Skip to main content

Advertisement

SpringerLink
Log in

Strong impact of sarcopenia as a risk factor of survival in resected gastric cancer patients: first Italian report of a Bicentric study

  • Original Article
  • Published:
Updates in Surgery Aims and scope Submit manuscript

Abstract

Gastric cancer (GC) accounts for 4% of all cancers in Europe. Sarcopenia is a complex syndrome characterized by a loss of muscle mass and function associated with age, often present in neoplastic patients. Recently, several studies have shown a significant association between sarcopenia and poor prognosis in various pathological conditions. The current observational retrospective study investigates the association between sarcopenia and overall survival (OS) and recurrence-free survival (RFS) in patients with GC undergoing up-front surgery with curative intent. Resected GC patients' clinical records and CT images were retrospectively assessed. The preoperative CT calculation of the skeletal muscle index (SMI) at L3 level allowed us to categorize patients as sarcopenic or not. Kaplan–Meyer and univariate and multivariate Cox regression analyses were performed to determine the difference in survival and presence of independent prognostic factors. Fifty-five patients, 28 male and 27 female, out of 298 studied for gastric cancer were enrolled in the current study from two cancer referral centers in Italy. The preoperative CT calculation of the SMI at L3 level allowed us to identify 39 patients with and 16 without sarcopenia. A statistically significant difference between the sarcopenic and non-sarcopenic groups was observed in both OS and RFS (p < 0.023; p < 0.006). Moreover, sarcopenia was strongly correlated to a higher risk of recurrence in univariate and multivariate analysis (p < 0.02). Sarcopenia can be considered a critical risk factor for survival in patients with resectable GC treated with up-front surgery. Identifying sarcopenic patients at the time of diagnosis would direct selection of patients who could benefit from early nutritional and/or physical treatments able to increase their muscle mass and possibly improve the prognosis. More extensive multicenter studies are needed to address this issue.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J et al (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49:1374–1403. https://doi.org/10.1016/j.ejca.2012.12.027

    Article  CAS  PubMed  Google Scholar 

  2. Anderson LA, Tavilla A, Brenner H et al (2015) Survival for oesophageal, stomach and small intestine cancers in Europe 1999–2007: Results from EUROCARE-5. Eur J Cancer 51:2144–2157. https://doi.org/10.1016/j.ejca.2015.07.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fielding RA, Vellas B, Evans WJ et al (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12:249–256. https://doi.org/10.1016/j.jamda.2011.01.003

    Article  PubMed  Google Scholar 

  4. Tian S, Xu Y (2016) Association of sarcopenic obesity with the risk of all-cause mortality: a meta-analysis of prospective cohort studies. Geriatr Gerontol Int 16:155–166. https://doi.org/10.1111/ggi.12579

    Article  PubMed  Google Scholar 

  5. Hanaoka M, Yasuno M, Ishiguro M et al (2017) Morphologic change of the psoas muscle as a surrogate marker of sarcopenia and predictor of complications after colorectal cancer surgery. Int J Colorectal Dis 32:847–856. https://doi.org/10.1007/s00384-017-2773-0

    Article  PubMed  Google Scholar 

  6. Mourtzakis M, Prado CMM, Lieffers JR et al (2008) A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 33:997–1006 https://doi.org/10.1139/H08-075

  7. Shen W, Punyanitya M, Wang Z et al (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol 97:2333–2338. https://doi.org/10.1152/japplphysiol.00744.2004

    Article  PubMed  Google Scholar 

  8. Lieffers JR, Bathe OF, Fassbender K et al (2012) Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer 107:931–936. https://doi.org/10.1038/bjc.2012.350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Reisinger KW, van Vugt JLA, Tegels JJW et al (2015) Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg 261:345–352. https://doi.org/10.1097/SLA.0000000000000628

    Article  PubMed  Google Scholar 

  10. Voron T, Tselikas L, Pietrasz D et al (2015) Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma. Ann Surg 261:1173–1183. https://doi.org/10.1097/SLA.0000000000000743

    Article  PubMed  Google Scholar 

  11. 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. https://doi.org/10.1002/jso.23862

    Article  PubMed  Google Scholar 

  12. Zhuang C-L, Huang D-D, Pang W-Y 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. https://doi.org/10.1097/MD.0000000000003164

    Article  Google Scholar 

  13. Huang D-D, Chen X-X, Chen X-Y et al (2016) Sarcopenia predicts 1-year mortality in elderly patients undergoing curative gastrectomy for gastric cancer: a prospective study. J Cancer Res Clin Oncol 142:2347–2356. https://doi.org/10.1007/s00432-016-2230-4

    Article  CAS  PubMed  Google Scholar 

  14. Aoyama T, Sato T, Segami K et al (2016) Risk factors for the loss of lean body mass after gastrectomy for gastric cancer. Ann Surg Oncol 23:1963–1970. https://doi.org/10.1245/s10434-015-5080-4

