Eur J Gastroenterol Hepatol. 2020 Jan;32(1):58-65. doi: 10.1097/MEG.0000000000001475.
Sarcopenia assessed using bioimpedance analysis is associated independently with significant liver fibrosis in patients with chronic liver diseases.
European journal of gastroenterology & hepatology
Kyung Hyun Kim, Beom Kyung Kim, Jun Yong Park, Do Young Kim, Sang Hoon Ahn, Kwang-Hyub Han, Seung Up Kim
Affiliations
Affiliations
- Department of Internal Medicine.
- Institute of Gastroenterology, Yonsei University College of Medicine.
- Yonsei Liver Center, Severance Hospital, Seoul, Republic of Korea.
PMID: 31283527
DOI: 10.1097/MEG.0000000000001475
Abstract
AIM: Sarcopenia is common in patients with advanced fibrosis or cirrhosis. We investigated the correlation between sarcopenia and other clinical variables, in particular, significant liver fibrosis in patients with chronic liver diseases (CLDs).
PATIENTS AND METHODS: Patients with CLDs who underwent transient elastography (TE) and bioelectrical impedance analysis between 2015 and 2017 were retrospectively recruited. The sarcopenia index (SI) was calculated as follows: SI = total appendicular skeletal muscle mass (kg)/ body mass index (BMI) (kg/m). Sarcopenia was defined as SI less than 0.789 for men and less than 0.521 for women. Significant liver fibrosis and fatty liver were defined using TE liver stiffness value more than 7 kPa and controlled attenuation parameter more than 250 dB/m, respectively.
RESULTS: Of 2168 patients recruited, 218 (10.1%) had sarcopenia. Age, BMI, diabetes, hypertension, fasting glucose, aspartate aminotransferase, and liver stiffness value were correlated positively with sarcopenia (all P < 0.05), whereas male sex, viral etiology, obesity (BMI > 25 kg/m), total bilirubin, and serum albumin were correlated negatively with sarcopenia (all P < 0.05). On multivariate analysis, TE-defined significant liver fibrosis was associated independently with sarcopenia (odds ratio = 1.597; 95% confidence interval: 1.174-2.172; P = 0.003), together with age, male sex, viral etiology, and TE-defined fatty liver (all P < 0.05). Among the subgroups with ultrasonography-defined nonalcoholic fatty liver disease (n = 957), sarcopenia was also associated independently with TE-defined significant liver fibrosis (odds ratio = 1.887; 95% confidence interval: 1.261-2.823; P < 0.001).
CONCLUSION: Sarcopenia is associated independently with significant liver fibrosis in patients with CLDs. Further studies are required to determine whether interventions to improve muscle mass can improve liver fibrosis.
References
- Rosenberg IH, Roubenoff R. Stalking sarcopenia. Ann Intern Med. 1995; 123:727–728 - PubMed
- Vetrano DL, Landi F, Volpato S, Corsonello A, Meloni E, Bernabei R, et al. Association of sarcopenia with short-and long-term mortality in older adults admitted to acute care wards: results from the CRIME study. J Gerontol A Biol Sci Med Sci. 2014; 69:1154–1161 - PubMed
- Janssen I, Heymsfield SB, Wang Z, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 year. J Appl Physiol. 2000; 89:81–88 - PubMed
- Ali S, Garcia JM. Sarcopenia, cachexia and aging: diagnosis, mechanisms and therapeutic options – a mini-review. Gerontology. 2014; 60:294–305 - PubMed
- Muscaritoli M, Lucia S, Molfino A, Cederholm T, Rossi Fanelli F. Muscle atrophy in aging and chronic diseases: is it sarcopenia or cachexia?. Intern Emerg Med. 2013; 8:553–560 - PubMed
- Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, et al. 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 - PubMed
- Van Vledder M, Levolger S, Ayez N, Verhoef C, Tran T, Ijzermans J. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg. 2012; 99:550–557 - PubMed
- Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL, et al. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax. 2015; 70:213–218 - PubMed
- Sanada K, Miyachi M, Tanimoto M, Yamamoto K, Murakami H, Okumura S, et al. A cross-sectional study of sarcopenia in Japanese men and women: reference values and association with cardiovascular risk factors. Eur J Appl Physiol. 2010; 110:57–65 - PubMed
- Chang YT, Wu HL, Guo HR, Cheng YY, Tseng CC, Wang MC, et al. Handgrip strength is an independent predictor of renal outcomes in patients with chronic kidney diseases. Nephrol Dial Transplant. 2011; 26:3588–3595 - PubMed
- Dasarathy S. Consilience in sarcopenia of cirrhosis. J Cachexia Sarcopenia Muscle. 2012; 3:225–237 - PubMed
- Glass C, Hipskind P, Tsien C, Malin SK, Kasumov T, Shah SN, et al. Sarcopenia and a physiologically low respiratory quotient in patients with cirrhosis: a prospective controlled study. J Appl Physiol. 2013; 114:559–565 - PubMed
- Merli M, Eriksson LS, Hagenfeldt L, Wahren J. Splanchnic and leg exchange of free fatty acids in patients with liver cirrhosis. J Hepatol. 1986; 3:348–355 - PubMed
- Tsien CD, McCullough AJ, Dasarathy S. Late evening snack: exploiting a period of anabolic opportunity in cirrhosis. J Gastroenterol Hepatol. 2012; 27:430–441 - PubMed
- Chen X, Iqbal N, Boden G. The effects of free fatty acids on gluconeogenesis and glycogenolysis in normal subjects. J Clin Invest. 1999; 103:365–372 - PubMed
