:1474–86.

    CAS  PubMed  Google Scholar 

  9. Andersen DK, Korc M, Petersen GM, Eibl G, Li D, Rickels MR, et al. Diabetes, pancreatogenic diabetes, and pancreatic cancer. Diabetes. 2017;66:1103–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Sharma A, Chari ST. Pancreatic cancer and diabetes mellitus. Curr Treat Options Gastroenterol. 2018;16:466–78.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Koyanagi YN, Matsuo K, Ito H, Tamakoshi A, Sugawara Y, Hidaka A, et al. Body-mass index and pancreatic cancer incidence: a pooled analysis of nine population-based cohort studies with more than 340,000 Japanese subjects. J Epidemiol. 2018;28:245–52.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rawla P, Thandra KC, Sunkara T. Pancreatic cancer and obesity: epidemiology, mechanism, and preventive strategies. Clin J Gastroenterol. 2019;12:285–91.

    Article  PubMed  Google Scholar 

  13. Zhou B, Wu D, Liu H, Du LT, Wang YS, Xu JW, et al. Obesity and pancreatic cancer: an update of epidemiological evidence and molecular mechanisms. Pancreatology. 2019;19:941–50.

    Article  CAS  PubMed  Google Scholar 

  14. Larsson SC, Orsini N, Wolk A. Body mass index and pancreatic cancer risk: a meta-analysis of prospective studies. Int J Cancer. 2007;120:1993–8.

    Article  CAS  PubMed  Google Scholar 

  15. Parr CL, Batty GD, Lam TH, Barzi F, Fang X, Ho SC, et al. Body-mass index and cancer mortality in the Asia-Pacific Cohort Studies Collaboration: pooled analyses of 424,519 participants. Lancet Oncol. 2010;11:741–52.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lin Y, Fu R, Grant E, Chen Y, Lee JE, Gupta PC, et al. Association of body mass index and risk of death from pancreas cancer in Asians: findings from the Asia Cohort Consortium. Eur J Cancer Prev. 2013;22:244–50.

    Article  PubMed  Google Scholar 

  17. Song SO, Jung CH, Song YD, Park CY, Kwon HS, Cha BS, 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  PubMed  PubMed Central  Google Scholar 

  18. Seong SC, Kim Y, Park SK, Khang YH, Kim HC, Park JH, et al. Cohort profile: the National Health Insurance Service-National Health Screening Cohort (NHIS-HEALS) in Korea. BMJ Open. 2017;7:e016640.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Chun HS. Policy tasks for improving the health examination rate. The National Assembly of the Republic of Korea. 2008.

  20. WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:57–63.

    Google Scholar 

  21. Greenland S. Concepts and pitfalls in measuring and interpreting attributable fractions, prevented fractions, and causation probabilities. Ann Epidemiol. 2015;25:155–61.

    Article  PubMed  Google Scholar 

  22. Untawale S, Odegaard AO, Koh W, Jin AZ, Yuan J, Anderson KE. Body mass index and risk of pancreatic cancer in a Chinese population. PLoS One. 2014;9:e85149.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Wang J, Yang D, Chen Z, Gou B. Associations of body mass index with cancer incidence among populations, genders, and menopausal status: a systematic review and meta-analysis. Cancer Epidemiol. 2016;42:1–8.

    Article  PubMed  Google Scholar 

  24. Kim DM, Ahn CW, Nam SY. Prevalence of obesity in Korea. Obes Rev. 2005;6:117–1121.

    Article  CAS  PubMed  Google Scholar 

  25. Liao K, Lai S, Li C, Chen W. Diabetes mellitus correlates with increased risk of pancreatic cancer: a population‐based cohort study in Taiwan. J Gastroenterol Hepatol. 2012;27:709–13.

    Article  PubMed  Google Scholar 

  26. Bosetti C, Rosato V, Li D, Silverman D, Petersen GM, Bracci PM, et al. Diabetes, antidiabetic medications, and pancreatic cancer risk: an analysis from the International Pancreatic Cancer Case-Control Consortium. Ann Oncol. 2014;25:2065–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Aggarwal G, Kamada P, Chari ST. Prevalence of diabetes mellitus in pancreatic cancer compared to common cancers. Pancreas. 2013;42:198–201.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Sah RP, Nagpal SJS, Mukhopadhyay D, Chari ST. New insights into pancreatic cancer-induced paraneoplastic diabetes. Nat Rev Gastroenterol Hepatol. 2013;10:423–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lugo A, Peveri G, Bosetti C, Bagnardi V, Crippa A, Orsini N, et al. Strong excess risk of pancreatic cancer for low frequency and duration of cigarette smoking: a comprehensive review and meta-analysis. Eur J Cancer. 2018;104:117–26.

