Myosteatosis is associated with poor physical fitness in patients undergoing hepatopancreatobiliary surgery

Malcolm A West, David P J van Dijk, Fredrick Gleadowe, Thomas Reeves, John N Primrose, Mohammed Abu Hilal, Mark R Edwards, Sandy Jack, Sander S S Rensen, Michael P W Grocott, Denny Z H Levett, Steven W M Olde Damink, Malcolm A West, David P J van Dijk, Fredrick Gleadowe, Thomas Reeves, John N Primrose, Mohammed Abu Hilal, Mark R Edwards, Sandy Jack, Sander S S Rensen, Michael P W Grocott, Denny Z H Levett, Steven W M Olde Damink

Abstract

Background: Body composition assessment, measured using single-slice computed tomography (CT) image at L3 level, and aerobic physical fitness, objectively measured using cardiopulmonary exercise testing (CPET), are each independently used for perioperative risk assessment. Sarcopenia (i.e. low skeletal muscle mass), myosteatosis [i.e. low skeletal muscle radiation attenuation (SM-RA)], and impaired objectively measured aerobic fitness (reduced oxygen uptake) have been associated with poor post-operative outcomes and survival in various cancer types. However, the association between CT body composition and physical fitness has not been explored. In this study, we assessed the association of CT body composition with selected CPET variables in patients undergoing hepatobiliary and pancreatic surgery.

Methods: A pragmatic prospective cohort of 123 patients undergoing hepatobiliary and pancreatic surgery were recruited. All patients underwent preoperative CPET. Preoperative CT scans were analysed using a single-slice CT image at L3 level to assess skeletal muscle mass, adipose tissue mass, and muscle radiation attenuation. Multivariate linear regression was used to test the association between CPET variables and body composition. Main outcomes were oxygen uptake at anaerobic threshold ( V̇ O2 at AT), oxygen uptake at peak exercise ( V̇ O2 peak), skeletal muscle mass, and SM-RA.

Results: Of 123 patients recruited [77 men (63%), median age 66.9 ± 11.7, median body mass index 27.3 ± 5.2], 113 patients had good-quality abdominal CT scans available and were included. Of the CT body composition variables, SM-RA had the strongest correlation with V̇ O2 peak (r = 0.57, P < 0.001) and V̇ O2 at AT (r = 0.45, P < 0.001) while skeletal muscle mass was only weakly associated with V̇ O2 peak (r = 0.24, P < 0.010). In the multivariate analysis, only SM-RA was associated with V̇ O2 peak (B = 0.25, 95% CI 0.15-0.34, P < 0.001, R2 = 0.42) and V̇ O2 at AT (B = 0.13, 95% CI 0.06-0.18, P < 0.001, R2 = 0.26).

Conclusions: There is a positive association between preoperative CT SM-RA and preoperative physical fitness ( V̇ O2 at AT and at peak). This study demonstrates that myosteatosis, and not sarcopenia, is associated with reduced aerobic physical fitness. Combining both myosteatosis and physical fitness variables may provide additive risk stratification accuracy and guide interventions during the perioperative period.

Keywords: Body composition; Cardiopulmonary exercise testing; Myosteatosis; Oxygen uptake; Physical fitness; Sarcopenia.

Conflict of interest statement

Malcolm A. West was supported by a National Institute for Health Research Academic Clinical Lecturer Award (CL‐2016‐26‐002) and declares that he has no conflict of interest. David P. J. van Dijk was supported by the Netherlands Organisation for Scientific Research (NWO Grant 022.003.011) and declares that he has no conflict of interest. Fredrick Gleadowe declares that he has no conflict of interest. Thomas Reeves declares that he has no conflict of interest. John Primrose declares that he has no conflict of interest. Mohammed Abu Hilal declares that he has no conflict of interest. Mark R. Edwards declares that he has no conflict of interest. Sandy Jack declares that she has no conflict of interest. Sander S. S. Rensen declares that he has no conflict of interest. Michael P. W. Grocott declares that he has no conflict of interest. Denny Z. H. Levett declares that she has no conflict of interest. Steven W. M. Olde Damink declares that he has no conflict of interest.

