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Published in: European Journal of Medical Research 1/2021

Open Access 01-12-2021 | Computed Tomography | Research

Risk factors for surgery-related muscle quantity and muscle quality loss and their impact on outcome

Authors: Laura van Wijk, Stijn van Duinhoven, Mike S. L. Liem, Donald E. Bouman, Alain R. Viddeleer, Joost M. Klaase

Published in: European Journal of Medical Research | Issue 1/2021

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Abstract

Background

Surgery-related loss of muscle quantity negatively affects postoperative outcomes. However, changes of muscle quality have not been fully investigated. A perioperative intervention targeting identified risk factors could improve postoperative outcome. This study investigated risk factors for surgery-related loss of muscle quantity and quality and outcomes after liver resection for colorectal liver metastasis (CRLM).

Methods

Data of patients diagnosed with CRLM who underwent liver resection between 2006 and 2016 were analysed. Muscle quantity (psoas muscle index [PMI]), and muscle quality, (average muscle radiation attenuation [AMA] of the psoas), were measured using computed tomography. Changes in PMI and AMA of psoas after surgery were assessed.

Results

A total of 128 patients were analysed; 67 (52%) had surgery-related loss of muscle quantity and 83 (65%) muscle quality loss. Chronic obstructive pulmonary disease (COPD) (P = 0.045) and diabetes (P = 0.003) were risk factors for surgery-related loss of muscle quantity. A higher age (P = 0.002), open resection (P = 0.003) and longer operation time (P = 0.033) were associated with muscle quality loss. Overall survival was lower in patients with both muscle quantity and quality loss compared to other categories (P = 0.049). The rate of postoperative complications was significantly higher in the group with surgery-related loss of muscle quality.

