Relationship between relative skeletal muscle mass and nonalcoholic fatty liver disease: a systematic review and meta-analysis

Changzhou Cai, Xin Song, Yishu Chen, Xueyang Chen, Chaohui Yu, Changzhou Cai, Xin Song, Yishu Chen, Xueyang Chen, Chaohui Yu

Abstract

Background and aim: Nonalcoholic fatty liver disease (NAFLD) has gradually become one of the most common chronic liver diseases in the world. More and more evidence shows that low skeletal muscle mass index (SMI) may play a role in the development of NAFLD. Our aim was to quantify the association between SMI, sarcopenia and the presence and severity of NAFLD.

Methods: We systematically searched English relevant studies from PubMed, Embase, the Web of Science and the Cochrane Library updated to December 20th, 2018. Studies in which SMI was compared between NAFLD cases and controls were included. So were studies concerning the odds ratio (OR) of NAFLD, non-alcoholic steatohepatitis (NASH) and significant fibrosis in sarcopenia patients. Pooled weighted mean differences and ORs were calculated.

Results: Of the 1331 retrieved studies, 19 articles were included. SMI level in NAFLD patients was 1.77 (95% CI 1.15, 2.39) lower than that in normal controls. We also found a significantly higher occurrence risk of NAFLD (OR = 1.33, 95% CI 1.20 to 1.48), NASH (OR = 2.42, 95% CI 1.27 to 3.57) and NAFLD-related significant fibrosis (OR = 1.56, 95% CI 1.34, 1.78) in sarcopenia subjects.

Conclusions: SMI level in patients with NAFLD was lower than healthy people, and patients with sarcopenia have higher occurrence risk of NAFLD, as well as its advanced stages including NASH or NAFLD-related significant fibrosis. Further well-designed prospective studies are required to strengthen the arguments.

Keywords: Liver fibrosis; Nonalcoholic fatty liver disease; Sarcopenia; Skeletal muscle mass; Steatohepatitis.

Conflict of interest statement

Changzhou Cai, Xin Song, Yishu Chen, Xueyang Chen and Chaohui Yu declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Flowchart showing the selection of articles included in the meta-analysis
Fig. 2
Fig. 2
Meta-analysis of skeletal muscle index (SMI) in nonalcoholic fatty liver disease (NAFLD). a A pooled weighted mean difference (WMD) of SMI in overall seven individual studies between NAFLD patients and normal people. b A pooled WMD of SMI in subgroup analysis based on the different SMM measurement methods. c A pooled WMD of SMI in subgroup analysis according to gender. d Sensitivity analysis according to whether the study was in or out of the funnel plot. For each estimate, the grey shaded area is the weight of the estimate in proportion to the overall effect. SMI skeletal muscle index, NAFLD nonalcoholic fatty liver disease, WMD weighted mean difference, NC normal control, SMM skeletal muscle mass, DEXA dual energy X-ray absorptiometry, BIA bioimpedance analysis
Fig. 3
Fig. 3
Meta-analysis of sarcopenia in nonalcoholic fatty liver disease (NAFLD). a A pooled odds ratio (OR) of NAFLD prevalence between sarcopenia patients and normal control (NC). b Subgroup analysis according to race. c Subgroup analysis based on the sample size. d Sensitivity analysis according to whether the study was in or out of the funnel plot. For each estimate, the grey shaded area is the weight of the estimate in proportion to the overall effect. NAFLD nonalcoholic fatty liver disease, NC normal control, OR odds ratio, HSI hepatic steatosis index, CNS comprehensive NAFLD score, NFS NAFLD fibrosis score, BMI body mass index
Fig. 4
Fig. 4
Meta-analysis of sarcopenia in nonalcoholic fatty liver disease (NAFLD). a A pooled odds ratio (OR) of NAFLD-related significant fibrosis between sarcopenia patients and normal control (NC). b Subgroup analysis according to race. c In NAFLD patients, a pooled OR of NASH between sarcopenia patients and control. d In analyzing the association in patients with sarcopenia and NAFLD-related significant fibrosis. Subgroup analysis was performed based on the diagnostic methods. NAFLD nonalcoholic fatty liver disease, OR: odds ratio, NFS NAFLD fibrosis score, FIB-4 fibrosis index based on the 4 factor, BMI body mass index

