Prognostic impact of myosteatosis in patients with colorectal cancer: a systematic review and meta-analysis

Chan Mi Lee, Jeonghyun Kang, Chan Mi Lee, Jeonghyun Kang

Abstract

Background: Myosteatosis has been reported to be a novel biomarker that could predict survival outcomes in patients with colorectal cancer. However, results have been conflicting. This systematic review and meta-analysis aimed to evaluate the long-term impact of myosteatosis on the survival of these patients.

Methods: A systematic search of PubMed, Embase, and Cochrane up to 27 November 2019 generated 7022 records. Studies that reported hazard ratio (HR) for overall survival, cancer-specific survival, or disease-free survival based on myosteatosis or radiodensity were included. A total of 110 full-text articles were considered for inclusion, and 14 were selected for qualitative analysis. Inverse variance method was used with random effects model for data analysis.

Results: The total number of enrolled patients included in the meta-analysis was 6518 for univariate and 8572 for multivariate HR analysis, from 12 and 10 studies, respectively. Patients with myosteatosis had a significant increase in overall mortality compared with non-myosteatosis patients by both univariate analysis [HR 1.38, 95% confidence interval (CI) 1.21 to 1.58, P < 0.00001] and multivariate analysis (HR 1.55, 95% CI 1.23 to 1.96, P < 0.00001). In subgroup analysis based on studies that reported HRs of both sarcopenia and myosteatosis, the negative effect of myosteatosis on overall survival was independent of sarcopenia using univariate values (sarcopenia HR 1.48, 95% CI 1.14 to 1.91, P = 0.003 vs. myosteatosis HR 1.51, 95% CI 1.17 to 1.96, P = 0.002) and multivariate values (sarcopenia HR 1.28, 95% CI 1.09 to 1.49, P = 0.002 vs. myosteatosis HR 1.38, 95% CI 1.07 to 1.80, P = 0.001).

Conclusions: This meta-analysis demonstrates that myosteatosis is associated with worse overall survival in patients with colorectal cancer. More investigation is needed to standardize the measurement protocol for myosteatosis and to further optimize its prognostic power for colorectal cancer patients.

Keywords: Colorectal cancer; Myosteatosis; Skeletal muscle density; Survival.

Conflict of interest statement

None declared.

© 2020 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by John Wiley & Sons Ltd on behalf of Society on Sarcopenia, Cachexia and Wasting Disorders.

Figures

Figure 1
Figure 1
Flow diagram depicting the selection process for studies. HR, hazard ratio.
Figure 2
Figure 2
Meta‐analysis of univariate results reporting impact of myosteatosis on overall survival in patients with colorectal cancer using the random effects model. CI, confidence interval; df, degrees of freedom; IV, inverse variance; SE, standard error.
Figure 3
Figure 3
Meta‐analysis of multivariate results reporting impact of myosteatosis on (A) overall survival and (B) cancer‐specific survival in patients with colorectal cancer using the random effects model. CI, confidence interval; df, degrees of freedom; IV, inverse variance; SE, standard error.
Figure 4
Figure 4
Meta‐analysis of univariate results reporting impact of (A) sarcopenia and (B) myosteatosis by random effects model in studies that report both findings in the same study cohort. CI, confidence interval; df, degrees of freedom; IV, inverse variance; SE, standard error.
Figure 5
Figure 5
Meta‐analysis of multivariate results reporting impact of (A) sarcopenia and (B) myosteatosis by random effects model in studies that report both findings in the same study cohort. CI, confidence interval; df, degrees of freedom; IV, inverse variance; SE, standard error.

