Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Epidemiology and Population Health

Sex-specific effect of body mass index and fasting glucose on gastric cancer risk and all causes mortality; a cohort study of 5.17 million

International Journal of Obesity volume 46, pages 1644–1651 (2022)Cite this article

Subjects

Abstract

Background

Simultaneous evaluation of sex-specific effect of body mass index (BMI) and hyperglycemia on the risk of gastric cancer has been rarely reported. Here, we investigated the sex-specific effect of BMI and hyperglycemia on gastric cancer.

Methods

Persons who underwent National gastric cancer screening from 2006 to 2007 and had no gastric cancer at baseline, were enrolled and followed up to 2015. The risk of gastric cancer by BMI and glucose was measured using risk ratios (RRs) and 95% confidence intervals (CI). Adjusted Cox analysis was performed to evaluate the risk of death.

Results

Gastric cancers developed in 29,775 of 5.17 million. In the adjusted analysis, low BMI (<18.5 kg/m2; RR, 1.44; 95% CI, 1.36–1.53) and high fasting glucose (≥126 mg/dL; RR, 1.09; 95% CI, 1.05–1.13) increased the risk of gastric cancer. In sex-specific analysis, its risk by BMI was modified L-shape with cut-off value of 23 kg/m2 in men and 18.5 kg/m2 in women. Low BMI increased gastric cancer risk in men (RR, 1.39; 95% CI, 1.30–1.50) and women (RR, 1.48; 95% CI, 1.33–1.64). High fasting glucose increased the risk of gastric cancer in women (RR, 1.19; 95% CI, 1.11–1.28), but not in men. Low BMI increased all-cause mortality with cut-off value of 23 kg/m2 in men and 18.5 kg/m2 in women.

Conclusions

Gastric cancer risk and all-cause mortality by BMI was L-shape with sex-specific cut-off value. The effect of fasting glucose on gastric cancer risk was different by sex.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Study flow.
Fig. 2: Adjusted analysis by body mass index.
Fig. 3: Kaplan-Meier curve by body mass index and fasting glucose.
Fig. 4: Adjusted hazard ratio by body mass index.

Similar content being viewed by others

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;68:394–424.

    PubMed  Google Scholar 

  2. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625–38.

    Article  Google Scholar 

  3. 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;22:1395–408.

    Article  Google Scholar 

  4. MacInnis RJ, English DR, Hopper JL, Giles GG. Body size and composition and the risk of gastric and oesophageal adenocarcinoma. Int J Cancer. 2006;118:2628–31.

    Article  CAS  Google Scholar 

  5. 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;17:901–9.

    Article  Google Scholar 

  6. Merry AH, 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;56:1503–11.

    Article  Google Scholar 

  7. 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;61:1261–8.

    Article  Google Scholar 

  8. Crawley DJ, Holmberg L, Melvin JC, Loda M, Chowdhury S, Rudman SM, et al. Serum glucose and risk of cancer: a meta-analysis. BMC Cancer. 2014;14:985.

    Article  Google Scholar 

  9. Jun JK, Gwack J, Park SK, Choi YH, Kim Y, Shin A, et al. (Fasting serum glucose level and gastric cancer risk in a nested case-control study). J Prev Med Public Health. 2006;39:493–8.

    PubMed  Google Scholar 

  10. Yamagata H, Kiyohara Y, Nakamura S, Kubo M, Tanizaki Y, Matsumoto T, et al. Impact of fasting plasma glucose levels on gastric cancer incidence in a general Japanese population: the Hisayama study. Diabetes Care. 2005;28:789–94.

    Article  Google Scholar 

  11. Ikeda F, Doi Y, Yonemoto K, Ninomiya T, Kubo M, Shikata K, et al. Hyperglycemia increases risk of gastric cancer posed by Helicobacter pylori infection: a population-based cohort study. Gastroenterology. 2009;136:1234–41.

    Article  CAS  Google Scholar 

  12. Kim SY, Song YS, Wee JH, Min C, Yoo DM, Lee CH, et al. Evaluation of the relationship between previous statin use and thyroid cancer using Korean National Health Insurance Service-Health Screening Cohort data. Sci Rep. 2021;11:7912.

