Abstract
Objective
To assess the effect of preoperative sarcopenia on the short-term and long-term outcomes in older patients with locally advanced gastric cancer (LAGC).
Methods
Clinicopathological data of older patients with LAGC who underwent radical surgery were retrospectively analyzed. Sarcopenia was defined as a skeletal muscle index of less than 36.4 cm2/m2 for men and less than 28.4 cm2/m2 for women. Comparing the postoperative complications and survival between sarcopenia and non-sarcopenia groups using multicenter data.
Results
A total of 406 older patients with LAGC were included in the analysis, including 145 (35.7%) with sarcopenia and 261 (64.3%) with non-sarcopenia. Multivariate logistic regression analysis showed that sarcopenia was an independent risk factor for postoperative complications with CD grade ≥ II (OR 1.616; P < 0.05). Kaplan–Meier survival curve analysis showed that the 5-year overall survival (OS) and 5-year recurrence-free survival (RFS) in the sarcopenia group were lower than those in the non-sarcopenia group (P both < 0.05). Multivariate Cox regression analyses showed that sarcopenia was an independent prognostic factor for 5-year OS and RFS (P both < 0.05). The 5-year recurrence rate in the sarcopenia group was 57.2%, which was significantly higher than that in the non-sarcopenia group (46.4%; P = 0.036). Recurrence pattern analysis showed that the incidence of distant metastases in patients with sarcopenia (42.8%) was significantly higher than non-sarcopenia (31.4%; P = 0.022).
Conclusion
Sarcopenia serves as a valuable predictor of both short-term and long-term outcomes in older patients with LAGC. Therefore, the significance of assessing preoperative nutritional status and implementing thorough postoperative follow-up for older LAGC patients with sarcopenia should be emphasized.
Similar content being viewed by others
References
Fock KM (2014) Review article: the epidemiology and prevention of gastric cancer. Aliment Pharmacol Ther 40:250–260
Marano L, Polom K, Patriti A et al (2016) Surgical management of advanced gastric cancer: an evolving issue. Eur J Surg Oncol 42:18–27
Visa L, Jimenez-Fonseca P, Martinez EA et al (2018) Efficacy and safety of chemotherapy in older versus non-older patients with advanced gastric cancer: a real-world data, non-inferiority analysis. J Geriatr Oncol 9:254–264
Huang DD, Yu DY, Song HN et al (2021) The relationship between the GLIM-defined malnutrition, body composition and functional parameters, and clinical outcomes in elderly patients undergoing radical gastrectomy for gastric cancer. Eur J Surg Oncol 47:2323–2331
Chen WZ, Zhang XZ, Zhang FM et al (2022) Coexistence of GLIM-defined malnutrition and sarcopenia have negative effect on the clinical outcomes in the elderly gastric cancer patients after radical gastrectomy. Front Nutr 9:960670
Keller K, Engelhardt M (2013) Strength and muscle mass loss with aging process. Age and strength loss. Muscles Ligaments Tendons J 3:346–350
Cruz-Jentoft AJ, Sayer AA (2019) Sarcopenia. The Lancet 393:2636–2646
Fukuda Y, Yamamoto K, Hirao M et al (2016) Sarcopenia is associated with severe postoperative complications in elderly gastric cancer patients undergoing gastrectomy. Gastric Cancer 19:986–993
Watanabe M, Miyata H, Gotoh M et al (2014) Total gastrectomy risk model: data from 20,011 Japanese patients in a nationwide internet-based database. Ann Surg 260:1034–1039
Williams GR, Dunne RF, Giri S et al (2021) Sarcopenia in the older adult with cancer. J Clin Oncol 39:2068–2078
Wang FH, Zhang XT, Li YF et al (2021) The Chinese Society of Clinical Oncology (CSCO): clinical guidelines for the diagnosis and treatment of gastric cancer, 2021. Cancer Commun (Lond) 41:747–795
Lourenco RA, Perez-Zepeda M, Gutierrez-Robledo L et al (2015) Performance of the European Working Group on Sarcopenia in Older People algorithm in screening older adults for muscle mass assessment. Age Ageing 44:334–338
Japanese Gastric Cancer Association (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14:113–123.