© 2019 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by John Wiley & Sons Ltd on behalf of the Society on Sarcopenia, Cachexia and Wasting Disorders.

Figures

Figure 1
Figure 1
Gender‐specific CT body composition. Boxes represent median and inter‐quartile range. Whiskers are set at either the 25th or 75th percentiles + 1.5 times the inter‐quartile range (Tukey method). Dots represent outliers. *Significant P‐value < 0.05. CT, computed tomography; RA, radiation attenuation; SAT, subcutaneous adipose tissue; SM, skeletal muscle; VAT, visceral adipose tissue.
Figure 2
Figure 2
Correlations and regression plots of skeletal muscle radiation attenuation with V˙O2 at AT (mL·kg−1·min−1) and V˙O2 peak (mL·kg−1·min−1). Five patients did not reach their anaerobic threshold, and these patients were excluded from this analyses. HU, Hounsfield unit; SM‐RA, skeletal muscle radiation attenuation.

References

    1. Moran J, Wilson F, Guinan E, McCormick P, Hussey J, Moriarty J. Role of cardiopulmonary exercise testing as a risk‐assessment method in patients undergoing intra‐abdominal surgery: a systematic review. Br J Anaesth 2016;116:177–191.
    1. 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;41:186–196.
    1. Mei KL, Batsis JA, Mills JB, Holubar SD. Sarcopenia and sarcopenic obesity: do they predict inferior oncologic outcomes after gastrointestinal cancer surgery. Perioper Med 2016;5:30.
    1. Ozola Zalite I, Zykus R, Francisco Gonzalez M, Saygili F, Pukitis A, Gaujoux S, et al. Influence of cachexia and sarcopenia on survival in pancreatic ductal adenocarcinoma: a systematic review. Pancreatology 2015;15:19–24.
    1. Jones K, Gordon‐Weeks A, Coleman C, Silva M. Radiologically determined sarcopenia predicts morbidity and mortality following abdominal surgery: a systematic review and meta‐analysis. World J Surg 2017;41:2266–2279.
    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 2013;31:1539–1547.
    1. Reeves T, Bates S, Sharp T, Richardson K, Bali S, Plumb J, et al. Cardiopulmonary exercise testing (CPET) in the United Kingdom—a national survey of the structure, conduct, interpretation and funding. Perioper Med 2018;7:2.
    1. Levett DZH, Jack S, Swart M, Carlisle J, Wilson J, Snowden C, et al. Preoperative Cardiopulmonary Exercise Testing (PCPET): consensus clinical guidelines on indications, organisation, conduct and physiological interpretation. Br J Anaesth 2017;120:484–500.
    1. Levett DZH, Edwards M, Grocott M, Mythen M. Preparing the patient for surgery to improve outcomes. Best Pract Res Clin Anaesthesiol 2016;30:145–157.
    1. West MA, Lythgoe D, Barben CP, Noble L, Kemp GJ, Jack S, et al. Cardiopulmonary exercise variables are associated with postoperative morbidity after major colonic surgery: a prospective blinded observational study. Br J Anaesth 2014;112:665–671.
    1. West MA, Asher R, Browning M, Minto G, Swart M, Richardson K, et al. Validation of preoperative cardiopulmonary exercise testing‐derived variables to predict in‐hospital morbidity after major colorectal surgery. Br J Surg 2016;103:744–752.
    1. West MA, Parry MG, Lythgoe D, Barben CP, Kemp GJ, Grocott MPW, et al. Cardiopulmonary exercise testing for the prediction of morbidity risk after rectal cancer surgery. Br J Surg 2014;101:1166–1172.
    1. West MA, Loughney L, Barben CP, Sripadam R, Kemp GJ, Grocott MPW, et al. The effects of neoadjuvant chemoradiotherapy on physical fitness and morbidity in rectal cancer surgery patients. Eur J Surg Oncol 2014;40:1421–1428.