    Article  CAS  Google Scholar 

  13. Chung HS, Lee JS, Song E, Kim JA, Roh E, Yu JH, et al. Effect of Metabolic Health and Obesity Phenotype on the Risk of Pancreatic Cancer: A Nationwide Population-Based Cohort Study. Cancer Epidemiol Biomarkers Prev. 2021;30:521–8.

    Article  Google Scholar 

  14. Kim Y, Jun JK, Choi KS, Lee HY, Park EC. Overview of the National Cancer screening programme and the cancer screening status in Korea. Asian Pac J Cancer Prev. 2011;12:725–30.

    PubMed  Google Scholar 

  15. Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia: Report of a WHO/IDF consultation (PDF). Geneva: World Health Organization. 2006. p. 21.

  16. Ranganathan P, Aggarwal R, Pramesh CS. Common pitfalls in statistical analysis: Odds versus risk. Perspect Clin Res. 2015;6:222–4.

    Article  Google Scholar 

  17. Bhaskaran K, Douglas I, Forbes H, dos-Santos-Silva I, Leon DA, Smeeth L. Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5.24 million UK adults. Lancet. 2014;384:755–65.

    Article  Google Scholar 

  18. Fan JH, Wang JB, Wang SM, Abnet CC, Qiao YL, Taylor PR. Body mass index and risk of gastric cancer: A 30-year follow-up study in the Linxian general population trial cohort. Cancer Sci. 2017;108:1667–72.

    Article  CAS  Google Scholar 

  19. Cui H, Lopez M, Rahmouni K. The cellular and molecular bases of leptin and ghrelin resistance in obesity. Nat Rev Endocrinol. 2017;13:338–51.

    Article  CAS  Google Scholar 

  20. Kim SH, Kim JW, Byun J, Jeong JB, Kim BG, Lee KL. Plasma ghrelin level and plasma ghrelin/obestatin ratio are related to intestinal metaplasia in elderly patients with functional dyspepsia. PLoS One. 2017;12:e0175231.

    Article  Google Scholar 

  21. Jee SH, Ohrr H, Sull JW, Yun JE, Ji M, Samet JM. Fasting serum glucose level and cancer risk in Korean men and women. JAMA. 2005;293:194–202.

    Article  CAS  Google Scholar 

  22. Nam SY, Park BJ, Nam JH, Ryu KH, Kook MC, Kim J. Association of current Helicobacter pylori infection and metabolic factors with gastric cancer in 35,519 subjects: A cross-sectional study. United European Gastroenterol J. 2019;7:287–96.

    Article  Google Scholar 

  23. Lindkvist B, Almquist M, Bjorge T, Stocks T, Borena W, Johansen D, et al. Prospective cohort study of metabolic risk factors and gastric adenocarcinoma risk in the Metabolic Syndrome and Cancer Project (Me-Can). Cancer Causes Control. 2013;24:107–16.

    Article  Google Scholar 

  24. LeRoith D, Baserga R, Helman L, Roberts CT Jr. Insulin-like growth factors and cancer. Ann Intern Med. 1995;122:54–9.

    Article  CAS  Google Scholar 

  25. Watkins LF, Lewis LR, Levine AE. Characterization of the synergistic effect of insulin and transferrin and the regulation of their receptors on a human colon carcinoma cell line. Int J Cancer. 1990;45:372–5.

    Article  CAS  Google Scholar 

  26. Kaaks R, Lukanova A. Energy balance and cancer: the role of insulin and insulin-like growth factor-I. Proc Nutr Soc. 2001;60:91–106.

    Article  CAS  Google Scholar 

  27. Ma J, Pollak MN, Giovannucci E, Chan JM, Tao Y, Hennekens CH, et al. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J Natl Cancer Inst. 1999;91:620–5.

    Article  CAS  Google Scholar 

  28. Giovannucci E, Pollak MN, Platz EA, Willett WC, Stampfer MJ, Majeed N, et al. A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol Biomarkers Prev. 2000;9:345–9.

    CAS  PubMed  Google Scholar 

  29. Lorenzi M, Montisano DF, Toledo S, Barrieux A. High glucose induces DNA damage in cultured human endothelial cells. J Clin Invest. 1986;77:322–5.