References

    1. Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013;10:686–690. doi: 10.1038/nrgastro.2013.171.
    1. Charlton MR, Burns JM, Pedersen RA, Watt KD, Heimbach JK, Dierkhising RA. Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the USA. Gastroenterology. 2011;141:1249–1253. doi: 10.1053/j.gastro.2011.06.061.
    1. Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology. 2011;53:810–820. doi: 10.1002/hep.24127.
    1. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005;129:113–121. doi: 10.1053/j.gastro.2005.04.014.
    1. Choe EK, Kang HY, Park B, Yang JI, Kim JS. The association between nonalcoholic fatty liver disease and CT-measured skeletal muscle mass. J Clin Med. 2018;7:310. doi: 10.3390/jcm7100310.
    1. Kim G, Lee SE, Lee YB, Jun JE, Ahn J, Bae JC, et al. Relationship between relative skeletal muscle mass and nonalcoholic fatty liver disease: a 7-Year longitudinal study. Hepatology. 2018;68:1755–1768. doi: 10.1002/hep.30049.
    1. Kim HY, Kim CW, Park CH, Choi JY, Han K, Merchant AT, et al. Low skeletal muscle mass is associated with non-alcoholic fatty liver disease in Korean adults: the Fifth Korea national health and nutrition examination survey. Hepatol Pancreat Dis Int. 2016;15:39–47. doi: 10.1016/S1499-3872(15)60030-3.
    1. Lee MJ, Kim EH, Bae SJ, Kim GA, Park SW, Choe J, et al. Age-related decrease in skeletal muscle mass is an independent risk factor for incident nonalcoholic fatty liver disease: a 10-year retrospective cohort study. Gut Liver. 2018;13:67. doi: 10.5009/gnl18070.
    1. Peng TC, Wu LW, Chen WL, Liaw FY, Chang YW, Kao TW. Nonalcoholic fatty liver disease and sarcopenia in a Western population (NHANES III): The importance of sarcopenia definition. Clin Nutr. 2019;38:422–428. doi: 10.1016/j.clnu.2017.11.021.
    1. Koo BK, Kim D, Joo SK, Kim JH, Chang MS, Kim BG, et al. Sarcopenia is an independent risk factor for non-alcoholic steatohepatitis and significant fibrosis. J Hepatol. 2017;66:123–131. doi: 10.1016/j.jhep.2016.08.019.
    1. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing. 2010;39:412–423. doi: 10.1093/ageing/afq034.
    1. Shen H, Liangpunsakul S. Association between sarcopenia and prevalence of nonalcoholic fatty liver disease: a cross-sectional study from the third national health and nutrition examination survey. Gastroenterology. 2016;150:S1143–S1144. doi: 10.1016/S0016-5085(16)33859-8.
    1. Hong HC, Hwang SY, Choi HY, Yoo HJ, Seo JA, Kim SG, et al. Relationship between sarcopenia and nonalcoholic fatty liver disease: the Korean sarcopenic obesity study. Hepatology. 2014;59:1772–1778. doi: 10.1002/hep.26716.
    1. Zhai Y, Xiao Q, Miao J. The Relationship between NAFLD and sarcopenia in elderly patients. Can J Gastroenterol Hepatol. 2018;2018:5016091. doi: 10.1155/2018/5016091.
    1. Lee YH, Jung KS, Kim SU, Yoon HJ, Yun YJ, Lee BW, et al. Sarcopaenia is associated with NAFLD independently of obesity and insulin resistance: nationwide surveys (KNHANES 2008–2011) J Hepatol. 2015;63:486–493. doi: 10.1016/j.jhep.2015.02.051.
    1. Petta S, Ciminnisi S, Di Marco V, Cabibi D, Cammà C, Licata A, et al. Sarcopenia is associated with severe liver fibrosis in patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2017;45:510–518. doi: 10.1111/apt.13889.
    1. Lee YH, Kim SU, Song K, Park JY, Kim DY, Ahn SH, et al. Sarcopenia is associated with significant liver fibrosis independently of obesity and insulin resistance in nonalcoholic fatty liver disease: nationwide surveys (KNHANES 2008–2011) Hepatology. 2016;63:776–786. doi: 10.1002/hep.28376.
