Abstract
Background
Excessive visceral fat may promote cancer development and progression because of metabolic derangements. The purpose of this study was to clarify the impact of abdominal fat distribution on patient prognosis after esophagectomy for esophageal squamous cell carcinoma (ESCC).
Methods
Computed tomography volumetry was performed in 150 patients who underwent curative esophagectomy for ESCC between 2012 and 2013. Visceral fat area (VFA) and subcutaneous fat area (SFA) at umbilicus level were measured, and the VFA/SFA ratio was calculated in each patient. Prognoses of the patients were compared between groups classified according to VFA/SFA ratio.
Results
Both relapse-free survival and overall survival of the low VFA/SFA group were significantly better than those of the high VFA/SFA group (log-rank test p = 0.005, p = 0.01). Univariate analysis also found that low VFA/SFA ratio significantly predicted an increase in relapse-free and overall survival. In multivariate analysis, low VFA/SFA ratio was an independent factor for relapse-free survival [p = 0.042, hazard ratio (HR) 0.12, 95 % confidence interval (CI) 0.01–0.93]. In addition, low VFA/SFA ratio tended to be a significant variable that predicted better overall survival (p = 0.057, HR 0.14, 95 % CI 0.01–1.05).
Conclusions
Low VFA/SFA ratio was significantly associated with better prognosis in patients who undergo curative esophagectomy for ESCC. Abdominal fat distribution may influence the biological features of ESCC.
Similar content being viewed by others
References
Flegal KM, Graubard BI, Williamson DF, Gail MH. Cause-specific excess deaths associated with underweight, overweight, and obesity. JAMA. 2007;298:2028–37.
Ryan AM, Healy LA, Power DG, et al. Barrett esophagus: prevalence of central adiposity, metabolic syndrome, and a proinflammatory state. Ann Surg. 2008;247:909–15.
Beddy P, Howard J, McMahon C, et al. Association of visceral adiposity with oesophageal and junctional adenocarcinomas. Br J Surg. 2010;97:1028–34.
Karelis AD, St-Pierre DH, Conus F, Rabasa-Lhoret R, Poehlman ET. Metabolic and body composition factors in subgroups of obesity: what do we know? J Clin Endocrinol Metab. 2004;89:2569–75.
van Kruijsdijk RC, van der Wall E, Visseren FL. Obesity and cancer: the role of dysfunctional adipose tissue. Cancer Epidemiol Biomarkers Prev. 2009;18:2569–78.
Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010;11:11–8.
Freese KE, Kokai L, Edwards RP, et al. Adipose-derived stems cells and their role in human cancer development, growth, progression, and metastasis: a systematic review. Cancer Res. 2015;75:1161–8.
Moon HG, Ju YT, Jeong CY, et al. Visceral obesity may affect oncologic outcome in patients with colorectal cancer. Ann Surg Oncol. 2008;15:1918–22.
Guiu B, Petit JM, Bonnetain F, et al. Visceral fat area is an independent predictive biomarker of outcome after first-line bevacizumab-based treatment in metastatic colorectal cancer. Gut. 2010;59:341–7.
Watanabe M, Ishimoto T, Baba Y, et al. Prognostic impact of body mass index in patients with squamous cell carcinoma of the esophagus. Ann Surg Oncol. 2013;20:3984–91.
Clark W, Siegel EM, Chen YA, et al. Quantitative measures of visceral adiposity and body mass index in predicting rectal cancer outcomes after neoadjuvant chemoradiation. J Am Coll Surg. 2013;216:1070–81.
Fujiwara N, Nakagawa H, Kudo Y, et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J Hepatol. 2015;63:131–40.
Mathur A, Luberice K, Paul H, Franka C, Rosemurgy A. Increasing body mass index portends abbreviated survival following pancreatoduodenectomy for pancreatic adenocarcinoma. Am J Surg. 2015;209:969–73.
Makino T, Trencheva K, Shukla PJ, et al. The influence of obesity on short- and long-term outcomes after laparoscopic surgery for colon cancer: a case-matched study of 152 patients. Surgery. 2014;156:661–8.