Conclusions

Risk factors for surgery-related muscle loss were identified. Overall survival was lowest in patients with both muscle quantity and quality loss. Complication rate was higher in patients with surgery-related loss of muscle quality.
Literature
1.
go back to reference van der Pool AE, Lalmahomed ZS, de Wilt JH, Eggermont AM, Ijzermans JN, Verhoef C. Trends in treatment for synchronous colorectal liver metastases: differences in outcome before and after 2000. J Surg Oncol. 2010;102(5):413–8.PubMedCrossRef van der Pool AE, Lalmahomed ZS, de Wilt JH, Eggermont AM, Ijzermans JN, Verhoef C. Trends in treatment for synchronous colorectal liver metastases: differences in outcome before and after 2000. J Surg Oncol. 2010;102(5):413–8.PubMedCrossRef
2.
go back to reference Lalmahomed ZS, Ayez N, van der Pool AE, Verheij J, IJzermans JN, Verhoef C. Anatomical versus nonanatomical resection of colorectal liver metastases: is there a difference in surgical and oncological outcome? World J Surg. 2011;35(3):656–61.PubMedCrossRef Lalmahomed ZS, Ayez N, van der Pool AE, Verheij J, IJzermans JN, Verhoef C. Anatomical versus nonanatomical resection of colorectal liver metastases: is there a difference in surgical and oncological outcome? World J Surg. 2011;35(3):656–61.PubMedCrossRef
3.
go back to reference Dimick JB, Cowan JA, Knol JA, Upchurch GR. Hepatic resection in the United States: indications, outcomes, and hospital procedural volumes from a nationally representative database. Arch Surg. 2003;138(2):185–91.PubMedCrossRef Dimick JB, Cowan JA, Knol JA, Upchurch GR. Hepatic resection in the United States: indications, outcomes, and hospital procedural volumes from a nationally representative database. Arch Surg. 2003;138(2):185–91.PubMedCrossRef
4.
go back to reference Jarnagin WR, Gonen M, Fong Y, DeMatteo RP, Ben-Porat L, Little S, et al. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg. 2002;236(4):397–407.PubMedPubMedCentralCrossRef Jarnagin WR, Gonen M, Fong Y, DeMatteo RP, Ben-Porat L, Little S, et al. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg. 2002;236(4):397–407.PubMedPubMedCentralCrossRef
5.
go back to reference Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006;94(7):982–99.PubMedPubMedCentralCrossRef Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006;94(7):982–99.PubMedPubMedCentralCrossRef
6.
go back to reference Laurent C, Sa Cunha A, Couderc P, Rullier E, Saric J. Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg. 2003;90(9):1131–6.PubMedCrossRef Laurent C, Sa Cunha A, Couderc P, Rullier E, Saric J. Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg. 2003;90(9):1131–6.PubMedCrossRef
7.
go back to reference Vigano L, Ferrero A, Lo Tesoriere R, Capussotti L. Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol. 2008;15(9):2458–64.PubMedCrossRef Vigano L, Ferrero A, Lo Tesoriere R, Capussotti L. Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol. 2008;15(9):2458–64.PubMedCrossRef
8.
go back to reference 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 (Oxford). 2011;13(7):439–46.CrossRef 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 (Oxford). 2011;13(7):439–46.CrossRef
9.
go back to reference 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(4):550–7.PubMedCrossRef 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(4):550–7.PubMedCrossRef
10.
go back to reference 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. 2016;57:58–67.PubMedCrossRef 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. 2016;57:58–67.PubMedCrossRef
11.
go back to reference Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Malpica L, Williams GR. Myosteatosis and prognosis in cancer: systematic review and meta-analysis. Crit Rev Oncol Hematol. 2020;145:102839.PubMedCrossRef Aleixo GFP, Shachar SS, Nyrop KA, Muss HB, Malpica L, Williams GR. Myosteatosis and prognosis in cancer: systematic review and meta-analysis. Crit Rev Oncol Hematol. 2020;145:102839.PubMedCrossRef
12.
go back to reference van Dijk DP, Bakens MJ, Coolsen MM, Rensen SS, van Dam RM, Bours MJ, 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(2):317–26.PubMedCrossRef van Dijk DP, Bakens MJ, Coolsen MM, Rensen SS, van Dam RM, Bours MJ, 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(2):317–26.PubMedCrossRef
13.
