Skip to main content

Advertisement

Log in

Sarcopenia predicts worse postoperative outcomes and decreased survival rates in patients with colorectal cancer: a systematic review and meta-analysis

  • Review
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Purpose

Previous studies have shown an association of sarcopenia with adverse short- and long-term outcomes in multiple gastrointestinal cancer types. We aimed to investigate the prognostic value of sarcopenia on the postoperative outcomes and survival rates of patients with colorectal cancer (CRC).

Methods

A systematic literature search was performed using the PubMed, Embase, Cochrane, Google Scholar, and Scopus databases. We included studies that compared postoperative outcomes or survival rates in sarcopenic and non-sarcopenic patients with CRC.

Results

A total of 44 observational studies, comprising 18,891 patients, were included. The pooled prevalence of sarcopenia was 37% (n = 7009). The pooled analysis revealed an association between sarcopenia and higher risk of total postoperative complications (23 studies, OR = 1.84; 95% CI 1.35–2.49), postoperative severe complications (OR = 1.72; 95% CI 1.10–2.68), postoperative mortality (OR = 3.21; 95% CI 2.01–5.11), postoperative infections (OR = 1.40; 95% CI 1.12–1.76), postoperative cardiopulmonary complications (OR = 2.92; 95% CI 1.96–4.37), and prolonged length of stay (MD = 0.77; 95% CI 0.44–1.11) after colorectal cancer surgery. However, anastomotic leakage showed comparable occurrence between sarcopenic and non-sarcopenic patients (OR = 0.99; 95% CI 0.72 to 1.36). Regarding survival outcomes, sarcopenic patients had significantly shorter overall survival (25 studies, HR = 1.83; 95% CI = 1.57–2.14), disease-free survival (HR = 1.55; 95% CI = 1.29–1.88), and cancer-specific survival (HR = 1.77; 95% CI 1.40–2.23) as compared with non-sarcopenic patients.

Conclusion

Among patients with colorectal cancer, sarcopenia is a strong predictor of increased postoperative complications and worse survival outcomes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data is available upon request.

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424

    Article  PubMed  Google Scholar 

  2. Sun G, Li Y, Peng Y, Lu D, Zhang F, Cui X, Zhang Q, Li Z (2018) Can sarcopenia be a predictor of prognosis for patients with non-metastatic colorectal cancer? A systematic review and meta-analysis. Int J Color Dis 33:1419–1427

    Article  Google Scholar 

  3. Okugawa Y, Toiyama Y, Hur K, Yamamoto A, Yin C, Ide S, Kitajima T, Fujikawa H, Yasuda H, Koike Y, Okita Y, Hiro J, Yoshiyama S, Araki T, Miki C, McMillan DC, Goel A, Kusunoki M (2019) Circulating miR-203 derived from metastatic tissues promotes myopenia in colorectal cancer patients. J Cachexia Sarcopenia Muscle 10:536–548

    Article  PubMed  PubMed Central  Google Scholar 

  4. Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Malpica L, Williams GR (2020) Myosteatosis and prognosis in cancer: systematic review and meta-analysis. Crit Rev Oncol Hematol 145:102839

    Article  CAS  PubMed  Google Scholar 

  5. Simonsen C, de Heer P, Bjerre E, Suetta C, Hojman P, Pedersen B et al (2018) Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology. Ann Surg 268:58–69

    Article  PubMed  Google Scholar 

  6. Lee CM, Kang J (2020) Prognostic impact of myosteatosis in patients with colorectal cancer: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 11(5):1270–1282

    Article  PubMed  PubMed Central  Google Scholar 

  7. Vergara-Fernandez O, Trejo-Avila M, Salgado-Nesme N (2020) Sarcopenia in patients with colorectal cancer: a comprehensive review. World Journal of Clinical Cases 8:1188–1202

    Article  PubMed  PubMed Central  Google Scholar 

  8. Rosenberg I (1989) Summary comments: epidemiological and methodological problems in determining nutritional status of older persons. Am J Clin Nutr 50:1231–1233

    Article  Google Scholar 

  9. Cruz-Jentoft A, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:601–601

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cespedes Feliciano E, Avrutin E, Caan B, Boroian A, Mourtzakis M (2018) Screening for low muscularity in colorectal cancer patients: a valid, clinic-friendly approach that predicts mortality. J Cachexia Sarcopenia Muscle 9:898–908

