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Prevalence of and risk factors for non-alcoholic fatty liver disease in a non-obese Japanese population, 2011–2012

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

Abstract

Background

Non-alcoholic fatty liver disease (NAFLD) in non-obese subjects is not rare in Japan, but it has not been clearly described. To clarify its prevalence and risk factors, we investigated the clinical characteristics of NAFLD in non-obese subjects in comparison with NAFLD in obese subjects in the Japanese general population.

Methods

A cross-sectional study was performed with 5433 subjects who received health checkups from 2011 to 2012. Subjects consuming more than 20 g of alcohol per day and those with autoimmune liver disease, viral hepatitis, uncontrolled biliary disease and insufficient data were excluded. Subjects with a body mass index (BMI) ≥25 kg/m2 were considered obese, and subjects with a BMI <25 kg/m2 were considered non-obese.

Results

A total of 3271 subjects were enrolled. The overall prevalence of NAFLD was 24.6 %: 68.5 % in obese subjects and 15.2 % in non-obese subjects. The multivariate logistic regression analysis revealed that ≥10 kg of weight gain since the age of 20 was significantly associated with NAFLD in non-obese subjects of both genders, and eating an evening meal within 2 h before going to bed 3 days or more per week and drinking <20 g of alcohol per day were negatively associated in non-obese females. Metabolic factors such as waist circumference and triglycerides were predictors of NAFLD in non-obese subjects, and body fat percentage was a predictor in non-obese males.

Conclusions

Lifestyle as well as metabolic factors may play crucial roles in the pathogenesis of NAFLD, even in the non-obese Japanese population.

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Abbreviations

Ht:

Body height

BW:

Body weight

BMI:

Body mass index

BFP:

Body fat percentage

WC:

Waist circumference

CRP:

C-reactive protein

SBP:

Systolic blood pressure

DBP:

Diastolic blood pressure

TP:

Total protein

ALB:

Serum albumin

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

ALP:

Alkaline phosphatase

GGT:

Gamma-glutamyl transpeptidase

ChE:

Cholinesterase

BUN:

Blood urea nitrogen

Cr:

Serum creatinine

eGFR:

Estimated glomerular filtration rate

UA:

Uric acid

TC:

Total cholesterol

TG:

Triglyceride

HDL:

High-density lipoprotein cholesterol

LDL:

Low-density lipoprotein cholesterol

FPG:

Fasting plasma glucose

HbA1c:

Hemoglobin A1c

NGSP:

National glycohemoglobin standardization program

References

  1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221–31.

    Article  CAS  PubMed  Google Scholar 

  2. Sung KC, Ryan MC, Wilson AM. The severity of nonalcoholic fatty liver disease is associated with increased cardiovascular risk in a large cohort of non-obese Asian subjects. Atherosclerosis. 2009;203:581–6.

    Article  CAS  PubMed  Google Scholar 

  3. Kojima S, Watanabe N, Numata M, Ogawa T, Matsuzaki S. Increase in the prevalence of fatty liver in Japan over the past 12 years: analysis of clinical background. J Gastroenterol. 2003;38:954–61.

    Article  PubMed  Google Scholar 

  4. Omagari K, Morikawa S, Nagaoka S, Egawa I, Sawa T, Hazama H, et al. Fatty liver in non-alcoholic non-overweight Japanese adults: incidence and clinical characteristics. J Gastroenterol Hepatol. 2002;17:1098–105.

    Article  PubMed  Google Scholar 

  5. Eguchi Y, Hyogo H, Ono M, Mizuta T, Ono N, Fujimoto K, JSG-NAFLD, et al. Prevalence and associated metabolic factors of nonalcoholic fatty liver disease in the general population from 2009 to 2010 in Japan: a multicenter large retrospective study. J Gastroenterol. 2012;47:586–95.

    Article  CAS  PubMed  Google Scholar 

  6. Committee for diagnostic criteria of Metabolic Syndrome. The definition and diagnostic criteria of Metabolic Syndrome (In Japanese). J Jpn Soc Int Med. 2005;94:794–809.

    Article  Google Scholar 

  7. A standard Health Checkup and Health Guidance Program (In Japanese). Health Department of the Ministry of Health, Labor and Welfare, Japan. 2007.

  8. International Obesity Task Force. The Asian-Pacific perspective: redefining obesity and its treatment. Sydney: Health Communications Australia Pty Limited; 2000.

