Sarcopenia defined by muscle quality rather than quantity predicts complications following laparoscopic right hemicolectomy

  • James TankelEmail author
  • Shlomo Yellinek
  • Elena Vainberg
  • Yotam David
  • Dmitry Greenman
  • James Kinross
  • Petachia Reissman
Original Article



While sarcopenia has prognostic value in elective colorectal surgery for predicting peri-operative morbidity and mortality, its role in elective laparoscopic surgery is poorly defined.


A retrospective single-center analysis of patients undergoing elective laparoscopic right hemicolectomy for adenocarcinoma between January 2010 and December 2016. Univariate analysis compared the robustness of total psoas index (TPI) with Hounsfield unit average calculation (HUAC) calculated from pre-operative CT imaging in predicting post-operative complications. Multivariate analysis compared these measures with American Society of Anesthesiologists (ASA) grade and Charlson scores in predicting post-operative complications.


Of the 580 patients identified, 185 met the inclusion criteria (91 males and 94 females, with a median age of 68). Using TPI and HUAC, 46 and 44 patients respectively were identified as sarcopenic, including 18 patients that were identified by both measures. HUAC-defined sarcopenia was significantly associated with pre-operative comorbidities, peri-operative mortality, and a greater incidence of respiratory, cardiac, and serious post-operative complications (Clavien-Dindo ≥ 3). Those with HUAC-defined sarcopenia aged > 75 were at particular risk of morbidity (OR 5.52, p = 0.002). No such relationships were found with TPI-defined sarcopenia. Only HUAC remained predictive of post-operative complications on multivariate analysis.


Sarcopenia is a novel methodology for stratifying surgical risk in elective colorectal cancer surgery. HUAC has a high prognostic accuracy for the prediction of complications following laparoscopic colorectal surgery compared with TPI, ASA grade, and Charlson score.


