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Abdominal obesity increases risk for esophageal cancer: a nationwide population-based cohort study of South Korea

  • Original Article—Alimentary Tract
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Abstract

Background

The relationship between overall obesity, as measured by body mass index (BMI) and risk of esophageal squamous cell carcinoma (ESCC) has been reported to show a negative correlation. However, the relationship of ESCC, which accounts for around 90% of esophageal cancers in South Korea, with abdominal obesity, as measured by waist circumference (WC), may be different. Thus, we investigated the association between abdominal obesity and esophageal cancer in a nationwide population-based cohort.

Methods

A retrospective cohort study of 22,809,722 individuals who had undergone regular health check-ups provided by the National Health Insurance Corporation between 2009 and 2012 (median follow-up period, 6.4 years) in South Korea was conducted. Abdominal obesity was defined as a WC > 90 cm for men and > 85 cm for women. We estimated hazard ratios (HRs) and 95% confidence intervals (CIs) using χ2 test and Cox proportional hazards model adjusted for confounding factors. The primary outcome was newly developed esophageal cancer.

Results

After adjusting for BMI, abdominal obesity increased the risk of esophageal cancer (HR 1.29, 95% CI 1.23–1.36). WC increased the risk for esophageal cancer in a dose-dependent manner (p values for trend < 0.0001). Among overweight (BMI 23–24.9 kg/m2) and obese I (BMI 25–29.9 kg/m2) individuals, abdominal obesity was a risk factor for esophageal cancer (HR 1.22, 95% CI 1.11–1.34; HR 1.28, 95% CI 1.18–1.39, respectively).

Conclusion

Increasing abdominal obesity may be associated with an increased risk for esophageal cancer. Further studies are warranted to confirm the relationship.

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References

  1. International Agency for Research on Cancer of World Health Organization. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx. Accessed 14 Feb 2019.

  2. Bray F, Ferlay J, Soerjomataram I, et al. 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 

  3. Pennathur A, Gibson MK, Jobe BA, et al. Oesophageal carcinoma. Lancet. 2013;381:400–12.

    PubMed  Google Scholar 

  4. Hongo M, Nagasaki Y, Shoji T. Epidemiology of esophageal cancer: orient to occident. Effects of chronology, geography and ethnicity. J Gastroenterol Hepatol. 2009;24:729–35.

    PubMed  Google Scholar 

  5. Bollschweiler E, Wolfgarten E, Gutschow C, et al. Demographic variations in the rising incidence of esophageal adenocarcinoma in white males. Cancer. 2001;92:549–55.

    CAS  PubMed  Google Scholar 

  6. Son JI, Park HJ, Song KS, et al. A single center’s 30 years’ experience of esophageal adenocarcinoma. Korean J Intern Med. 2001;16:250–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003;349:2241–52.

    CAS  PubMed  Google Scholar 

  8. Stoner GD, Gupta A. Etiology and chemoprevention of esophageal squamous cell carcinoma. Carcinogenesis. 2001;22:1737–46.

    CAS  PubMed  Google Scholar 

  9. Vaughan TL, Davis S, Kristal A, et al. Obesity, alcohol, and tobacco as risk factors for cancers of the esophagus and gastric cardia: adenocarcinoma versus squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 1995;4:85–92.

    CAS  PubMed  Google Scholar 

  10. Lindkvist B, Johansen D, Stocks T, et al. Metabolic risk factors for esophageal squamous cell carcinoma and adenocarcinoma: a prospective study of 580 000 subjects within the Me-Can project. BMC Cancer. 2014;14:103.

    PubMed  PubMed Central  Google Scholar 

  11. Engeland A, Tretli S, Bjørge T. Height and body mass index in relation to esophageal cancer; 23-year follow-up of two million norwegian men and women. Cancer Causes Control. 2004;15:837–43.

    PubMed  Google Scholar 

  12. Shen W, Punyanitya M, Chen J, et al. Waist circumference correlates with metabolic syndrome indicators better than percentage fat. Obesity (Silver Spring). 2006;14:727–36.

    Google Scholar 

  13. Janssen I, Katzmarzyk PT, Ross R. Waist circumference and not body mass index explains obesity-related health risk. Am J Clin Nutr. 2004;79:379–84.