    Google Scholar 

  9. Kashiwagi A, Kasuga M, Arai E, Oka Y, Hanafusa T, Ito H, et al. International clinical harmonization of glycated hemoglobin in Japan. From Japan Diabetes Society to National Glycohemoglobin Standardization Program Values. Diabetol Int. 2012;3:8–10.

    Article  Google Scholar 

  10. Kim HJ, Kim HJ, Lee KE, Kim DJ, Kim SK, Ahn CW, Lim SK, et al. Metabolic significance of nonalcoholic fatty liver disease in nonobese, nondiabetic adults. Arch Intern Med. 2004;164:2169–75.

    Article  PubMed  Google Scholar 

  11. Pagadala MR, McCullough AJ. Non-alcoholic fatty liver disease and obesity: not all about body mass index. Am J Gastroenterol. 2012;107:1859–61.

    Article  PubMed  Google Scholar 

  12. Das K, Das K, Mukherjee PS, Ghosh A, Ghosh S, Mridha AR, et al. Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver and significant liver disease. Hepatology. 2010;51:1593–602.

    Article  CAS  PubMed  Google Scholar 

  13. Younossi ZM, Stepanova M, Negro F, Hallaji S, Younossi Y, Lam B, Srishord M. Nonalcoholic fatty liver disease in lean individuals in the United States. Medicine (Baltimore). 2012;91:319–27.

    Article  Google Scholar 

  14. Kwon YM, Oh SW, Hwang SS, Lee C, Kwon H, Chung GE. Association of nonalcoholic fatty liver disease with components of metabolic syndrome according to body mass index in Korean adults. Am J Gastroenterol. 2012;107:1852–8.

    Article  CAS  PubMed  Google Scholar 

  15. Chen CH, Huang MH, Yang JC, Nien CK, Yang CC, Yeh YH, Yueh SK. Prevalence and risk factors of nonalcoholic fatty liver disease in an adult population of Taiwan: metabolic significance of nonalcoholic fatty liver disease in nonobese adults. J Clin Gastroenterol. 2006;40:745–52.

    Article  CAS  PubMed  Google Scholar 

  16. Xu C, Yu C, Ma H, Xu L, Miao M, Li Y. Prevalence and risk factors for the development of nonalcoholic Fatty liver disease in a nonobese Chinese population: the Zhejiang Zhenhai study. Am J Gastroenterol. 2013;108:1299–304.

    Article  PubMed  Google Scholar 

  17. Hamaguchi M, Kojima T, Takeda N, Nakagawa T, Taniguchi H, Fujii K, Omatsu T, et al. The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann Intern Med. 2005;143:722–8.

    Article  CAS  PubMed  Google Scholar 

  18. Chang Y, Ryu S, Sung E, Woo HY, Cho SI, Yoo SH, et al. Weight gain within the normal weight range predicts ultrasonographically detected fatty liver in healthy Korean men. Gut. 2009;58:1419–25.

    Article  CAS  PubMed  Google Scholar 

  19. Saida T, Fukushima W, Ohfuji S, Kondo K, Matsunaga I, Hirota Y. Effect modification of body mass index and body fat percentage on fatty liver disease in a Japanese population. J Gastroenterol Hepatol. 2013;. doi:10.1111/jgh.12377.

    Google Scholar 

  20. Johnson NA, Keating SE, George J. Exercise and the liver: implications for therapy in fatty liver disorders. Semin Liver Dis. 2012;32:65–79.

    Article  CAS  PubMed  Google Scholar 

  21. Dunn W, Xu R, Schwimmer JB. Modest wine drinking and decreased prevalence of suspected nonalcoholic fatty liver disease. Hepatology. 2008;47:1947–54.

    Article  PubMed  Google Scholar 

  22. Gunji T, Matsuhashi N, Sato H, Fujibayashi K, Okumura M, Sasabe N, Urabe A. Light and moderate alcohol consumption significantly reduces the prevalence of fatty liver in the Japanese male population. Am J Gastroenterol. 2009;104:2189–95.

    Article  PubMed  Google Scholar 

  23. Davies MJ, Baer DJ, Judd JT, Brown ED, Campbell WS, Taylar PR. Effects of moderate alcohol intake on fasting insulin and glucose concentrations and insulin sensitivity in postmenopausal women: a randomized controlled trial. JAMA. 2002;287:2559–62.

    Article  CAS  PubMed  Google Scholar 

  24. Hamabe A, Uto H, Imamura Y, Kusano K, Mawatari S, Kumagai K, et al. Impact of cigarette smoking on onset of nonalcoholic fatty liver disease: a 10-year longitudinal study. J Gastroenterol. 2011;46:769–78.