go back to reference Weerink LBM, van der Hoorn A, van Leeuwen BL, de Bock GH. Low skeletal muscle mass and postoperative morbidity in surgical oncology: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2020;11:636–49.PubMedPubMedCentralCrossRef Weerink LBM, van der Hoorn A, van Leeuwen BL, de Bock GH. Low skeletal muscle mass and postoperative morbidity in surgical oncology: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle. 2020;11:636–49.PubMedPubMedCentralCrossRef
14.
go back to reference Otsuji H, Yokoyama Y, Ebata T, Igami T, Sugawara G, Mizuno T, et al. Surgery-related muscle loss and its association with postoperative complications after major Hepatectomy with Extrahepatic bile duct resection. World J Surg. 2017;41(2):498–507.PubMedCrossRef Otsuji H, Yokoyama Y, Ebata T, Igami T, Sugawara G, Mizuno T, et al. Surgery-related muscle loss and its association with postoperative complications after major Hepatectomy with Extrahepatic bile duct resection. World J Surg. 2017;41(2):498–507.PubMedCrossRef
15.
go back to reference Zarinsefat A, Terjimanian MN, Sheetz KH, Stein IC, Mazurek AA, Waits SA, et al. Perioperative changes in trunk musculature and postoperative outcomes. J Surg Res. 2014;191(1):106–12.PubMedCrossRef Zarinsefat A, Terjimanian MN, Sheetz KH, Stein IC, Mazurek AA, Waits SA, et al. Perioperative changes in trunk musculature and postoperative outcomes. J Surg Res. 2014;191(1):106–12.PubMedCrossRef
16.
go back to reference Huang DD, Ji YB, Zhou DL, Li B, Wang SL, Chen XL, et al. Effect of surgery-induced acute muscle wasting on postoperative outcomes and quality of life. J Surg Res. 2017;218:58–66.PubMedCrossRef Huang DD, Ji YB, Zhou DL, Li B, Wang SL, Chen XL, et al. Effect of surgery-induced acute muscle wasting on postoperative outcomes and quality of life. J Surg Res. 2017;218:58–66.PubMedCrossRef
17.
go back to reference Choi MH, Yoon SB, Lee K, Song M, Lee IS, Lee MA, et al. Preoperative sarcopenia and post-operative accelerated muscle loss negatively impact survival after resection of pancreatic cancer. J Cachexia Sarcopenia Muscle. 2018;9(2):326–34.PubMedPubMedCentralCrossRef Choi MH, Yoon SB, Lee K, Song M, Lee IS, Lee MA, et al. Preoperative sarcopenia and post-operative accelerated muscle loss negatively impact survival after resection of pancreatic cancer. J Cachexia Sarcopenia Muscle. 2018;9(2):326–34.PubMedPubMedCentralCrossRef
18.
go back to reference Kobayashi A, Kaido T, Hamaguchi Y, Okumura S, Taura K, Hatano E, et al. Impact of postoperative changes in sarcopenic factors on outcomes after hepatectomy for hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2016;23(1):57–64.PubMedCrossRef Kobayashi A, Kaido T, Hamaguchi Y, Okumura S, Taura K, Hatano E, et al. Impact of postoperative changes in sarcopenic factors on outcomes after hepatectomy for hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2016;23(1):57–64.PubMedCrossRef
19.
go back to reference Chong CCN, Chung WY, Cheung YS, Fung AKY, Fong AKW, Lok HT, et al. Enhanced recovery after surgery for liver resection. Hong Kong Med J. 2019;25(2):94–101.PubMed Chong CCN, Chung WY, Cheung YS, Fung AKY, Fong AKW, Lok HT, et al. Enhanced recovery after surgery for liver resection. Hong Kong Med J. 2019;25(2):94–101.PubMed
20.
go back to reference 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(3):489–97.CrossRef 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(3):489–97.CrossRef
21.
go back to reference Okugawa Y, Toiyama Y, Yamamoto A, Shigemori T, Kitamura A, Ichikawa T, et al. close relationship between immunological/inflammatory markers and myopenia and myosteatosis in patients with colorectal cancer: a propensity score matching analysis. JPEN J Parenter Enteral Nutr. 2019;43(4):508–15.PubMedCrossRef Okugawa Y, Toiyama Y, Yamamoto A, Shigemori T, Kitamura A, Ichikawa T, et al. close relationship between immunological/inflammatory markers and myopenia and myosteatosis in patients with colorectal cancer: a propensity score matching analysis. JPEN J Parenter Enteral Nutr. 2019;43(4):508–15.PubMedCrossRef
22.
go back to reference Sun Z, Liu L, Liu N, Liu Y. Muscular response and adaptation to diabetes mellitus. Front Biosci. 2008;13:4765–94.PubMedCrossRef Sun Z, Liu L, Liu N, Liu Y. Muscular response and adaptation to diabetes mellitus. Front Biosci. 2008;13:4765–94.PubMedCrossRef
23.
24.
