Skip to main content

Advertisement

Log in

Increase in the skeletal muscle mass to body fat mass ratio predicts the decline in transaminase in patients with nonalcoholic fatty liver disease

  • Original Article—Liver, Pancreas, and Biliary Tract
  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

A Letter to the Editor to this article was published on 24 July 2018

Abstract

Background

The aim of this retrospective study was to determine the effect of skeletal muscle and body fat on liver function in patients with nonalcoholic fatty liver disease (NAFLD) diagnosed by liver biopsy.

Methods

Among the 219 patients with NAFLD enrolled in this study was a cohort of 139 patients who had their body composition measured with Inbody720 at baseline and at ≥ 1 year postbaseline, to elucidate the relationship between liver function and changes in skeletal muscle and body fat mass. Multivariate analysis was used to identify factors influencing low skeletal muscle mass index (SMI, defined as 7 kg/m2 in men, and 5.7 kg/m2 in women) and the skeletal muscle mass to body fat mass ratio (SF ratio).

Results

Of the 219 patients enrolled, 27 (12.3%) had a low SMI. Patient age (> 70 years) and female gender were identified as risk factors for low SMI. Hepatic fibrosis was not associated with SMI. In the cohort followed up at baseline and 12 months later, transaminase activity, body fat mass, and SMI significantly decreased over time. Changes in the SF ratio were significantly associated with changes in liver function. An increase in the SF ratio [hazard ratio (HR) 10.99 in men, 6.849 in women] was a predictor of reduced ALT, independent of age and other backgrounds.

Conclusions

In the patients with NAFLD, SMI was decreased, even in the early stages of NAFLD. Therapeutic strategies for NAFLD require a reduction in body fat mass and the maintenance of skeletal muscle is also needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ALT:

Alanine aminotransferase

AST:

Aspartate aminotransferase

BFMI:

Body fat mass index

BMI:

Body mass index

BMR:

Basal metabolic rate

CI:

Confidence interval

FPG:

Fasting plasma glucose

GGT:

γ Glutamyl transpeptidase

HbA1c:

Hemoglobin A1c

HDL-C:

High-density lipoprotein cholesterol

HR:

Hazard ratio

SF ratio:

SMI to BFMI ratio

LDL-C:

Low-density lipoprotein cholesterol

NAFLD:

Nonalcoholic fatty liver disease

NAS:

NAFLD activity score

NASH:

Nonalcoholic steatohepatitis

SMI:

Skeletal mass index

References

  1. Younossi ZM, Koenig AB, Abdelatif D, et al. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64:73–84.

    Article  PubMed  Google Scholar 

  2. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005–23.

    Article  PubMed  Google Scholar 

  3. Watanabe S, Hashimoto E, Ikejima K, et al. Evidence based clinical practice guidelines for nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. J Gastroenterol. 2015;50:364–77.

    Article  PubMed  Google Scholar 

  4. Montano-Loza AJ, Meza-Junco J, Prado CM, et al. Muscle wasting is associated with mortality in patients with cirrhosis. Clin Gastroenterol Hepatol. 2012;10:166–73 (173.e1).

    Article  PubMed  Google Scholar 

  5. Shiraki M, Nishiguchi S, Saito M, et al. Nutritional status and quality of life in current patients with liver cirrhosis as assessed in 2007–2011. Hepatol Res. 2013;43:106–12.

    Article  PubMed  Google Scholar 

  6. Huisman EJ, Trip EJ, Siersema PD, van Hoek B, van Erpecum KJ. Protein energy steatosis grades of 0, 1, 2, and 3, malnutrition predicts complications in liver cirrhosis. Eur J Gastroenterol Hepatol. 2011;23:982–9.

    Article  CAS  PubMed  Google Scholar 

  7. Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, Pichard C. Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur J Clin Nutr. 2001;55:663–72.

    Article  CAS  PubMed  Google Scholar 

  8. Scaglione S, Kliethermes S, Cao G, et al. The epidemiology of cirrhosis in the United States: a population-based study. J Clin Gastroenterol. 2015;49:690–6.