    Article  PubMed  Google Scholar 

  30. Lynch SM, Vrieling A, Lubin JH, Kraft P, Mendelsohn JB, Hartge P, et al. Cigarette smoking and pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Am J Epidemiol. 2009;170:403–13.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gandini S, Botteri E, Iodice S, Boniol M, Lowenfels AB, Maisonneuve P, et al. Tobacco smoking and cancer: a meta-analysis. Int J Cancer. 2008;122:155–64.

    Article  CAS  PubMed  Google Scholar 

  32. van Osch FH, Jochems SH, van Schooten FJ, Bryan RT, Zeegers MP. Quantified relations between exposure to tobacco smoking and bladder cancer risk: a meta-analysis of 89 observational studies. Int J Epidemiol. 2016;45:857–70.

    Article  PubMed  Google Scholar 

  33. Huang Y, You L, Xie W, Ning L, Lang J. Smoking and risk of cholangiocarcinoma: a systematic review and meta-analysis. Oncotarget. 2017;8:100570–81.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Paek HJ, Dewhirst T, Hove T. Can removing tar information from cigarette packages reduce smokers’ misconceptions about low-tar cigarettes? An experiment from one of the world’s lowest tar yield markets, South Korea. Nicotine Tob Res. 2020;22:990–6.

    Article  PubMed  Google Scholar 

  35. Lee PN. Tar level of cigarettes smoked and risk of smoking-related diseases. Inhal Toxicol. 2018;30:5–13.

    Article  CAS  PubMed  Google Scholar 

  36. Benowitz NL, Pérez-Stable EJ, Herrera B, Jacob P 3rd. Slower metabolism and reduced intake of nicotine from cigarette smoking in Chinese-Americans. J Natl Cancer Inst. 2002;94:108–15.

    Article  PubMed  Google Scholar 

  37. Zou L, Zhong R, Shen N, Chen W, Zhu B, Ke J, et al. Non-linear dose-response relationship between cigarette smoking and pancreatic cancer risk: evidence from a meta-analysis of 42 observational studies. Eur J Cancer. 2014;50:193–203.

    Article  CAS  PubMed  Google Scholar 

  38. Koyanagi YN, Ito H, Matsuo K, Sugawara Y, Hidaka A, Sawada N, et al. Smoking and pancreatic cancer incidence: a pooled analysis of 10 population-based cohort studies in Japan. Cancer Epidemiol Biomark Prev. 2019;28:1370–8.

    Article  Google Scholar 

  39. Ansary-Moghaddam A, Huxley R, Barzi F, Lawes C, Ohkubo T, Fang X, et al. The effect of modifiable risk factors on pancreatic cancer mortality in populations of the Asia-Pacific region. Cancer Epidemiol Biomark Prev. 2006;15:2435–40.

    Article  Google Scholar 

  40. Bosetti C, Lucenteforte E, Silverman DT, Petersen G, Bracci PM, Ji BT, et al. Cigarette smoking and pancreatic cancer: an analysis from the International Pancreatic Cancer Case-Control Consortium (Panc4). Ann Oncol. 2012;23:1880–8.

    Article  CAS  PubMed  Google Scholar 

  41. Hassan MM, Bondy ML, Wolff RA, Abbruzzese JL, Vauthey JN, Pisters PW, et al. Risk factors for pancreatic cancer: case-control study. Am J Gastroenterol. 2007;102:2696–707.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Heinen MM, Verhage BAJ, Goldbohm RA, Lumey LH, van den Brandt PA. Physical activity, energy restriction, and the risk of pancreatic cancer: a prospective study in the Netherlands. Am J Clin Nutr. 2011;94:1314–23.

    Article  CAS  PubMed  Google Scholar 

  43. Brenner DR, Wozniak MB, Feyt C, Holcatova I, Janout V, Foretova L, et al. Physical activity and risk of pancreatic cancer in a central European multicenter case-control study. Cancer Causes Control. 2014;25:669–81.

    Article  PubMed  Google Scholar 

  44. Inoue M, Iso H, Yamamoto S, Kurahashi N, Iwasaki M, Sasazuki S, et al. Daily total physical activity level and premature death in men and women: results from a large-scale population-based cohort study in Japan (JPHC study). Ann Epidemiol. 2008;18:522–30.

    Article  PubMed  Google Scholar 

  45. Behrens G, Jochem C, Schmid D, Keimling M, Ricci C, Leitzmann MF. Physical activity and risk of pancreatic cancer: a systematic review and meta-analysis. Eur J Epidemiol. 2015;30:279–98.