    CAS  PubMed  Google Scholar 

  14. Du X, Hidayat K, Shi BM. Abdominal obesity and gastroesophageal cancer risk: systematic review and meta-analysis of prospective studies. Biosci Rep. 2017;37:BSR20160474.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  16. O’Doherty MG, Freedman ND, Hollenbeck AR, et al. 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.

    PubMed  Google Scholar 

  17. Hardikar S, Onstad L, Blount PL, et al. The role of tobacco, alcohol, and obesity in neoplastic progression to esophageal adenocarcinoma: a prospective study of Barrett’s esophagus. PLoS One. 2013;8:e52192.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Steffen A, Huerta JM, Weiderpass E, et al. General and abdominal obesity and risk of esophageal and gastric adenocarcinoma in the European prospective investigation into cancer and nutrition. Int J Cancer. 2015;137:646–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Lin Y, Ness-Jensen E, Hveem K, et al. Metabolic syndrome and esophageal and gastric cancer. Cancer Causes Control. 2015;26:1825–34.

    PubMed  Google Scholar 

  20. Corley DA, Kubo A, Zhao W. Abdominal obesity and the risk of esophageal and gastric cardia carcinomas. Cancer Epidemiol Biomark Prev. 2008;17:352–8.

    Google Scholar 

  21. Steffen A, Schulze MB, Pischon T, et al. Anthropometry and esophageal cancer risk in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomark Prev. 2009;18:2079–89.

    Google Scholar 

  22. Alberti KG, Zimmet P, Shaw J. IDF epidemiology task force consensus group. The metabolic syndrome—a new worldwide definition. Lancet. 2005;366:1059–62.

    PubMed  Google Scholar 

  23. KOrean statistical information service (KOSIS). http://kosis.kr/statHtml/statHtml.do?orgId=117&tblId=DT_11702_N101&conn_path=I2. Accessed 14 Feb 2019.

  24. National Cancer Information Center (NCIC). https://www.cancer.go.kr/lay1/program/S1T211C223/cancer/view.do?cancer_seq=4277&menu_seq=4282. Accessed 14 Feb 2019.

  25. Lee YH, Jung KS, Kim SU, et al. Sarcopaenia is associated with NAFLD independently of obesity and insulin resistance: nationwide surveys (KNHANES 2008–2011). J Hepatol. 2015;63:486–93.

    PubMed  Google Scholar 

  26. Yang HK, Han K, Kwon HS, et al. Obesity, metabolic health, and mortality in adults: a nationwide population-based study in Korea. Sci Rep. 2016;6:30329.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. International Obesity Task Force. The Asia-Pacific perspective:redefinining obesity and its treatment. Sydney: Health Communications Australia Pty Ltd; 2000.

    Google Scholar 

  28. Oh SW. Obesity and metabolic syndrome in Korea. Diabetes Metab J. 2011;35:561–6.

    PubMed  PubMed Central  Google Scholar 

  29. Lee SY, Park HS, Kim DJ, et al. Appropriate waist circumference cutoff points for central obesity in Korean adults. Diabetes Res Clin Pract. 2007;75:72–80.

    PubMed  Google Scholar 

  30. Lee J, Lee JS, Park SH, et al. Cohort profile: the national health insurance service-national sample cohort (NHIS-NSC), South Korea. Int J Epidemiol. 2017;46:e15.

    PubMed  Google Scholar 

  31. Lee YH, Kim JE, Roh YH, et al. The combination of vitamin D deficiency and mild to moderate chronic kidney disease is associated with low bone mineral density and deteriorated femoral microarchitecture: results from the KNHANES 2008–2011. J Clin Endocrinol Metab. 2014;99:3879–88.

    CAS  PubMed  Google Scholar 

  32. 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.

    PubMed  PubMed Central  Google Scholar 

  33. Choi YJ, Lee DH, Han K, et al. Joint effects of low body mass index and alcohol consumption on developing esophageal squamous cell cancer: a korean nationwide population-based cohort study. Asian Pac J Cancer Prev. 2017;18:1881–7.

    PubMed  PubMed Central  Google Scholar 

  34. Choi YJ, Lee DH, Han KD, et al. Elevated serum gamma-glutamyltransferase is associated with an increased risk of oesophageal carcinoma in a cohort of 8,388,256 Korean subjects. PLoS One. 2017;12:e0177053.

