Journal of Gastrointestinal Surgery

, Volume 19, Issue 2, pp 272–281 | Cite as

Sarcopenia Adversely Impacts Postoperative Complications Following Resection or Transplantation in Patients with Primary Liver Tumors

  • Vicente ValeroIII
  • Neda Amini
  • Gaya Spolverato
  • Matthew J. Weiss
  • Kenzo Hirose
  • Nabil N. Dagher
  • Christopher L. Wolfgang
  • Andrew A. Cameron
  • Benjamin Philosophe
  • Ihab R. Kamel
  • Timothy M. PawlikEmail author
Original Article



Sarcopenia is a surrogate marker of patient frailty that estimates the physiologic reserve of an individual patient. We sought to investigate the impact of sarcopenia on short- and long-term outcomes in patients having undergone surgical intervention for primary hepatic malignancies.


Ninety-six patients who underwent hepatic resection or liver transplantation for HCC or ICC at the John Hopkins Hospital between 2000 and 2013 met inclusion criteria. Sarcopenia was assessed by the measurement of total psoas major volume (TPV) and total psoas area (TPA). The impact of sarcopenia on perioperative complications and survival was assessed.


Mean age was 61.9 years and most patients were men (61.4 %). Mean adjusted TPV was lower in women (23.3 cm3/m) versus men (34.9 cm3/m) (P < 0.01); 47 patients (48.9 %) had sarcopenia. The incidence of a postoperative complication was 40.4 % among patients with sarcopenia versus 18.4 % among patients who did not have sarcopenia (P = 0.01). Of note, all Clavien grade ≥3 complications (n = 11, 23.4 %) occurred in the sarcopenic group. On multivariable analysis, the presence of sarcopenia was an independent predictive factor of postoperative complications (OR = 3.06). Sarcopenia was not associated with long-term survival (HR = 1.23; P = 0.51).


Sarcopenia, as assessed by TPV, was an independent factor predictive of postoperative complications following surgical intervention for primary hepatic malignancies.


Sarcopenia Liver cancer Hepatocellular carcinoma Intrahepatic cholangiocarcinoma Outcomes Liver surgery 

Supplementary material

11605_2014_2680_MOESM1_ESM.docx (24 kb)
ESM 1 (DOC 23 kb)


