Sarcopenia as a prognostic factor for survival in patients with locally advanced gastroesophageal adenocarcinoma

Autoři: Christine Koch aff001;  Cornelius Reitz aff001;  Teresa Schreckenbach aff002;  Katrin Eichler aff003;  Natalie Filmann aff004;  Salah-Eddin Al-Batran aff005;  Thorsten Götze aff005;  Stefan Zeuzem aff001;  Wolf Otto Bechstein aff002;  Thomas Kraus aff006;  Jörg Bojunga aff001;  Markus Düx aff007;  Jörg Trojan aff001;  Irina Blumenstein aff001
Působiště autorů: Department of Gastroenterology, Hepatology, Endocrinology and Nutrition, University Hospital, Goethe University, Frankfurt am Main, Germany aff001;  Department of General and Visceral Surgery, University Hospital, Goethe University, Frankfurt am Main, Germany aff002;  Institute for Diagnostic and Interventional Radiology, University Hospital, Goethe University, Frankfurt am Main, Germany aff003;  Institute for Biostatistics and Mathematical Modelling, Goethe University, Frankfurt am Main, Germany aff004;  Institute for Clinical Research, (IKF), Hospital Nordwest, Frankfurt am Main, Germany aff005;  Central Institute for Radiology and Neuroradiology, Nordwest Hospital, Frankfurt am Main, Germany aff006;  Department of General and Viseral Surgery, Hospital Nordwest, Frankfurt am Main, Germany aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Background and aims

Patients with gastric cancer often show signs of malnutrition. We sought to evaluate the influence of sarcopenia in patients with locally advanced, not metastasized, gastric or gastro-esophageal junction (GEJ) cancer undergoing curative treatment (perioperative chemotherapy and surgery) on morbidity and mortality in order to identify patients in need for nutritional intervention.

Patients and methods

Two-centre study, conducted in the Frankfurt University Clinic and Krankenhaus Nordwest (Frankfurt) as part of the University Cancer Center Frankfurt (UCT). 47/83 patients were treated in the FLOT trial (NCT01216644). Patients´ charts were reviewed for clinical data. Two consecutive CT scans were retrospectively analyzed to determine the degree of sarcopenia. Survival was calculated using the Kaplan-Meier method, multivariate analysis was performed using the Cox regression.


60 patients (72.3%) were male and 23 (27.7%) female. 45 patients (54.2%) had GEJ type 1–3 and 38 (45.8%) gastric tumors, respectively. Sarcopenic patients were significantly older than non-sarcopenic patients (mean age 65.1 years vs. 59.5 years, p = 0.042), terminated the chemotherapy significantly earlier (50% vs. 22.6%, p = 0.037) and showed higher Clavien-Dindo scores, indicating more severe perioperative complications (score ≥3 43.3 vs. 17.0%, p = 0.019). Sarcopenic patients had a significantly shorter survival than non-sarcopenic patients (139.6 ± 19.5 [95% CI, 101.3–177.9] vs. 206.7 ± 13.8 [95% CI, 179.5–233.8] weeks, p = 0.004). Multivariate Cox regression analysis showed that, besides UICC stage, sarcopenia significantly influenced survival.


Sarcopenia is present in a large proportion of patients with locally advanced gastric or GEJ cancer and significantly influences tolerability of chemotherapy, surgical complications and survival.

Klíčová slova:

Cancer chemotherapy – Cancer treatment – Digestive system procedures – Gastric cancer – Regression analysis – Sarcopenia – Surgical and invasive medical procedures – Surgical oncology


1. Ronellenfitsch U, Schwarzbach M, Hofheinz R, Kienle P, Kieser M, Slanger TE, et al. Perioperative chemo(radio)therapy versus primary surgery for resectable adenocarcinoma of the stomach, gastroesophageal junction, and lower esophagus. Cochrane Database Syst Rev [Internet]. 2013 May 31 [cited 2018 May 18];(5):CD008107. Available from: doi: 10.1002/14651858.CD008107.pub2 23728671