go back to reference Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32(11):1993–7.PubMedPubMedCentralCrossRef Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32(11):1993–7.PubMedPubMedCentralCrossRef
25.
go back to reference Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R, et al. An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;189(9):15.CrossRef Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R, et al. An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;189(9):15.CrossRef
26.
27.
go back to reference Jaitovich A, Barreiro E. Skeletal muscle dysfunction in chronic obstructive pulmonary disease. What we know and can do for our patients. Am J Respir Crit Care Med. 2018;198(2):175–86.PubMedPubMedCentralCrossRef Jaitovich A, Barreiro E. Skeletal muscle dysfunction in chronic obstructive pulmonary disease. What we know and can do for our patients. Am J Respir Crit Care Med. 2018;198(2):175–86.PubMedPubMedCentralCrossRef
28.
go back to reference Barreiro E, Jaitovich A. Muscle atrophy in chronic obstructive pulmonary disease: molecular basis and potential therapeutic targets. J Thorac Dis. 2018;10(Suppl 12):S1415–24.PubMedPubMedCentralCrossRef Barreiro E, Jaitovich A. Muscle atrophy in chronic obstructive pulmonary disease: molecular basis and potential therapeutic targets. J Thorac Dis. 2018;10(Suppl 12):S1415–24.PubMedPubMedCentralCrossRef
29.
go back to reference Abrigo J, Elorza AA, Riedel CA, Vilos C, Simon F, Cabrera D, et al. Role of oxidative stress as key regulator of muscle wasting during cachexia. Oxid Med Cell Longev. 2018;2018:2063179.PubMedPubMedCentralCrossRef Abrigo J, Elorza AA, Riedel CA, Vilos C, Simon F, Cabrera D, et al. Role of oxidative stress as key regulator of muscle wasting during cachexia. Oxid Med Cell Longev. 2018;2018:2063179.PubMedPubMedCentralCrossRef
31.
go back to reference Wilkinson DJ, Piasecki M, Atherton PJ. The age-related loss of skeletal muscle mass and function: measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev. 2018;47:123–32.PubMedPubMedCentralCrossRef Wilkinson DJ, Piasecki M, Atherton PJ. The age-related loss of skeletal muscle mass and function: measurement and physiology of muscle fibre atrophy and muscle fibre loss in humans. Ageing Res Rev. 2018;47:123–32.PubMedPubMedCentralCrossRef
32.
go back to reference van Vugt JLA, van den Coebergh 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. 2018;37(5):1707–14.PubMedCrossRef van Vugt JLA, van den Coebergh 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. 2018;37(5):1707–14.PubMedCrossRef
33.
go back to reference McMahon CJ, Wu JS, Eisenberg RL. Muscle edema. AJR Am J Roentgenol. 2010;194(4):284.CrossRef McMahon CJ, Wu JS, Eisenberg RL. Muscle edema. AJR Am J Roentgenol. 2010;194(4):284.CrossRef
34.
go back to reference Goodpaster BH, Kelley DE, Leland Thaete F, He J, Ross R. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol. 2000;89(1):104–10.PubMedCrossRef Goodpaster BH, Kelley DE, Leland Thaete F, He J, Ross R. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol. 2000;89(1):104–10.PubMedCrossRef
35.
go back to reference Aoyama T, Kawabe T, Hirohito F, Hayashi T, Yamada T, Tsuchida K, et al. Body composition analysis within 1 month after gastrectomy for gastric cancer. Gastric Cancer. 2016;19(2):645–50.PubMedCrossRef Aoyama T, Kawabe T, Hirohito F, Hayashi T, Yamada T, Tsuchida K, et al. Body composition analysis within 1 month after gastrectomy for gastric cancer. Gastric Cancer. 2016;19(2):645–50.PubMedCrossRef
36.
go back to reference Helander EM, Webb MP, Menard B, Prabhakar A, Helmstetter J, Cornett EM, et al. Metabolic and the surgical stress response considerations to improve postoperative recovery. Curr Pain Headache Rep. 2019;23(5):33–4.PubMedCrossRef Helander EM, Webb MP, Menard B, Prabhakar A, Helmstetter J, Cornett EM, et al. Metabolic and the surgical stress response considerations to improve postoperative recovery. Curr Pain Headache Rep. 2019;23(5):33–4.PubMedCrossRef
37.
go back to reference Carli F. Physiologic considerations of Enhanced Recovery After Surgery (ERAS) programs: implications of the stress response. Can J Anaesth. 2015;62(2):110–9.PubMedCrossRef Carli F. Physiologic considerations of Enhanced Recovery After Surgery (ERAS) programs: implications of the stress response. Can J Anaesth. 2015;62(2):110–9.PubMedCrossRef
38.