Laparoscopic Sarcopenia Colorectal cancer Complications 


Author contribution

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by JT, SY, EV, YD, and DG. The first draft of the manuscript was written by JT, SY, and JK, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of our institutional research committee (0105-17-SZMC) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39:412–423. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Levolger S, Van Vugt JLA, De Bruin RWF, IJzermans JNM (2015) Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg 102:1448–1458CrossRefGoogle Scholar
  3. 3.
    Prado CMM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, Mackey JR, Koski S, Pituskin E, Sawyer MB (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res 15:2920–2926. CrossRefPubMedGoogle Scholar
  4. 4.
    Buettner S, Wagner D, Kim Y, Margonis GA, Makary MA,Wilson A, Sasaki K, Amini N, Gani F, Pawlik TM (2016) Inclusion of Sarcopenia Outperforms the Modified Frailty Index in Predicting 1-Year Mortality among 1,326 Patients Undergoing Gastrointestinal Surgery for a Malignant Indication. J Am Coll Surg 222(4):397–407. CrossRefGoogle Scholar
  5. 5.
    Bokshan SL, Han AL, DePasse JM, Eltorai AE, Marcaccio SE, Palumbo MA, Daniels AH (2016) Effect of sarcopenia on postoperative morbidity and mortality after thoracolumbar spine surgery. Orthopedics 39:e1159–e1164. CrossRefPubMedGoogle Scholar
  6. 6.
    Lieffers JR, Bathe OF, Fassbender K et al (2012) Sarcopenia is associated with postoperative infection and delayed recovery from colorectal cancer resection surgery. Br J Cancer 107:931–936. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Reisinger KW, Van Vugt JLA, Tegels JJW et al (2015) Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg. CrossRefGoogle Scholar
  8. 8.
    Huang DD, Wang SL, Zhuang CL, Zheng BS, Lu JX, Chen FF, Zhou CJ, Shen X, Yu Z (2015) Sarcopenia, as defined by low muscle mass, strength and physical performance, predicts complications after surgery for colorectal cancer. Color Dis 17:O256–O264. CrossRefGoogle Scholar
  9. 9.
    Boer BC, de Graaff F, Brusse-Keizer M, Bouman DE, Slump CH, Slee-Valentijn M, Klaase JM (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. CrossRefGoogle Scholar
  10. 10.
    Wagner D, DeMarco MM, Amini N, Buttner S, Segev D, Gani F, Pawlik TM (2016) Role of frailty and sarcopenia in predicting outcomes among patients undergoing gastrointestinal surgery. World J Gastrointest Surg 8(1):27–40. CrossRefGoogle Scholar
  11. 11.
    Jones KI, Doleman B, Scott S, Lund JN, Williams JP (2015) 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. CrossRefGoogle Scholar
  12. 12.
    (AJCC) AJC on C (2017) AJCC Cancer Staging ManualGoogle Scholar
  13. 13.
    Peng P, Hyder O, Firoozmand A, Kneuertz P, Schulick RD, Huang D, Makary M, Hirose K, Edil B, Choti MA, Herman J, Cameron JL, Wolfgang CL, Pawlik TM (2012) Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg 16:1478–1486. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Peng PD, Van Vledder MG, Tsai S et al (2011) Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB 13:439–446. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Prado CM, Lieffers JR, McCargar LJ et al (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. CrossRefGoogle Scholar
  16. 16.
    Joglekar S, Asghar A, Mott SL et al (2015) Sarcopenia is an independent predictor of complications following pancreatectomy for adenocarcinoma. In: Journal of Surgical Oncology. pp 771–775CrossRefGoogle Scholar
  17. 17.
    Zuckerman J, Ades M, Mullie L et al (2017) Psoas muscle area and length of stay in older adults undergoing cardiac operations. Ann Thorac Surg. CrossRefGoogle Scholar
  18. 18.
    Tan KY, Kawamura YJ, Tokomitsu A, Tang T (2012) Assessment for frailty is useful for predicting morbidity in elderly patients undergoing colorectal cancer resection whose comorbidities are already optimized. Am J Surg. CrossRefGoogle Scholar
  19. 19.
    Nakanishi R, Oki E, Sasaki S, Hirose K, Jogo T, Edahiro K, Korehisa S, Taniguchi D, Kudo K, Kurashige J, Sugiyama M, Nakashima Y, Ohgaki K, Saeki H, Maehara Y (2018) Sarcopenia is an independent predictor of complications after colorectal cancer surgery. Surg Today 48:151–157. CrossRefPubMedGoogle Scholar
  20. 20.
    Schneider EB, Hyder O, Brooke BS et al (2012) Patient readmission and mortality after colorectal surgery for colon cancer: impact of length of stay relative to other clinical factors. J Am Coll Surg. CrossRefGoogle Scholar
  21. 21.
    Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy AM, Colon cancer Laparoscopic or Open Resection Study Group (COLOR) (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484. CrossRefPubMedGoogle Scholar