    1. Jack S, West MA, Raw D, Marwood S, Ambler G, Cope TM, et al. The effect of neoadjuvant chemotherapy on physical fitness and survival in patients undergoing oesophagogastric cancer surgery. Eur J Surg Oncol 2014;40:1313–1320.
    1. Ausania F, Snowden CP, Prentis JM, Holmes LR, Jaques BC, White SA, et al. Effects of low cardiopulmonary reserve on pancreatic leak following pancreaticoduodenectomy. Br J Surg 2012;99:1290–1294.
    1. Snowden CP, Prentis JM, Anderson HL, Roberts DR, Randles D, Renton M, et al. Submaximal cardiopulmonary exercise testing predicts complications and hospital length of stay in patients undergoing major elective surgery. Ann Surg 2010;251:535–541.
    1. Snowden CP, Prentis J, Jacques B, Anderson H, Manas D, Jones D, et al. Cardiorespiratory fitness predicts mortality and hospital length of stay after major elective surgery in older people. Ann Surg 2013;257:999–1004.
    1. Junejo MA, Mason JM, Sheen AJ, Moore J, Foster P, Atkinson D, et al. Cardiopulmonary exercise testing for preoperative risk assessment before hepatic resection. Br J Surg 2012;99:1097–1104.
    1. Junejo MA, Mason JM, Sheen AJ, Bryan A, Moore J, Foster P, et al. Cardiopulmonary exercise testing for preoperative risk assessment before pancreaticoduodenectomy for cancer. Ann Surg Oncol 2014;21:1929–1936.
    1. Mourtzakis M, Prado CMM, 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.
    1. Malietzis G, Johns N, Al‐Hassi HO, Knight SC, Kennedy RH, Fearon KCH, et al. Low muscularity and myosteatosis is related to the host systemic inflammatory response in patients undergoing surgery for colorectal cancer. Ann Surg 2016;263:320–325.
    1. Richards CH, Roxburgh CSD, MacMillan MT, Isswiasi S, Robertson EG, Guthrie GK, et al. The relationships between body composition and the systemic inflammatory response in patients with primary operable colorectal cancer. PLoS ONE 2012;7:e41883.
    1. Aubrey J, Esfandiari N, Baracos VE, Buteau FA, Frenette J, Putman CT, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol 2014;210:489–497.
    1. van Dijk DPJ, Bakens MJAM, Coolsen MME, Rensen SS, van Dam RM, Bours MJL, et al. Low skeletal muscle radiation attenuation and visceral adiposity are associated with overall survival and surgical site infections in patients with pancreatic cancer. J Cachexia Sarcopenia Muscle 2017;8:317–326.
    1. Reisinger KW, Van Vugt JLA, Tegels JJW, Snijders C, Hulsewé KWE, Hoofwijk AGM, et al. Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg 2015;261:345–352.
    1. Miyamoto Y, Baba Y, Sakamoto Y, Ohuchi M, Tokunaga R, Kurashige J, et al. Sarcopenia is a negative prognostic factor after curative resection of colorectal cancer. Ann Surg Oncol 2015;22:2663–2668.
    1. Palmela C, Velho S, Agostinho L, Branco F, Santos M, Santos M, et al. Body composition as a prognostic factor of neoadjuvant chemotherapy toxicity and outcome in patients with locally advanced gastric cancer. J Gastric Cancer 2017;17:74–87.
    1. Elliott JA, Doyle SL, Murphy CF, King S, Guinan EM, Beddy P, et al. Sarcopenia: prevalence, and impact on operative and oncologic outcomes in the multimodal management of locally advanced esophageal cancer. Ann Surg 2017;266:822–830.
    1. Yip C, Goh V, Davies A, Gossage J, Mitchell‐Hay R, Hynes O, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol 2014;24:998–1005.
    1. Rutten IJG, van Dijk DPJ, Kruitwagen RFPM, Beets‐Tan RGH, Olde Damink SWM, van Gorp T. Loss of skeletal muscle during neoadjuvant chemotherapy is related to decreased survival in ovarian cancer patients. J Cachexia Sarcopenia Muscle 2016;7:458–466.
