Ewha Med J.  2024 Apr;47(2):e19. 10.12771/emj.2024.e19.

Effect of body mass index on gastric cancer risk according to sex in Korea: a nationwide cohort study and literature review

Affiliations
  • 1Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea
  • 2Division of Clinical Research, Research Institute, National Cancer Center, Goyang, Korea
  • 3Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea

Abstract


Objectives
Gastric cancer (GC) demonstrates a sex disparity that may also be associated with body mass index (BMI). This study explored whether the effect of BMI on the risk of GC varies by sex.
Methods
The study cohort included 341,999 Koreans aged 40 years or older from the National Health Insurance Service–Health Screening Cohort, with a median follow-up period of 10 years. Participants were categorized into five groups based on their BMI. The effect of BMI was evaluated using Cox proportional hazard regression. Additionally, stratification analysis was performed according to waist circumference.
Results
An increased risk of developing GC was observed across the study population among those with obesity (BMI 25.0–29.9 kg/m2 ; hazard ratio [HR], 1.11; 95% CI , 1.03–1.20) and severe obesity (BMI ≥30.0 kg/m2 ; HR, 1.22; 95% CI, 1.01–1.47), considering a 2-year latency period. Notably, the rise in GC risk was particularly pronounced among women with obesity and men with severe obesity. In the age-stratified analysis, severe obesity (BMI ≥30.0 kg/m2 ) was associated with an increased risk of GC in men under 50 years old (HR, 1.83; 95% CI, 0.99–3.37). For individuals aged ≥50 years, obesity was linked to a heightened risk of GC in both sexes. Furthermore, normal BMI (18.5–22.9 kg/m2 ) was associated with an increased GC risk in women.
Conclusion
These findings indicate a positive association between excess body weight and the risk of GC in Koreans, particularly among men with severe obesity.

Keyword

Body mass index; Obesity; Sex characteristics; Stomach neoplasm; Waist circumference

Figure

  • Fig. 1. Study scheme. (A) Time points for measuring body mass index (BMI) and initiating follow-up. The orange box represents the period during which BMI was measured in 2009–2010, with follow-up extending until 2019. (B) Flowchart depicting the selection of study participants. NHIS-HEALS, National Health Insurance Service-Health Screening Cohort.