  22. 22.
    Boni L, Benevento A, Rovera F et al (2006) Infective complications in laparoscopic surgery. Surg Infect. CrossRefGoogle Scholar
  23. 23.
    Novitsky YW, Litwin DEM, Callery MP (2004) The net immunologic advantage of laparoscopic surgery. Surg. Endosc. Other Interv, TechCrossRefGoogle Scholar
  24. 24.
    Zerey M, Hawver LM, Awad Z et al (2013) SAGES evidence-based guidelines for the laparoscopic resection of curable colon and rectal cancer. Surg EndoscGoogle Scholar
  25. 25.
    Masoomi H, Buchberg B, Dang P et al (2011) Outcomes of right vs. left colectomy for colon cancer. J Gastrointest Surg. CrossRefGoogle Scholar
  26. 26.
    Nfonsam V, Aziz H, Pandit V, Khalil M, Jandova J, Joseph B (2016) Analyzing clinical outcomes in laparoscopic right vs. left colectomy in colon cancer patients using the NSQIP database. Cancer Treat Commun 8:1–4. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kwaan MR, Al-Refaie WB, Parsons HM et al (2013) Are right-sided colectomy outcomes different from left-sided colectomy outcomes?: study of patients with colon cancer in the ACS NSQIP database. JAMA Surg 148:504–510. CrossRefPubMedGoogle Scholar
  28. 28.
    Benedix F, Kube R, Meyer F et al (2010) Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. CrossRefGoogle Scholar
  29. 29.
    Delmonico MJ, Harris TB, Visser M et al (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr.
  30. 30.
    Malietzis G, Johns N, Al-Hassi HO et al (2015) Low muscularity and myosteatosis is related to the host systemic inflammatory response in patients undergoing surgery for colorectal cancer. Ann Surg. CrossRefGoogle Scholar
  31. 31.
    Sabel MS, Terjimanian M, Conlon ASC et al (2013) Analytic morphometric assessment of patients undergoing colectomy for colon cancer. J Surg Oncol. CrossRefGoogle Scholar
  32. 32.
    Okumura S, Kaido T, Hamaguchi Y et al (2016) Impact of the preoperative quantity and quality of skeletal muscle on outcomes after resection of extrahepatic biliary malignancies. Surgery (United States). CrossRefGoogle Scholar
  33. 33.
    Rutten IJG, Ubachs J, Kruitwagen RFPM, Beets-Tan RGH, Olde Damink SWM, van Gorp T (2017) Psoas muscle area is not representative of total skeletal muscle area in the assessment of sarcopenia in ovarian cancer. J Cachexia Sarcopenia Muscle 8:630–638. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Amini N, Spolverato G, Gupta R, Margonis GA, Kim Y, Wagner D, Rezaee N, Weiss MJ, Wolfgang CL, Makary MM, Kamel IR, Pawlik TM (2015) Impact total psoas volume on short- and long-term outcomes in patients undergoing curative resection for pancreatic adenocarcinoma: a new tool to assess sarcopenia. J Gastrointest Surg 19:1593–1602. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Barbat-Artigas S, Rolland Y, Vellas B, Aubertin-Leheudre M (2013) Muscle quantity is not synonymous with muscle quality. J Am Med Dir Assoc. CrossRefGoogle Scholar
  36. 36.
    Goodpaster BH, Park SW, Harris TB et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. CrossRefGoogle Scholar
  37. 37.
    Correa CS, Baroni BM, Radaelli R, Lanferdini FJ, Cunha GDS, Reischak-Oliveira Á, Vaz MA, Pinto RS (2013) Effects of strength training and detraining on knee extensor strength, muscle volume and muscle quality in elderly women. Age (Omaha) 35:1899–1904. CrossRefGoogle Scholar
  38. 38.
    Boutin RD, Kaptuch JM, Bateni CP et al (2016) Influence of IV contrast administration on CT measures of muscle and bone attenuation: implications for sarcopenia and osteoporosis evaluation. Am J Roentgenol. CrossRefGoogle Scholar
  39. 39.
    Motoori M, Fujitani K, Sugimura K et al (2018) Skeletal muscle loss during neoadjuvant chemotherapy is an independent risk factor for postoperative infectious complications in patients with advanced esophageal cancer. Oncology. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • James Tankel
    • 1
    • 2
    Email author
  • Shlomo Yellinek
    • 1
  • Elena Vainberg
    • 3
  • Yotam David
    • 1
  • Dmitry Greenman
    • 1
    • 4
  • James Kinross
    • 2
  • Petachia Reissman
    • 1
  1. 1.Department of General Surgery, Shaare Zedek Medical CenterThe Hebrew University School of MedicineJerusalemIsrael
  2. 2.Department of Surgery and Cancer, Imperial College Healthcare TrustSt Mary’s HospitalLondonUK
  3. 3.Department of Radiology, Shaare Zedek Medical CenterThe Hebrew University School of MedicineJerusalemIsrael
  4. 4.Department of Anesthesiology, Perioperative Medicine and Pain Treatment, Shaare Zedek Medical CenterThe Hebrew Univeristy School of MedicineJerusalemIsrael

Personalised recommendations