Sarcopenia, sarcopenic obesity, myosteatosis as factors of poor prognosis in gastrointestinal tract tumors: sistematic review

Cover Page

Cite item

Full Text

Abstract

Background. Gastrointestinal (GI) tract cancer includes a broad spectrum of tumors with generally high prevalence and poor prognosis. Over the past decade sarcopenia (skeletal muscle depletion), myosteatosis, sarcopenic obesity were all shown to have a negative prognostic impact in patients with various malignancies. However, the role of myosteatosis in patients with GI tumors remains controversial.

Aim. To summarize recent literature regarding the impact of myosteatosis on the surgical treatment of patients with GI malignancies.

Materials and methods. PubMed, Cochrane Library and ClinicalTrials.gov databases were searched for relevant original studies published between Jan. 2011 and Dec. 2021. The risk of bias of the included studies was assessed using Newcastle-Ottawa Scale (NOS).

Results. 34 studies comprising 15 295 patients were included. Patients with myosteatosis had significantly poorer overall survival (hazard ratio 0,506, 95% confidence interval 0,431–0,595; p<0,05). There was no significant influence of myosteatosis on recurrence-free survival (hazard ratio 0,658, 95% confidence interval 0,389–1,112; p<0,05). Myosteatosis was significantly associated with the occurrence of major postoperative complications in 6 studies. However, only 3 studies supported the impact of myosteatosis on mortality.

Conclusion. This meta-analysis demonstrates that patients with preoperative myosteatosis have poor long-term survival following treatment for GI malignancy. Therefore, myosteatosis might be used as a prognostic tool. However, more studies with standardized definitions and cut-offs are required.

About the authors

Vladimir K. Lyadov

Russian Medical Academy of Continuous Professional Education; Novokuznetsk State Institute for Postgraduate Medical Education – branch of the Russian Medical Academy of Continuous Professional Education; City Clinical Oncology Hospital №1

Author for correspondence.
Email: vlyadov@gmail.com
ORCID iD: 0000-0002-7281-3591
SPIN-code: 5385-7889

D. Sci. (Med.)

Russian Federation, Moscow; Novokuznetsk; Moscow

Tatyana S. Dikova

Russian Medical Academy of Continuous Professional Education

Email: dikovatatyanasergeevna@gmail.com
SPIN-code: 7597-3600

Resident

Russian Federation, Moscow

Alina Yu. Zatsepina

Sechenov First Moscow State Medical University (Sechenov University)

Email: zatsepina.alina@gmail.com

Resident

Russian Federation, Moscow

Dmitrii V. Ivashchenko

Russian Medical Academy of Continuous Professional Education; Penza Institute for Postgraduate Medical Education – branch of the Russian Medical Academy of Continuous Professional Education