    Article  PubMed  Google Scholar 

  9. Hanai T, Shiraki M, Ohnishi S, et al. Rapid skeletal muscle wasting predicts worse survival in patients with liver cirrhosis. Hepatol Res. 2016;46:743–51.

    Article  CAS  PubMed  Google Scholar 

  10. Matteoni CA, Younossi ZM, Gramlich T, et al. Nonalcoholic fatty liver diseases: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413–9.

    Article  CAS  PubMed  Google Scholar 

  11. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–21.

    Article  PubMed  Google Scholar 

  12. Brunt EM, Janney CG, Di Bisceglie AM, et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–74.

    Article  CAS  PubMed  Google Scholar 

  13. Nishikawa H, Shiraki M, Hiramatsu A, et al. Japan Society of Hepatology guidelines for sarcopenia in liver disease (1st edition): recommendation from the working group for creation of sarcopenia assessment criteria. Hepatol Res. 2016;46:951–63.

    Article  PubMed  Google Scholar 

  14. Koo BK, Kim D, Joo SK, et al. Sarcopenia is an independent risk factor for non-alcoholic steatohepatitis and significant fibrosis. J Hepatol. 2017;66:123–31.

    Article  PubMed  Google Scholar 

  15. Lee YH, Kim SU, Song K, 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;63:776–86.

    Article  CAS  PubMed  Google Scholar 

  16. Messier V, Rabasa-Lhoret R, Barbat-Artigas S, et al. Menopause and sarcopenia: a potential role for sex hormones. Maturitas. 2011;68:331–6.

    Article  CAS  PubMed  Google Scholar 

  17. Anagnostis P, Dimopoulou C, Karras S, et al. Sarcopenia in post-menopausal women: is there any role for vitamin D? Maturitas. 2015;82:56–64.

    Article  CAS  PubMed  Google Scholar 

  18. Brown M. Skeletal muscle and bone: effect of sex steroids and aging. Adv Physiol Educ. 2008;32:120–6.

    Article  PubMed  Google Scholar 

  19. Visser M, Deeg DJ, Lips P. Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): the Longitudinal Aging Study Amsterdam. J Clin Endocrinol Metab. 2003;88:5766–72.

    Article  CAS  PubMed  Google Scholar 

  20. Flicker L, Mead K, MacInnis RJ, et al. Serum vitamin D and falls in older women in residential care in Australia. J Am Geriatr Soc. 2003;51:1533–8.

    Article  PubMed  Google Scholar 

  21. Park S, Ham JO, Lee BK. A positive association of vitamin D deficiency and sarcopenia in 50 year old women, but not men. Clin Nutr. 2014;33:900–5.

    Article  CAS  PubMed  Google Scholar 

  22. Finelli C, Tarantino G. Is visceral fat reduction necessary to favour metabolic changes in the liver? J Gastrointestin Liver Dis. 2012;21:205–8.

    PubMed  Google Scholar 

  23. Bouchi R, Nakano Y, Fukuda T, et al. Reduction of visceral fat by liraglutide is associated with ameliorations of hepatic steatosis, albuminuria, and micro-inflammation in type 2 diabetic patients with insulin treatment: a randomized control trial. Endocr J. 2017;64:269–81.

    Article  CAS  PubMed  Google Scholar 

  24. Houghton D, Thoma C, Hallsworth K, et al. Exercise reduces liver lipids and visceral adiposity in patients with nonalcoholic steatohepatitis in a randomized controlled Trial. Clin Gastroenterol Hepatol. 2017;15:96–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yusuf S, Hawken S, Ounpuu S, et al. Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case–control study. Lancet. 2005;366:1640–9.

    Article  PubMed  Google Scholar 

  26. Fujimoto WY, Bergstrom RW, Boyko EJ, et al. Visceral adiposity and incident coronary heart disease in Japanese-American men. The 10-year follow-up results of the Seattle Japanese-American Community Diabetes Study. Diabetes Care. 1999;22:1808–12.