Amin MB, Greene FL, Edge SB et al (2017) The Eighth Edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin 67:93–99
Kengsakul M, Nieuwenhuyzen-de Boer GM, Udomkarnjananun S et al (2022) Factors predicting 30-day grade IIIa-V Clavien-Dindo classification complications and delayed chemotherapy initiation after cytoreductive surgery for advanced-stage ovarian cancer: a prospective cohort study. Cancers (Basel) 14:4181
Sasako M, Sakuramoto S, Katai H et al (2011) Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol 29:4387–4393
Bang YJ, Kim YW, Yang HK et al (2012) Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial. The Lancet 379:315–321
Dello SA, Lodewick TM, van Dam RM et al (2013) Sarcopenia negatively affects preoperative total functional liver volume in patients undergoing liver resection. HPB (Oxford) 15:165–169
Prado CM, Lieffers JR, McCargar LJ et al (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9:629–635
Kawaguchi Y, Hanaoka J, Ohshio Y et al (2019) Sarcopenia predicts poor postoperative outcome in elderly patients with lung cancer. Gen Thorac Cardiovasc Surg 67:949–954
Morlino D, Marra M, Cioffi I et al (2022) Prevalence of sarcopenia in women with breast cancer. Nutrients 14:1839
Lin JX, Lin JP, Xie JW et al (2019) Prognostic value and association of sarcopenia and systemic inflammation for patients with gastric cancer following radical gastrectomy. Oncologist 24:e1091–e1101
Dodds RM, Syddall HE, Cooper R et al (2014) Grip strength across the life course: normative data from twelve British studies. PLoS ONE 9:e113637
Fearon K, Strasser F, Anker SD et al (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12:489–495
Yuki A, Ando F, Shimokata H (2014) Transdisciplinary approach for sarcopenia. Sarcopenia: definition and the criteria for Asian elderly people. Clin Calcium 24:1441–1448
Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–423
Anker SD, Morley JE, von Haehling S (2016) Welcome to the ICD-10 code for sarcopenia. J Cachexia Sarcopenia Muscle 7:512–514
Erkul O, Cekic AB, Cansu A et al (2022) Effects of sarcopenia on postoperative outcomes in patients who underwent gastrectomy for gastric cancer. J Surg Res 274:196–206
Ida S, Watanabe M, Yoshida N et al (2015) Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol 22:4432–4437
Wang SL, Zhuang CL, Huang DD et al (2016) Sarcopenia adversely impacts postoperative clinical outcomes following gastrectomy in patients with gastric cancer: a prospective study. Ann Surg Oncol 23:556–564
Nakashima Y, Saeki H, Nakanishi R et al (2018) Assessment of sarcopenia as a predictor of poor outcomes after esophagectomy in elderly patients with esophageal cancer. Ann Surg 267:1100–1104
Peixoto da Silva S, Santos JMO, Costa ESMP et al (2020) Cancer cachexia and its pathophysiology: links with sarcopenia, anorexia and asthenia. J Cachexia Sarcopenia Muscle 11:619–635
Ney DM, Weiss JM, Kind AJ, Robbins J (2009) Senescent swallowing: impact, strategies, and interventions. Nutr Clin Pract 24:395–413
Kawamura T, Makuuchi R, Tokunaga M et al (2018) Long-term outcomes of gastric cancer patients with preoperative sarcopenia. Ann Surg Oncol 25:1625–1632
Cruz-Jentoft AJ, Landi F, Schneider SM et al (2014) Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 43:748–759
Wang JB, Xue Z, Lu J et al (2020) Effect of sarcopenia on short- and long-term outcomes in patients with gastric neuroendocrine neoplasms after radical gastrectomy: results from a large, two-institution series. BMC Cancer 20:1002
Zhuang CL, Huang DD, Pang WY et al (2016) Sarcopenia is an independent predictor of severe postoperative complications and long-term survival after radical gastrectomy for gastric cancer: analysis from a large-scale cohort. Medicine (Baltimore) 95:e3164
Ricciardolo AA, De Ruvo N, Serra F et al (2022) Strong impact of sarcopenia as a risk factor of survival in resected gastric cancer patients: first Italian report of a bicentric study. Updates Surg 74:283–293
Dodson S, Baracos VE, Jatoi A et al (2011) Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med 62:265–279
Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8:457–465
Bertagnolli MM, Singh H (2021) Treatment of older adults with cancer—addressing gaps in evidence. N Engl J Med 385:1062–1065
Gerard S, Brechemier D, Lefort A et al (2016) Body composition and anti-neoplastic treatment in adult and older subjects—a systematic review. J Nutr Health Aging 20:878–888
Hopkins JJ, Sawyer MB (2018) Interactions of lean soft-tissue and chemotherapy toxicities in patients receiving anti-cancer treatments. Cancer Chemother Pharmacol 82:1–29
Chen F, Chi J, Liu Y et al (2022) Impact of preoperative sarcopenia on postoperative complications and prognosis of gastric cancer resection: a meta-analysis of cohort studies. Arch Gerontol Geriatr 98:104534
Vinel C, Lukjanenko L, Batut A et al (2018) The exerkine apelin reverses age-associated sarcopenia. Nat Med 24:1360–1371
Barillaro C, Liperoti R, Martone AM et al (2013) The new metabolic treatments for sarcopenia. Aging Clin Exp Res 25:119–127
Acknowledgements
This study was supported by Fujian Research and Training Grants for Young and Middle-aged Leaders in Healthcare (No.[2022]954) and Fujian third batch of "Innovation star" talent project (No.[2022]22).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Disclosures
Zi-Fang Zheng, Guang-Tan Lin, Qing Zhong, Dong Wu, Jun Lu, Jia-Bin Wang, Qi-Yue Chen, Jian-Xian Lin, Long-Long Cao, Mi Lin, Shu-Ping Zheng, Jian-Wei Xie, Chao-Hui Zheng, Chang-Ming Huang, and Ping Li have no conflicts of interest or financial ties to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file1 (JPG 253 kb)
eFigure 1. Flowchart of the patient selection process. FMUUH Fujian Medical University Union Hospital, AHPTU Affiliated Hospital of Putian University.
Supplementary file2 (TIF 6136 kb)
eFigure 2. Measurement of skeletal muscle index (SMI) in GC patients. Axial CT slice of the third lumbar vertebra (L3). Red areas indicate skeletal muscle mass. (a Typical non-sarcopenia; b Typical sarcopenia).
Supplementary file3 (TIF 14679 kb)
eFigure 3. Initial recurrence patterns after gastrectomy for gastric cancer. a All recurrence patterns (n = 204); b Non-sarcopenia recurrence patterns (n = 121); c Sarcopenia recurrence patterns (n = 83).
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zheng, ZF., Lin, GT., Zhong, Q. et al. Effect of sarcopenia on short-term and long-term outcomes of older patients with locally advanced gastric cancer: a multicenter study. Surg Endosc 38, 1151–1162 (2024). https://doi.org/10.1007/s00464-023-10638-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-023-10638-1