Abstract
Background/objectives
The aim of this study was to examine the impact of visceral fat on surgical complications and long-term survival for patients undergoing radical gastrectomy.
Subjects/methods
From 2009 to 2013, 859 patients who underwent curative resection for gastric cancer were enrolled from a prospectively maintained database. Visceral fat area (VFA) was assessed by preoperative CT scans. Patients were divided into two groups by VFA. Perioperative variables and postoperative outcomes were compared between the high VFA group and low VFA group. Univariable and multivariable analysis were performed to investigate independent risk factors of postoperative complications and survival.
Results
Some 859 patients were included in the study, 308 of whom were classified as high VFA. High VFA was correlated with advance age (P = 0.020), higher albumin levels (P = 0.001), hemoglobin levels (P < 0.05), ASA grade (P = 0.043) and Charlson Comorbidity Index (P = 0.004). Relative to patients with low VFA, those with high VFA had longer surgical durations (P = 0.004), higher rate of postoperative complications (P = 0.004), and longer hospital stays (P = 0.004). High VFA was identified as the only determinant for surgical complications by logistic regression analysis (OR, 2.236, 95% CI, 1.537–3.254; P < 0.001). Cox proportional hazards regression revealed no correlation between VFA and overall survival (OS) or disease-free survival (DFS).
Conclusions
Increased VFA independently predicts surgical complications in patients after gastrectomy. However, VFA is not a prognostic biomarker of OS or DFS in patients with gastric cancer.
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References
Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014;311:806–14. https://doi.org/10.1001/jama.2014.732
Ji CY, Chen TJ. Working Group on Obesity in C. Empirical changes in the prevalence of overweight and obesity among Chinese students from 1985 to 2010 and corresponding preventive strategies. Biomed Environ Sci. 2013;26:1–12. https://doi.org/10.3967/0895-3988.2013.01.001
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;371:569–78. https://doi.org/10.1016/S0140-6736(08)60269-X
Malietzis G, Currie AC, Athanasiou T, Johns N, Anyamene N, Glynne-Jones R, et al. Influence of body composition profile on outcomes following colorectal cancer surgery. Br J Surg. 2016;103:572–80. https://doi.org/10.1002/bjs.10075
Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9:629–35. https://doi.org/10.1016/S1470-2045(08)70153-0
Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93:359–404. https://doi.org/10.1152/physrev.00033.2011
Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, et al. Visceral Adiposity Index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care. 2010;33:920–2. https://doi.org/10.2337/dc09-1825
Despres JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature. 2006;444:881–7. https://doi.org/10.1038/nature05488
Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation. 2007;116:1234–41. https://doi.org/10.1161/CIRCULATIONAHA.107.710509
Kang J, Baek SE, Kim T, Hur H, Min BS, Lim JS, et al. Impact of fat obesity on laparoscopic total mesorectal excision: more reliable indicator than body mass index. Int J Colorectal Dis. 2012;27:497–505. https://doi.org/10.1007/s00384-011-1333-2
Tanaka K, Miyashiro I, Yano M, Kishi K, Motoori M, Seki Y, et al. Accumulation of excess visceral fat is a risk factor for pancreatic fistula formation after total gastrectomy. Ann Surg Oncol. 2009;16:1520–5. https://doi.org/10.1245/s10434-009-0391-y
Nishigori T, Tsunoda S, Okabe H, Tanaka E, Hisamori S, Hosogi H, et al. Impact of sarcopenic obesity on surgical site infection after laparoscopic total gastrectomy. Ann Surg Oncol. 2016;23:524–31. https://doi.org/10.1245/s10434-016-5385-y
Kehlet H, Jorgensen CC. Advancing surgical outcomes research and quality improvement within an enhanced recovery program framework. Ann Surg. 2016;264:237–8. https://doi.org/10.1097/SLA.0000000000001674
Japanese Gastric Cancer A. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer: Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc. 2011;14:113–23. https://doi.org/10.1007/s10120-011-0042-4
Doyle SL, Bennett AM, Donohoe CL, Mongan AM, Howard JM, Lithander FE, et al. Establishing computed tomography-defined visceral fat area thresholds for use in obesity-related cancer research. Nutr Res. 2013;33:171–9. https://doi.org/10.1016/j.nutres.2012.12.007
Examination Committee of Criteria for ‘Obesity Disease’ in J. Japan Society for the Study of O. New criteria for ‘obesity disease’ in Japan. Circ J: Off J Jpn Circ Soc. 2002;66: 987–92.
Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.
Ford ES, Maynard LM, Li C. Trends in mean waist circumference and abdominal obesity among US adults, 1999-2012. JAMA. 2014;312:1151–3. https://doi.org/10.1001/jama.2014.8362
Heid IM, Jackson AU, Randall JC, Winkler TW, Qi L, Steinthorsdottir V, et al. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nat Genet. 2010;42:949–60. https://doi.org/10.1038/ng.685
Seidell JC, Bakker CJ, van der Kooy K. Imaging techniques for measuring adipose-tissue distribution—a comparison between computed tomography and 1.5-T magnetic resonance. Am J Clin Nutr. 1990;51:953–7.