    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 survival of patients with metastatic colorectal cancer. J Clin Oncol 2016;34:1339–1344.
    1. Peng PD, Van Vledder MG, Tsai S, De Jong MC, Makary M, Ng J, et al. Sarcopenia negatively impacts short‐term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. Hpb 2011;13:439–446.
    1. Van Vledder MG, Levolger S, Ayez N, Verhoef C, Tran TCK, Ijzermans JNM. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 2012;99:550–557.
    1. Lodewick TM, Van Nijnatten TJA, Van Dam RM, Van Mierlo K, Dello SAWG, Neumann UP, et al. Are sarcopenia, obesity and sarcopenic obesity predictive of outcome in patients with colorectal liver metastases? Hpb 2015;17:438–446.
    1. Gould DW, Lahart I, Carmichael AR, Koutedakis Y, Metsios GS. Cancer cachexia prevention via physical exercise: molecular mechanisms. J Cachexia Sarcopenia Muscle 2013;4:111–124.
    1. Proctor MJ, Morrison DS, Talwar D, Balmer SM, O'Reilly DSJ, Foulis AK, et al. An inflammation‐based prognostic score (mGPS) predicts cancer survival independent of tumour site: a Glasgow Inflammation Outcome Study. Br J Cancer 2011;104:726–734.
    1. Williams BA, Mandrekar JN, Mandrekar SJ, Cha SS, Furth AF. Finding optimal cutpoints for continuous covariates with binary and time‐to‐event outcomes. Mayo Clin Dep Heal Sci Res Tech Rep Ser 2006;79:1–26.
    1. Okumura S, Kaido T, Hamaguchi Y, Fujimoto Y, Masui T, Mizumoto M, et al. Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer. Surgery 2015;157:1088–1098.
    1. Fujiwara N, Nakagawa H, Kudo Y, Tateishi R, Taguri M, Watadani T, et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J Hepatol 2015;63:131–140.
    1. Rollins KE, Tewari N, Ackner A, Awwad A, Madhusudan S, Macdonald IA, et al. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin Nutr 2016;35:1103–1109.
    1. Heymsfield SB, Gonzalez MC, Lu J, Jia G, Zheng J. Skeletal muscle mass and quality: evolution of modern measurement concepts in the context of sarcopenia. Proc Nutr Soc 2015;74:355–366.
    1. Simioni C, Zauli G, Martelli AM, Vitale M, Sacchetti G, Gonelli A, et al. Oxidative stress: role of physical exercise and antioxidant nutraceuticals in adulthood and aging. Oncotarget 2018;9:17181–17198.
    1. Cortese‐Krott MM, Koning A, Kuhnle GGC, Nagy P, Bianco CL, Pasch A, et al. The reactive species interactome: evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine. Antioxid Redox Signal 2017;27:684–712.
    1. Dela F, Helge JW. Insulin resistance and mitochondrial function in skeletal muscle. Int J Biochem Cell Biol 2013;45:11–15.
    1. Robertson R, Boyce T, Dixon A. Commissioning and behaviour change: kicking bad habits final report. 2008. King's Fund. . Accessed 15 Oct 2018.
    1. Fiuza‐Luces C, Garatachea N, Berger NA, Lucia A. Exercise is the real polypill. Phys Ther 2013;28:330–358.
    1. Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN, Katzmarzyk PT, et al. Effect of physical inactivity on major non‐communicable diseases worldwide: an analysis of burden of disease and life expectancy. Lancet 2012;380:219–229.
    1. Kohl HW, Craig CL, Lambert EV, Inoue S, Alkandari JR, Leetongin G, et al. The pandemic of physical inactivity: global action for public health. Lancet 2012;380:294–305.
    1. Moore SC, Lee I‐M, Weiderpass E, Campbell PT, Sampson JN, Kitahara CM, et al. Association of leisure‐time physical activity with risk of 26 types of cancer in 1.44 million adults. JAMA Intern Med 2016;176:816–825.
    1. Kerr J, Anderson C, Lippman SM. Physical activity, sedentary behaviour, diet, and cancer: an update and emerging new evidence. Lancet Oncol 2017;18:457–471.