2. Al-Batran S-E, Hofheinz RD, Pauligk C, Kopp H-G, Haag GM, Luley KB, et al. Histopathological regression after neoadjuvant docetaxel, oxaliplatin, fluorouracil, and leucovorin versus epirubicin, cisplatin, and fluorouracil or capecitabine in patients with resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4-AIO): results from the phase 2 part of a multicentre, open-label, randomised phase 2/3 trial. Lancet Oncol [Internet]. 2016 Dec [cited 2018 Jun 27];17(12):1697–708. Available from: doi: 10.1016/S1470-2045(16)30531-9 27776843

3. Al-Batran S-E, Homann N, Schmalenberg H, Kopp H-G, Haag GM, Luley KB, et al. Perioperative chemotherapy with docetaxel, oxaliplatin, and fluorouracil/leucovorin (FLOT) versus epirubicin, cisplatin, and fluorouracil or capecitabine (ECF/ECX) for resectable gastric or gastroesophageal junction (GEJ) adenocarcinoma (FLOT4-AIO): A mul. J Clin Oncol [Internet]. 2017 May 20;35(15_suppl):4004. Available from:

4. Di Fiore F, Van Cutsem E. Acute and long-term gastrointestinal consequences of chemotherapy. Best Pract Res Clin Gastroenterol [Internet]. 2009 Feb [cited 2018 May 18];23(1):113–24. Available from: doi: 10.1016/j.bpg.2008.11.016 19258191

5. Zheng Z-F, Lu J, Zheng C-H, Li P, Xie J-W, Wang J-B, et al. A Novel Prognostic Scoring System Based on Preoperative Sarcopenia Predicts the Long-Term Outcome for Patients After R0 Resection for Gastric Cancer: Experiences of a High-Volume Center. Ann Surg Oncol [Internet]. 2017 Jul 17 [cited 2018 May 17];24(7):1795–803. Available from: 28213789

6. Laviano A, Gori C, Rianda S. Sarcopenia and Nutrition. In: Advances in food and nutrition research [Internet]. 2014 [cited 2018 Jun 1]. p. 101–36. Available from:

7. Nishigori T, Tsunoda S, Obama K, Hisamori S, Hashimoto K, Itatani Y, et al. Optimal Cutoff Values of Skeletal Muscle Index to Define Sarcopenia for Prediction of Survival in Patients with Advanced Gastric Cancer. Ann Surg Oncol [Internet]. 2018 Nov 30 [cited 2019 Feb 3];25(12):3596–603. Available from: 30167910

8. Tan BHL, Brammer K, Randhawa N, Welch NT, Parsons SL, James EJ, et al. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur J Surg Oncol [Internet]. 2015 Mar [cited 2018 May 17];41(3):333–8. Available from: doi: 10.1016/j.ejso.2014.11.040 25498359

9. Tegels JJW, van Vugt JLA, Reisinger KW, Hulsewé KWE, Hoofwijk AGM, Derikx JPM, et al. Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes. J Surg Oncol [Internet]. 2015 Aug [cited 2018 May 17];112(4):403–7. Available from: doi: 10.1002/jso.24015 26331988

10. Tamandl D, Paireder M, Asari R, Baltzer PA, Schoppmann SF, Ba-Ssalamah A. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol [Internet]. 2016 May 3 [cited 2018 May 17];26(5):1359–67. Available from: 26334504

11. Fukuda Y, Yamamoto K, Hirao M, Nishikawa K, Nagatsuma Y, Nakayama T, et al. Sarcopenia is associated with severe postoperative complications in elderly gastric cancer patients undergoing gastrectomy. Gastric Cancer [Internet]. 2016 Jul 25 [cited 2018 May 17];19(3):986–93. Available from: 26407875

12. Wang S-L, Zhuang C-L, Huang D-D, Pang W-Y, Lou N, Chen F-F, et al. Sarcopenia Adversely Impacts Postoperative Clinical Outcomes Following Gastrectomy in Patients with Gastric Cancer: A Prospective Study. Ann Surg Oncol [Internet]. 2016 Feb 14 [cited 2018 May 17];23(2):556–64. Available from: 26668085