References

    1. NCCN clinical practice guidelines in oncology, NCCN Guidelines for Treatment of Cancer by Site (2019). (accessed September 2, 2019).
    1. Dolan RD, Lim J, McSorley ST, Horgan PG, McMillan DC. The role of the systemic inflammatory response in predicting outcomes in patients with operable cancer: systematic review and meta‐analysis. Sci Rep 2017;7:16717.
    1. Dolan RD, McSorley ST, Horgan PG, Laird B, McMillan DC. The role of the systemic inflammatory response in predicting outcomes in patients with advanced inoperable cancer: systematic review and meta‐analysis. Crit Rev Oncol Hematol 2017;116:134–146.
    1. McSorley ST, Black DH, Horgan PG, McMillan DC. The relationship between tumour stage, systemic inflammation, body composition and survival in patients with colorectal cancer. Clin Nutr Edinb Scotl 2018;37:1279–1285.
    1. Brown JC, Cespedes Feliciano EM, Caan BJ. The evolution of body composition in oncology—epidemiology, clinical trials, and the future of patient care: facts and numbers. J Cachexia Sarcopenia Muscle 2018;9:1200–1208.
    1. Shachar SS, Williams GR, Muss HB, Nishijima TF. Prognostic value of sarcopenia in adults with solid tumours: a meta‐analysis and systematic review. Eur J Cancer Oxf Engl 2016;1990:58–67.
    1. Simonsen C, de Heer P, Bjerre ED, Suetta C, Hojman P, Pedersen BK, et al. Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta‐analysis. Ann Surg 2018;268:58–69.
    1. Malietzis G, Currie AC, Athanasiou T, Johns N, Anyamene N, Glynne‐Jones R, et al. Influence of body composition profile on outcomes following colorectal cancer surgery. BJS 2016;103:572–580.
    1. Kroenke CH, Prado CM, Meyerhardt JA, Weltzien EK, Xiao J, Cespedes Feliciano EM, et al. Muscle radiodensity and mortality in patients with colorectal cancer. Cancer 2018;124:3008–3015.
    1. Xiao J, Caan BJ, Weltzien E, Cespedes Feliciano EM, Kroenke CH, Meyerhardt JA, et al. Associations of pre‐existing co‐morbidities with skeletal muscle mass and radiodensity in patients with non‐metastatic colorectal cancer. J Cachexia Sarcopenia Muscle 2018;9:654–663.
    1. 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 Off J Am Soc Clin Oncol 2013;31:1539–1547.
    1. Sueda T, Takahasi H, Nishimura J, Hata T, Matsuda C, Mizushima T, 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;61:364–374.
    1. Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Malpica L, Williams GR. Myosteatosis and prognosis in cancer: systematic review and meta&hyphen;analysis. Crit Rev Oncol Hematol 2019;145:102839.
    1. Okugawa Y, Toiyama Y, Yamamoto A, Shigemori T, Yin C, Narumi A, et al., Clinical impact of muscle quantity and quality in colorectal cancer patients: a propensity score matching analysis, JPEN J Parenter Enteral Nutr 2018;42:1322–1333.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta&hyphen;analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
    1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–174.
    1. Dolan RD, Almasaudi AS, Dieu LB, Horgan PG, McSorley ST, McMillan DC. The relationship between computed tomography&hyphen;derived body composition, systemic inflammatory response, and survival in patients undergoing surgery for colorectal cancer. J Cachexia Sarcopenia Muscle 2019;10:111–122.
    1. DerSimonian R, Laird N. Meta‐analysis in clinical trials. Control Clin Trials 1986;7:177–188.
    1. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. A basic introduction to fixed‐effect and random‐effects models for meta‐analysis. Res Synth Methods 2010;1:97–111.
    1. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta&hyphen;analyses. BMJ 2003;327:557–560.
    1. Deeks JJ, Higgins JP, Altman DG. Analysing data and undertaking meta‐analyses In Cochrane Handbook for Systematic Reviews of Interventions. John Wiley & Sons, Ltd; 2008; p 243–296.
    1. Duval S, Tweedie R. Trim and fill: a simple funnel‐plot‐based method of testing and adjusting for publication bias in meta‐analysis. Biometrics 2000;56:455–463.
    1. Suurmond R, van Rhee H, Hak T. Introduction, comparison, and validation of Meta‐Essentials: a free and simple tool for meta‐analysis. Res Synth Methods 2017;8:537–553.
    1. Wells GA, Tugwell P, O'Connell D, Welch V, Peterson J, Shea B, & Losos, M . The Newcastle–Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta‐analyses, (2001). (accessed August 11, 2019).
    1. Hayden JA, van der Windt DA, Cartwright JL, Côté P, Bombardier C. Assessing bias in studies of prognostic factors. Ann Intern Med 2013;158:280–286.
    1. Meader N, King K, Llewellyn A, Norman G, Brown J, Rodgers M, et al. A checklist designed to aid consistency and reproducibility of GRADE assessments: development and pilot validation. Syst Rev 2014;3:82.