    1. Hashimoto Y, Osaka T, Fukuda T, Tanaka M, Yamazaki M, Fukui M. The relationship between hepatic steatosis and skeletal muscle mass index in men with type 2 diabetes. Endocr J. 2016;63:877–884. doi: 10.1507/endocrj.EJ16-0124.
    1. Moon JS, Yoon JS, Won KC, Lee HW. The role of skeletal muscle in development of nonalcoholic fatty liver disease. Diabetes Metab J. 2013;37:278–285. doi: 10.4093/dmj.2013.37.4.278.
    1. Choi YJ, Kim SK, Kwak JJ, Park SW, Lee EJ, Huh KB. Age-related skeletal muscle loss as an independent predictor of NAFLD risk in Korean women with type 2 diabetes. Diabetes Res Clin Pract. 2014;106:S162–S163. doi: 10.1016/S0168-8227(14)70516-9.
    1. Kang MK, Park JG, Kim MC, Park SY, Lee HJ, Tak WY, et al. Sarcopenia is associated with advanced liver fibrosis in patients with non-alcoholic fatty liver disease. Hepatology. 2018;68:1306A.
    1. Kim W, Koo BK, Joo SK, Kim JH, Park SC. Sarcopenia is an independent risk factor for biopsyproven non-alcoholic steatohepatitis. J Hepatol. 2016;64:S502. doi: 10.1016/S0168-8278(16)00867-9.
    1. Kwanten WJ, De Fré C, De Fré M, Vonghia L, Vanwolleghem T, Michielsen PP, et al. Sarcopenia is less prevalent in an obese population with NAFLD compared to patients with obesity alone, but increases with severity of disease. Hepatology. 2018;68:1282A–1283A.
    1. Wijarnpreecha K, Scribani M, Kim D. Associations between sarcopenia and nonalcoholic fatty liver disease and advanced fibrosis in the USA. J Hepatol. 2018;68:S827–S828. doi: 10.1016/S0168-8278(18)31929-9.
    1. Treeprasertsuk S, Bjornsson E, Enders F, Suwanwalaikorn S, Lindor KD. NAFLD fibrosis score: a prognostic predictor for mortality and liver complications among NAFLD patients. World J Gastroenterol. 2013;19:1219–1229. doi: 10.3748/wjg.v19.i8.1219.
    1. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes. 1981;30:1000–1007. doi: 10.2337/diab.30.12.1000.
    1. Bhanji RA, Narayanan P, Allen AM, Malhi H, Watt KD. Sarcopenia in hiding: the risk and consequence of underestimating muscle dysfunction in nonalcoholic steatohepatitis. Hepatology. 2017;66:2055–2065. doi: 10.1002/hep.29420.
    1. Phillips T, Leeuwenburgh C. Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J. 2005;19:668–670. doi: 10.1096/fj.04-2870fje.
    1. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology. 2010;52:1836–1846. doi: 10.1002/hep.24001.
    1. Miller AM, Wang H, Bertola A, Park O, Horiguchi N, Ki SH, et al. Inflammation-associated interleukin-6/signal transducer and activator of transcription 3 activation ameliorates alcoholic and nonalcoholic fatty liver diseases in interleukin-10-deficient mice. Hepatology. 2011;54:846–856. doi: 10.1002/hep.24517.
    1. Stienstra R, Saudale F, Duval C, Keshtkar S, Groener JE, van Rooijen N, et al. Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity. Hepatology. 2010;51:511–522. doi: 10.1002/hep.23337.
    1. Seo JA, Cho H, Eun CR, Yoo HJ, Kim SG, Choi KM, et al. Association between visceral obesity and sarcopenia and vitamin D deficiency in older Koreans: the Ansan geriatric study. J Am Geriatr Soc. 2012;60:700–706. doi: 10.1111/j.1532-5415.2012.03887.x.
    1. Kim KH, Kim SU. Sarcopenia is independently associated with significant fibrosis as assessed using transient elastography in patients with chronic liver disease. Hepatology. 2018;68:1134A. doi: 10.1002/hep.30049.

Source: PubMed

3
Abonnieren