Reference

References

1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018; 68(6):394–424. DOI: 10.3322/caac.21492. PMID: 30207593.
2. López MJ, Carbajal J, Alfaro AL, Saravia LG, Zanabria D, Araujo JM, et al. Characteristics of gastric cancer around the world. Crit Rev Oncol Hematol. 2023; 181:103841. DOI: 10.1016/j.critrevonc.2022.103841. PMID: 36240980.
3. Kumar S, Metz DC, Ellenberg S, Kaplan DE, Goldberg DS. Risk factors and incidence of gastric cancer after detection of Helicobacter pylori infection: a large cohort study. Gastroenterology. 2020; 158(3):527–536.E7. DOI: 10.1053/j.gastro.2019.10.019. PMID: 31654635. PMCID: PMC7010558.
4. Shin A, Park S, Shin HR, Park EH, Park SK, Oh JK, et al. Population attributable fraction of infection-related cancers in Korea. Ann Oncol. 2011; 22(6):1435–1442. DOI: 10.1093/annonc/mdq592. PMID: 20974652.
5. Tramacere I, Negri E, Pelucchi C, Bagnardi V, Rota M, Scotti L, et al. A meta-analysis on alcohol drinking and gastric cancer risk. Ann Oncol. 2012; 23(1):28–36. DOI: 10.1093/annonc/mdr135. PMID: 21536659.
6. Pi-Sunyer X. The medical risks of obesity. Postgrad Med. 2009; 121(6):21–33. DOI: 10.3810/pgm.2009.11.2074. PMID: 19940414. PMCID: PMC2879283.
7. NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet. 2017; 390(10113):2627–2642. DOI: 10.1016/S0140-6736(17)32129-3. PMID: 29029897.
8. Basen-Engquist K, Chang M. Obesity and cancer risk: recent review and evidence. Curr Oncol Rep. 2011; 13(1):71–76. DOI: 10.1007/s11912-010-0139-7. PMID: 21080117. PMCID: PMC3786180.
9. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 2008; 371(9612):569–578. DOI: 10.1016/S0140-6736(08)60269-X. PMID: 18280327.
10. Mukaisho K, Nakayama T, Hagiwara T, Hattori T, Sugihara H. Two distinct etiologies of gastric cardia adenocarcinoma: interactions among pH, Helicobacter pylori, and bile acids. Front Microbiol. 2015; 6:412. DOI: 10.3389/fmicb.2015.00412. PMID: 26029176. PMCID: PMC4426758.
11. Chen Y, Liu L, Wang X, Wang J, Yan Z, Cheng J, et al. Body mass index and risk of gastric cancer: a meta-analysis of a population with more than ten million from 24 prospective studies. Cancer Epidemiol Biomarkers Prev. 2013; 22(8):1395–1408. DOI: 10.1158/1055-9965.EPI-13-0042. PMID: 23697611.
12. Jang J, Wang T, Cai H, Ye F, Murphy G, Shimazu T, et al. The U-shaped association between body mass index and gastric cancer risk in the Helicobacter pylori biomarker cohort consortium: a nested case-control study from eight East Asian cohort studies. Int J Cancer. 2020; 147(3):777–784. DOI: 10.1002/ijc.32790. PMID: 31745972. PMCID: PMC7234914.
13. Lou L, Wang L, Zhang Y, Chen G, Lin L, Jin X, et al. Sex difference in incidence of gastric cancer: an international comparative study based on the Global Burden of Disease Study 2017. BMJ Open. 2020; 10(1):e033323. DOI: 10.1136/bmjopen-2019-033323. PMID: 31988231. PMCID: PMC7044958.
14. Choi Y, Kim N, Kim KW, Jo HH, Park J, Yoon H, et al. Sex-based differences in histology, staging, and prognosis among 2983 gastric cancer surgery patients. World J Gastroenterol. 2022; 28(9):933–947. DOI: 10.3748/wjg.v28.i9.933. PMID: 35317055. PMCID: PMC8908285.
15. Sanikini H, Biessy C, Rinaldi S, Navionis AS, Gicquiau A, Keski-Rahkonen P, et al. Circulating hormones and risk of gastric cancer by subsite in three cohort studies. Gastric Cancer. 2023; 26(6):969–987. DOI: 10.1007/s10120-023-01414-0. PMID: 37455285. PMCID: PMC10640529.
16. Kyoung DS, Kim HS. Understanding and utilizing claim data from the Korean National Health Insurance Service (NHIS) and Health Insurance Review & Assessment (HIRA) Database for Research. J Lipid Atheroscler. 2022; 11(2):103–110. DOI: 10.12997/jla.2022.11.2.103. PMID: 35656154. PMCID: PMC9133780.
17. Kim MK, Han K, Lee SH. Current trends of big data research using the Korean national health information database. Diabetes Metab J. 2022; 46(4):552–563. DOI: 10.4093/dmj.2022.0193. PMID: 35929173. PMCID: PMC9353560.
18. Kim KK, Haam JH, Kim BT, Kim EM, Park JH, Rhee SY, et al. Evaluation and treatment of obesity and its comorbidities: 2022 update of clinical practice guidelines for obesity by the Korean Society for the Study of Obesity. J Obes Metab Syndr. 2023; 32(1):1–24. DOI: 10.7570/jomes23016. PMID: 36945077. PMCID: PMC10088549.
19. Samanic C, Gridley G, Chow WH, Lubin J, Hoover RN, Fraumeni JF Jr. Obesity and cancer risk among white and black United States veterans. Cancer Causes Control. 2004; 15(1):35–43. DOI: 10.1023/B:CACO.0000016573.79453.ba. PMID: 14970733.
20. Lindblad M, Rodríguez LAG, Lagergren J. Body mass, tobacco and alcohol and risk of esophageal, gastric cardia, and gastric non-cardia adenocarcinoma among men and women in a nested case-control study. Cancer Causes Control. 2005; 16(3):285–294. DOI: 10.1007/s10552-004-3485-7. PMID: 15947880.