    PubMed  PubMed Central  Google Scholar 

  35. Tran GD, Sun XD, Abnet CC, et al. Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer. 2005;113:456–63.

    CAS  PubMed  Google Scholar 

  36. Umar SB, Fleischer DE. Esophageal cancer: epidemiology, pathogenesis and prevention. Nat Clin Pract Gastroenterol Hepatol. 2008;5:517–26.

    Google Scholar 

  37. Dieudonne MN, Bussiere M, Dos Santos E, et al. Adiponectin mediates antiproliferative and apoptotic responses in human MCF7 breast cancer cells. Biochem Biophys Res Commun. 2006;345:271–9.

    CAS  PubMed  Google Scholar 

  38. Renehan AG, Zwahlen M, Minder C, et al. Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet. 2004;363:1346–53.

    CAS  PubMed  Google Scholar 

  39. Mercer CD, Rue C, Hanelin L, Hill LD. Effect of obesity on esophageal transit. Am J Surg. 1985;149:177–81.

    CAS  PubMed  Google Scholar 

  40. Jaffin BW, Knoepflmacher P, Greenstein R. High prevalence of asymptomatic esophageal motility disorders among morbidly obese patients. Obes Surg. 1999;9:390–5.

    CAS  PubMed  Google Scholar 

  41. Li SD, Mobarhan S. Association between body mass index and adenocarcinoma of the esophagus and gastric cardia. Nutr Rev. 2000;58:54–6.

    CAS  PubMed  Google Scholar 

  42. Iyengar NM, Gucalp A, Dannenberg AJ, et al. Obesity and cancer mechanisms: tumor microenvironment and inflammation. J Clin Oncol. 2016;34:4270–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Ellulu MS, Patimah I, Khaza’ai H, et al. Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci. 2017;13:851–63.

    CAS  PubMed  Google Scholar 

  44. Dalamaga M, Diakopoulos KN, Mantzoros CS. The role of adiponectin in cancer: a review of current evidence. Endocr Rev. 2012;33:547–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Yildirim A, Bilici M, Cayir K, et al. Serum adiponectin levels in patients with esophageal cancer. Jpn J Clin Oncol. 2009;39:92–6.

    PubMed  Google Scholar 

  46. Nakajima TE, Yamada Hamano T, et al. Adipocytokines and squamous cell carcinoma of the esophagus. J Cancer Res Clin Oncol. 2010;136:261–6.

    CAS  PubMed  Google Scholar 

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Author information

Author notes

  1. Jae Ho Cho and Cheol Min Shin contributed equally to this work.

Authors and Affiliations

  1. Division of Gastroenterology, Department of Internal Medicine, Seoul National University Bundang Hospital, 82, Gumi-ro 173 Beon-gil, Bundang-gu, Seongnam, Gyeonggi-do, 13620, Republic of Korea

    Jae Ho Cho, Cheol Min Shin, Hyuk Yoon, Young Soo Park, Nayoung Kim & Dong Ho Lee

  2. Department of Biostatistics, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    Kyung-Do Han

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  1. Jae Ho Cho
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  2. Cheol Min Shin
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Contributions

CMS and DHL conceptualized and designed the study outline. DHL and KDH acquired data from the National Health Insurance Corporation. DHL supervised the analysis of data and critically revised the paper. KDH statistically analyzed the data. JHC, CMS, HY, YSP, and NK analyzed and interpreted the data. JHC and CMS wrote and revised the paper. All authors have reviewed and approved the final manuscript.

Corresponding authors

Correspondence to Kyung-Do Han or Dong Ho Lee.

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The authors declare that they have no conflict of interest.

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All procedures involving human participants were performed in accordance with the ethical standards of the institutional and national research committees, and the 1964 Helsinki Declaration including its later amendments or comparable ethical standards. Informed consent for using information was exempted by the institutional and national research committees because this study used only previously collected data.

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Cho, J.H., Shin, C.M., Han, KD. et al. Abdominal obesity increases risk for esophageal cancer: a nationwide population-based cohort study of South Korea. J Gastroenterol 55, 307–316 (2020). https://doi.org/10.1007/s00535-019-01648-9

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  • DOI: https://doi.org/10.1007/s00535-019-01648-9

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