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ryan A, Power D, Daly L, Cushen S, Ní Bhuachalla Ē, Prado C (2016) Cancer-associated malnutrition, cachexia and sarcopenia: the skeleton in the hospital closet 40 years later. Proc Nutr Soc 75:199–211

    Article  PubMed  Google Scholar 

  12. Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B (2017) Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: a systematic review and meta-analysis. Maturitas 103:16–22

    Article  PubMed  Google Scholar 

  13. Hua H, Xu X, Tang Y, Ren Z, Xu Q, Chen L (2019) Effect of sarcopenia on clinical outcomes following digestive carcinoma surgery: a meta-analysis. Supportive Care Cancer 27:2385–2394

    Article  Google Scholar 

  14. Weerink L, Hoorn A, Leeuwen B, Bock G (2020) Low skeletal muscle mass and postoperative morbidity in surgical oncology: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 11:636–649

    Article  PubMed  PubMed Central  Google Scholar 

  15. Su H, Ruan J, Chen T, Lin E, Shi L (2019) CT-assessed sarcopenia is a predictive factor for both long-term and short-term outcomes in gastrointestinal oncology patients: a systematic review and meta-analysis. Cancer Imaging 19:82

    Article  PubMed  PubMed Central  Google Scholar 

  16. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals Intern Med 151:264

    Article  Google Scholar 

  17. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012

    Article  CAS  PubMed  Google Scholar 

  18. Goossen K, Tenckhoff S, Probst P, Grummich K, Mihaljevic A, Büchler M et al (2017) Optimal literature search for systematic reviews in surgery. Langenbeck's Arch Surg 403:119–129

    Article  Google Scholar 

  19. Clavien P, Barkun J, de Oliveira M, Vauthey J, Dindo D, Schulick R et al (2009) The Clavien-Dindo classification of surgical complications. Ann Surg 250:187–196

    Article  PubMed  Google Scholar 

  20. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M et al (2020) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in metaanalyses [accessed 15 Jun 2020] Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

  21. Wan X, Wang W, Liu J, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 14:135

    Article  PubMed  PubMed Central  Google Scholar 

  22. Higgins J, Altman D, Gotzsche P, Juni P, Moher D, Oxman A et al (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928–d5928

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wang S, Xie H, Gong Y, Kuang J, Yan L, Ruan G, Gao F, Gan J (2020) The value of L3 skeletal muscle index in evaluating preoperative nutritional risk and long-term prognosis in colorectal cancer patients. Sci Rep 10:8153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Richards S, Senadeera S, Frizelle F (2020) Sarcopenia, as assessed by psoas cross-sectional area, is predictive of adverse postoperative outcomes in patients undergoing colorectal cancer surgery. Dis Colon Rectum 63:807–815

    Article  PubMed  Google Scholar 

  25. Giani A, Famularo S, Riva L, Tamini N, Ippolito D, Nespoli L, Conconi P, Sironi S, Braga M, Gianotti L (2020) Association between specific presurgical anthropometric indexes and morbidity in patients undergoing rectal cancer resection. Nutrition 75-76:110779

    Article  PubMed  Google Scholar 

  26. Tokunaga R, Nakagawa S, Miyamoto Y, Ohuchi M, Izumi D, Kosumi K et al (2019) The clinical impact of preoperative body composition differs between male and female colorectal cancer patients. Color Dis 22:62–70

    Article  Google Scholar 

  27. Pereira M, Pereira A, Silva P, Costa C, Martins S (2020) Sarcopenia as a risk factor of morbimortality in colorectal cancer surgery. Gastrointestinal Dis 2:107–117

    Article  Google Scholar 

  28. Han JS, Ryu H, Park I, Kim K, Shin Y, Kim S et al (2020) Association of body composition with long-term survival in non-metastatic rectal cancer patients. Cancer Res Treat 52:563–572

    Article  PubMed  Google Scholar 

  29. Xie H, Gong Y, Kuang J, Yan L, Ruan G, Tang S, Gao F, Gan J (2020) Computed-tomography-determined sarcopenia is a useful imaging biomarker for predicting postoperative outcomes in elderly colorectal cancer patients. Cancer Res Treat 52(3):957–972

