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Assessment of Computed Tomography (CT)-Defined Muscle and Adipose Tissue Features in Relation to Short-Term Outcomes After Elective Surgery for Colorectal Cancer: A Multicenter Approach

  • Gastrointestinal Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Sarcopenia, visceral obesity (VO), and reduced muscle radiodensity (myosteatosis) are suggested risk factors for postoperative morbidity in colorectal cancer (CRC), but usually are not concurrently assessed. Published thresholds used to define these features are not CRC-specific and are defined in relation to mortality, not postoperative outcomes. This study aimed to evaluate body composition in relation to length of hospital stay (LOS) and postoperative outcomes.

Methods

Pre-surgical computed tomography (CT) images were assessed for total area and radiodensity of skeletal muscle and visceral adipose tissue in a pooled Canadian and UK cohort (n = 2100). Sex- and age-specific values for these features were calculated. For 1139 of 2100 patients, LOS data were available, and sex- and age-specific thresholds for sarcopenia, myosteatosis, and VO were defined on the basis of LOS. Association of CT-defined features with LOS and readmissions was explored using negative binomial and logistic regression models, respectively.

Results

In the multivariable analysis, the predictors of LOS (P < 0.001) were age, surgical approach, major complications (incidence rate ratio [IRR] 2.42; 95% confidence interval [CI] 2.18–2.68), study cohort, and three body composition profiles characterized by myosteatosis combined with either sarcopenia (IRR, 1.27; 95% CI 1.12–1.43) or VO (IRR, 1.25; 95% CI 1.10–1.42), and myosteatosis combined with both sarcopenia and VO (IRR, 1.58; 95% CI 1.29–1.93). In the multivariable analysis, risk of readmission was associated with VO alone (odds ratio [OR] 2.66; 95% CI 1.18–6.00); P = 0.018), VO combined with myosteatosis (OR, 2.72; 95% CI 1.36–5.46; P = 0.005), or VO combined with myosteatosis and sarcopenia (OR, 2.98; 95% CI 1.06–5.46; P = 0.038). Importantly, the effect of body composition profiles on LOS and readmission was independent of major complications.

Conclusion

The findings showed that CT-defined multidimensional body habitus is independently associated with LOS and hospital readmission.

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References

  1. Cakir H, Heus C, van der Ploeg TJ, Houdijk AP. Visceral obesity determined by CT scan and outcomes after colorectal surgery; a systematic review and meta-analysis. Int J Colorectal Dis. 2015;30:875–82.

    Article  PubMed  Google Scholar 

  2. Kazemi-Bajestani SM, Mazurak VC, Baracos V. Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes. Semin Cell Dev Biol. 2016;54:2–10.

    Article  PubMed  Google Scholar 

  3. Malietzis G, Aziz O, Bagnall NM, Johns N, Fearon KC, Jenkins JT. The role of body composition evaluation by computerized tomography in determining colorectal cancer treatment outcomes: a systematic review. Eur J Surg Oncol. 2015;41:186–96.

    Article  PubMed  CAS  Google Scholar 

  4. Mei KL, Batsis JA, Mills JB, Holubar SD. Sarcopenia and sarcopenic obesity: do they predict inferior oncologic outcomes after gastrointestinal cancer surgery? Periop Med London. 2016;5:30.

    Article  Google Scholar 

  5. Martin L, Birdsell L, MacDonald N, 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. 2013;31:1539–47.

    Article  PubMed  Google Scholar 

  6. Yip C, Dinkel C, Mahajan A, Siddique M, Cook GJ, Goh V. Imaging body composition in cancer patients: visceral obesity, sarcopenia, and sarcopenic obesity may impact on clinical outcome. Insights Imaging. 2015;6:489–97.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Boer BC, de Graaff F, Brusse-Keizer M, et al. Skeletal muscle mass and quality as risk factors for postoperative outcome after open colon resection for cancer. Int J Colorectal Dis. 2016;31:1117–24.

    Article  PubMed  CAS  Google Scholar 

  8. Lodewick TM, van Nijnatten TJ, van Dam RM, et al. Are sarcopenia, obesity, and sarcopenic obesity predictive of outcome in patients with colorectal liver metastases? HPB Oxford. 2015;17:438–46.