  1. 1.
    SEER Cancer Statistics Review, 1975–2011 []
  2. 2.
    Jarnagin WR, Gonen M, Fong Y, DeMatteo RP, Ben-Porat L, Little S, Corvera C, Weber S, Blumgart LH: Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg 2002, 236:397–406– discussion 406–7PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Agopian VG, Petrowsky H, Kaldas FM, Zarrinpar A, Farmer DG, Yersiz H, Holt C, Harlander-Locke M, Hong JC, Rana AR, Venick R, McDiarmid SV, Goldstein LI, Durazo F, Saab S, Han S, Xia V, Hiatt JR, Busuttil RW: The evolution of liver transplantation during 3 decades: analysis of 5347 consecutive liver transplants at a single center. Ann Surg 2013, 258:409–421.PubMedCrossRefGoogle Scholar
  4. 4.
    Shimoda M, Farmer DG, Colquhoun SD, Rosove M, Ghobrial RM, Yersiz H, Chen P, Busuttil RW: Liver transplantation for cholangiocellular carcinoma: analysis of a single-center experience and review of the literature. Liver Transpl 2001, 7:1023–1033.PubMedCrossRefGoogle Scholar
  5. 5.
    Hong JC, Jones CM, Duffy JP, Petrowsky H, Farmer DG, French S, Finn R, Durazo FA, Saab S, Tong MJ, Hiatt JR, Busuttil RW: Comparative analysis of resection and liver transplantation for intrahepatic and hilar cholangiocarcinoma: a 24-year experience in a single center. Arch Surg 2011, 146:683–689.PubMedCrossRefGoogle Scholar
  6. 6.
    Rea DJ, Heimbach JK, Rosen CB, Haddock MG, Alberts SR, Kremers WK, Gores GJ, Nagorney DM: Liver transplantation with neoadjuvant chemoradiation is more effective than resection for hilar cholangiocarcinoma. Ann Surg 2005, 242:451–8– discussion 458–61PubMedCentralPubMedGoogle Scholar
  7. 7.
    Meyer CG, Penn I, James L: Liver transplantation for cholangiocarcinoma: results in 207 patients. Transplantation 2000, 69:1633–1637.PubMedCrossRefGoogle Scholar
  8. 8.
    Sharma P, Schaubel DE, Sima CS, Merion RM, Lok ASF: Re-weighting the model for end-stage liver disease score components. Gastroenterology 2008, 135:1575–1581.PubMedCrossRefGoogle Scholar
  9. 9.
    Nathan H, Schulick RD, Choti MA, Pawlik TM: Predictors of survival after resection of early hepatocellular carcinoma. Ann Surg 2009, 249:799–805.PubMedCrossRefGoogle Scholar
  10. 10.
    Papadopoulos I, Rudolph P, Weichert-Jacobsen K, Thiemann O, Papadopoulou D: Prognostic indicators for response to therapy and survival in patients with metastatic renal cell cancer treated with interferon alpha-2 beta and vinblastine. Urology 1996, 48:373–378.PubMedCrossRefGoogle Scholar
  11. 11.
    Buccheri G, Ferrigno D, Tamburini M: Karnofsky and ECOG performance status scoring in lung cancer: a prospective, longitudinal study of 536 patients from a single institution. Eur J Cancer 1996, 32A:1135–1141.PubMedCrossRefGoogle Scholar
  12. 12.
    Reuben DB, Mor V, Hiris J: Clinical symptoms and length of survival in patients with terminal cancer. Arch Intern Med 1988, 148:1586–1591.PubMedCrossRefGoogle Scholar
  13. 13.
    Mor V, Laliberte L, Morris JN, Wiemann M: The Karnofsky Performance Status Scale. An examination of its reliability and validity in a research setting. Cancer 1984, 53:2002–2007PubMedCrossRefGoogle Scholar
  14. 14.
    List MA, Ritter-Sterr C, Lansky SB: A performance status scale for head and neck cancer patients. Cancer 1990, 66:564–569.PubMedCrossRefGoogle Scholar
  15. 15.
    Khan RB, Sanford RA, Kun LE, Thompson SJ: Morbidity of second-look surgery in pediatric central nervous system tumors. Pediatr Neurosurg 2001, 35:225–229.PubMedCrossRefGoogle Scholar
  16. 16.
    Sloan JA, Loprinzi CL, Laurine JA, Novotny PJ, Vargas-Chanes D, Krook JE, O’Connell MJ, Kugler JW, Tirona MT, Kardinal CG, Wiesenfeld M, Tschetter LK, Hatfield AK, Schaefer PL: A simple stratification factor prognostic for survival in advanced cancer: the good/bad/uncertain index. J Clin Oncol 2001, 19:3539–3546.PubMedGoogle Scholar
  17. 17.
    Lang P-O, Michel J-P, Zekry D: Frailty syndrome: a transitional state in a dynamic process. Gerontology 2009, 55:539–549.PubMedCrossRefGoogle Scholar
  18. 18.
    Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, Harbaugh C, Holcombe SA, Wang SC, Segev DL, Sonnenday CJ: Sarcopenia and mortality after liver transplantation. Journal of the American College of Surgeons 2010, 211:271–278.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Dodson RM, Firoozmand A, Hyder O, Tacher V, Cosgrove DP, Bhagat N, Herman JM, Wolfgang CL, Geschwind J-FH, Kamel IR, Pawlik TM: Impact of Sarcopenia on Outcomes Following Intra-arterial Therapy of Hepatic Malignancies. J Gastrointest Surg 2013:1–10.Google Scholar