    Article  PubMed  Google Scholar 

  15. Sakurai K, Kubo N, Tamura T et al (2017) Adverse effects of low preoperative skeletal muscle mass in patients undergoing gastrectomy for gastric cancer. Ann Surg Oncol 24:2712–2719. https://doi.org/10.1245/s10434-017-5875-6

    Article  PubMed  Google Scholar 

  16. (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. Switzerland

  17. Marchet A, Mocellin S, Ambrosi A et al (2007) The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 245:543–552. https://doi.org/10.1097/01.sla.0000250423.43436.e1

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213. https://doi.org/10.1097/01.sla.0000133083.54934.ae

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mitsiopoulos N, Baumgartner RN, Heymsfield SB et al (1998) Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol 85:115–122. https://doi.org/10.1152/jappl.1998.85.1.115

    Article  CAS  PubMed  Google Scholar 

  20. Prado CMM, 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. https://doi.org/10.1016/S1470-2045(08)70153-0

    Article  PubMed  Google Scholar 

  21. O’Brien S, Twomey M, Moloney F et al (2018) Sarcopenia and post-operative morbidity and mortality in patients with gastric cancer. J Gastric Cancer 18:242–252. https://doi.org/10.5230/jgc.2018.18.e25

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kudou K, Saeki H, Nakashima Y et al (2017) Prognostic significance of sarcopenia in patients with esophagogastric junction cancer or upper gastric cancer. Ann Surg Oncol 24:1804–1810. https://doi.org/10.1245/s10434-017-5811-9

    Article  PubMed  Google Scholar 

  23. Zheng Z-F, Lu J, Zheng C-H et al (2017) 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 24:1795–1803. https://doi.org/10.1245/s10434-017-5813-7

    Article  PubMed  Google Scholar 

  24. Zhou C-J, Zhang F-M, Zhang F-Y et al (2017) Sarcopenia: a new predictor of postoperative complications for elderly gastric cancer patients who underwent radical gastrectomy. J Surg Res 211:137–146. https://doi.org/10.1016/j.jss.2016.12.014

    Article  PubMed  Google Scholar 

  25. Huang D-D, Zhou C-J, Wang S-L et al (2017) Impact of different sarcopenia stages on the postoperative outcomes after radical gastrectomy for gastric cancer. Surgery 161:680–693. https://doi.org/10.1016/j.surg.2016.08.030

    Article  PubMed  Google Scholar 

  26. Wang S-L, Zhuang C-L, Huang D-D 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. https://doi.org/10.1245/s10434-015-4887-3

    Article  PubMed  Google Scholar 

  27. Tegels JJW, van Vugt JLA, Reisinger KW et al (2015) Sarcopenia is highly prevalent in patients undergoing surgery for gastric cancer but not associated with worse outcomes. J Surg Oncol 112:403–407. https://doi.org/10.1002/jso.24015

    Article  PubMed  Google Scholar 

  28. Cruz-Jentoft AJ, Bahat G, Bauer J et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:16–31. https://doi.org/10.1093/ageing/afy169

    Article  PubMed  Google Scholar 

  29. Nishigori T, Tsunoda S, Okabe H et al (2016) Impact of sarcopenic obesity on surgical site infection after laparoscopic total gastrectomy. Ann Surg Oncol 23:524–531. https://doi.org/10.1245/s10434-016-5385-y

    Article  PubMed  Google Scholar 

  30. Spira D, Norman K, Nikolov J et al (2016) Prevalence and definition of sarcopenia in community dwelling older people. Data from the Berlin aging study II (BASE-II). Z Gerontol Geriatr 49:94–99. https://doi.org/10.1007/s00391-015-0886-z

    Article  CAS  PubMed  Google Scholar 

  31. Iannuzzi-Sucich M, Prestwood KM, Kenny AM (2002) Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J Gerontol A Biol Sci Med Sci 57:M772–M777. https://doi.org/10.1093/gerona/57.12.m772

    Article  PubMed  Google Scholar 

  32. Kim Y-S, Lee Y, Chung Y-S et al (2012) Prevalence of sarcopenia and sarcopenic obesity in the Korean population based on the Fourth Korean National Health and Nutritional Examination Surveys. J Gerontol A Biol Sci Med Sci 67:1107–1113. https://doi.org/10.1093/gerona/gls071

    Article  PubMed  Google Scholar 

  33. 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. https://doi.org/10.1146/annurev-med-061509-131248

    Article  CAS  PubMed  Google Scholar 

  34. Aoi W, Naito Y, Takagi T et al (2013) A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise. Gut 62:882–889. https://doi.org/10.1136/gutjnl-2011-300776

    Article  CAS  PubMed  Google Scholar 

  35. Palmela C, Velho S, Agostinho L et al (2017) Body composition as a prognostic factor of neoadjuvant chemotherapy toxicity and outcome in patients with locally advanced gastric cancer. J Gastric Cancer 17:74–87. https://doi.org/10.5230/jgc.2017.17.e8

