Abstract
Background
The impact of postoperative sarcopenia on the Textbook Oncological Outcome (TOO) in locally advanced gastric cancer (LAGC) remains uncertain. This study investigates the relationship between sarcopenia and TOO, explores its long-term prognostic value, and develops a prognostic model incorporating sarcopenia and TOO for survival prediction.
Methods
We performed a retrospective analysis of clinical and pathological data from patients with LAGC who underwent radical surgery at two Chinese tertiary referral hospitals. Sarcopenia was defined as an SMI < 36.4 cm2/m2 in males and < 28.4 cm2/m2 in females. TOO was defined as the addition of perioperative chemotherapy to the textbook outcomes (TO). A nomogram was developed to predict postoperative overall survival (OS) and recurrence-free survival (RFS) in LAGC patients.
Results
The study included 972 patients with LAGC. The overall TOO achievement rate was 67.1%. The TOO achievement rate was significantly higher in patients non-sarcopenia compared to those with sarcopenia (68.9% vs. 61.1%, P = 0.031). Logistic regression revealed that age ≥ 65, high ASA score, and sarcopenia were independent risk factors for TOO failure. Cox regression analysis identified TOO, sarcopenia, tumor size, differentiation, vascular invasion, pT stage, and pN stage as independent predictors of OS and RFS. Nomogram models based on sarcopenia and TOO accurately predicted the 3-year and 5-year OS and RFS.
Conclusion
Preoperative sarcopenia was an independent predictor of TOO implementation. A prognostic prediction model that integrates preoperative sarcopenia and TOO, which outperforms the current staging system, can aid clinicians in effectively assessing the prognosis of patients with LAGC.
Similar content being viewed by others
References
Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
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
Fearon K, Strasser F, Anker SD et al (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12:489–495
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
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
Levy J, Gupta V, Amirazodi E et al (2022) Textbook outcome and survival in patients with gastric cancer: an analysis of the population registry of esophageal and stomach tumours in ontario (PRESTO). Ann Surg 275:140–148
Chen JY, Lin GT, Chen QY et al (2022) Textbook outcome, chemotherapy compliance, and prognosis after radical gastrectomy for gastric cancer: a large sample analysis. Eur J Surg Oncol 48:2141–2148
Zhang Q, Zhuang LP, Liu ZK (2021) Comment on “Textbook outcome and survival in patients with gastric cancer: an analysis of the population registry of esophageal and stomach tumors in ontario (PRESTO).” Ann Surg 274:e885–e886
Dal Cero M, Román M, Grande L et al (2022) Textbook outcome and survival after gastric cancer resection with curative intent: a population-based analysis. Eur J Surg Oncol 48:768–775
Sędłak K, Rawicz-Pruszyński K, Mlak R et al (2023) Textbook oncological outcome in European GASTRODATA. Ann Surg 278:823–831
Wu DH, Liao CY, Wang DF et al (2023) Textbook outcomes of hepatocellular carcinoma patients with sarcopenia: a multicenter analysis. Eur J Surg Oncol 49:802–810
Zhong Q, Huang JB, Lu J et al (2024) Predictive value of a new muscle parameter in patients with resectable gastric cancer: a pooled analysis of three prospective trials. Ann Surg Oncol 31:3005–3016
Japanese Gastric Cancer Treatment Guidelines (2021) Japanese gastric cancer treatment guidelines. Gastric Cancer 2023(26):1–25
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
Zheng ZF, Lin GT, Zhong Q et al (2024) 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
Ajani JA, D’Amico TA, Barzi A et al (2024) Gastric cancer, version 1.2024, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 20:167–192
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
