DOI QR코드

DOI QR Code

The Association Between Metabolic Syndrome and Colorectal Cancer Risk by Obesity Status in Korean Women: A Nationwide Cohort Study

  • Moon, Seong-geun (Department of Preventive Medicine, Hanyang University College of Medicine) ;
  • Park, Boyoung (Department of Preventive Medicine, Hanyang University College of Medicine)
  • Received : 2022.06.24
  • Accepted : 2022.08.23
  • Published : 2022.09.30

Abstract

Objectives: This study aimed to determine the association between metabolic syndrome (MetS) and the incidence of colorectal cancer (CRC) in Korean women with obesity. Methods: Cancer-free women (n=6 142 486) aged 40-79 years, who underwent National Health Insurance Service health examinations in 2009 and 2010 were included. The incidence of CRC was followed until 2018. The hazard ratio (HR) of MetS for the incidence of colon and rectal cancer was analyzed according to body mass index (BMI) categories, adjusting for confounders such as women's reproductive factors. In addition, the heterogeneity of associations across BMI categories was assessed. Results: Women with MetS were at increased risk of colon and rectal cancer compared to women without MetS (HR, 1.20; 95% confidence interval [CI], 1.16 to 1.23 and HR,1.15; 95% CI, 1.11 to 1.20), respectively. The HR of MetS for colon cancer across BMI categories was 1.12 (95% CI, 1.06 to 1.19), 1.14 (95% CI, 1.08 to 1.20), and 1.16 (95% CI, 1.12 to 1.21) in women with BMIs <23.0 kg/m2, 23.0-24.9 kg/m2, and ≥25.0 kg/m2, respectively. The HR of MetS for rectal cancer across corresponding BMI categories was 1.16 (95% CI, 1.06 to 1.26), 1.14 (95% CI, 1.05 to 1.23), and 1.13 (95% CI, 1.06 to 1.20). The heterogeneity of associations across BMI categories was not significant in either colon or rectal cancer (p=0.587 for colon cancer and p=0.927 for rectal cancer). Conclusions: Women with MetS were at increased risk of colon and rectal cancer. Clinical and public health strategies should be considered for primary CRC prevention with an emphasis on improving women's metabolic health across all BMI groups.

Keywords

Acknowledgement

This work was supported by a National Research Foundation of Korea grant funded by the Korean government's Ministry of Science and Information and Communication Technologies (grant No. 2021R1A2C1011958).