    Article  PubMed  PubMed Central  Google Scholar 

  30. Shirdel M, Andersson F, Myte R, Axelsson J, Rutegård M, Blomqvist L, Riklund K, van Guelpen B, Palmqvist R, Gylling B (2020) Body composition measured by computed tomography is associated with colorectal cancer survival, also in early-stage disease. Acta Oncol 59(7):799–808

    Article  PubMed  Google Scholar 

  31. Aro R, Mäkäräinen-Uhlbäck E, Ämmälä N, Rautio T, Ohtonen P, Saarnio J, Meriläinen S (2020) 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 46(9):1656–1662

    Article  PubMed  Google Scholar 

  32. Souwer E, Moos S, van Rooden C, Bijlsma A, Bastiaannet E, Steup W et al (2020) Physical performance has a strong association with poor surgical outcome in older patients with colorectal cancer. Eur J Surg Oncol 46:462–469

    Article  PubMed  Google Scholar 

  33. Olmez T, Karakose E, Keklikkiran Z, Ofluoglu C, Bas T, Uzun O et al (2020) Relationship between sarcopenia and surgical site infection in patients undergoing colorectal cancer surgical procedures. Surg Infect 21:451–456

    Article  Google Scholar 

  34. Tankel J, Yellinek S, Vainberg E, David Y, Greenman D, Kinross J et al (2019) Sarcopenia defined by muscle quality rather than quantity predicts complications following laparoscopic right hemicolectomy. Int J Colorect Dis 35:85–94

    Article  Google Scholar 

  35. Chen WS, Huang YS, Xu LB, Shi MM, Chen XD, Ye GQ, Wu TT, Zhu GB (2020) Effects of sarcopenia, hypoalbuminemia, and laparoscopic surgery on postoperative complications in elderly patients with colorectal cancer: a prospective study. Neoplasma 67(4):922–932

    Article  CAS  PubMed  Google Scholar 

  36. Ojima Y, Harano M, Sumitani D, Okajima M (2019) Impact of preoperative skeletal muscle mass and quality on the survival of elderly patients after curative resection of colorectal cancer. J Anus Rectum Colon 3:143–151

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hopkins J, Reif R, Bigam D, Baracos V, Eurich D, Sawyer M (2019) The impact of muscle and adipose tissue on long-term survival in patients with stage I to III colorectal cancer. Dis Colon Rectum 62:549–560

    Article  PubMed  Google Scholar 

  38. Hopkins J, Reif R, Bigam D, Baracos V, Eurich D, Sawyer M (2019) Change in skeletal muscle following resection of stage I–III colorectal cancer is predictive of poor survival: a cohort study. World J Surg 43:2518–2526

    Article  PubMed  Google Scholar 

  39. Dolan D, Knight K, Maguire S, Moug S (2019) The relationship between sarcopenia and survival at 1 year in patients having elective colorectal cancer surgery. Tech Coloproctol 23:877–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Jochum S, Kistner M, Wood E, Hoscheit M, Nowak L, Poirier J et al (2019) Is sarcopenia a better predictor of complications than body mass index? Sarcopenia and surgical outcomes in patients with rectal cancer. Color Dis 21:1372–1378

    Article  CAS  Google Scholar 

  41. Vashi P, Gorsuch K, Wan L, Hill D, Block C, Gupta D (2019) Sarcopenia supersedes subjective global assessment as a predictor of survival in colorectal cancer. PLoS One 14:e0218761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Maurício S, Xiao J, Prado C, Gonzalez M, Correia M (2018) Different nutritional assessment tools as predictors of postoperative complications in patients undergoing colorectal cancer resection. Clin Nutr 37:1505–1511

    Article  PubMed  Google Scholar 

  43. Park S, Hwang I, Choi C, Kang H, Kim B, Park B et al (2018) Sarcopenia is poor prognostic factor in older patients with locally advanced rectal cancer who received preoperative or postoperative chemoradiotherapy. Medicine 97:e13363