Noh SH, Park SR, Yang HK et al (2014) 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 15:1389–1396
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 CMM, Liefers 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
Levy J, Gupta V, Amirazodi E et al (2020) Gastrectomy case volume and textbook outcome: an analysis of the population registry of esophageal and stomach tumours of Ontario (PRESTO). Gastric Cancer 23:391–402
Wu C, Wang N, Zhou H et al (2020) Effects of neoadjuvant chemotherapy toxicity and postoperative complications on short-term and long-term outcomes after curative resection of gastric cancer. J Gastrointest Surg 24:1278–1289
van der Zanden V, van Soolingen NJ, Viddeleer AR et al (2022) Loss of skeletal muscle density during neoadjuvant chemotherapy in older women with advanced stage ovarian cancer is associated with postoperative complications. Eur J Surg Oncol 48:896–902
Motoori M, Fujitani K, Sugimura K et al (2018) Skeletal muscle loss during neoadjuvant chemotherapy is an independent risk factor for postoperative infectious complications in patients with advanced esophageal cancer. Oncology 95:281–287
Cohen S, Gal J, Freifeld Y et al (2021) Nutritional status impairment due to neoadjuvant chemotherapy predicts post-radical cystectomy complications. Nutrients 13:4471
den Boer RB, Jones KI, Ash S et al (2020) Impact on postoperative complications of changes in skeletal muscle mass during neoadjuvant chemotherapy for gastro-oesophageal cancer. BJS Open 4:847–854
Luo L, Fan Y, Wang Y et al (2024) Prevalence and clinical outcomes of sarcopenia in patients with esophageal, gastric or colorectal cancers receiving preoperative neoadjuvant therapy: a meta-analysis. Asia Pac J Oncol Nurs 11:100436
Kondrup J, Rasmussen HH, Hamberg O et al (2003) Nutritional risk screening (NRS 2002): a new method based on an analysis of controlled clinical trials [J]. Clin Nutr 22:321–336
Kulshrestha S, Bunn C, Patel PM et al (2020) Textbook oncologic outcome is associated with increased overall survival after esophagectomy. Surgery 168:953–961
Sędłak K, Rawicz-Pruszyński K, Mlak R et al (2022) Union is strength: textbook outcome with perioperative chemotherapy compliance decreases the risk of death in advanced gastric cancer patients. Eur J Surg Oncol 48:356–361
Kolfschoten NE, Kievit J, Gooiker GA et al (2013) Focusing on desired outcomes of care after colon cancer resections; hospital variations in ‘textbook outcome.’ Eur J Surg Oncol 39:156–163
Cibulas MA, Avila A, Mahendra AM et al (2022) Impact of textbook oncologic outcome attainment on survival after gastrectomy: a review of the national cancer database. Ann Surg Oncol 29:8239–8248
Sweigert PJ, Eguia E, Baker MS et al (2020) Assessment of textbook oncologic outcomes following pancreaticoduodenectomy for pancreatic adenocarcinoma. J Surg Oncol 121:936–944
Peng PD, van Vledder MG, Tsai S et al (2011) Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB (Oxford) 13:439–446
Joglekar S, Asghar A, Mott SL et al (2015) Sarcopenia is an independent predictor of complications following pancreatectomy for adenocarcinoma. J Surg Oncol 111:771–775
Tamura T, Sakurai K, Nambara M et al (2019) Adverse effects of preoperative sarcopenia on postoperative complications of patients with gastric cancer. Anticancer Res 39:987–992
Chen XY, Li B, Ma BW et al (2019) Sarcopenia is an effective prognostic indicator of postoperative outcomes in laparoscopic-assisted gastrectomy. Eur J Surg Oncol 45:1092–1098
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
McLeay SC, Morrish GA, Kirkpatrick CM et al (2012) The relationship between drug clearance and body size: systematic review and meta-analysis of the literature published from 2000 to 2007. Clin Pharmacokinet 51:319–330
Antoun S, Borget I, Lanoy E (2013) Impact of sarcopenia on the prognosis and treatment toxicities in patients diagnosed with cancer. Curr Opin Support Palliat Care 7:383–389