References

  1. Bellastella G, Scappaticcio L, Esposito K, Giugliano D, Maiorino MI. Metabolic syndrome and cancer: "the common soil hypothesis". Diabetes Res Clin Pract 2018;143:389-397. https://doi.org/10.1016/j.diabres.2018.05.024
  2. Bluher M. Metabolically healthy obesity. Endocr Rev 2020;41(3):bnaa004. https://doi.org/10.1210/endrev/bnaa004
  3. Smith GI, Mittendorfer B, Klein S. Metabolically healthy obesity: facts and fantasies. J Clin Invest 2019;129(10):3978-3989. https://doi.org/10.1172/JCI129186
  4. GBD 2019 Colorectal Cancer Collaborators. Global, regional, and national burden of colorectal cancer and its risk factors, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Gastroenterol Hepatol 2022;7(7):627-647. https://doi.org/10.1016/S2468-1253(22)00044-9
  5. Shen X, Wang Y, Zhao R, Wan Q, Wu Y, Zhao L, et al. Metabolic syndrome and the risk of colorectal cancer: a systematic review and meta-analysis. Int J Colorectal Dis 2021;36(10):2215-2225. https://doi.org/10.1007/s00384-021-03974-y
  6. Ma Y, Yang Y, Wang F, Zhang P, Shi C, Zou Y, et al. Obesity and risk of colorectal cancer: a systematic review of prospective studies. PLoS One 2013;8(1):e53916. https://doi.org/10.1371/journal.pone.0053916
  7. Goodarzi G, Mozaffari H, Raeisi T, Mehravar F, Razi B, Ghazi ML, et al. Metabolic phenotypes and risk of colorectal cancer: a systematic review and meta-analysis of cohort studies. BMC Cancer 2022;22(1):89. https://doi.org/10.1186/s12885-021-09149-w
  8. Choi YJ, Lee DH, Han KD, Shin CM, Kim N. Abdominal obesity, glucose intolerance and decreased high-density lipoprotein cholesterol as components of the metabolic syndrome are associated with the development of colorectal cancer. Eur J Epidemiol 2018;33(11):1077-1085. https://doi.org/10.1007/s10654-018-0440-6
  9. Tran TT, Gunathilake M, Lee J, Kim J. Association between metabolic syndrome and its components and incident colorectal cancer in a prospective cohort study. Cancer 2022;128(6):1230-1241. https://doi.org/10.1002/cncr.34027
  10. Jin EH, Han K, Lee DH, Shin CM, Lim JH, Choi YJ, et al. Association between metabolic syndrome and the risk of colorectal cancer diagnosed before age 50 years according to tumor location. Gastroenterology 2022;163(3):637-648.e2. https://doi.org/10.1053/j.gastro.2022.05.032
  11. Ko S, Yoon SJ, Kim D, Kim AR, Kim EJ, Seo HY. Metabolic risk profile and cancer in Korean men and women. J Prev Med Public Health 2016;49(3):143-152. https://doi.org/10.3961/jpmph.16.021
  12. Fuhrman BJ, Moore SC, Byrne C, Makhoul I, Kitahara CM, Berrington de Gonzalez A, et al. Association of the age at menarche with site-specific cancer risks in pooled data from nine cohorts. Cancer Res 2021;81(8):2246-2255. https://doi.org/10.1158/0008-5472.CAN-19-3093
  13. Lin KJ, Cheung WY, Lai JY, Giovannucci EL. The effect of estrogen vs. combined estrogen-progestogen therapy on the risk of colorectal cancer. Int J Cancer 2012;130(2):419-430. https://doi.org/10.1002/ijc.26026
  14. Bosetti C, Bravi F, Negri E, La Vecchia C. Oral contraceptives and colorectal cancer risk: a systematic review and meta-analysis. Hum Reprod Update 2009;15(5):489-498. https://doi.org/10.1093/humupd/dmp017
  15. Lee J, Lee JS, Park SH, Shin SA, Kim K. Cohort profile: the National Health Insurance Service-National Sample Cohort (NHIS-NSC), South Korea. Int J Epidemiol 2017;46(2):e15.
  16. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome. An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Executive summary. Cardiol Rev 2005;13(6):322-327. https://doi.org/10.1097/01.crd.0000380842.14048.7e
  17. World Health Organization Regional Office for the Western Pacific. The Asia-Pacific perspective: redefining obesity and its treatment; 2000 [cited 2022 May 27]. Available from: https://apps.who.int/iris/handle/10665/206936.
