Prognostic value of sarcopenia in patients with liver cirrhosis: A systematic review and meta-analysis

Gaeun Kim, Seong Hee Kang, Moon Young Kim, Soon Koo Baik, Gaeun Kim, Seong Hee Kang, Moon Young Kim, Soon Koo Baik

Abstract

Background: Sarcopenia is a common syndrome in chronic diseases such as liver cirrhosis. The association between sarcopenia and outcomes, such as complications and survival has recently been described in various patient groups. However, study results remain inconclusive. Therefore, the aim of this study was to systematically review the impact of sarcopenia on outcome in patients with cirrhosis.

Methods and findings: We conducted a systematic review (SR) and meta-analysis (MA) on the impact of sarcopenia on outcome in liver cirrhosis was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines. Of the 312 studies identified, 20 were eligible according to our inclusion criteria. Most of the studies used CT to diagnose sarcopenia. Two studies used bioelectrical impedance analysis (BIA), 10 studies used skeletal muscle index (SMI) and 8 studies used total psoas muscle area (TPA). Seven studies included Asian participants and the remaining 13 studies included Western participants. The prevalence rate of sarcopenia among participants was mean 48.1%, and appeared more among men with a rate of 61.6% whereas the rate was 36% for women. With respect to clinical outcomes, patients with sarcopenia had poorer survival rates and an increased risk of complications such as infection compared to those without sarcopenia. According to the analysis of race subgroup, Asians had a HR 2.45 (95% confidence interval (CI) = 1.44-4.16, P = 0.001) of mortality whereas Westerners had a HR 1.45 (95% CI = 1.002-2.09, P<0.05).

Conclusions: Based on this SR and MA, the presence of sarcopenia is related to a poor prognosis and occurrence of cirrhotic complications and could be used for risk assessment. Moreover, Asian participants had higher mortality related to sarcopenia compared to the Western participants.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. The flow diagram of study…
Fig 1. The flow diagram of study selection for the systematic review and meta-analysis.
Fig 2. Forest plot for the mortality…
Fig 2. Forest plot for the mortality in accordance to muscle mass.
Fig 3. Forest plot for the mortality…
Fig 3. Forest plot for the mortality for the sarcopenia group.
(A) The odds ratio (OR) of mortality for the sarcopenia group (B) The hazard ratio (HR) of mortality for the sarcopenia group.
Fig 4. Forest plot for the complications…
Fig 4. Forest plot for the complications occurrence.
(A) The HR of complications occurrence such as severe infection (B) The HR of complications occurrence such as sepsis or severe infection to sarcopenia.