Email: dvi1991@yandex.ru
SPIN-code: 9435-7794

D. Sci. (Med.)

Russian Federation, Moscow; Penza

References

  1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209-49. doi: 10.3322/caac.21660
  2. Каприн А.Д., Старинский В.В., Петрова Г.В. Злокачественные новообразования в России в 2018 году (заболеваемость и смертность). М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «НМИЦ радиологии» Минздрава России, 2019 [Kaprin AD, Starinskiy VV, Petrova GV. Zlokachestvennye novoobrazovaniia v Rossii v 2018 godu (zabolevaemost' i smertnost'). Moscow: Herzen Moscow Scientific and Research Oncological Institute, 2019 (in Russian)].
  3. Fearon K, Arends J, Baracos V. Understanding the mechanisms and treatment options in cancer cachexia. Nat Rev Clin Oncol. 2013;10(2):90-9. doi: 10.1038/nrclinonc.2012.209
  4. Hanaoka M, Yasuno M, Ishiguro M. Morphologic change of the psoas muscle as a surrogate marker of sarcopenia and predictor of complications after colorectal cancer surgery. Int J Colorectal Dis. 2017;32(6):847-56. doi: 10.1007/s00384-017-2773-0
  5. Pamoukdjian F, Bouillet T, Lévy V, et al. Prevalence and predictive value of pre-therapeutic sarcopenia in cancer patients: A systematic review. Clin Nutr. 2018;37(4):1101-13.
  6. Williams GR, Rier HN, McDonald A, Shachar SS. Sarcopenia and aging in cancer. J Geriatr Oncol. 2019;10(3):374-77. doi: 10.1016/j.jgo.2018.10.009
  7. Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol Biol Sci Med Sci. 2005;60(3):324-33. doi: 10.1093/gerona/60.3.324
  8. Aubrey J, Esfandiari N, Baracos VE, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol (Oxf). 2014;210(3):489-97. doi: 10.1111/apha.12224
  9. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264-9. doi: 10.7326/0003-4819-151-4-200908180-00135
  10. OpenMeta [Analyst]. Available at: http://www.cebm.brown.edu/openmeta. Accessed: 06.02.2022.
  11. Wells GA, Shea B, O’Connell D, et al. The Newcastle Ottawa Scale (NOS) for Assessing the Quality of Non-randomised Studies in Meta-analyses. Ottawa Hospital Research Institue: University of Ottawa, Ottawa, Ontario, Canada; 2001. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford. Accessed: 06.02.2022.
  12. Gabiatti CTB, Martins MCL, Miyazaki DL, et al. Myosteatosis in a systemic inflammation-dependent manner predicts favorable survival outcomes in locally advanced esophageal cancer. Cancer Med. 2019;8(16):6967-76. doi: 10.1002/cam4.2593
  13. Srpcic M, Jordan T, Popuri K, Sok M. Sarcopenia and myosteatosis at presentation adversely affect survival after esophagectomy for esophageal cancer. Radiol Oncol. 2020;54(2):237-46. doi: 10.2478/raon-2020-0016
  14. Zhuang CL, Shen X, Huang YY, et al. Myosteatosis predicts prognosis after radical gastrectomy for gastric cancer: a propensity score-matched analysis from a large-scale cohort. Surgery. 2019;166:297-304. doi: 10.1016/j.surg.2019.03.020
  15. Murnane LC, Forsyth AK, Koukounaras J, et al. Myosteatosis predicts higher complications and reduced overall survival following radical oesophageal and gastric cancer surgery. Eur J Surg Oncol. 2021;47(9):2295-303. doi: 10.1016/j.ejso.2021.02.008
  16. Stretch C, Aubin JM, Mickiewicz B, et al. Sarcopenia and myosteatosis are accompanied by distinct biological profiles in patients with pancreatic and periampullary adenocarcinomas. PloS One. 2018;13(5):e0196235. doi: 10.1371/journal.pone.0196235
  17. Rollins KE, Tewari N, Ackner A, et al. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin Nutr. 2016;35:1103-9.
  18. Van Dijk DPJ, Bakers FCH, Sanduleanu S, et al. Myosteatosis predicts survival after surgery for periampullary cancer: a novel method using MRI. HPB (Oxford). 2018;20(8):715-20.
  19. Sueda T, Takahasi H, Nishimura J, et al. Impact of Low Muscularity and Myosteatosis on Long-term Outcome After Curative Colorectal Cancer Surgery: A Propensity Score-Matched Analysis. Dis Colon Rectum. 2018;61(3):v364-74.
  20. Aro R, Mäkäräinen-Uhlbäck E, Ämmälä N, et al. The impact of sarcopenia and myosteatosis on postoperative outcomes and 5-year survival in curatively operated colorectal cancer patients – A retrospective register study. Eur J Surg Oncol. 2020;46(9):1656-62. doi: 10.1016/j.ejso.2020.03.206
  21. Hopkins JJ, Reif RL, Bigam DL, et al. The impact of muscle and adipose tissue on long-term survival in patients with stage I to III colorectal cancer. Dis Colon Rectum. 2019;62:549-60. doi: 10.1097/DCR.0000000000001352
  22. Pozzuto L, Silveira MN, Mendes MCS, et al. Myosteatosis Differentially Affects the Prognosis of Non-Metastatic Colon and Rectal Cancer Patients: An Exploratory Study. Front Oncol. 2021;11:762444. doi: 10.3389/fonc.2021.762444
  23. Carcamo L, Penailillo E, Bellolio F, et al. Computed tomography-measured body composition parameters do not influence survival in non-metastatic colorectal cancer. ANZ J Surg. 2021;91(5):E298-306. doi: 10.1111/ans.16708
  24. Blauwhoff-Buskermolen S, Versteeg IS, Van der Schuerenmae D, 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.
  25. Charette N, Vandeputte C, Ameye L, et al. Prognostic value of adipose tissue and muscle mass in advanced colorectal cancer: a post hoc analysis of two non-randomized phase II trials. BMC Cancer. 2019;19:134. doi: 10.1186/s12885-019-5319-8
  26. Dolan RD, Almasaudi AS, Dieu LB. The relationship between computed tomography-derived body composition, systemic inflammatory response, and survival in patients undergoing surgery for colorectal cancer. J Cachexia Sarcopenia Muscle. 2019;10:111-22. doi: 10.1002/jcsm.12357