  18. National Health Insurance Service. 2022 National Health Insurance & long-term care insurance system in Republic of Korea [cited 2022 Aug 9]. Available from: https://www.nhis.or.kr/ english/wbheaa03500m01.do?mode=view&articleNo=10814171&article.offset=0&articleLimit=10.
  19. Yang MS, Park M, Back JH, Lee GH, Shin JH, Kim K, et al. Validation of cancer diagnosis based on the National Health Insurance Service Database versus the National Cancer Registry Database in Korea. Cancer Res Treat 2022;54(2):352-361. https://doi.org/10.4143/crt.2021.044
  20. Bouras E, Papandreou C, Tzoulaki I, Tsilidis KK. Endogenous sex steroid hormones and colorectal cancer risk: a systematic review and meta-analysis. Discov Oncol 2021;12(1):8. https://doi.org/10.1007/s12672-021-00402-z
  21. Morch LS, Lidegaard O, Keiding N, Lokkegaard E, Kjaer SK. The influence of hormone therapies on colon and rectal cancer. Eur J Epidemiol 2016;31(5):481-489. https://doi.org/10.1007/s10654-016-0116-z
  22. Iacopetta B. Are there two sides to colorectal cancer? Int J Cancer 2002;101(5):403-408. https://doi.org/10.1002/ijc.10635
  23. van der Sijp MP, Bastiaannet E, Mesker WE, van der Geest LG, Breugom AJ, Steup WH, et al. Differences between colon and rectal cancer in complications, short-term survival and recurrences. Int J Colorectal Dis 2016;31(10):1683-1691. https://doi.org/10.1007/s00384-016-2633-3
  24. de Kort S, Simons CC, van den Brandt PA, Goldbohm RA, Arts IC, de Bruine AP, et al. Diabetes mellitus type 2 and subsitespecific colorectal cancer risk in men and women: results from the Netherlands Cohort Study on diet and cancer. Eur J Gastroenterol Hepatol 2016;28(8):896-903. https://doi.org/10.1097/MEG.0000000000000626
  25. Murphy G, Devesa SS, Cross AJ, Inskip PD, McGlynn KA, Cook MB. Sex disparities in colorectal cancer incidence by anatomic subsite, race and age. Int J Cancer 2011;128(7):1668-1675. https://doi.org/10.1002/ijc.25481
  26. Bufill JA. Colorectal cancer: evidence for distinct genetic categories based on proximal or distal tumor location. Ann Intern Med 1990;113(10):779-788. https://doi.org/10.7326/0003-4819-113-10-779
  27. Shin A, Joo J, Bak J, Yang HR, Kim J, Park S, et al. Site-specific risk factors for colorectal cancer in a Korean population. PLoS One 2011;6(8):e23196. https://doi.org/10.1371/journal.pone.0023196
  28. Tian Y, Wang K, Li J, Wang J, Wang Z, Fan Y, et al. The association between serum lipids and colorectal neoplasm: a systemic review and meta-analysis. Public Health Nutr 2015;18(18):3355-3370. https://doi.org/10.1017/S1368980015000646
  29. Yang Z, Tang H, Lu S, Sun X, Rao B. Relationship between serum lipid level and colorectal cancer: a systemic review and meta-analysis. BMJ Open 2022;12(6):e052373. https://doi.org/10.1136/bmjopen-2021-052373
  30. O'Neill S, O'Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev 2015;16(1):1-12. https://doi.org/10.1111/obr.12229
  31. Murphy N, Carreras-Torres R, Song M, Chan AT, Martin RM, Papadimitriou N, et al. Circulating levels of insulin-like growth factor 1 and insulin-like growth factor binding protein 3 associate with risk of colorectal cancer based on serologic and mendelian randomization analyses. Gastroenterology 2020;158(5):1300-1312.e20. https://doi.org/10.1053/j.gastro.2019.12.020
  32. Cho YK, Lee J, Kim HS, Park JY, Lee WJ, Kim YJ, et al. Metabolic health is a determining factor for incident colorectal cancer in the obese population: a nationwide population-based cohort study. Cancer Med 2021;10(1):220-229. https://doi.org/10.1002/cam4.3607
  33. Farvid MS, Sidahmed E, Spence ND, Mante Angua K, Rosner BA, Barnett JB. Consumption of red meat and processed meat and cancer incidence: a systematic review and meta-analysis of prospective studies. Eur J Epidemiol 2021;36(9):937-951. https://doi.org/10.1007/s10654-021-00741-9
  34. Seong SC, Kim YY, Khang YH, Park JH, Kang HJ, Lee H, et al. Data resource profile: the National Health Information Database of the National Health Insurance Service in South Korea. Int J Epidemiol 2017;46(3):799-800.