    Article  PubMed  Google Scholar 

  9. 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.

    Article  PubMed  CAS  Google Scholar 

  10. Moon HG, Ju YT, Jeong CY, et al. Visceral obesity may affect oncologic outcome in patients with colorectal cancer. Ann Surg Oncol. 2008;15:1918–22.

    Article  PubMed  Google Scholar 

  11. Ouchi A, Asano M, Aono K, Watanabe T, Oya S. Laparoscopic colorectal resection in patients with sarcopenia: a retrospective case-control study. J Laparoendosc Adv Surg Tech A. 2016;26:366–70.

    Article  PubMed  Google Scholar 

  12. Ozoya OO, Siegel EM, Srikumar T, Bloomer AM, DeRenzis A, Shibata DA-OhooX. Quantitative assessment of visceral obesity and postoperative colon cancer outcomes. J Gastrointest Surg. 2017;21:534–42.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Pedziwiatr M, Pisarska M, Major P, et al. 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. 2016;42:779–87.

    Article  PubMed  CAS  Google Scholar 

  14. Sabel MS, Terjimanian M, Conlon AS, et al. Analytic morphometric assessment of patients undergoing colectomy for colon cancer. J Surg Oncol. 2013;108:169–75.

    Article  PubMed  Google Scholar 

  15. van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TC, Ijzermans JN. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012;99:550–7.

    Article  PubMed  Google Scholar 

  16. Yu H, Joh YG, Son GM, Kim HS, Jo HJ, Kim HY. Distribution and impact of the visceral fat area in patients with colorectal cancer. Ann Coloproctol. 2016;32:20–6.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jones KI, Doleman B, Scott S, Lund JN, Williams JP. Simple psoas cross-sectional area measurement is a quick and easy method to assess sarcopenia and predicts major surgical complications. Colorectal Dis. 2015;17:O20–26.

    Article  PubMed  CAS  Google Scholar 

  18. Margadant CC, Bruns ER, Sloothaak DA, et al. Lower muscle density is associated with major postoperative complications in older patients after surgery for colorectal cancer. Eur J Surg Oncol. 2016;42:1654–9.

    Article  PubMed  CAS  Google Scholar 

  19. Cecchini S, Cavazzini E, Marchesi F, Sarli L, Roncoroni L. Computed tomography volumetric fat parameters versus body mass index for predicting short-term outcomes of colon surgery. World J Surg. 2011;35:415–23.

    Article  PubMed  Google Scholar 

  20. Chen B, Zhang Y, Zhao S, et al. The impact of general/visceral obesity on completion of mesorectum and perioperative outcomes of laparoscopic TME for rectal cancer: a STARD-compliant article. Medicine. 2016;95:e4462.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Heus C, Cakir H, Lak A, Doodeman HJ, Houdijk AP. Visceral obesity, muscle mass, and outcome in rectal cancer surgery after neoadjuvant chemoradiation. Int J Surg. 2016;29:159–64.

    Article  PubMed  Google Scholar 

  22. Huang DD, Wang SL, Zhuang CL, et al. Sarcopenia, as defined by low muscle mass, strength, and physical performance, predicts complications after surgery for colorectal cancer. Colorectal Dis. 2015;17:O256–64.

    Article  PubMed  Google Scholar 

  23. Park BK, Park JW, Ryoo SB, Jeong SY, Park KJ, Park JG. Effect of visceral obesity on surgical outcomes of patients undergoing laparoscopic colorectal surgery. World J Surg. 2015;39:2343–53.

    Article  PubMed  Google Scholar 

  24. Scott SI, Farid S, Mann C, Jones R, Kang P, Evans J. Abdominal fat ratio: a novel parameter for predicting conversion in laparoscopic colorectal surgery. Ann R Coll Surg Engl. 2017;99:46–50.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Cespedes Feliciano EM, Kroenke CH, Meyerhardt JA, 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.

    Article  Google Scholar 

  26. Chen WZ, Chen XD, Ma LL, et al. Impact of visceral obesity and sarcopenia on short-term outcomes after colorectal cancer surgery. Dig Dis Sci. 2018;63:1620–30.