    Article  PubMed  Google Scholar 

  46. Maisonneuve P. Epidemiology and burden of pancreatic cancer. Presse Med. 2019;48:e113–e123.

    Article  PubMed  Google Scholar 

  47. Islami F, Goding Sauer A, Miller KD, Siegel RL, Fedewa SA, Jacobs EJ, et al. Proportion and number of cancer cases and deaths attributable to potentially modifiable risk factors in the United States. CA Cancer J Clin. 2018;68:31–54.

    Article  PubMed  Google Scholar 

  48. Brown KF, Rumgay H, Dunlop C, Ryan M, Quartly F, Cox A, et al. The fraction of cancer attributable to modifiable risk factors in England, Wales, Scotland, Northern Ireland, and the United Kingdom in 2015. Br J Cancer. 2018;118:1130–41.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Park S, Kim Y, Shin HR, Lee B, Shin A, Jung KW, et al. Population-attributable causes of cancer in Korea: obesity and physical inactivity. PLoS One. 2014;9:e90871.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Lin Y, Kikuchi S, Tamakoshi A, Yagyu K, Obata Y, Inaba I, et al. Obesity, physical activity and the risk of pancreatic cancer in a large Japanese cohort. Int J Cancer. 2007;120:2665–71.

    Article  CAS  PubMed  Google Scholar 

  51. Larsson SC, Permert J, Håkansson N, Näslund I, Bergkvist L, Wolk A. Overall obesity, abdominal adiposity, diabetes and cigarette smoking in relation to the risk of pancreatic cancer in two Swedish population-based cohorts. Br J Cancer. 2005;93:1310–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Naudin S, Viallon V, Hashim D, Freisling H, Jenab M, Weiderpass E, et al. Healthy lifestyle and the risk of pancreatic cancer in the EPIC study. Eur J Epidemiol. 2020;35:975–86.

    Article  PubMed  Google Scholar 

  53. La Torre G, Sferrazza A, Gualano MR, de Waure C, Clemente G, De Rose AM, et al. Investigating the synergistic interaction of diabetes, tobacco smoking, alcohol consumption, and hypercholesterolemia on the risk of pancreatic cancer: a case-control study in Italy. Biomed Res Int. 2014;2014:481019.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Jiao L, de Gonzalez AB, Hartge P, Pfeiffer RM, Park Y, Freedman DM, et al. Body mass index, effect modifiers, and risk of pancreatic cancer: a pooled study of seven prospective cohorts. Cancer Causes Control. 2010;21:1305–14.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Luijckx E, Lohse T, Faeh D, Rohrmann S. Joints effects of BMI and smoking on mortality of all-causes, CVD, and cancer. Cancer Causes Control. 2019;30:549–57.

    Article  PubMed  Google Scholar 

  56. Korea Central Cancer Registry, National Cancer Center. Annual report of cancer statistics in Korea in 2018, Ministry of Health and Welfare, 2020.

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Acknowledgements

This study used the NHIS 2002–2017 database (NHIS 2021-1-242), made by the National Health Insurance Service. The authors alone are responsible for the content and writing of the paper.

Funding

This work was supported by the National Health Insurance Ilsan Hospital grant (NHIMC 2019-20-005).

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Authors and Affiliations

  1. Division of Gastroenterology, Department of Internal Medicine, National Health Insurance Service Ilsan Hospital, Goyang, Republic of Korea

    Byung Kyu Park, Jeong Hun Seo & Jae Bock Chung

  2. Department of Policy Research Affairs, National Health Insurance Service Ilsan Hospital, Goyang, Republic of Korea

    Jung Kyu Choi

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Contributions

BKP and JHS designed the paper and performed the interpretation. BKP wrote the manuscript. JBC supervised the development of the work and helped in data interpretation and manuscript evaluation. JKC performed the statistical analysis. All authors read and approved the manuscript and agree to be accountable for all aspects of the research in ensuring that the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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Correspondence to Jeong Hun Seo.

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The authors declare no competing interests.

Ethics approval and consent to participate

This study was approved by the Institutional Review Board of the National Health Insurance Service Ilsan Hospital (NHIMC 2020-11-016). Informed consent was waived by the board because anonymous raw data were obtained from the National Health Insurance Service of Korea. The study was done in accordance with the Declaration of Helsinki.

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Park, B.K., Seo, J.H., Chung, J.B. et al. Lifestyle, body mass index, diabetes, and the risk of pancreatic cancer in a nationwide population-based cohort study with 7.4 million Korean subjects. Br J Cancer 127, 549–557 (2022). https://doi.org/10.1038/s41416-022-01807-5

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