Guo Z, Zhang J, Jiang JH, Li LQ, Xiang BD. Obesity does not influence outcomes in hepatocellular carcinoma patients following curative hepatectomy. PloS One. 2015;10:e0125649.
Kayani B, Okabayashi K, Ashrafian H, et al. Does obesity affect outcomes in patients undergoing esophagectomy for cancer? A meta-analysis. World J Surg. 2012;36:1785–95.
Harada K, Baba Y, Ishimoto T, et al. Low visceral fat content is associated with poor prognosis in a database of 507 upper gastrointestinal cancers. Ann Surg Oncol. 2015;22:3946–53.
Miao L, Chen H, Xiang J, Zhang Y. A high body mass index in esophageal cancer patients is not associated with adverse outcomes following esophagectomy. J Cancer Res Clin Oncol. 2015;141:941–50.
Morgan MA, Lewis WG, Hopper AN, et al. Prognostic significance of body mass indices for patients undergoing esophagectomy for cancer. Dis Esophagus. 2007;20:29–35.
Hayashi Y, Correa AM, Hofstetter WL, et al. The influence of high body mass index on the prognosis of patients with esophageal cancer after surgery as primary therapy. Cancer. 2010;116:5619–27.
Bouchard C, Despres JP, Mauriege P. Genetic and nongenetic determinants of regional fat distribution. Endocr Rev. 1993;14:72–93.
Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev. 2000;21:697–738.
Maurovich-Horvat P, Massaro J, Fox CS, Moselewski F, O’Donnell CJ, Hoffmann U. Comparison of anthropometric, area- and volume-based assessment of abdominal subcutaneous and visceral adipose tissue volumes using multi-detector computed tomography. Int J Obes (Lond). 2007;31:500–6.
Sobin LH, Gospodarowicz MK, Wittekind C, International Union against Cancer. TNM classification of malignant tumors. 7th edn. Chichester, West Sussex, UK; Hoboken, NJ: Wiley-Blackwell; 2010.
Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.
Cao Y. Angiogenesis modulates adipogenesis and obesity. J Clin Invest. 2007;117:2362–2368.
Frezza EE, Wachtel MS, Chiriva-Internati M. Influence of obesity on the risk of developing colon cancer. Gut. 2006;55:285–91.
Yip C, Goh V, Davies A, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol. 2014;24:998–1005.
Tran TT, Yamamoto Y, Gesta S, Kahn CR. Beneficial effects of subcutaneous fat transplantation on metabolism. Cell Metab. 2008;7:410–20.
Hall RG, 2nd, Jean GW, Sigler M, Shah S. Dosing considerations for obese patients receiving cancer chemotherapeutic agents. Ann Pharmacother. 2013;47:1666–74.
Lashinger LM, Rossi EL, Hursting SD. Obesity and resistance to cancer chemotherapy: interacting roles of inflammation and metabolic dysregulation. Clin Pharmacol Ther. 2014;96:458–63.
Kobayashi J, Tadokoro N, Watanabe M, Shinomiya M. A novel method of measuring intra-abdominal fat volume using helical computed tomography. Int J Obes Relat Metab Disord. 2002;26:398–402.
Cecchini S, Cavazzini E, Marchesi F, Sarli L, Roncoroni L. Computed tomography volumetric fat parameters versus body mass index for predicting short-term outcomes of colon surgery. World J Surg. 2011;35:415–23.
Toh Y, Oki E, Minami K, Okamura T. Follow-up and recurrence after a curative esophagectomy for patients with esophageal cancer: the first indicators for recurrence and their prognostic values. Esophagus. 2010;7:37-43.
Acknowledgments
This work was supported in part by the Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Scientific Research (Grant number 15K10122).
Disclosure
There are no financial or other relations that could lead to a conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Okamura, A., Watanabe, M., Mine, S. et al. Clinical Impact of Abdominal Fat Distribution on Prognosis After Esophagectomy for Esophageal Squamous Cell Carcinoma. Ann Surg Oncol 23, 1387–1394 (2016). https://doi.org/10.1245/s10434-015-5018-x
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-015-5018-x