- Blonde-Cynober F, Aussel C, Cynober L. Abnormalities in branched-chain amino acid metabolismin cirrhosis: influence of hormonal and nutritional factors and directions for future research. Clin Nutr. 1999; 18:5–13 - PubMed
- 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 - PubMed
- Lee YH, Kim SU, Song K, Park JY, Ahn SH, Lee BW, 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 - PubMed
- Han E, Lee YH, Kim B, Park J, Kim D, Ahn S, et al. Sarcopenia is associated with the risk of significant liver fibrosis in metabolically unhealthy subjects with chronic hepatitis B. Aliment Pharmacol Ther. 2018; 48:300–312 - PubMed
- Vallet-Pichard A, Mallet V, Nalpas B, Verkarre V, Nalpas A, Dhalluin-Venier V, et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology. 2007; 46:32–36 - PubMed
- Kotronen A, Peltonen M, Hakkarainen A, Sevastianova K, Bergholm R, Johansson LM, et al. Prediction of non-alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology. 2009; 137:865–872 - PubMed
- Forns X, Ampurdanes S, Llovet JM, Aponte J, Quintó L, Martínez-Bauer E, et al. Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model. Hepatology. 2002; 36:986–992 - PubMed
- Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014; 69:547–558 - PubMed
- Kim SU, Kim JK, Park JY, Ahn SH, Lee JM, Baatarkhuu O, et al. Variability in liver stiffness values from different intercostal spaces. Liver Int. 2009; 29:760–766 - PubMed
- Chon YE, Jung KS, Kim SU, Park JY, Park YN, Kim DY, et al. Controlled attenuation parameter (CAP) for detection of hepatic steatosis in patients with chronic liver diseases: a prospective study of a native Korean population. Liver Int. 2014; 34:102–109 - PubMed
- Jung KS, Kim SU. Clinical applications of transient elastography. Clin Mol Hepatol. 2012; 18:163–173 - PubMed
- Carvalhana S, Leitão J, Alves AC, Bourbon M, Cortez-Pinto H. How good is controlled attenuation parameter and fatty liver index for assessing liver steatosis in general population: correlation with ultrasound. Liver Int. 2014; 34:e111–e117 - PubMed
- Oh SW. Obesity and metabolic syndrome in Korea. Diabetes Metab J. 2011; 35:561–566 - PubMed
- Castera L, Forns X, Alberti A. Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol. 2008; 48:835–847 - PubMed
- 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 - PubMed
- 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 - PubMed
- Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003; 29:1705–1713 - PubMed
- Kim DY, Song KJ, Kim SU, Yoo EJ, Park JY, Ahn SH, et al. Transient elastography-based risk estimation of hepatitis B virus-related occurrence of hepatocellular carcinoma: development and validation of a predictive model. Onco Targets Ther. 2013; 6:1463–1469 - PubMed
- Kim MN, Kim SU, Kim BK, Park JY, Kim DY, Ahn SH, et al. Increased risk of hepatocellular carcinoma in chronic hepatitis B patients with transient elastography-defined subclinical cirrhosis. Hepatology. 2015; 61:1851–1859 - PubMed
- Kim JH, Kim MN, Han KH, Kim SU. Clinical application of transient elastography in patients with chronic viral hepatitis receiving antiviral treatment. Liver Int. 2015; 35:1103–1115 - PubMed
- Hiraoka A, Michitaka K, Ueki H, Kaneto M, Aibiki T, Okudaira T, et al. Sarcopenia and two types of presarcopenia in Japanese patients with chronic liver disease. Eur J Gastroenterol Hepatol. 2016; 28:940–947 - PubMed
- Kim HS, Kim BK, Kim SU, Park JY, Song KJ, Park JW, et al. Association between level of fibrosis, rather than antiviral regimen, and outcomes of patients with chronic hepatitis B. Clin Gastroenterol Hepatol. 2016; 14:1647–1656e6 - PubMed
- Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006; 44:865–873 - PubMed
- Wang C, Bai L. Sarcopenia in the elderly: basic and clinical issues. Geriatr Gerontol Int. 2012; 12:388–396 - PubMed
- Abbatecola AM, Paolisso G, Fattoretti P, Evans W, Fiore V, Dicioccio L, et al. Discovering pathways of sarcopenia in older adults: a role for insulin resistance on mitochondria dysfunction. J Nutr Health Aging. 2011; 15:890–895 - PubMed
- Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001; 344:495–500 - PubMed
- Cadranel JF, Rufat P, Degos F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF). Hepatology. 2000; 32:477–481 - PubMed
- Castera L, Negre I, Samii K, Buffet C. Pain experienced during percutaneous liver biopsy. Hepatology. 1999; 30:1529–1530 - PubMed
- Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003; 38:1449–1457 - PubMed
- Rousselet MC, Michalak S, Dupre F, Croue A, Bedossa P, Saint-Andre JP, et al. Sources of variability in histological scoring of chronic viral hepatitis. Hepatology. 2005; 41:257–264 - PubMed
- Foucher J, Chanteloup E, Vergniol J, Castera L, Le Bail B, Adhoute X, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006; 55:403–408 - PubMed
- Miyauchi S, Miyake T, Miyazaki M, Eguchi T, Niiya T, Yamamoto S, et al. Free testosterone concentration is inversely associated with markers of liver fibrosis in men with type 2 diabetes mellitus. Endocr J. 2017; 64:1137–1142 - PubMed
- Johnson TM, Overgard EB, Cohen AE, DiBaise JK. Nutrition assessment and management in advanced liver disease. Nutr Clin Pract. 2013; 28:15–29 - PubMed
MeSH terms
Publication Types