    Article  PubMed  Google Scholar 

  27. Hanaoka M, Yasuno M, Ishiguro M, et al. 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;32:847–56.

    Article  PubMed  Google Scholar 

  28. Nakanishi R, Oki E, Sasaki S, et al. Sarcopenia is an independent predictor of complications after colorectal cancer surgery. Surg Today. 2017;48:151–7.

    Article  PubMed  Google Scholar 

  29. van der Kroft G, Bours D, Janssen-Heijnen DM, van Berlo D, Konsten D. 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. 2018;24:114–9.

    Google Scholar 

  30. Womer AL, Brady JT, Kalisz K, et al. Do psoas muscle area and volume correlate with postoperative complications in patients undergoing rectal cancer resection? Am J Surg. 2018;215:503–6.

    Article  PubMed  Google Scholar 

  31. Hopkins JJ, Skubleny D, Bigam DL, Baracos VE, Eurich DT, Sawyer MB. Barriers to the interpretation of body composition in colorectal cancer: a review of the methodological inconsistency and complexity of the CT-defined body habitus. Ann Surg Oncol. 2018;25:1381–94.

    Article  PubMed  Google Scholar 

  32. Baracos VE. Psoas as a sentinel muscle for sarcopenia: a flawed premise. J Cachexia Sarcopenia Muscle. 2017;8:527–8.

  33. Rutten IJG, Ubachs J, Kruitwagen R, Beets-Tan RGH, Olde Damink SWM, Van Gorp T. Psoas muscle area is not representative of total skeletal muscle area in the assessment of sarcopenia in ovarian cancer. J Cachexia Sarcopenia Muscle. 2017;8:630–8.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Simonsen C, de Heer P, Bjerre ED, et al. Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis. Ann Surg. 2018;268:58–69.

    PubMed  Google Scholar 

  35. Doyle SL, Bennett AM, Donohoe CL, et al. Establishing computed tomography-defined visceral fat area thresholds for use in obesity-related cancer research. Nutr Res. 2013;33:171–9.

    Article  PubMed  CAS  Google Scholar 

  36. Prado CM, Lieffers JR, McCargar LJ, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9:629–35.

    Article  PubMed  Google Scholar 

  37. Martin L. Diagnostic criteria for cancer cachexia: data versus dogma. Curr Opin Clin Nutr Metab Care. 2016;19:188–98.

    PubMed  Google Scholar 

  38. Bye A, Sjoblom B, Wentzel-Larsen T, et al. Muscle mass and association to quality of life in non-small cell lung cancer patients. J Cachexia Sarcopenia Muscle. 2017;8:759–67.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kuk JL, Saunders TJ, Davidson LE, Ross R. Age-related changes in total and regional fat distribution. Ageing Res Rev. 2009;8:339–48.

    Article  PubMed  Google Scholar 

  40. Rolland Y, Czerwinski S Fau-Abellan Van Kan G, Abellan Van Kan G Fau-Morley JE, et al. Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutr Health Aging. 2008;12:433–50.

  41. Kuchnia AJ, Teigen LM, Cole AJ, et al. Phase angle and impedance ratio: reference cut-points from the United States National Health and Nutrition Examination Survey 1999–2004 From Bioimpedance Spectroscopy Data. J Parenter Enteral Nutr. 2017;41:1310–15.

    Article  Google Scholar 

  42. Kirk PS, Friedman JF, Cron DC, et al. One-year postoperative resource utilization in sarcopenic patients. J Surg Res. 2015;199:51–5.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Lieffers JR, Bathe OF, Fassbender K, Winget M, Baracos VE. Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer. 2012;107:931–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Du Y, Karvellas CJ, Baracos V, et al. Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery. Surgery. 2014;156:521–7.

    Article  PubMed  Google Scholar 

  45. Nelson G, Kiyang LN, Crumley ET, et al. Implementation of enhanced recovery after surgery (ERAS) across a provincial healthcare system: the ERAS Alberta Colorectal Surgery Experience. World J Surg. 2016;40:1092–103.

    Article  PubMed  Google Scholar 

  46. Dindo D, Demartines N, Clavien P-A. Classification of surgical complications. Ann Surg. 2004;240:205–13.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE. 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. 2008;33:997–1006.