    Article  CAS  Google Scholar 

  30. Dandona P, Thusu K, Cook S, Snyder B, Makowski J, Armstrong D, et al. Oxidative damage to DNA in diabetes mellitus. Lancet. 1996;347:444–5.

    Article  CAS  Google Scholar 

  31. Kim JY, Lee HS, Kim N, Snyder B, Makowski J, Armstrong D, et al. Prevalence and clinicopathologic characteristics of gastric cardia cancer in South Korea. Helicobacter. 2012;17:358–68.

    Article  Google Scholar 

  32. Jee SH, Yun JE, Park EJ, Cho ER, Park IS, Sull JW, et al. Body mass index and cancer risk in Korean men and women. Int J Cancer. 2008;123:1892–6.

    Article  CAS  Google Scholar 

  33. Minami Y, Tateno H. Associations between cigarette smoking and the risk of four leading cancers in Miyagi Prefecture, Japan: a multi-site case-control study. Cancer Sci. 2003;94:540–7.

    Article  CAS  Google Scholar 

  34. 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;23:28–36.

    Article  CAS  Google Scholar 

  35. Global BMIMC, Di Angelantonio E, Bhupathiraju Sh N, Wormser D, Gao P, Kaptoge S, et al. Body-mass index and all-cause mortality: individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet. 2016;388:776–86.

    Article  Google Scholar 

  36. Padwal R, Leslie WD, Lix LM, Majumdar SR. Relationship Among Body Fat Percentage, Body Mass Index, and All-Cause Mortality: A Cohort Study. Ann Intern Med. 2016;164:532–41.

    Article  Google Scholar 

  37. Hirakawa Y, Ninomiya T, Mukai N, Doi Y, Hata J, Fukuhara M, et al. Association between glucose tolerance level and cancer death in a general Japanese population: the Hisayama Study. Am J Epidemiol. 2012;176:856–64.

    Article  Google Scholar 

  38. Derr RL, Ye X, Islas MU, Desideri S, Saudek CD, Grossman SA. Association between hyperglycemia and survival in patients with newly diagnosed glioblastoma. J Clin Oncol. 2009;27:1082–6.

    Article  Google Scholar 

  39. Hosokawa T, Kurosaki M, Tsuchiya K, Matsuda S, Muraoka M, Suzuki Y, et al. Hyperglycemia is a significant prognostic factor of hepatocellular carcinoma after curative therapy. World J Gastroenterol. 2013;19:249–57.

    Article  Google Scholar 

Download references

Funding

This study was funded by the National R&D Program for Cancer Control, Ministry of Health & Welfare, Republic of Korea (1631100) and the National Research Foundation, Republic of Korea (NRF-2015R1D1A1A01059219, NRF-2022R1A2C2013044) (SY Nam). The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript. Funding source provided the cost for the use of big data.

Author information

Authors and Affiliations

  1. Gastroenterology, Kyungpook National University Hospital, Buk-gu, Daegu, Korea

    Su Youn Nam & Seong Woo Jeon

  2. Department of Statistics, Kyungpook National University, Buk-gu, Daegu, Korea

    Jihyeon Jeong

  3. Biostatistics, Medical Research Collaboration Center, Kyunpook National University Hospital & Kyungpook National University School of Medicine, Buk-gu, Daegu, Korea

    Won Kee Lee

Authors
  1. Su Youn Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jihyeon Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Won Kee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seong Woo Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SYN: Conceptualization, formal analysis, supervision, visualization, methodology, writing–original draft, writing–review and editing, data management, data analysis and interpretation. Responsibility for data accuracy and decision to submit for publication. JHJ: Data management and analysis, writing–review and editing. WKL: Data analysis and interpretation, writing–review and editing. SWJ: Data interpretation, writing–review and editing. All authors wrote the manuscript and approved the final approval.

Corresponding author

Correspondence to Su Youn Nam.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics statement

This study was approved by the Institutional Review Board of the Kyungpook National University Hospital Chilgok (KNUHC 2016-08-024).

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nam, S.Y., Jeong, J., Lee, W.K. et al. Sex-specific effect of body mass index and fasting glucose on gastric cancer risk and all causes mortality; a cohort study of 5.17 million. Int J Obes 46, 1644–1651 (2022). https://doi.org/10.1038/s41366-022-01161-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-022-01161-9

Search

Advanced search

Quick links