The relationship between hepatic steatosis and skeletal muscle mass index in men with type 2 diabetes

Endocrine Journal

Volumn 63, Issue 10, 2016, Pages 877-884

  Hashimoto, Yoshitaka ^a   Osaka, Takafumi ^a   Fukuda, Takuya ^a   Tanaka, Muhei ^a   Yamazaki, Masahiro ^a   Fukui, Michiaki ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Hepatic steatosis; Non alcoholic fatty liver disease; Sarcopenia; Skeletal muscle mass; Type 2 diabetes

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; C REACTIVE PROTEIN; GAMMA GLUTAMYLTRANSFERASE; HEMOGLOBIN A1C; TRIACYLGLYCEROL;

ADULT; AGE; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL CONSUMPTION; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BIOENERGY; BODY COMPOSITION; BODY MASS; BODY WEIGHT; CONTROLLED ATTENUATION PARAMETER; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS-SECTIONAL STUDY; DIASTOLIC BLOOD PRESSURE; DISEASE ASSOCIATION; DUAL ENERGY X RAY ABSORPTIOMETRY; FATTY LIVER; FEMALE; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; GLUCOSE INTAKE; HEMOGLOBIN BLOOD LEVEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INTRAPERITONEAL FAT; JAPANESE (PEOPLE); LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MALE; MATHEMATICAL PARAMETERS; MUSCLE MASS; MUSCULOSKELETAL SYSTEM PARAMETERS; NON INSULIN DEPENDENT DIABETES MELLITUS; SKELETAL MUSCLE MASS INDEX; SYSTOLIC BLOOD PRESSURE; TRANSIENT ELASTOGRAPHY; TRIACYLGLYCEROL BLOOD LEVEL; COMPLICATION; DIABETES MELLITUS, TYPE 2; JAPAN; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGAN SIZE; PATHOLOGY; SARCOPENIA; SEX DIFFERENCE; SKELETAL MUSCLE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BODY COMPOSITION; BODY MASS INDEX; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; JAPAN; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NON-ALCOHOLIC FATTY LIVER DISEASE; ORGAN SIZE; SARCOPENIA; SEX FACTORS;

EID: 84993982625     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.EJ16-0124     Document Type: Article

References (51)

1. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, et al. (2009) Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 32: 1993-1997.
2. Srikanthan P, Hevener AL, Karlamangla AS (2010) Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One 5: e10805.
3. Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, et al. (2006) Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 55: 1813-1818.
4. Moon SS (2014) Low skeletal muscle mass is associated with insulin resistance, diabetes, and metabolic syndrome in the Korean population: the Korea National Health and Nutrition Examination Survey (KNHANES) 2009-2010. Endocr J 61: 61-70.
5. Kohara K (2014) Sarcopenic obesity in aging population: current status and future directions for research. Endocrine 45: 15-25.
6. Chin SO, Rhee SY, Chon S, Hwang YC, Jeong IK, et al. (2013) Sarcopenia is independently associated with cardiovascular disease in older Korean adults: the Korea National Health and Nutrition Examination Survey (KNHANES) from 2009. PLoS One 8: e60119.
7. Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ (2014) Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin Nutr 68: 1001-1007.
8. Atkins JL, Whincup PH, Morris RW, Lennon LT, Papacosta O, et al. (2014) Sarcopenic obesity and risk of cardiovascular disease and mortality: a populationbased cohort study of older men. J Am Geriatr Soc 62: 253-260.
9. Rasmussen BB, Fujita S, Wolfe RR, Mittendorfer B, Roy M, et al. (2006) Insulin resistance of muscle protein metabolism in aging. FASEB J 20: 768-769.
10. Hamaguchi M, Kojima T, Takeda N, Nakagawa T, Taniguchi H, et al. (2005) The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann Intern Med 143: 722-728.
11. Fukuda T, Hamaguchi M, Kojima T, Hashimoto Y, Ohbora A, et al. (2016) The impact of non-alcoholic fatty liver disease on incident type 2 diabetes mellitus in non-overweight individuals. Liver Int 36: 275-283.
12. Park SK, Seo MH, Shin HC, Ryoo JH (2013) Clinical availability of nonalcoholic fatty liver disease as an early predictor of type 2 diabetes mellitus in Korean men: 5-year prospective cohort study. Hepatology 57: 1378-1383.
13. Musso G, Gambino R, Tabibian JH, Ekstedt M, Kechagias S, et al. (2014) Association of non-alcoholic fatty liver disease with chronic kidney disease: a systematic review and meta-analysis. PLoS Med 11: e1001680.
14. Hamaguchi M, Kojima T, Takeda N, Nagata C, Takeda J, et al. (2007) Nonalcoholic fatty liver disease is a novel predictor of cardiovascular disease. World J Gastroenterol 13: 1579-1584.
15. Akabame S, Hamaguchi M, Tomiyasu K, Tanaka M, Kobayashi-Takenaka Y, et al. (2008) Evaluation of vulnerable coronary plaques and non-alcoholic fatty liver disease (NAFLD) by 64-detector multislice computed tomography (MSCT). Circ J 72: 618-625.
16. Wong VW, Wong GL, Yip GW, Lo AO, Limquiaco J, et al. (2011) Coronary artery disease and cardiovascular outcomes in patients with non-alcoholic fatty liver disease. Gut 60: 1721-1727.
17. Hong HC, Hwang SY, Choi HY, Yoo HJ, Seo JA, et al. (2014) Relationship between sarcopenia and nonalcoholic fatty liver disease: the Korean Sarcopenic Obesity Study. Hepatology 59: 1772-1778.
18. Moon JS, Yoon JS, Won KC, Lee HW (2013) The role of skeletal muscle in development of nonalcoholic Fatty liver disease. Diabetes Metab J 37: 278-285.
19. Lee YH, Jung KS, Kim SU, Yoon HJ, Yun YJ, et al. (2015) Sarcopaenia is associated with NAFLD independently of obesity and insulin resistance: Nationwide surveys (KNHANES 2008-2011). J Hepatol 63: 486-493.
20. American Diabetes Association (2013) Diagnosis and classification of diabetes mellitus. Diabetes Care 36 Suppl 1: S67-S74.
21. Fukuda Y, Hashimoto Y, Hamaguchi M, Fukuda T, Nakamura N, et al. (2016) Triglycerides to high-density lipoprotein cholesterol ratio is an independent predictor of incident fatty liver; a population-based cohort study. Liver Int 36: 713-720.
22. de Lédinghen V, Vergniol J, Foucher J, Merrouche W, le Bail B (2012) Non-invasive diagnosis of liver steatosis using controlled attenuation parameter (CAP) and transient elastography. Liver Int 32: 911-918.
23. Sasso M, Miette V, Sandrin L, Beaugrand M (2012) The controlled attenuation parameter (CAP): a novel tool for the non-invasive evaluation of steatosis using Fibroscan. Clin Res Hepatol Gastroenterol 36: 13-20.
24. Sasso M, Beaugrand M, de Ledinghen V, Douvin C, Marcellin P, et al. (2010) Controlled attenuation parameter (CAP): a novel VCTE™ guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med Biol 36: 1825-1835.
25. Karlas T, Petroff D, Garnov N, Böhm S, Tenckhoff H, et al. (2014) Non-invasive assessment of hepatic steatosis in patients with NAFLD using controlled attenuation parameter and 1H-MR spectroscopy. PLoS One 9: e91987.
26. Shah A, Lydecker A, Murray K, Tetri BN, Contos MJ, et al. (2009) Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 7: 1104-1112.
27. Kim M, Shinkai S, Murayama H, Mori S (2015) Comparison of segmental multifrequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for the assessment of body composition in a community-dwelling older population. Geriatr Gerontol Int 15: 1013-1022.