    1. Jones LW, Liang Y, Pituskin EN, Battaglini CL, Scott JM, Hornsby WE, et al. Effect of exercise training on peak oxygen consumption in patients with cancer: a meta‐analysis. Oncologist 2011;16:112–120.
    1. Levett DZH, Grocott MPW. Cardiopulmonary exercise testing, prehabilitation, and enhanced recovery after surgery (ERAS). Can J Anesth 2015;62:131–142.
    1. Dunne DFJ, Jones RP, Lythgoe DT, Pilkington FJ, Palmer DH, Malik HZ, et al. Cardiopulmonary exercise testing before liver surgery. J Surg Oncol 2014;110:439–444.
    1. Van Blarigan EL, Meyerhardt JA. Role of physical activity and diet after colorectal cancer diagnosis. J Clin Oncol 2015;33:1825–1834.
    1. Burke S, Wurz A, Bradshaw A, Saunders S, West MA, Brunet J. Physical activity and quality of life in cancer survivors: a meta‐synthesis of qualitative research. Cancer 2017;9:1–29.
    1. Fearon KC, Jenkins JT, Carli F, Lassen K. Patient optimization for gastrointestinal cancer surgery. Br J Surg 2013;100:15–27.
    1. Gillis C, Buhler K, Bresee L, Carli F, Gramlich L, Culos‐Reed N, et al. Effects of nutritional prehabilitation, with and without exercise, on outcomes of patients who undergo colorectal surgery: a systematic review and meta‐analysis. Gastroenterology 2018;155:391–410.
    1. Minnella EM, Bousquet‐Dion G, Awasthi R, Scheede‐Bergdahl C, Carli F. Multimodal prehabilitation improves functional capacity before and after colorectal surgery for cancer: a five‐year research experience. Acta Oncol 2017;56:295–300.
    1. van Rooijen SJ, Engelen MA, Scheede‐Bergdahl C, Carli F, Roumen RMH, Slooter GD, et al. Systematic review of exercise training in colorectal cancer patients during treatment. Scand J Med Sci Sports 2018;28:360–370.
    1. West MA, Wischmeyer PE, Grocott MPW. Prehabilitation and nutritional support to improve perioperative outcomes. Current Anesthesiology Reports 2017;7:340–349.
    1. O'Doherty AF, West M, Jack S, Grocott MPW. Preoperative aerobic exercise training in elective intra‐cavity surgery: a systematic review. Br J Anaesth 2013;110:679–689.
    1. Rebelo‐Marques A, Lages ADS, Andrade R, Ribeiro CF, Mota‐Pinto A, Carrilho F, et al. Aging hallmarks: the benefits of physical exercise. Front Endocrinol 2018;9:258.
    1. Maddocks M, Jones LW, Wilcock A. Immunological and hormonal effects of exercise: implications for cancer cachexia. Curr Opin Support Palliat Care 2013;7:376–382.
    1. Arthur H, Daniels C, McKelvie R, Hirsh J, Rush B. Effect of a preoperative intervention on preoperative and postoperative outcomes in low‐risk patients awaiting elective coronary artery bypass graft surgery. Ann Intern Med 2000;133:253–262.
    1. Barberan‐Garcia A, Ubré M, Roca J, Lacy AM, Burgos F, Risco R, et al. Personalised prehabilitation in high‐risk patients undergoing elective major abdominal surgery: a randomized blinded controlled trial. Ann Surg 2018;267:50–56.
    1. West MA, Loughney L, Lythgoe D, Barben CP, Sripadam R, Kemp GJ, et al. Effect of prehabilitation on objectively measured physical fitness after neoadjuvant treatment in preoperative rectal cancer patients: a blinded interventional pilot study. Br J Anaesth 2015;114:244–251.
    1. Stretch C, Aubin JM, Mickiewicz B, Leugner D, Al‐manasra T, Tobola E, et al. Sarcopenia and myosteatosis are accompanied by distinct biological profiles in patients with pancreatic and periampullary adenocarcinomas. PLoS ONE 2018;13:1–17.
    1. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2017. J Cachexia Sarcopenia Muscle 2017;8:1081–1083.

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