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kroenke C, Prado C, Meyerhardt J, Weltzien E, Xiao J, Cespedes Feliciano E et al (2018) Muscle radiodensity and mortality in patients with colorectal cancer. Cancer 124:3008–3015

    Article  PubMed  Google Scholar 

  45. Nakanishi R, Oki E, Sasaki S, Hirose K, Jogo T, Edahiro K et al (2017) Sarcopenia is an independent predictor of complications after colorectal cancer surgery. Surg Today 48:151–157

    Article  PubMed  Google Scholar 

  46. Deng C, Lin Y, Wu J, Cheung Y, Fan C, Yeh K et al (2018) Progressive sarcopenia in patients with colorectal cancer predicts survival. AJR Am J Roentgenol 210:526–532

    Article  PubMed  Google Scholar 

  47. Choi M, Oh S, Lee I, Oh S, Won D (2018) Sarcopenia is negatively associated with long-term outcomes in locally advanced rectal cancer. J Cachexia Sarcopenia Muscle 9:53–59

    Article  PubMed  Google Scholar 

  48. Mosk C, van Vugt J, de Jonge H, Witjes C, Buettner S, Ijzermans J et al (2018) Low skeletal muscle mass as a risk factor for postoperative delirium in elderly patients undergoing colorectal cancer surgery. Clin Interv Aging 13:2097–2106

    Article  PubMed  PubMed Central  Google Scholar 

  49. Takeda Y, Akiyoshi T, Matsueda K, Fukuoka H, Ogura A, Miki H, Hiyoshi Y, Nagasaki T, Konishi T, Fujimoto Y, Fukunaga Y, Ueno M (2018) Skeletal muscle loss is an independent negative prognostic factor in patients with advanced lower rectal cancer treated with neoadjuvant chemoradiotherapy. PLoS One 13:e0195406

    Article  PubMed  PubMed Central  Google Scholar 

  50. Sueda T, Takahasi H, Nishimura J, Hata T, Matsuda C, Mizushima T et al (2018) Impact of low muscularity and myosteatosis on long-term outcome after curative colorectal cancer surgery. Dis Colon Rectum 61:364–374

    Article  PubMed  Google Scholar 

  51. Chen W, Chen X, Ma L, Zhang F, Lin J, Zhuang C et al (2018) Impact of visceral obesity and sarcopenia on short-term outcomes after colorectal cancer surgery. Dig Dis Sci 63:1620–1630

    Article  PubMed  Google Scholar 

  52. Van Der Kroft G, Bours D, Janssen-Heijnen D, van Berlo D, Konsten D (2018) Value of sarcopenia assessed by computed tomography for the prediction of postoperative morbidity following oncological colorectal resection: a comparison with the malnutrition screening tool. Clin Nutr ESPEN 24:114–119

    Article  PubMed  Google Scholar 

  53. Van Vugt J, Coebergh van den Braak R, Lalmahomed Z, Vrijland W, Dekker J, Zimmerman D et al (2018) 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 44:1354–1360

    Article  PubMed  Google Scholar 

  54. Cespedes-Feliciano E, Kroenke C, Meyerhardt J, Prado C, Bradshaw P, Kwan M et al (2017) Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer. JAMA Oncol 3:e172319

    Article  PubMed Central  Google Scholar 

  55. Hanaoka M, Yasuno M, Ishiguro M, Yamauchi S, Kikuchi A, Tokura M, Ishikawa T, Nakatani E, Uetake H (2017) Morphologic change of the psoas muscle as a surrogate marker of sarcopenia and predictor of complications after colorectal cancer surgery. Int J Color Dis 32:847–856

    Article  Google Scholar 

  56. Boer B, de Graaff F, Brusse-Keizer M, Bouman D, Slump C, Slee-Valentijn M et al (2016) Skeletal muscle mass and quality as risk factors for postoperative outcome after open colon resection for cancer. Int J Color Dis 31:1117–1124

    Article  CAS  Google Scholar 

  57. Malietzis G, Currie A, Athanasiou T, Johns N, Anyamene N, Glynne-Jones R et al (2016) Influence of body composition profile on outcomes following colorectal cancer surgery. Br J Surg 103:572–580