13. Zhuang C-L, Huang D-D, Pang W-Y, Zhou C-J, Wang S-L, Lou N, et al. 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) [Internet]. 2016 Mar [cited 2018 May 17];95(13):e3164. Available from:

14. Kawamura T, Makuuchi R, Tokunaga M, Tanizawa Y, Bando E, Yasui H, et al. Long-Term Outcomes of Gastric Cancer Patients with Preoperative Sarcopenia. Ann Surg Oncol [Internet]. 2018 Jun 9 [cited 2018 May 17];25(6):1625–32. Available from: 29633095

15. Palmela C, Velho S, Agostinho L, Branco F, Santos MMPC, Santos MMPC, et al. Body Composition as a Prognostic Factor of Neoadjuvant Chemotherapy Toxicity and Outcome in Patients with Locally Advanced Gastric Cancer. J Gastric Cancer [Internet]. 2017 Mar [cited 2018 May 17];17(1):74–87. Available from: 28337365

16. Kudou K, Saeki H, Nakashima Y, Edahiro K, Korehisa S, Taniguchi D, et al. Prognostic Significance of Sarcopenia in Patients with Esophagogastric Junction Cancer or Upper Gastric Cancer. Ann Surg Oncol [Internet]. 2017 Jul 21 [cited 2018 May 17];24(7):1804–10. Available from: 28224363

17. Martin L, Birdsell L, MacDonald N, Reiman T, Clandinin MT, McCargar LJ, 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 [Internet]. 2013 Apr 20 [cited 2018 May 18];31(12):1539–47. Available from: doi: 10.1200/JCO.2012.45.2722 23530101

18. Schreckenbach T, Zeller MV, El Youzouri H, Bechstein WO, Woeste G. Identification of factors predictive of postoperative morbidity and short-term mortality in older patients after colorectal carcinoma resection: A single-center retrospective study. J Geriatr Oncol [Internet]. 2018 Nov [cited 2019 Jan 10];9(6):649–58. Available from: doi: 10.1016/j.jgo.2018.05.001 29779798

19. Sakurai K, Kubo N, Tamura T, Toyokawa T, Amano R, Tanaka H, et al. Adverse Effects of Low Preoperative Skeletal Muscle Mass in Patients Undergoing Gastrectomy for Gastric Cancer. Ann Surg Oncol [Internet]. 2017 Sep 5 [cited 2018 May 17];24(9):2712–9. Available from: 28477088

20. Huang D-D, Chen X-X, Chen X-Y, Wang S-L, Shen X, Chen X-L, et al. Sarcopenia predicts 1-year mortality in elderly patients undergoing curative gastrectomy for gastric cancer: a prospective study. J Cancer Res Clin Oncol [Internet]. 2016 Nov 29 [cited 2018 May 17];142(11):2347–56. Available from: 27573385

21. Kudou K, Saeki H, Nakashima Y, Sasaki S, Jogo T, Hirose K, et al. Postoperative development of sarcopenia is a strong predictor of a poor prognosis in patients with adenocarcinoma of the esophagogastric junction and upper gastric cancer. Am J Surg [Internet]. 2018 Jul 10 [cited 2019 Feb 4]; Available from:

22. Ma B-W, Chen X-Y, Fan S-D, Zhang F-M, Huang D-D, Li B, et al. Impact of sarcopenia on clinical outcomes after radical gastrectomy for patients without nutritional risk. Nutrition [Internet]. 2019 May 24 [cited 2019 Feb 18];61:61–6. Available from: doi: 10.1016/j.nut.2018.10.025 30703570

23. TAMURA T, SAKURAI K, NAMBARA M, MIKI Y, TOYOKAWA T, KUBO N, et al. Adverse Effects of Preoperative Sarcopenia on Postoperative Complications of Patients With Gastric Cancer. Anticancer Res [Internet]. 2019 Feb 2 [cited 2019 Feb 4];39(2):987–92. Available from: doi: 10.21873/anticanres.13203 30711985

