Abstract
Background
There is increasing interest in the influence of body composition on oncological outcomes. We evaluated the role of skeletal muscle and fat among patients with gastric cancer (GC) who underwent gastrectomy with or without adjuvant chemotherapy, as well as those changes’ associations with survival outcomes.
Methods
The present study evaluated 136 patients with GC who were enrolled in the CLASSIC Trial at Yonsei Cancer Center. Baseline body compositions including skeletal muscle area, Hounsfield units (HU), visceral fat area, and subcutaneous fat area were measured by preoperative computed tomography (CT). CT before and after the gastrectomy were used to determine the 6-month relative changes in body composition parameters. Continuous variables were dichotomized according to the best cutoff values by Contal and O’Quigley method.
Results
Seventy-three patients (53.7%) underwent surgery alone, and 63 patients (46.3%) underwent surgery followed by adjuvant chemotherapy. The baseline body composition parameters were not associated with disease-free survival (DFS) or overall survival (OS). Except for the HU, the marked loss of muscle, visceral fat, or subcutaneous fat significantly predicted shorter DFS and OS. Patients with a marked loss in at least one significant body composition parameter had significantly shorter DFS (hazard ratio 2.9, 95% confidence interval 1.7–4.8, P < 0.001) and OS (hazard ratio 2.9, 95% confidence interval 1.7–5.0, P < 0.001).
Conclusions
Marked loss in body composition parameters significantly predicted shorter DFS and OS among patients with GC who underwent gastrectomy. Postoperative nutrition and active healthcare interventions could improve the prognosis of these GC patients.
Similar content being viewed by others
References
Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2014. Cancer Res Treat. 2017;49:292–305.
Digklia A, Wagner AD. Advanced gastric cancer: Current treatment landscape and future perspectives. World J Gastroenterol. 2016;22:2403–14.
Noh SH, Park SR, Yang HK, et al. Adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): 5-year follow-up of an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15:1389–96.
Dicken BJ, Bigam DL, Cass C, Mackey JR, Joy AA, Hamilton SM. Gastric adenocarcinoma: review and considerations for future directions. Ann Surg. 2005;241:27–39.
Ongaro E, Buoro V, Cinausero M, et al. Sarcopenia in gastric cancer: when the loss costs too much. Gastric Cancer. 2017;20:563–72.
Kuwada K, Kuroda S, Kikuchi S, et al. Sarcopenia and comorbidity in gastric cancer surgery as a useful combined factor to predict eventual death from other causes. Ann Surg Oncol. 2018. https://doi.org/10.1245/s10434-018-6354-4.
Shizgal HM. Body composition of patients with malnutrition and cancer. Summary of methods of assessment. Cancer. 1985;55:250–3.
Prado CM, Lieffers JR, McCargar LJ, 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.
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.
Janssen I, Heymsfield SB, Allison DB, Kotler DP, Ross R. Body mass index and waist circumference independently contribute to the prediction of nonabdominal, abdominal subcutaneous, and visceral fat. Am J Clin Nutr. 2002;75:683–8.
Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE. Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer. 2012;107:931–6.
Yip C, Dinkel C, Mahajan A, Siddique M, Cook GJ, Goh V. Imaging body composition in cancer patients: visceral obesity, sarcopenia and sarcopenic obesity may impact on clinical outcome. Insights Imaging. 2015;6:489–97.
Kim JH, Chin HM, Hwang SS, Jun KH. Impact of intra-abdominal fat on surgical outcome and overall survival of patients with gastric cancer. Int J Surg. 2014;12:346–52.
Blauwhoff-Buskermolen S, Versteeg KS, de van der Schueren MA, et al. Loss of muscle mass during chemotherapy is predictive for poor survival of patients with metastatic colorectal cancer. J Clin Oncol. 2016;34:1339–44.
Tegels JJ, van Vugt JL, Reisinger KW, et al. Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes. J Surg Oncol. 2015;112:403–7.
Li XT, Tang L, Chen Y, Li YL, Zhang XP, Sun YS. Visceral and subcutaneous fat as new independent predictive factors of survival in locally advanced gastric carcinoma patients treated with neo-adjuvant chemotherapy. J Cancer Res Clin Oncol. 2015;141:1237–47.
Greene FL, Page DL, Fleming ID, et al. AJCC cancer staging manual. 6th ed. New York: Springer; 2003.
Mukaka MM. Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 2012;24:69–71.
Contal C OQJ. An application of changepoint methods in studying the effect of age on survival in breast cancer. Comput Stat Data Anal. 1999;30:253–70.
Martin L, Birdsell L, Macdonald N, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47.
Caccialanza R, Pedrazzoli P, Cereda E, et al. Nutritional support in cancer patients: a position paper from the Italian society of medical oncology (AIOM) and the Italian society of artificial nutrition and metabolism (SINPE). J Cancer. 2016;7:131–5.
Prado CM, Baracos VE, McCargar LJ, et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clin Cancer Res. 2007;13:3264–8.
Prado CM, Baracos VE, McCargar LJ, et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res. 2009;15:2920–6.
Zhou CJ, Zhang FM, Zhang FY, et al. Sarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy. J Surg Res. 2017;211:137–46.
Antoun S, Bayar A, Ileana E, et al. High subcutaneous adipose tissue predicts the prognosis in metastatic castration-resistant prostate cancer patients in post chemotherapy setting. Eur J Cancer. 2015;51:2570–7.
Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010;11:11–8.
Yoon DY, Kim HK, Kim JA, et al. Changes in the abdominal fat distribution after gastrectomy: computed tomography assessment. ANZ J Surg. 2007;77:121–5.
Yamaoka Y, Fujitani K, Tsujinaka T, Yamamoto K, Hirao M, Sekimoto M. Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy. Gastric Cancer. 2015;18:382–9.
Funding
This study was supported by a 2014 faculty research Grant from the Yonsei University College of Medicine (6-2014-0177 to M Jung).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Human and animal Rights
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The protocol was reviewed and approved by the local Institutional Review Board (IRB Approval No. 2017-2283-001).
Informed consent
The institutional IRB decided to waive the informed consent of this study because it was an observation study using retrospectively collected data.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10434_2018_6624_MOESM1_ESM.tif
Measurements of muscle mass, Hounsfield units (HU), visceral fat, and subcutaneous fat at lumbar vertebra 3 (L3) level using computed tomography (CT) scan. (a) Measured axial CT image which was selected by reference images with (b) 3D reconstruction image, (c) coronal image and (d) sagittal image. (e) Measurements of muscle area and HU (blue area). (f) Visceral (green area) and subcutaneous (blue area) fat area measurements
10434_2018_6624_MOESM2_ESM.tif
Correlations between each body composition factor. The correlations are shown for (a) 6-month relative muscle change and 6-month relative visceral fat change, (b) 6-month relative muscle change and 6 month relative subcutaneous fat change, and (c) 6 month relative visceral fat change and 6 month relative subcutaneous fat change
Rights and permissions
About this article
Cite this article
Park, H.S., Kim, H.S., Beom, S.H. et al. Marked Loss of Muscle, Visceral Fat, or Subcutaneous Fat After Gastrectomy Predicts Poor Survival in Advanced Gastric Cancer: Single-Center Study from the CLASSIC Trial. Ann Surg Oncol 25, 3222–3230 (2018). https://doi.org/10.1245/s10434-018-6624-1
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-018-6624-1