    Article  CAS  PubMed  Google Scholar 

  27. Britton KA, Massaro JM, Murabito JM, et al. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62:921–5.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hall AM, Kou K, Chen Z, et al. Evidence for regulated monoacylglycerol acyltransferase expression and activity in human liver. J Lipid Res. 2012;53:990–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Farrell GC, Chitturi S, Lau GK, Sollano JD, Asia-Pacific Working Party on NAFLD. Guidelines for the assessment and management of non-alcoholic fatty liver disease in the Asia-Pacific region: executive summary. J Gastroenterol Hepatol. 2007;22:775–7.

    Article  PubMed  Google Scholar 

  30. WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–63.

    Article  Google Scholar 

  31. Alberti KG, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group. The metabolic syndrome—a new worldwide definition. Lancet. 2005;366:1059–62.

    Article  PubMed  Google Scholar 

  32. Merli M, Lucidi C, Giannelli V, et al. Cirrhotic patients are at risk for health care-associated bacterial infections. Clin Gastroenterol Hepatol. 2010;8:979–85.

    Article  PubMed  Google Scholar 

  33. Fujiwara N, Nakagawa H, Kudo Y, et al. Sarcopenia, intramuscular fat deposition, and visceral adiposity independently predict the outcomes of hepatocellular carcinoma. J Hepatol. 2015;63:131–40.

    Article  CAS  PubMed  Google Scholar 

  34. Kob R, Bollheimer LC, Bertsch T, et al. Sarcopenic obesity: molecular clues to a better understanding of its pathogenesis? Biogerontology. 2015;16:15–29.

    Article  CAS  PubMed  Google Scholar 

  35. Prado CM, Wells JC, Smith SR, et al. Sarcopenic obesity: a critical appraisal of the current evidence. Clin Nutr. 2012;31:583–601.

    Article  CAS  PubMed  Google Scholar 

  36. Shida T, Akiyama K, Oh S, et al. Skeletal muscle mass to visceral fat area ratio is an important determinant affecting hepatic conditions of non-alcoholic fatty liver disease. J Gastroenterol. 2017. https://doi.org/10.1007/s00535-017-1377-3.

    Article  PubMed  Google Scholar 

  37. Dyck DJ. Adipokines as regulators of muscle metabolism and insulin sensitivity. Appl Physiol Nutr Metab. 2009;34:396–402.

    Article  CAS  PubMed  Google Scholar 

  38. Kohara K, OchiM Tabara Y, et al. Leptin in sarcopenic visceral obesity: possible link between adipocytes and myocytes. PLoS ONE. 2011;6:e24633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cesari M, Kritchevsky SB, Baumgartner RN, et al. Sarcopenia, obesity, and inflammation—results from the trial of angiotensin converting enzyme inhibition and novel cardiovascular risk factors study. Am J Clin Nutr. 2005;82:428–34.

    Article  CAS  PubMed  Google Scholar 

  40. Schrager ME, Metter EJ, Simonsick E, et al. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol. 2007;102:919–25.

    Article  PubMed  Google Scholar 

  41. Hashida R, Kawaguchi T, Bekki M, et al. Aerobic vs. resistance exercise in non-alcoholic fatty liver disease: a systematic review. J Hepatol. 2017;66:142–52.

    Article  PubMed  Google Scholar 

  42. Yu SC, Powell A, Khow KS, Visvanathan R. The performance of five bioelectrical impedance analysis prediction equations against dual X-ray absorptiometry in estimating appendicular skeletal muscle mass in an adult Australian population. Nutrients. 2016;29(8):189.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Financial support: This study was not supported by any institution funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuya Seko.

Ethics declarations

Conflict of interest

The authors do not have any disclosures to report.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplement Figure 1.

Correlations between changes in AST, ALT, and SF ratio. (PPTX 69 kb)

Supplementary material 2 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mizuno, N., Seko, Y., Kataoka, S. et al. Increase in the skeletal muscle mass to body fat mass ratio predicts the decline in transaminase in patients with nonalcoholic fatty liver disease. J Gastroenterol 54, 160–170 (2019). https://doi.org/10.1007/s00535-018-1485-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-018-1485-8

Keywords

Navigation