    Article  CAS  PubMed  Google Scholar 

  25. Ohkuma T, Fujii H, Iwase M, Kikuchi Y, Ogata S, Idewaki Y, Ide H, et al. Impact of eating rate on obesity and cardiovascular risk factors according to glucose tolerance status: the Fukuoka Diabetes Registry and the Hisayama Study. Diabetologia. 2013;56:70–7.

    Article  CAS  PubMed  Google Scholar 

  26. Eguchi Y, Eguchi T, Mizuta T, Ide Y, Yasutake T, Iwakiri R, et al. Visceral fat accumulation and insulin resistance are important factors in nonalcoholic fatty liver disease. J Gastroenterol. 2006;41:462–9.

    Article  CAS  PubMed  Google Scholar 

  27. Eguchi Y, Mizuta T, Sumida Y, Ishibashi E, Kitajima Y, Isoda H, et al. The pathological role of visceral fat accumulation in steatosis, inflammation, and progression of nonalcoholic fatty liver disease. J Gastroenterol. 2011;46:70–8.

    Article  CAS  PubMed  Google Scholar 

  28. van der Poorten D, Milner KL, Hui J, Hodge A, Trenell MI, Kench JG, et al. Visceral fat: a key mediator of steatohepatitis in metabolic liver disease. Hepatology. 2008;48:449–57.

    Article  PubMed  Google Scholar 

  29. Imamura Y, Uto H, Oketani M, Hiramie Y, Hosoyamada K, Sho Y, et al. Association between changes in body composition an d the increasing prevalence of fatty liver in Japanese men. Hepatol Res. 2008;38:1083–6.

    Article  CAS  PubMed  Google Scholar 

  30. Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD. Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol. 1991;43:26–31.

    Article  CAS  PubMed  Google Scholar 

  31. Friedman GD, Collen MF, Fireman BH. Multiphasic health checkup evaluation: a 16-year follow-up. J Chronic Dis. 1986;39:453–63.

    Article  CAS  PubMed  Google Scholar 

  32. Abid A, Taha O, Nseir W, Farah R, Grosovski M, Assy N. Soft drinks consumption is associated with fatty liver disease independent of metabolic syndrome. J Hepatol. 2009;51:918–24.

    Article  CAS  PubMed  Google Scholar 

  33. Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, et al. Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology. 2003;37:909–15.

    Article  CAS  PubMed  Google Scholar 

  34. Solga S, Alkhuraishe AR, Clark JM, Torbenson M, Greenwald A, Diehl AM, Magnuson T. Dietary composition and nonalcoholic fatty liver disease. Dig Dis Sci. 2004;49:1578–83.

    Article  PubMed  Google Scholar 

  35. Yasutake K, Nakamuta M, Shima Y, Ohyama A, Masuda K, Haruta N, et al. Nutritional investigation of non-obese patients with non-alcoholic fatty liver disease: the significance of dietary cholesterol. Scand J Gastroenterol. 2009;44:471–7.

    Article  CAS  PubMed  Google Scholar 

  36. McCarthy EM, Rinella ME. The role of diet and nutrient composition in nonalcoholic fatty liver disease. J Acad Nutr Diet. 2012;112:401–9.

    Article  CAS  PubMed  Google Scholar 

  37. Vega GL, Chandalia M, Szczepaniak LS, Grundy SM. Metabolic correlates of nonalcoholic fatty liver in women and men. Hepatology. 2007;46:716–22.

    Article  CAS  PubMed  Google Scholar 

  38. Korenblat KM, Fabbrini E, Mohammed BS, Klein S. Liver, muscle, and adipose tissue insulin action is directly related to intrahepatic triglyceride content in obese subjects. Gastroenterology. 2008;134:1369–75.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Jimba S, Nakagami T, Takahashi M, Wakamatsu T, Hirota Y, Iwamoto Y, et al. Prevalence of non-alcoholic fatty liver disease and its association with impaired glucose metabolism in Japanese adults. Diabetes Med. 2005;22:1141–5.

    Article  CAS  Google Scholar 

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Conflict of interest

Yoshito Itoh received commercial research funds from Dainippon Sumitomo Pharma Co., Ltd.

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Correspondence to Kenichi Nishioji.

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Nishioji, K., Sumida, Y., Kamaguchi, M. et al. Prevalence of and risk factors for non-alcoholic fatty liver disease in a non-obese Japanese population, 2011–2012. J Gastroenterol 50, 95–108 (2015). https://doi.org/10.1007/s00535-014-0948-9

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  • DOI: https://doi.org/10.1007/s00535-014-0948-9

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