28. Anderson LJ, Erceg DN, Schroeder ET (2012) Utility of multifrequency bioelectrical impedance compared with dual-energy x-ray absorptiometry for assessment of total and regional body composition varies between men and women. Nutr Res 32: 479-485.
29. Tanimoto Y, Watanabe M, Sun W, Hirota C, Sugiura Y, et al. (2012) Association between muscle mass and disability in performing instrumental activities of daily living (IADL) in community-dwelling elderly in Japan. Arch Gerontol Geriatr 54: e230-e233.
30. Tanimoto Y, Watanabe M, Kono R, Hirota C, Takasaki K, et al. (2010) Aging changes in muscle mass of Japanese. Nihon Ronen Igakkai Zasshi 47: 52-57 (In Japanese).
31. Hamaguchi M, Kojima T, Ohbora A, Takeda N, Fukui M, et al. (2012) Aging is a risk factor of nonalcoholic fatty liver disease in premenopausal women. World J Gastroenterol 18: 237-243.
32. Hashimoto Y, Hamaguchi M, Kojima T, Ohshima Y, Ohbora A, et al. (2015) Modest alcohol consumption reduces the incidence of fatty liver in men: a population-based large-scale cohort study. J Gastroenterol Hepatol 30: 546-552.
33. Ma H, Xu C, Xu L, Yu C, Miao M, et al. (2013) Independent association of HbA1c and nonalcoholic fatty liver disease in an elderly Chinese population. BMC Gastroenterol 13: 3.
34. Sanada K, Miyachi M, Tanimoto M, Yamamoto K, Murakami H, et al (2010) A cross-sectional study of sarcopenia in Japanese men and women: reference values and association with cardiovascular risk factors. Eur J Appl Physiol 110: 57-65.
35. Nomura T, Ikeda Y, Nakao S, Ito K, Ishida K, et al. (2007) Muscle strength is a marker of insulin resistance in patients with type 2 diabetes: a pilot study. Endocr J 54: 791-796.
36. Srikanthan P, Karlamangla AS (2011) Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 96: 2898-2903.
37. O’Neill ED, Wilding JP, Kahn CR, Van Remmen H, McArdle A, et al. (2010) Absence of insulin signaling in skeletal muscle is associated with reduced muscle mass and function: evidence for decreased protein synthesis and not increased degradation. Age (Dordr) 32: 209-222.
38. Mavalli MD, DiGirolamo DJ, Fan Y, Riddle RC, Campbell KS, et al. (2010) Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest 120: 4007-4020.
39. Vincent HK, Raiser SN, Vincent KR (2012) The aging musculoskeletal system and obesity-related considerations with exercise. Ageing Res Rev 11: 361-373.
40. Polyzos SA, Kountouras J, Zavos C (2009) Nonalcoholic fatty liver disease: the pathogenetic roles of insulin resistance and adipocytokines. Curr Mol Med 9: 299-314.
41. Sumida Y, Yonei Y, Tanaka S, Mori K, Kanemasa K, et al. (2015) Lower levels of insulin-like growth factor-1 standard deviation score are associated with histological severity of non-alcoholic fatty liver disease. Hepatol Res 45: 771-781.
42. Kato K, Takeshita Y, Misu H, Zen Y, Kaneko S, et al. (2015) Liver steatosis is associated with insulin resistance in skeletal muscle rather than in the liver in Japanese patients with non-alcoholic fatty liver disease. J Diabetes Investig 6: 158-163.
43. Fukui M, Kitagawa Y, Ose H, Hasegawa G, Yoshikawa T, et al. (2007) Role of endogenous androgen against insulin resistance and athero- sclerosis in men with type 2 diabetes. Curr Diabetes Rev 3: 25-31.
44. Roy TA, Blackman MR, Harman SM, Tobin JD, Schrager M, et al. (2002) Interrelationships of serum testosterone and free testosterone index with FFM and strength in aging men. Am J Physiol Endocrinol Metab 283: E284-E294.
45. Senmaru T, Fukui M, Okada H, Mineoka Y, Yamazaki M, et al. (2013) Testosterone deficiency induces markedly decreased serum triglycerides, increased small dense LDL, and hepatic steatosis mediated by dysregulation of lipid assembly and secretion in mice fed a high-fat diet. Metabolism 62: 851-860.
46. Yoo KD, Jun DW, Lee KN, Lee HL, Lee OY, et al. (2015) Sarcopenia is a risk factor for elevated aminotransferase in men independently of body mass index, dietary habits, and physical activity. Dig Liver Dis 47: 303-308.
47. Enns DL, Tiidus PM (2010) The influence of estrogen on skeletal muscle: sex matters. Sports Med 40: 41-58.
48. Hewitt KN, Pratis K, Jones ME, Simpson ER (2004) Estrogen replacement reverses the hepatic steatosis phenotype in the male aromatase knockout mouse. Endocrinology 145: 1842-1848.
49. Gutierrez-Grobe Y, Ponciano-Rodríguez G, Ramos MH, Uribe M, Méndez-Sánchez N (2010) Prevalence of non alcoholic fatty liver disease in premenopausal, posmenopausal and polycystic ovary syndrome women. The role of estrogens. Ann Hepatol 9: 402-409.
50. Jimba S, Nakagami T, Takahashi M, Wakamatsu T, Hirota Y, et al. (2005) Prevalence of non-alcoholic fatty liver disease and its association with impaired glucose metabolism in Japanese adults. Diabet Med 22: 1141-1145.
51. Leite NC, Salles GF, Araujo AL, Villela-Nogueira CA, Cardoso CR (2009) Prevalence and associated factors of non-alcoholic fatty liver disease in patients with type-2 diabetes mellitus. Liver Int 29: 113-119.