Zhang FM, Zhang XZ, Zhu GL et al (2022) Impact of sarcopenia on clinical outcomes of patients with stage I gastric cancer after radical gastrectomy: a prospective cohort study. Eur J Surg Oncol 48:541–547
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
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
Wang S, Xu L, Wang Q et al (2019) Postoperative complications and prognosis after radical gastrectomy for gastric cancer: a systematic review and meta-analysis of observational studies. World J Surg Oncol 17:52
Li J, Zhang Y, Hu DM et al (2020) Impact of postoperative complications on long-term outcomes of patients following surgery for gastric cancer: a systematic review and meta-analysis of 64 follow-up studies. Asian J Surg 43:719–729
Kubota T, Hiki N, Sano T et al (2014) Prognostic significance of complications after curative surgery for gastric cancer. Ann Surg Oncol 21:891–898
Jin LX, Sanford DE, Squires MH et al (2016) Interaction of postoperative morbidity and receipt of adjuvant therapy on long-term survival after resection for gastric adenocarcinoma: results from the U.S. gastric cancer collaborative. Ann Surg Oncol 23:2398–2408
Tan BH, Brammer K, Randhawa N et al (2015) Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur J Surg Oncol 41:333–338
Barillaro C, Liperoti R, Martone AM et al (2013) The new metabolic treatments for sarcopenia. Aging Clin Exp Res 25:119–127
Zhu LY, Chan R, Kwok T et al (2019) Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: a randomized controlled trial. Age Ageing 48:220–228
Mori H, Tokuda Y (2018) Effect of whey protein supplementation after resistance exercise on the muscle mass and physical function of healthy older women: a randomized controlled trial. Geriatr Gerontol Int 18:1398–1404
Chen X, Xu Y, Cao X et al (2015) Associations of Il-1 family-related polymorphisms with gastric cancer risk and the role of Mir-197 In Il-1f5 expression. Medicine (Baltimore) 94:e1982
Acknowledgements
This study was supported by the Fujian Research and Training Grants for Young and Middle-aged Leaders in Healthcare (No.[2022] 954).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Disclosures
Qing Zhong, Zi-Fang Zheng, Dong Wu, Zhi-Xin Shang-Guan, Zhi-Yu Liu, Yi-Ming Jiang, Jian-Xian Lin, Jia-Bin Wang, Qi-Yue Chen, Jian-Wei Xie, Wei Lin, 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.
464_2024_11397_MOESM1_ESM.jpg
Supplementary file1 (JPG 249 KB)—Flowchart of the patient selection process. FMUUH: Fujian Medical University Union Hospital; AHPTU: Affiliated Hospital of Putian University
464_2024_11397_MOESM2_ESM.jpg
Supplementary file2 (JPG 164 KB)—Measurement of skeletal muscle index (SMI) in GC patients. Axial computed tomography slice of the third lumbar vertebra (L3). Red areas indicate skeletal muscle mass. (a: Typical non-sarcopenia; b: Typical sarcopenia)
464_2024_11397_MOESM3_ESM.jpg
Supplementary file3 (JPG 204 KB)—Calibration plot of the nomogram for (A) 3-year and (B) 5-year OS; Calibration plot of the nomogram for (C) 3-year and (D) 5-year RFS
464_2024_11397_MOESM4_ESM.jpg
Supplementary file4 (JPG 164 KB)—Decision curve analysis of the nomogram and pTN for the survival prediction of patients with GC. A, B 3-year and 5-year OS. C, D 3-year and 5-year RFS
464_2024_11397_MOESM5_ESM.jpg
Supplementary file5 (JPG 109 KB)—Time-dependent receiver operating characteristic (ROC) curves for the nomogram and pTN for the prediction. The horizontal axis represents year after surgery, and the vertical axis represents the estimated area under the ROC curve for survival at the time of interest. A: OS, B: RFS
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
Zhong, Q., Zheng, ZF., Wu, D. et al. Textbook oncological outcome of locally advanced gastric cancer patients with preoperative sarcopenia: a multicenter clinical study. Surg Endosc 39, 356–367 (2025). https://doi.org/10.1007/s00464-024-11397-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-024-11397-3