  20. 20.
    Makary MA, Segev DL, Pronovost PJ, Syin D, Bandeen-Roche K, Patel P, Takenaga R, Devgan L, Holzmueller CG, Tian J, Fried LP: Frailty as a predictor of surgical outcomes in older patients. Journal of the American College of Surgeons 2010, 210:901–908.PubMedCrossRefGoogle Scholar
  21. 21.
    Harimoto N, Shirabe K, Yamashita Y-I, Ikegami T, Yoshizumi T, Soejima Y, Ikeda T, Maehara Y, Nishie A, Yamanaka T: Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma. Br J Surg 2013, 100:1523–1530.PubMedCrossRefGoogle Scholar
  22. 22.
    Peng PD, van Vledder MG, Tsai S, de Jong MC, Makary M, Ng J, Edil BH, Wolfgang CL, Schulick RD, Choti MA, Kamel I, Pawlik TM: Sarcopenia negatively impacts short-term outcomes in patients undergoing hepatic resection for colorectal liver metastasis. HPB (Oxford) 2011, 13:439–446.CrossRefGoogle Scholar
  23. 23.
    Reisinger KW, van Vugt JLA, Tegels JJW, Snijders C, Hulsewé KWE, Hoofwijk AGM, Stoot JH, Meyenfeldt Von MF, Beets GL, Derikx JPM, Poeze M: Functional Compromise Reflected by Sarcopenia, Frailty, and Nutritional Depletion Predicts Adverse Postoperative Outcome After Colorectal Cancer Surgery. Ann Surg 2014:1.Google Scholar
  24. 24.
    Silver JK, Baima J: Cancer prehabilitation: an opportunity to decrease treatment-related morbidity, increase cancer treatment options, and improve physical and psychological health outcomes. Am J Phys Med Rehabil 2013, 92:715–727.PubMedCrossRefGoogle Scholar
  25. 25.
    Debes C, Aissou M, Beaussier M: [Prehabilitation. Preparing patients for surgery to improve functional recovery and reduce postoperative morbidity]. Ann Fr Anesth Reanim 2014, 33:33–40.PubMedCrossRefGoogle Scholar
  26. 26.
    Santa Mina D, Clarke H, Ritvo P, Leung YW, Matthew AG, Katz J, Trachtenberg J, Alibhai SMH: Effect of total-body prehabilitation on postoperative outcomes: a systematic review and meta-analysis. Physiotherapy 2013.Google Scholar
  27. 27.
    Prado CMM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE: 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, 9:629–635.PubMedCrossRefGoogle Scholar
  28. 28.
    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: Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg 2012, 16:1478–1486.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Clavien PA, Camargo CA, Croxford R, Langer B, Levy GA, Greig PD: Definition and classification of negative outcomes in solid organ transplantation. Application in liver transplantation. Ann Surg 1994, 220:109–120.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012, 9:671–675.PubMedCrossRefGoogle Scholar
  31. 31.
    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, 138:185–191.PubMedCrossRefGoogle Scholar
  32. 32.
    de Jong MC, Pulitano C, Ribero D, Strub J, Mentha G, Schulick RD, Choti MA, Aldrighetti L, Capussotti L, Pawlik TM: Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients. Ann Surg 2009, 250:440–448.PubMedGoogle Scholar
  33. 33.
    Nathan H, Cameron JL, Choti MA, Schulick RD, Pawlik TM: The volume-outcomes effect in hepato-pancreato-biliary surgery: hospital versus surgeon contributions and specificity of the relationship. Journal of the American College of Surgeons 2009, 208:528–538.PubMedCrossRefGoogle Scholar
  34. 34.
    Mavros MN, de Jong M, Dogeas E, Hyder O, Pawlik TM: Impact of complications on long-term survival after resection of colorectal liver metastases. Br J Surg 2013, 100:711–718.PubMedCrossRefGoogle Scholar
  35. 35.
    Reddy SK, Barbas AS, Turley RS, Gamblin TC, Geller DA, Marsh JW, Tsung A, Clary BM, Lagoo-Deenadayalan S: Major liver resection in elderly patients: a multi-institutional analysis. Journal of the American College of Surgeons 2011, 212:787–795.PubMedCrossRefGoogle Scholar
  36. 36.
    Saxton A, Velanovich V: Preoperative frailty and quality of life as predictors of postoperative complications. Ann Surg 2011, 253:1223–1229.PubMedCrossRefGoogle Scholar
  37. 37.
    Schnadig ID, Fromme EK, Loprinzi CL, Sloan JA, Mori M, Li H, Beer TM: Patient-physician disagreement regarding performance status is associated with worse survivorship in patients with advanced cancer. Cancer 2008, 113:2205–2214.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Sabel MS, Lee J, Cai S, Englesbe MJ, Holcombe S, Wang S: Sarcopenia as a prognostic factor among patients with stage III melanoma. Ann Surg Oncol 2011, 18:3579–3585.PubMedCrossRefGoogle Scholar