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lee JS, Kim YS, Kim EY, Jin W (2018) Prognostic significance of CT-determined sarcopenia in patients with advanced gastric cancer. PLoS ONE 13:e0202700. https://doi.org/10.1371/journal.pone.0202700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Awad S, Tan BH, Cui H et al (2012) Marked changes in body composition following neoadjuvant chemotherapy for oesophagogastric cancer. Clin Nutr 31:74–77. https://doi.org/10.1016/j.clnu.2011.08.008

    Article  PubMed  Google Scholar 

  38. Feliciano EMC, Kroenke CH, Meyerhardt JA et al (2017) Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer: results from the C SCANS study. JAMA Oncol 3:e172319. https://doi.org/10.1001/jamaoncol.2017.2319

    Article  PubMed  Google Scholar 

  39. Szor DJ, Dias AR, Pereira MA et al (2018) Prognostic role of neutrophil/lymphocyte ratio in resected gastric cancer: a systematic review and meta-analysis. Clinics (Sao Paulo) 73:e360. https://doi.org/10.6061/clinics/2018/e360

    Article  Google Scholar 

  40. Goodpaster BH, Park SW, Harris TB et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61:1059–1064. https://doi.org/10.1093/gerona/61.10.1059

    Article  PubMed  Google Scholar 

  41. Martin L, Birdsell L, Macdonald N et al (2013) Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol Off J Am Soc Clin Oncol 31:1539–1547. https://doi.org/10.1200/JCO.2012.45.2722

    Article  Google Scholar 

  42. Hayashi N, Ando Y, Gyawali B et al (2016) Low skeletal muscle density is associated with poor survival in patients who receive chemotherapy for metastatic gastric cancer. Oncol Rep 35:1727–1731. https://doi.org/10.3892/or.2015.4475

    Article  CAS  PubMed  Google Scholar 

  43. Sjøblom B, Grønberg BH, Wentzel-Larsen T et al (2016) Skeletal muscle radiodensity is prognostic for survival in patients with advanced non-small cell lung cancer. Clin Nutr 35:1386–1393. https://doi.org/10.1016/j.clnu.2016.03.010

    Article  PubMed  Google Scholar 

  44. Antoun S, Lanoy E, Iacovelli R et al (2013) Skeletal muscle density predicts prognosis in patients with metastatic renal cell carcinoma treated with targeted therapies. Cancer 119:3377–3384. https://doi.org/10.1002/cncr.28218

    Article  PubMed  Google Scholar 

Download references

Funding

The authors did not receive support from any organization for the submitted work.

Author information

Author notes

  1. A. A. Ricciardolo, F. Serra, G. Missori, S. Fenocchi, E. G. Rossi, L. Sorrentino, N. Cautero & R. Gelmini

    Present address: Department of General and Specialistic Surgery, Unit of General, Emergency and Oncological Surgery, Policlinico, AOU of Modena University of Modena and Reggio Emilia, Via del Pozzo 71, 41125, Modena, Italy

  2. F. Prampolini & A. Pecchi

    Present address: Department of Radiology, AOU of Modena, University of Modena and Reggio Emilia, via del Pozzo 71, 41125 Modena Italy, Modena, Italy

  3. L. Solaini & G. Ercolani

    Present address: Department Of Medical and Surgical Sciences, University of Bologna, Morgagni-Pierantoni Hospital, Forli, Italy

  4. S. Battisti

    Present address: Istituto Scientifico Romagnolo Per Lo Studio E La Cura Dei Tumori (IRST) IRCCS, Meldola, Italy

  5. M. Salati & A. Spallanzani

    Present address: Department of Oncology, AOU of Modena, University of Modena and Reggio Emilia, via del Pozzo 71, 41125 Modena Italy, Modena, Italy

  6. A. A. Ricciardolo and N. De Ruvo equally contributed as first authors.

Authors and Affiliations

  1. Department of General and Specialistic Surgery, Unit of General, Emergency and Oncological Surgery, Policlinico, AOU of Modena University of Modena and Reggio Emilia, Via del Pozzo 71, 41125, Modena, Italy

    N. De Ruvo

Authors
  1. A. A. Ricciardolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. De Ruvo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Serra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Prampolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Solaini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Battisti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Missori
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Fenocchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. E. G. Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. L. Sorrentino
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. M. Salati
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. Spallanzani
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. N. Cautero
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. A. Pecchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. G. Ercolani
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. R. Gelmini
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Protocol/project development: NDR, AAR, AP, AS, GE, RG. Data collection or management: AAR, GM, SF, EGR. Data analysis: NDR, FP, FS, MS, LS, SB. Manuscript writing/editing: AAR, FS, NC, LS.

Corresponding author

Correspondence to N. De Ruvo.

Ethics declarations

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Ethical approval

All procedures performed in the study were in accordance with ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

For this type of study formal consent is not required by local regulations.

Consent for publication

All authors give their consent for publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ricciardolo, A.A., De Ruvo, N., Serra, F. et al. 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 (2022). https://doi.org/10.1007/s13304-021-01175-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13304-021-01175-4

Keywords

Search

Navigation