21. MacInnis RJ, English DR, Hopper JL, Giles GG. Body size and composition and the risk of gastric and oesophageal adenocarcinoma. Int J Cancer. 2006; 118(10):2628–2631. DOI: 10.1002/ijc.21638. PMID: 16353151.
22. Samanic C, Chow WH, Gridley G, Jarvholm B, Fraumeni JF Jr. Relation of body mass index to cancer risk in 362,552 Swedish men. Cancer Causes Control. 2006; 17(7):901–909. DOI: 10.1007/s10552-006-0023-9. PMID: 16841257.
23. Merry AHH, Schouten LJ, Goldbohm RA, van den Brandt PA. Body mass index, height and risk of adenocarcinoma of the oesophagus and gastric cardia: a prospective cohort study. Gut. 2007; 56(11):1503–1511. DOI: 10.1136/gut.2006.116665. PMID: 17337464. PMCID: PMC2095659.
24. Corley DA, Kubo A, Zhao W. Abdominal obesity and the risk of esophageal and gastric cardia carcinomas. Cancer Epidemiol Biomarkers Prev. 2008; 17(2):352–358. DOI: 10.1158/1055-9965.EPI-07-0748. PMID: 18268119. PMCID: PMC2670999.
25. O'Doherty MG, Freedman ND, Hollenbeck AR, Schatzkin A, Abnet CC. A prospective cohort study of obesity and risk of oesophageal and gastric adenocarcinoma in the NIH–AARP Diet and Health Study. Gut. 2012; 61(9):1261–1268. DOI: 10.1136/gutjnl-2011-300551. PMID: 22174193. PMCID: PMC3504700.
26. Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F, Straif K, et al. Body fatness and cancer: viewpoint of the IARC Working Group. N Engl J Med. 2016; 375(8):794–798. DOI: 10.1056/NEJMsr1606602. PMID: 27557308. PMCID: PMC6754861.
27. World Cancer Research Fund, American Institute for Cancer Research. Diet, nutrition, physical activity and oesophageal cancer. London: World Cancer Research Fund International;2018.
28. Derakhshan MH, Malekzadeh R, Watabe H, Yazdanbod A, Fyfe V, Kazemi A, et al. Combination of gastric atrophy, reflux symptoms and histological subtype indicates two distinct aetiologies of gastric cardia cancer. Gut. 2008; 57(3):298–305. DOI: 10.1136/gut.2007.137364. PMID: 17965056.
29. Alemán JO, Eusebi LH, Ricciardiello L, Patidar K, Sanyal AJ, Holt PR. Mechanisms of obesity-induced gastrointestinal neoplasia. Gastroenterol Hepatol. 2014; 146(2):357–373. DOI: 10.1053/j.gastro.2013.11.051. PMID: 24315827. PMCID: PMC3978703.
30. Olefson S, Moss SF. Obesity and related risk factors in gastric cardia adenocarcinoma. Gastric Cancer. 2015; 18(1):23–32. DOI: 10.1007/s10120-014-0425-4. PMID: 25209115.
31. Cameron AJ, Lomboy CT, Pera M, Carpenter HA. Adenocarcinoma of the esophagogastric junction and Barrett's esophagus. Gastroenterology. 1995; 109(5):1541–1546. DOI: 10.1016/0016-5085(95)90642-8. PMID: 7557137.
32. Fullard M, Kang JY, Neild P, Poullis A, Maxwell JD. Systematic review: does gastro-oesophageal reflux disease progress? Aliment Pharmacol Ther. 2006; 24(1):33–45. DOI: 10.1111/j.1365-2036.2006.02963.x. PMID: 16803601.
33. Cohen DH, LeRoith D. Obesity, type 2 diabetes, and cancer: the insulin and IGF connection. Endocr Relat Cancer. 2012; 19(5):F27–F45. DOI: 10.1530/ERC-11-0374. PMID: 22593429.
34. Tseng CH, Chen CJ, Landolph JR. Diabetes and cancer: epidemiological, clinical, and experimental perspectives. Exp Diabetes Res. 2012; 2012:101802. DOI: 10.1155/2012/101802. PMID: 23082075. PMCID: PMC3469104.
35. Muscogiuri G, Verde L, Vetrani C, Barrea L, Savastano S, Colao A. Obesity: a gender-view. J Endocrinol Invest. 2024; 47(2):299–306. DOI: 10.1007/s40618-023-02196-z. PMID: 37740888. PMCID: PMC10859324.
36. Guglielmi V, Sbraccia P. Obesity phenotypes: depot-diferences in adipose tissue and their clinical implications. Eat Weight Disord. 2018; 23(1):3–14. DOI: 10.1007/s40519-017-0467-9. PMID: 29230714.
37. Chandanos E, Lagergren J. Oestrogen and the enigmatic male predominance of gastric cancer. Eur J Cancer. 2008; 44(16):2397–2403. DOI: 10.1016/j.ejca.2008.07.031. PMID: 18755583.
38. Camargo MC, Goto Y, Zabaleta J, Morgan DR, Correa P, Rabkin CS. Sex hormones, hormonal interventions, and gastric cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev. 2012; 21(1):20–38. DOI: 10.1158/1055-9965.EPI-11-0834. PMID: 22028402. PMCID: PMC3315355.
39. Kim SM, Min BH, Lee J, An JY, Lee JH, Sohn TS, et al. Protective effects of female reproductive factors on Lauren intestinal-type gastric adenocarcinoma. Yonsei Med J. 2018; 59(1):28–34. DOI: 10.3349/ymj.2018.59.1.28. PMID: 29214773. PMCID: PMC5725360.
40. Jo HH, Kim N, Jang J, Choi Y, Park J, Park YM, et al. Impact of body mass index on survival depending on sex in 14,688 patients with gastric cancer in a tertiary hospital in South Korea. Gut Liver. 2023; 17(2):243–258. DOI: 10.5009/gnl220104. PMID: 36317512. PMCID: PMC10018295.
41. Watabe H, Mitsushima T, Derakhshan MH, Yamaji Y, Okamoto M, Kawabe T, et al. Study of association between atrophic gastritis and body mass index: a cross-sectional study in 10,197 Japanese subjects. Dig Dis Sci. 2009; 54(5):988–995. DOI: 10.1007/s10620-008-0468-7. PMID: 18787953.
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