  39. 39.
    Tan BHL, Birdsell LA, Martin L, Baracos VE, Fearon KCH: Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res 2009, 15:6973–6979.PubMedCrossRefGoogle Scholar
  40. 40.
    Galvão DA, Taaffe DR, Spry N, Joseph D, Newton RU: Combined resistance and aerobic exercise program reverses muscle loss in men undergoing androgen suppression therapy for prostate cancer without bone metastases: a randomized controlled trial. Journal of Clinical Oncology 2010, 28:340–347.PubMedCrossRefGoogle Scholar
  41. 41.
    Antoun S, Baracos VE, Birdsell L, Escudier B, Sawyer MB: Low body mass index and sarcopenia associated with dose-limiting toxicity of sorafenib in patients with renal cell carcinoma. Ann Oncol 2010, 21:1594–1598.PubMedCrossRefGoogle Scholar
  42. 42.
    Antoun S, Birdsell L, Sawyer MB, Venner P, Escudier B, Baracos VE: Association of skeletal muscle wasting with treatment with sorafenib in patients with advanced renal cell carcinoma: results from a placebo-controlled study. Journal of Clinical Oncology 2010, 28:1054–1060.PubMedCrossRefGoogle Scholar
  43. 43.
    Bonekamp D, Bonekamp S, Halappa VG, Geschwind J-FH, Eng J, Corona-Villalobos CP, Pawlik TM, Kamel IR: Interobserver agreement of semi-automated and manual measurements of functional MRI metrics of treatment response in hepatocellular carcinoma. Eur J Radiol 2014, 83:487–496.PubMedCrossRefGoogle Scholar
  44. 44.
    Bonekamp S, Bonekamp D, Geschwind J-FH, Corona-Villalobos CP, Reyes DK, Pawlik TM, Kamel IR: Response stratification and survival analysis of hepatocellular carcinoma patients treated with intra-arterial therapy using MR imaging-based arterial enhancement fraction. J Magn Reson Imaging 2013:n/a–n/a.Google Scholar
  45. 45.
    Bonekamp S, Halappa VG, Geschwind J-FH, Li Z, Corona-Villalobos CP, Reyes D, Bhagat N, Cosgrove DP, Pawlik TM, Mezey E, Eng J, Kamel IR: Unresectable hepatocellular carcinoma: MR imaging after intraarterial therapy. Part II. Response stratification using volumetric functional criteria after intraarterial therapy. Radiology 2013, 268:431–439.PubMedCrossRefGoogle Scholar
  46. 46.
    Bonekamp S, Li Z, Geschwind J-FH, Halappa VG, Corona-Villalobos CP, Reyes D, Pawlik TM, Bonekamp D, Eng J, Kamel IR: Unresectable hepatocellular carcinoma: MR imaging after intraarterial therapy. Part I. Identification and validation of volumetric functional response criteria. Radiology 2013, 268:420–430.PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Gowdra Halappa V, Corona-Villalobos CP, Bonekamp S, Li Z, Reyes D, Cosgrove D, Pawlik TM, Diaz LA, Bhagat N, Eng J, Geschwind J-F, Kamel IR: Neuroendocrine liver metastasis treated by using intraarterial therapy: volumetric functional imaging biomarkers of early tumor response and survival. Radiology 2013, 266:502–513.PubMedCrossRefGoogle Scholar
  48. 48.
    Kostis WJ, Yankelevitz DF, Reeves AP, Fluture SC, Henschke CI: Small pulmonary nodules: reproducibility of three-dimensional volumetric measurement and estimation of time to follow-up CT. Radiology 2004, 231:446–452.PubMedCrossRefGoogle Scholar
  49. 49.
    Wormanns D, Kohl G, Klotz E, Marheine A, Beyer F, Heindel W, Diederich S: Volumetric measurements of pulmonary nodules at multi-row detector CT: in vivo reproducibility. Eur Radiol 2004, 14:86–92.PubMedCrossRefGoogle Scholar
  50. 50.
    Revel M-P, Bissery A, Bienvenu M, Aycard L, Lefort C, Frija G: Are two-dimensional CT measurements of small noncalcified pulmonary nodules reliable? Radiology 2004, 231:453–458.PubMedCrossRefGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2014

Authors and Affiliations

  • Vicente ValeroIII
    • 1
  • Neda Amini
    • 1
  • Gaya Spolverato
    • 1
  • Matthew J. Weiss
    • 1
  • Kenzo Hirose
    • 1
  • Nabil N. Dagher
    • 1
  • Christopher L. Wolfgang
    • 1
  • Andrew A. Cameron
    • 1
  • Benjamin Philosophe
    • 1
  • Ihab R. Kamel
    • 2
  • Timothy M. Pawlik
    • 1
    Email author
  1. 1.Department of SurgeryThe Johns Hopkins University School of MedicineBaltimoreUSA
  2. 2.Department of RadiologyThe Johns Hopkins University School of MedicineBaltimoreUSA

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