24. Tan BHL, Brammer K, Randhawa N, Welch NT, Parsons SL, James EJ, et al. Sarcopenia is associated with toxicity in patients undergoing neo-adjuvant chemotherapy for oesophago-gastric cancer. Eur J Surg Oncol [Internet]. 2015 Mar [cited 2018 May 17];41(3):333–8. Available from: doi: 10.1016/j.ejso.2014.11.040 25498359

25. Kamarajah SK, Bundred J, Tan BHL. Body composition assessment and sarcopenia in patients with gastric cancer: a systematic review and meta-analysis. Gastric Cancer [Internet]. 2019 Jan 1 [cited 2019 Feb 4];22(1):10–22. Available from: doi: 10.1007/s10120-018-0882-2 30276574

26. Ronellenfitsch U, Schwarzbach M, Hofheinz R, Kienle P, Nowak K, Kieser M, et al. Predictors of overall and recurrence-free survival after neoadjuvant chemotherapy for gastroesophageal adenocarcinoma: Pooled analysis of individual patient data (IPD) from randomized controlled trials (RCTs). Eur J Surg Oncol [Internet]. 2017 Aug [cited 2019 Apr 15];43(8):1550–8. Available from: doi: 10.1016/j.ejso.2017.05.005 28551325

27. Davies AR, Gossage JA, Zylstra J, Mattsson F, Lagergren J, Maisey N, et al. Tumor Stage After Neoadjuvant Chemotherapy Determines Survival After Surgery for Adenocarcinoma of the Esophagus and Esophagogastric Junction. J Clin Oncol [Internet]. 2014 Sep 20 [cited 2019 Apr 15];32(27):2983–90. Available from: doi: 10.1200/JCO.2014.55.9070 25071104

28. Mirkin KA, Luke FE, Gangi A, Pimiento JM, Jeong D, Hollenbeak CS, et al. Sarcopenia related to neoadjuvant chemotherapy and perioperative outcomes in resected gastric cancer: a multi-institutional analysis. J Gastrointest Oncol [Internet]. 2017 Jun [cited 2018 May 17];8(3):589–95. Available from: doi: 10.21037/jgo.2017.03.02 28736646

29. Huang D-D, Zhou C-J, Wang S-L, Mao S-T, Zhou X-Y, Lou N, et al. Impact of different sarcopenia stages on the postoperative outcomes after radical gastrectomy for gastric cancer. Surgery [Internet]. 2017 Mar [cited 2018 May 17];161(3):680–93. Available from: doi: 10.1016/j.surg.2016.08.030 27712873

30. Baracos VE, Arribas L. Sarcopenic obesity: hidden muscle wasting and its impact for survival and complications of cancer therapy. Ann Oncol [Internet]. 2018 Feb 1 [cited 2018 Jul 4];29(suppl_2):ii1–ii9. Available from: doi: 10.1093/annonc/mdx810 29506228

31. Kugimiya N, Harada E, Oka K, Kawamura D, Suehiro Y, Takemoto Y, et al. Loss of skeletal muscle mass after curative gastrectomy is a poor prognostic factor. Oncol Lett [Internet]. 2018 May 18 [cited 2019 Feb 4];16(1):1341–7. Available from: doi: 10.3892/ol.2018.8747 30061954

32. Park HS, Kim HS, Beom SH, Rha SY, Chung HC, Kim JH, 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 [Internet]. 2018 Oct 26 [cited 2019 Feb 4];25(11):3222–30. Available from: doi: 10.1245/s10434-018-6624-1 30051367

33. Evans WJ, Campbell WW. Sarcopenia and Age-Related Changes in Body Composition and Functional Capacity. J Nutr [Internet]. 1993 Feb 1 [cited 2018 Jun 1];123(suppl_2):465–8. Available from:

34. Liguori I, Russo G, Aran L, Bulli G, Curcio F, Della-Morte D, et al. Sarcopenia: assessment of disease burden and strategies to improve outcomes. Clin Interv Aging [Internet]. 2018 May [cited 2018 Jun 1];Volume 13:913–27. Available from: doi: 10.2147/CIA.S149232 29785098

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