    Article  PubMed  Google Scholar 

  48. Shuster A, Patlas M, Pinthus JH, Mourtzakis M. The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol. 2012;85:1–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. van der Werf A, Dekker IM, Meijerink MR, Wierdsma NJ, de van der Schueren MAE, Langius JAE. Skeletal muscle analyses: agreement between non-contrast and contrast CT scan measurements of skeletal muscle area and mean muscle attenuation. Clin Physiol Funct Imaging. 2017;38:366–72.

    Article  PubMed  Google Scholar 

  50. van Vugt JLA, Coebergh van den Braak RRJ, Schippers HJW, et al. Contrast-enhancement influences skeletal muscle density, but not skeletal muscle mass, measurements on computed tomography. Clin Nutr. 2017. https://doi.org/10.1016/j.clnu.2017.07.007.

  51. Weaver BW, Wuensch K.L. SPSS and SAS programs for comparing Pearson correlations and OLS regression coefficients. Behav Res Methods. 2013;45:880–95.

  52. Austin P. A comparison of statistical modeling strategies for analyzing length of stay after CABG surgery. Health Serv Outcomes Res Methodol. 2003;3:107–33.

    Article  Google Scholar 

  53. Martin RCG, Brennan MF, Jaques DP. Quality of complication reporting in the surgical literature. Ann Surg. 2002;235:803–13.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Xiao J, Caan BJ, Weltzien E, et al. Associations of preexisting comorbidities with skeletal muscle mass and radiodensity in patients with non-metastatic colorectal cancer. J Cachexia Sarcopenia Muscle. 2018 https://doi.org/10.1002/jcsm.12301. Retrieved online 19 April 2018.

  55. 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;263:320–5.

    Article  PubMed  Google Scholar 

  56. Lohsiriwat V, Pongsanguansuk W, Lertakyamanee N, Lohsiriwat D. Impact of metabolic syndrome on the short-term outcomes of colorectal cancer surgery. Dis Colon Rectum. 2010;53:186–91.

    Article  PubMed  Google Scholar 

  57. Carli F, Gillis C, Scheede-Bergdahl C. Promoting a culture of prehabilitation for the surgical cancer patient. Acta Oncol. 2017;56:128–33.

    Article  PubMed  Google Scholar 

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Acknowledgment

Funding for Lisa Martin was provided by the Izaak Walton Killam Memorial Scholarship, an Alberta Innovates Health Solutions Graduate Research Studentship, and a C. Richard Fleming Grant from the ASPEN Rhoads Research Foundation. Project funding was provided by the Alberta Innovates Health Solutions Partnership for Research and Innovation in the Health System Grant and Alberta Health Services Cancer Strategic Clinical Network.

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Authors and Affiliations

  1. Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada

    Lisa Martin MSc, RD

  2. Department of Surgery, University of Alberta, Edmonton, AB, Canada

    Jessica Hopkins MD & Ron Brisebois MD

  3. Department of Oncology, 4023 Cross Cancer Institute, University of Alberta, Edmonton, AB, Canada

    Jessica Hopkins MD, Michael B. Sawyer MD & Vickie E. Baracos PhD

  4. Department of Surgery, St. Mark’s Hospital, Harrow, London, UK

    Georgios Malietzis PhD, MD & J. T. Jenkins MD

  5. Department of Surgery and Cancer, Imperial College, London, UK

    Georgios Malietzis PhD, MD & J. T. Jenkins MD

  6. Department of Surgery, University of Calgary, Calgary, AB, Canada

    Anthony MacLean MD

  7. Department of Oncology, University of Calgary, Calgary, AB, Canada

    Gregg Nelson PhD, MD

  8. Department of Medicine, University of Alberta, Edmonton, AB, Canada

    Leah Gramlich MD

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  1. Lisa Martin MSc, RD
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  2. Jessica Hopkins MD
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  10. Vickie E. Baracos PhD
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Correspondence to Vickie E. Baracos PhD.

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Martin, L., Hopkins, J., Malietzis, G. et al. Assessment of Computed Tomography (CT)-Defined Muscle and Adipose Tissue Features in Relation to Short-Term Outcomes After Elective Surgery for Colorectal Cancer: A Multicenter Approach. Ann Surg Oncol 25, 2669–2680 (2018). https://doi.org/10.1245/s10434-018-6652-x

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