go back to reference Thorell A, Nygren J, Ljungqvist O. Insulin resistance: a marker of surgical stress. Curr Opin Clin Nutr Metab Care. 1999;2(1):69–78.PubMedCrossRef Thorell A, Nygren J, Ljungqvist O. Insulin resistance: a marker of surgical stress. Curr Opin Clin Nutr Metab Care. 1999;2(1):69–78.PubMedCrossRef
39.
go back to reference Scott MJ, Miller TE. Pathophysiology of major surgery and the role of enhanced recovery pathways and the anesthesiologist to improve outcomes. Anesthesiol Clin. 2015;33(1):79–91.PubMedCrossRef Scott MJ, Miller TE. Pathophysiology of major surgery and the role of enhanced recovery pathways and the anesthesiologist to improve outcomes. Anesthesiol Clin. 2015;33(1):79–91.PubMedCrossRef
40.
go back to reference Judith EK, Laura VW, Carlijn IB, Alain RV, Geertruida H, Cees P, et al. Impact and risk factors for clinically relevant surgery-related muscle loss in patients after major abdominal cancer surgery: study protocol for a prospective observational cohort study (MUSCLE POWER). Int J Clin Trials. 2019;6(3):138.CrossRef Judith EK, Laura VW, Carlijn IB, Alain RV, Geertruida H, Cees P, et al. Impact and risk factors for clinically relevant surgery-related muscle loss in patients after major abdominal cancer surgery: study protocol for a prospective observational cohort study (MUSCLE POWER). Int J Clin Trials. 2019;6(3):138.CrossRef
41.
go back to reference Deutz NE, Bauer JM, Barazzoni R, Biolo G, Boirie Y, Bosy-Westphal A, et al. Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Clin Nutr. 2014;33(6):929–36.PubMedPubMedCentralCrossRef Deutz NE, Bauer JM, Barazzoni R, Biolo G, Boirie Y, Bosy-Westphal A, et al. Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Clin Nutr. 2014;33(6):929–36.PubMedPubMedCentralCrossRef
42.
go back to reference Snijders T, Trommelen J, Kouw IWK, Holwerda AM, Verdijk LB, van Loon LJC. The impact of pre-sleep protein ingestion on the skeletal muscle adaptive response to exercise in humans: an update. Front Nutr. 2019;6:17.PubMedPubMedCentralCrossRef Snijders T, Trommelen J, Kouw IWK, Holwerda AM, Verdijk LB, van Loon LJC. The impact of pre-sleep protein ingestion on the skeletal muscle adaptive response to exercise in humans: an update. Front Nutr. 2019;6:17.PubMedPubMedCentralCrossRef
43.
go back to reference Beaudart C, Dawson A, Shaw SC, Harvey NC, Kanis JA, Binkley N, et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int. 2017;28(6):1817–33.PubMedPubMedCentralCrossRef Beaudart C, Dawson A, Shaw SC, Harvey NC, Kanis JA, Binkley N, et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int. 2017;28(6):1817–33.PubMedPubMedCentralCrossRef
44.
go back to reference Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, et al. Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2012;13(8):713–9.PubMedCrossRef Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, et al. Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. 2012;13(8):713–9.PubMedCrossRef
45.
go back to reference Kouw IW, Holwerda AM, Trommelen J, Kramer IF, Bastiaanse J, Halson SL, et al. Protein ingestion before sleep increases overnight muscle protein synthesis rates in healthy older men: a randomized controlled trial. J Nutr. 2017;147(12):2252–61.PubMedCrossRef Kouw IW, Holwerda AM, Trommelen J, Kramer IF, Bastiaanse J, Halson SL, et al. Protein ingestion before sleep increases overnight muscle protein synthesis rates in healthy older men: a randomized controlled trial. J Nutr. 2017;147(12):2252–61.PubMedCrossRef
46.
go back to reference Hanada M, Soyama A, Hidaka M, Nagura H, Oikawa M, Tsuji A, et al. Effects of quadriceps muscle neuromuscular electrical stimulation in living donor liver transplant recipients: phase-II single-blinded randomized controlled trial. Clin Rehabil. 2019;33(5):875–84.PubMedCrossRef Hanada M, Soyama A, Hidaka M, Nagura H, Oikawa M, Tsuji A, et al. Effects of quadriceps muscle neuromuscular electrical stimulation in living donor liver transplant recipients: phase-II single-blinded randomized controlled trial. Clin Rehabil. 2019;33(5):875–84.PubMedCrossRef
Metadata
Title
Risk factors for surgery-related muscle quantity and muscle quality loss and their impact on outcome
Authors
Laura van Wijk
Stijn van Duinhoven
Mike S. L. Liem
Donald E. Bouman
Alain R. Viddeleer
Joost M. Klaase
Publication date
01-12-2021
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2021
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-021-00507-9

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