References

    1. Prasad S, Dhiman RK, Duseja A, Chawla YK, Sharma A, et al. (2007) Lactulose improves cognitive functions and health-related quality of life in patients with cirrhosis who have minimal hepatic encephalopathy. Hepatology 45: 549–559. doi:
    1. Kim MY, Suk KT, Baik SK, Kim HA, Kim YJ, et al. (2012) Hepatic vein arrival time as assessed by contrast-enhanced ultrasonography is useful for the assessment of portal hypertension in compensated cirrhosis. Hepatology 56: 1053–1062. doi:
    1. D'Amico G, Garcia-Tsao G, Pagliaro L (2006) Natural history and prognostic indicators of survival in cirrhosis: a systematic review of 118 studies. J Hepatol 44: 217–231. doi:
    1. Kim G, Lee SS, Baik SK, Cho YZ, Kim MY, et al. (2016) The need for histological subclassification of cirrhosis: a systematic review and meta-analysis. Liver Int 36: 847–855. doi:
    1. Kang SH, Kim MY, Baik SK (2017) Novelties in the pathophysiology and management of portal hypertension: new treatments on the horizon. Hepatol Int.
    1. Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60: 646–649.
    1. Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, et al. (2000) A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology 31: 864–871. doi:
    1. Merli M, Giusto M, Gentili F, Novelli G, Ferretti G, et al. (2010) Nutritional status: its influence on the outcome of patients undergoing liver transplantation. Liver Int 30: 208–214. doi:
    1. Doherty TJ (2003) Invited review: Aging and sarcopenia. J Appl Physiol (1985) 95: 1717–1727. doi:
    1. Freeman RB Jr., Wiesner RH, Harper A, McDiarmid SV, Lake J, et al. (2002) The new liver allocation system: moving toward evidence-based transplantation policy. Liver Transpl 8: 851–858. doi:
    1. Merion RM, Wolfe RA, Dykstra DM, Leichtman AB, Gillespie B, et al. (2003) Longitudinal assessment of mortality risk among candidates for liver transplantation. Liver Transpl 9: 12–18. doi:
    1. Eom YW, Shim KY, Baik SK (2015) Mesenchymal stem cell therapy for liver fibrosis. Korean J Intern Med 30: 580–589. doi:
    1. Kim G, Cho YZ, Baik SK (2015) Assessment for Risk of Bias in Systematic Reviews and Meta-Analyses in the Field of Hepatology. Gut Liver 9: 701–706. doi:
    1. Kim G, Eom YW, Baik SK, Shin Y, Lim YL, et al. (2015) Therapeutic Effects of Mesenchymal Stem Cells for Patients with Chronic Liver Diseases: Systematic Review and Meta-analysis. J Korean Med Sci 30: 1405–1415. doi:
    1. Kim G, Huh JH, Lee KJ, Kim MY, Shim KY, et al. (2017) Relative Adrenal Insufficiency in Patients with Cirrhosis: A Systematic Review and Meta-Analysis. Dig Dis Sci 62: 1067–1079. doi:
    1. Kim G, Kim J, Lim YL, Kim MY, Baik SK (2016) Renin-angiotensin system inhibitors and fibrosis in chronic liver disease: a systematic review. Hepatol Int 10: 819–828. doi:
    1. Kim G, Kim MY, Baik SK (2017) Transient elastography versus hepatic venous pressure gradient for diagnosing portal hypertension: a systematic review and meta-analysis. Clin Mol Hepatol 23: 34–41. doi:
    1. Kim G, Shim KY, Baik SK (2017) Diagnostic Accuracy of Hepatic Vein Arrival Time Performed with Contrast-Enhanced Ultrasonography for Cirrhosis: A Systematic Review and Meta-Analysis. Gut Liver 11: 93–101. doi:
    1. Higgins J, Green S, Cochrane C (2008) Cochrane handbook for systematic reviews of interventions. Chichester, West Sussex;: Hoboken NJ:.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151: 264–269, w264.
    1. Kim G, Bae JH (2016) Vitamin D and atopic dermatitis: A systematic review and meta-analysis. Nutrition 32: 913–920. doi:
    1. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539–1558. doi:
    1. Light RJ, Singer JD, Willett JB (1994) Displaying and communicating findings from a meta-analysis In: Cooper H, Hedges LV, editors. The handbook of research synthesis. New York: Russell Sage Foundation, cop. pp. 439–453.
    1. DiMartini A, Cruz RJ Jr., Dew MA, Myaskovsky L, Goodpaster B, et al. (2013) Muscle mass predicts outcomes following liver transplantation. Liver Transpl 19: 1172–1180. doi:
    1. Durand F, Buyse S, Francoz C, Laouenan C, Bruno O, et al. (2014) Prognostic value of muscle atrophy in cirrhosis using psoas muscle thickness on computed tomography. J Hepatol 60: 1151–1157. doi:
    1. Englesbe MJ, Patel SP, He K, Lynch RJ, Schaubel DE, et al. (2010) Sarcopenia and mortality after liver transplantation. J Am Coll Surg 211: 271–278. doi:
    1. Giusto M, Lattanzi B, Albanese C, Galtieri A, Farcomeni A, et al. (2015) Sarcopenia in liver cirrhosis: the role of computed tomography scan for the assessment of muscle mass compared with dual-energy X-ray absorptiometry and anthropometry. Eur J Gastroenterol Hepatol 27: 328–334. doi:
    1. Hamaguchi Y, Kaido T, Okumura S, Fujimoto Y, Ogawa K, et al. (2014) Impact of quality as well as quantity of skeletal muscle on outcomes after liver transplantation. Liver Transpl 20: 1413–1419. doi:
    1. Krell RW, Kaul DR, Martin AR, Englesbe MJ, Sonnenday CJ, et al. (2013) Association between sarcopenia and the risk of serious infection among adults undergoing liver transplantation. Liver Transpl 19: 1396–1402. doi:
    1. Lee CS, Cron DC, Terjimanian MN, Canvasser LD, Mazurek AA, et al. (2014) Dorsal muscle group area and surgical outcomes in liver transplantation. Clin Transplant 28: 1092–1098. doi:
    1. Montano-Loza AJ, Meza-Junco J, Baracos VE, Prado CM, Ma M, et al. (2014) Severe muscle depletion predicts postoperative length of stay but is not associated with survival after liver transplantation. Liver Transpl 20: 640–648. doi:
    1. Montano-Loza AJ, Meza-Junco J, Prado CM, Lieffers JR, Baracos VE, et al. (2012) Muscle wasting is associated with mortality in patients with cirrhosis. Clin Gastroenterol Hepatol 10: 166–173, 173 e161. doi:
    1. Tandon P, Ney M, Irwin I, Ma MM, Gramlich L, et al. (2012) Severe muscle depletion in patients on the liver transplant wait list: its prevalence and independent prognostic value. Liver Transpl 18: 1209–1216. doi:
    1. Tsien C, Garber A, Narayanan A, Shah SN, Barnes D, et al. (2014) Post-liver transplantation sarcopenia in cirrhosis: a prospective evaluation. J Gastroenterol Hepatol 29: 1250–1257. doi:
    1. Yadav A, Chang YH, Carpenter S, Silva AC, Rakela J, et al. (2015) Relationship between sarcopenia, six-minute walk distance and health-related quality of life in liver transplant candidates. Clin Transplant 29: 134–141. doi:
    1. Cruz RJ Jr., Dew MA, Myaskovsky L, Goodpaster B, Fox K, et al. (2013) Objective radiologic assessment of body composition in patients with end-stage liver disease: going beyond the BMI. Transplantation 95: 617–622. doi:
    1. Hanai T, Shiraki M, Nishimura K, Ohnishi S, Imai K, et al. (2015) Sarcopenia impairs prognosis of patients with liver cirrhosis. Nutrition 31: 193–199. doi:
    1. Hanai T, Shiraki M, Ohnishi S, Miyazaki T, Ideta T, et al. (2016) Rapid skeletal muscle wasting predicts worse survival in patients with liver cirrhosis. Hepatol Res 46: 743–751. doi:
    1. Hara N, Iwasa M, Sugimoto R, Mifuji-Moroka R, Yoshikawa K, et al. (2016) Sarcopenia and Sarcopenic Obesity Are Prognostic Factors for Overall Survival in Patients with Cirrhosis. Intern Med 55: 863–870. doi:
    1. Kaido T, Ogawa K, Fujimoto Y, Ogura Y, Hata K, et al. (2013) Impact of sarcopenia on survival in patients undergoing living donor liver transplantation. Am J Transplant 13: 1549–1556. doi:
    1. Waits SA, Kim EK, Terjimanian MN, Tishberg LM, Harbaugh CM, et al. (2014) Morphometric age and mortality after liver transplant. JAMA Surg 149: 335–340. doi:
    1. Kim TY, Kim MY, Sohn JH, Kim SM, Ryu JA, et al. (2014) Sarcopenia as a useful predictor for long-term mortality in cirrhotic patients with ascites. J Korean Med Sci 29: 1253–1259. doi:
    1. Masuda T, Shirabe K, Ikegami T, Harimoto N, Yoshizumi T, et al. (2014) Sarcopenia is a prognostic factor in living donor liver transplantation. Liver Transpl 20: 401–407. doi:
    1. van Vugt JL, Levolger S, de Bruin RW, van Rosmalen J, Metselaar HJ, et al. (2016) Systematic Review and Meta-Analysis of the Impact of Computed Tomography-Assessed Skeletal Muscle Mass on Outcome in Patients Awaiting or Undergoing Liver Transplantation. Am J Transplant 16: 2277–2292. doi:
    1. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, 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 9: 629–635. doi:
    1. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, et al. (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147: 755–763.
    1. Lau EM, Lynn HS, Woo JW, Kwok TC, Melton LJ 3rd (2005) Prevalence of and risk factors for sarcopenia in elderly Chinese men and women. J Gerontol A Biol Sci Med Sci 60: 213–216.
    1. Biggins SW, Rodriguez HJ, Bacchetti P, Bass NM, Roberts JP, et al. (2005) Serum sodium predicts mortality in patients listed for liver transplantation. Hepatology 41: 32–39. doi:
    1. Kim WR, Biggins SW, Kremers WK, Wiesner RH, Kamath PS, et al. (2008) Hyponatremia and mortality among patients on the liver-transplant waiting list. N Engl J Med 359: 1018–1026. doi:
    1. Merli M, Riggio O, Dally L (1996) Does malnutrition affect survival in cirrhosis? PINC (Policentrica Italiana Nutrizione Cirrosi). Hepatology 23: 1041–1046. doi:
    1. Amodio P, Caregaro L, Patteno E, Marcon M, Del Piccolo F, et al. (2001) Vegetarian diets in hepatic encephalopathy: facts or fantasies? Dig Liver Dis 33: 492–500.
    1. Cheung K, Lee SS, Raman M (2012) Prevalence and mechanisms of malnutrition in patients with advanced liver disease, and nutrition management strategies. Clin Gastroenterol Hepatol 10: 117–125. doi:
    1. O'Brien A, Williams R (2008) Nutrition in end-stage liver disease: principles and practice. Gastroenterology 134: 1729–1740. doi:
    1. Quigley EM (1996) Gastrointestinal dysfunction in liver disease and portal hypertension. Gut-liver interactions revisited. Dig Dis Sci 41: 557–561.
    1. Argiles JM, Busquets S, Stemmler B, Lopez-Soriano FJ (2015) Cachexia and sarcopenia: mechanisms and potential targets for intervention. Curr Opin Pharmacol 22: 100–106. doi:
    1. Pratesi A, Tarantini F, Di Bari M (2013) Skeletal muscle: an endocrine organ. Clin Cases Miner Bone Metab 10: 11–14. doi:

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