    1. Blauwhoff‐Buskermolen S, Versteeg KS, de van der Schueren MAE, den Braver NR, Berkhof J, Langius JAE, et al. Loss of muscle mass during chemotherapy is predictive for poor survivalof patients with metastatic colorectal cancer. J Clin Oncol Off J Am Soc Clin Oncol 2016;34:1339–1344.
    1. van Baar H, Beijer S, Bours MJL, Weijenberg MP, van Zutphen, M , van Duijnhoven, FJB , 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;144:2139–2147.
    1. van Vugt JLA, Coebergh van den Braak RRJ, Lalmahomed ZS, Vrijland WW, Dekker JWT, Zimmerman DDE, 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;44:1354–1360.
    1. Charette N, Vandeputte C, Ameye L, Bogaert CV, Krygier J, Guiot T, 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.
    1. Hopkins JJ, Reif RL, Bigam DL, Baracos VE, Eurich DT, Sawyer MB. The impact of muscle and adipose tissue on long‐term survival in patients with stage I to III colorectal cancer. Dis Colon rectum 2019;62:549–560.
    1. Deng C‐Y, Lin Y‐C, Wu JS, Cheung Y‐C, Fan C‐W, Yeh K‐Y, et al. Progressive sarcopenia in patients with colorectal cancer predicts survival. Am J Roentgenol 2018;210:526–532.
    1. Looijaard SMLM, Meskers CGM, Slee‐Valentijn MS, Bouman DE, Wymenga ANM, Klaase JM, et al. Computed tomography-based body composition is not consistently associated with outcome in older patients with colorectal cancer. Oncologist 2019;25:1–10.
    1. Sabel MS, Terjimanian M, Conlon ASC, Griffith KA, Morris AM, Mulholland MW, et al. Analytic morphometric assessment of patients undergoing colectomy for colon cancer. J Surg Oncol 2013;108:169–175.
    1. da Cunha LP, Silveira MN, Mendes MCS, Costa FO, Macedo LT, de Siqueira NS, et al. Sarcopenia as an independent prognostic factor in patients with metastatic colorectal cancer: a retrospective evaluation. Clin Nutr ESPEN 2019;32:107–112.
    1. Feliciano EC, Chen WY. Clinical implications of low skeletal muscle mass in early stage breast and colorectal cancer. Proc Nutr Soc 2018;77:382–387.
    1. Thuijs DJ, Head SJ, Stone GW, Puskas JD, Taggart DP, Serruys PW, et al. Outcomes following surgical revascularization with single versus bilateral internal thoracic arterial grafts in patients with left main coronary artery disease undergoing coronary artery bypass grafting: insights from the EXCEL trial. Eur. J. Cardio‐Thorac. Surg. Off. J. Eur. Assoc. Cardio‐Thorac. Surg. 2019;55:501–510.
    1. Choi MH, Oh SN, Lee IK, Oh ST, Won DD. Sarcopenia is negatively associated with long‐term outcomes in locally advanced rectal cancer. J Cachexia Sarcopenia Muscle 2018;9:53–59.
    1. Chung E, Lee HS, Cho E‐S, Park EJ, Baik SH, Lee KY, et al. Prognostic significance of sarcopenia and skeletal muscle mass change during preoperative chemoradiotherapy in locally advanced rectal cancer, Clin. Nutr. Edinb. Scotl 2020;39:820–828.
    1. Feliciano EMC, Kroenke CH, Meyerhardt JA, Prado CM, Bradshaw PT, Kwan ML, et al. Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer: results from the C SCANS study. JAMA Oncol 2017;3:e172319–e172319.
    1. Perkisas S, Lamers S, Degerickx R, Van Mieghem E, Vandewoude M, Verhoeven V, et al. The relation between mortality, intramuscular adipose tissue and sarcopenia in hospitalized geriatric patients. Eur Geriatr Med 2018;9:801–807.
    1. Cruz‐Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019;48:16–31.
    1. Deans DA, Wigmore SJ, Gilmour H, Paterson‐Brown S, Ross JA, Fearon KC. Elevated tumour interleukin‐1β is associated with systemic inflammation: a marker of reduced survival in gastro‐oesophageal cancer. Br. J. Cancer. 2006;95:1568–1575.
    1. Abdel‐Rahman O, Cheung WY. Revisiting the prognostic relevance of muscle mass among non‐metastatic colorectal cancer. Transl. Gastroenterol. Hepatol. 2018;3.
    1. van Vugt JLA, Coebergh van den Braak RRJ, Schippers HJW, Veen KM, Levolger S, de Bruin RWF, et al. Contrast‐enhancement influences skeletal muscle density, but not skeletal muscle mass, measurements on computed tomography. Clin. Nutr. Edinb. Scotl. 2018;37:1707–1714.
    1. Miljkovic I, Kuipers A, Cvejkus R, Bunker C, Patrick A, Gordon C, et al. Myosteatosis increases with aging and is associated with incident diabetes in African ancestry men. Obes Silver Spring Md 2016;24:476–482.
    1. Hausman GJ, Basu U, Du M, Fernyhough‐Culver M, Dodson MV. Intermuscular and intramuscular adipose tissues: bad vs. good adipose tissues. Adipocyte 2014;3:242–255.
    1. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2019. J Cachexia Sarcopenia Muscle 2019;10:1143‐1145.

Source: PubMed

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