Deurenberg P, Deurenberg-Yap M, Guricci S. Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obesity Rev: Off J Int Assoc Study Obes. 2002;3:141–6.
Pecorelli N, Carrara G, De Cobelli F, Cristel G, Damascelli A, Balzano G, et al. Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery. Br J Surg. 2016;103:434–42. https://doi.org/10.1002/bjs.10063
Cakir H, Heus C, Verduin WM, Lak A, Doodeman HJ, Bemelman WA, et al. Visceral obesity, body mass index and risk of complications after colon cancer resection: A retrospective cohort study. Surgery. 2015;157:909–15. https://doi.org/10.1016/j.surg.2014.12.012
Sandini M, Bernasconi DP, Fior D, Molinelli M, Ippolito D, Nespoli L, et al. A high visceral adipose tissue-to-skeletal muscle ratio as a determinant of major complications after pancreatoduodenectomy for cancer. Nutrition. 2016;32:1231–7. https://doi.org/10.1016/j.nut.2016.04.002
Tsujinaka S, Konishi F, Kawamura YJ, Saito M, Tajima N, Tanaka O, et al. Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Dis Colon Rectum. 2008;51:1757–65; discussion1765-1757. https://doi.org/10.1007/s10350-008-9395-0.
Park BK, Park JW, Ryoo SB, Jeong SY, Park KJ, Park JG. Effect of visceral obesity on surgical outcomes of patients undergoing laparoscopic colorectal surgery. World J Surg. 2015;39:2343–53. https://doi.org/10.1007/s00268-015-3085-6
Sugisawa N, Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M. Intra-abdominal infectious complications following gastrectomy in patients with excessive visceral fat. Gastric Cancer: Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc. 2012;15:206–12. https://doi.org/10.1007/s10120-011-0099-0
Kehlet H. Enhanced Recovery After Surgery (ERAS): good for now, but what about the future? Can J Anaesthesia. 2015;62:99–104. https://doi.org/10.1007/s12630-014-0261-3
van Bree SH, Cailotto C, Di Giovangiulio M, Jansen E, van der Vliet J, Costes L, et al. Systemic inflammation with enhanced brain activation contributes to more severe delay in postoperative ileus. Neurogastroenterol Motility: Off J Eur Gastroint Motility Soc. 2013;25:e540–9. https://doi.org/10.1111/nmo.12157
Balentine CJ, Enriquez J, Fisher W, Hodges S, Bansal V, Sansgiry S, et al. Intra-abdominal fat predicts survival in pancreatic cancer. J Gastrointest Surg. 2010;14:1832–7. https://doi.org/10.1007/s11605-010-1297-5
Moon HG, Ju YT, Jeong CY, Jung EJ, Lee YJ, Hong SC, et al. Visceral obesity may affect oncologic outcome in patients with colorectal cancer. Ann Surg Oncol. 2008;15:1918–22. https://doi.org/10.1245/s10434-008-9891-4
Harada K, Baba Y, Ishimoto T, Kosumi K, Tokunaga R, Izumi D, 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. https://doi.org/10.1245/s10434-015-4432-4
Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol: Off J Am Soc Clin Oncol. 2005;23:7114–24. https://doi.org/10.1200/JCO.2005.14.621
Miyazawa-Hoshimoto S, Takahashi K, Bujo H, Hashimoto N, Saito Y. Elevated serum vascular endothelial growth factor is associated with visceral fat accumulation in human obese subjects. Diabetologia. 2003;46:1483–88. https://doi.org/10.1007/s00125-003-1221-6
Otake S, Takeda H, Suzuki Y, Fukui T, Watanabe S, Ishihama K, et al. Association of visceral fat accumulation and plasma adiponectin with colorectal adenoma: evidence for participation of insulin resistance. Clin Cancer Res. 2005;11:3642–46. https://doi.org/10.1158/1078-0432.CCR-04-1868
Acknowledgements
This work was supported by the foundation of the Health Department of Shanghai (20124017), the Shanghai Science and Technology Committee (16411954200) and the foundation of the Health Department of Zhejiang province (2016139771). The funders had no role in the design, analysis or writing of this article.
Author contributions
C-LZ and XS designed the study. L-LM and X-YC collected the data. BL, D-LZ, D-DH, and ZY did the analysis and interpretation of data. S-LW wrote the article. C-LZ revised the article and took the decision to submit the article for publication.
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The authors declare that they have no competing interests.
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Su-Lin Wang and Liang-Liang Ma have contributed equally to this work.
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Wang, SL., Ma, LL., Chen, XY. et al. Impact of visceral fat on surgical complications and long-term survival of patients with gastric cancer after radical gastrectomy. Eur J Clin Nutr 72, 436–445 (2018). https://doi.org/10.1038/s41430-017-0032-7
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DOI: https://doi.org/10.1038/s41430-017-0032-7
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