    Article  CAS  PubMed  Google Scholar 

  58. Pędziwiatr M, Pisarska M, Major P, Grochowska A, Matłok M, Przęczek K, Stefura T, Budzyński A, Kłęk S (2016) Laparoscopic colorectal cancer surgery combined with enhanced recovery after surgery protocol (ERAS) reduces the negative impact of sarcopenia on short-term outcomes. Eur J Surg Oncol 42:779–787

    Article  PubMed  Google Scholar 

  59. Ouchi A, Asano M, Aono K, Watanabe T, Oya S (2016) Laparoscopic colorectal resection in patients with sarcopenia: a retrospective case-control study. J Laparoendosc Adv Surg Tech A 26:366–370

    Article  PubMed  Google Scholar 

  60. Reisinger K, Derikx J, van Vugt J, Von Meyenfeldt M, Hulsewé K, Olde Damink S et al (2016) Sarcopenia is associated with an increased inflammatory response to surgery in colorectal cancer. Clin Nutr 35:924–927

    Article  PubMed  Google Scholar 

  61. Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R, Kurashige J, Hiyoshi Y, Iwagami S, Yoshida N, Yoshida M, Watanabe M, Baba H (2015) Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer. Ann Surg Oncol 22:2663–2668

    Article  PubMed  Google Scholar 

  62. Huang D, Wang S, Zhuang C, Zheng B, Lu J, Chen F et al (2015) Sarcopenia, as defined by low muscle mass, strength and physical performance, predicts complications after surgery for colorectal cancer. Color Dis 17:O256–O264

    Article  Google Scholar 

  63. Jones K, Doleman B, Scott S, Lund J, Williams J (2014) Simple psoas cross-sectional area measurement is a quick and easy method to assess sarcopenia and predicts major surgical complications. Color Dis 17:O20–O26

    Article  Google Scholar 

  64. Jung H, Kim J, Kim J, Kim S, Yang H, Lee J et al (2015) Effect of muscle mass on toxicity and survival in patients with colon cancer undergoing adjuvant chemotherapy. Support Care Cancer 23:687–694

    Article  PubMed  Google Scholar 

  65. Lieffers J, Bathe O, Fassbender K, Winget M, Baracos V (2012) Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer 107:931–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fearon K, Strasser F, Anker S, Bosaeus I, Bruera E, Fainsinger R et al (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12:489–495

    Article  PubMed  Google Scholar 

  67. Prado C, Baracos V, McCargar L, Reiman T, Mourtzakis M, Tonkin K et al (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Rep 15:2920–2926

    Article  CAS  Google Scholar 

  68. Camp R, Dolled-Filhart M, Rimm DL (2004) X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res 10:7252–7259

    Article  CAS  PubMed  Google Scholar 

  69. Martin L, Birdsell L, MacDonald N, Reiman T, Clandinin M, McCargar L 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 31:1539–1547

    Article  PubMed  Google Scholar 

  70. Joglekar S, Asghar A, Mott S, Johnson B, Button A, Clark E et al (2014) Sarcopenia is an independent predictor of complications following pancreatectomy for adenocarcinoma. J Surg Oncol 111:771–775

    Article  PubMed  PubMed Central  Google Scholar 

  71. Zhuang C, Huang D, Pang W, Zhou C, Wang S, Lou N et al (2016) Sarcopenia is an independent predictor of severe postoperative complications and long-term survival after radical gastrectomy for gastric cancer. Medicine 95:e3164

    Article  PubMed  PubMed Central  Google Scholar 

  72. Okumura S, Kaido T, Hamaguchi Y, Fujimoto Y, Masui T, Mizumoto M, Hammad A, Mori A, Takaori K, Uemoto S (2015) Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery 157:1088–1098

    Article  PubMed  Google Scholar 

  73. Kim E, Kim Y, Park I, Ahn H, Cho E, Jeong Y (2015) Prognostic significance of CT-determined sarcopenia in patients with small-cell lung cancer. J Thorac Oncol 10:1795–1799

    Article  CAS  PubMed  Google Scholar 

  74. Caan B, Meyerhardt J, Kroenke C, Alexeeff S, Xiao J, Weltzien E et al (2017) Explaining the obesity paradox: the association between body composition and colorectal cancer survival (C-SCANS study). Cancer Epidemiol Biomark Prev 26:1008–1015

    Article  Google Scholar 

  75. Avrutin E, Moisey L, Zhang R, Khattab J, Todd E, Premji T et al (2018) Clinically practical approach for screening of low muscularity using electronic linear measures on computed tomography images in critically ill patients. JPEN J Parenter Enteral Nutr 42:885–891

    Article  PubMed  Google Scholar 

  76. Inokuchi S, Sugamiya H, Shibata M, Suzuki M, Ito J, Matsumara A (2001) Age related changes of the trunk muscle observed by CT image. Anthropol Sci 109:71–83

    Google Scholar 

  77. Peng P, van Vledder M, Tsai S, de Jong M, Makary M, Ng J et al (2011) Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB 13:439–446

    Article  PubMed  PubMed Central  Google Scholar 

  78. Bijlsma A, Meskers C, Ling C, Narici M, Kurrle S, Cameron I et al (2012) Defining sarcopenia: the impact of different diagnostic criteria on the prevalence of sarcopenia in a large middle aged cohort. Age (Dordr) 35:871–881

    Article  Google Scholar 

  79. Mourtzakis M, Prado C, Lieffers J, Reiman T, McCargar L, Baracos V (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

    Article  PubMed  Google Scholar 

  80. Han S, Kim K, Kim K, Na K, Chae D, Kim S et al (2010) Lean mass index: a better predictor of mortality than body mass index in elderly Asians. J Am Geriat Societ 58:312–317

    Article  Google Scholar 

  81. Shachar S, Williams G, Muss H, Nishijima T (2016) Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur J Cancer 57:58–67

    Article  PubMed  Google Scholar 

  82. Levolger S, van Vugt J, de Bruin R, IJzermans J (2015) Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg 102:1448–1458

    Article  CAS  PubMed  Google Scholar 

  83. Williams G, Chen Y, Kenzik K, McDonald A, Shachar S, Klepin H et al (2020) Assessment of sarcopenia measures, survival, and disability in older adults before and after diagnosis with cancer. JAMA Netw Open 3:e204783

    Article  PubMed  PubMed Central  Google Scholar 

  84. Kim T, Choi K (2013) Sarcopenia: definition, epidemiology, and pathophysiology. J Bone Metab 20:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  85. Peterson S, Mozer M (2017) Differentiating sarcopenia and cachexia among patients with cancer. Nutr Clin Pract 32:30–39

    Article  PubMed  Google Scholar 

  86. Van Vledder M, Levolger S, Ayez N, Verhoef C, Tran T, IJzermans J (2012) Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 99:550–557

    Article  PubMed  Google Scholar 

  87. Langlois F, Vu T, Kergoat M, Chassé K, Dupuis G, Bherer L (2012) The multiple dimensions of frailty: physical capacity, cognition, and quality of life. Int Psychogeriatr 24:1429–1436

    Article  PubMed  Google Scholar 

  88. Reisinger K, van Vugt J, Tegels J, Snijders C, Hulsewé K, Hoofwijk A 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

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Mario Trejo-Avila: study conception design, data acquisition, data analysis, data interpretation, drafting the article, overall supervision, critical revision, and final approval.

Katya Bozada-Gutiérrez: data acquisition, data interpretation, drafting the article, overall supervision, critical revision, and final approval.

Carlos Valenzuela-Salazar: data acquisition and interpretation, drafting the article, overall supervision, critical revision, and final approval.

José Herrera-Esquivel: data acquisition and interpretation, drafting the article, overall supervision, critical revision, and final approval.

Mucio Moreno-Portillo: data acquisition and analysis, data interpretation, drafting the article, overall supervision, critical revision, and final approval.

Corresponding author

Correspondence to Mario Trejo-Avila.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All required data were retrieved from published articles. Hence, informed consent or ethical approval was not required.

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

Trejo-Avila, M., Bozada-Gutiérrez, K., Valenzuela-Salazar, C. et al. Sarcopenia predicts worse postoperative outcomes and decreased survival rates in patients with colorectal cancer: a systematic review and meta-analysis. Int J Colorectal Dis 36, 1077–1096 (2021). https://doi.org/10.1007/s00384-021-03839-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00384-021-03839-4

Keywords

Navigation