  27. Kroenke CH, Prado CM, Meyerhardt JA, et al. Muscle radiodensity and mortality in patients with colorectal cancer. Cancer. 2018;124:3008-15. DOI:10.1002/ cncr.31405
  28. Okumura S, Kaido T, Hamaguchi Y, et al. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery. 2015;157(6):1088-98.
  29. Hamaguchi Y, Kaido T, Okumura S, et al. Preoperative visceral adiposity and muscularity predict poor outcomes after hepatectomy for hepatocellular carcinoma. Liver Cancer. 2019;8:92-109. doi: 10.1159/000488779
  30. Okumura S, Kaido T, Hamaguchi Y, et al. Impact of skeletal muscle mass, muscle quality, and visceral adiposity on outcomes following resection of intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2017;24:1037-45. doi: 10.1245/s10434-016-5668-3
  31. McSorley ST, Black DH, Horgan PG, et al. The relationship between tumour stage, systemic inflammation, body composition and survival in patients with colorectal cancer. Clin Nutr. 2018;37:1279-85. doi: 10.1016/j.clnu.2017.05.017
  32. Van Rijssen LB, van Huijgevoort NC, Coelen RJ, et al. Skeletal muscle quality is associated with worse survival after pancreatoduodenectomy for periampullary, nonpancreatic cancer. Ann Surg Oncol. 2017;24:272–280. doi: 10.1245/s10434-016-5495-6
  33. Chakedis J, Spolverato G, Beal EW, et al. Pre-operative sarcopenia identifies patients at risk for poor survival after resection of biliary tract cancers. J Gastrointest Surg. 2018;22:1697-708. doi: 10.1007/s11605-018-3802-1
  34. Van Vugt JLA, Gaspersz MP, Vugts J, et al. Low skeletal muscle density Is associated with early death in patients with perihilar cholangiocarcinoma regardless of subsequent treatment. Dig Surg. 2019;36:144–152. doi: 10.1159/000486867
  35. Fujiwara N, Nakagawa H, KudoY, et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J Hepatol. 2015;63:131-40. doi: 10.1016/j.jhep.2015.02.031
  36. Kaibori M, Ishizaki M, Iida H, et al. Effect of intramuscular adipose tissue content on prognosis in patients undergoing hepatocellular carcinoma resection. J Gastrointest Surg. 2015;19(7):1315-23.
  37. Hamaguchi Y, Kaido T, Okumura S, et al. Preoperative visceral adiposity and muscularity predict poor outcomes after hepatectomy for hepatocellular carcinoma. Liver Cancer. 2019;8:92-109. doi: 10.1159/000488779.37
  38. Tamandl D, Paireder M, Asari R, et al. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol. 2016;26:1359-67. doi: 10.1007/s00330-015-3963-1
  39. Hayashi N, Ando Y, Gyawali B, et al. Low skeletal muscle density is associated with poor survival in patients who receive chemotherapy for metastatic gastric. Cancer Oncol Rep. 2016;35(3):1727-31.
  40. Park HS, Kim HS, Beom SH, 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. 2018;25(11):3222-30. doi: 10.1245/s10434-018-6624-1
  41. Dohzono S, Sasaoka R, Takamatsu K, et al. Prognostic value of paravertebral muscle density in patients with spinal metastases from gastrointestinal cancer. Support Care Cancer. 2019;27(4):1207-13.
  42. Dijksterhuis WPM, Pruijt MJ, van der Woude SO, et al. Association between body composition, survival, and toxicity in advanced esophagogastric cancer patients receiving palliative chemotherapy. J Cachexia Sarcopenia Muscle. 2019;10(1):199-206. doi: 10.1002/jcsm.12371
  43. Malietzis G, Currie AC, Athanasiou T, et al. Influence of body composition profile on outcomes following colorectal cancer surgery. Br J Surg. 2016;103:572-80.doi: 10.1002/bjs.10075
  44. Van Baar H, Beijer S, Bours MJL, et al. Low radiographic muscle density is associated with lower overall and disease-free survival in early-stage colorectal cancer patients. J Cancer Res Clin Oncol. 2018;144:2139-47. DOI:10.1007/ s00432-018-2736-z
  45. van Vugt JLA, Coebergh van den Braak RRJ, Lalmahomed ZS, et al. Impact of low skeletal muscle mass and density on short and long-term outcome after resection of stage I-III colorectal cancer. Eur J Surg Oncol. 2018;44:1354-60. doi: 10.1016/j.ejso.2018.05.029
  46. Malietzis G, Johns N, Al-Hassi HO, et al. Low muscularity and myosteatosis is related to the host systemic inflammatory response in patients undergoing surgery for colorectal cancer. Ann Surg. 2016;263(2):320-5.
  47. Malietzis G, Lee GH, Bernardo D, et al. The prognostic significance and relationship with body composition of CCR7-positive cells in colorectal cancer. J Surg Oncol. 2015;112(1):86-92.
  48. Miljkovic I, Kuipers AL, Cvejkus R, et al. Myosteatosis increases with aging and is associated with incident diabetes in African ancestry men. Obesity (Silver Spring). 2016;24(2):476-82.
  49. Aleixo GFP, Shachar SS, Nyrop KA, et al. Myosteatosis and prognosis in cancer: Systematic review and meta-analysis. Crit Rev Oncol Hematol. 2020;145:102839
  50. Lee CM, Kang J. Prognostic Impact of Myosteatosis in Patients With Colorectal Cancer: A Systematic Review and Meta-Analysis. J Cachexia Sarcopenia Muscle. 2020;11(5):1270-82. doi: 10.1002/jcsm.12575

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Article selection process (PRISMA flowchart).

Download (112KB)
3. Fig. 2. Myosteatosis effect on overall 5-year survival.

Download (164KB)
4. Fig. 3. The effect of myosteatosis on relapse-free 5-year survival.

Download (99KB)

Copyright (c) 2022 Consilium Medicum

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies