Endocrinol Metab.  2019 Sep;34(3):226-233. 10.3803/EnM.2019.34.3.226.

Nonalcoholic Fatty Liver Disease and Diabetes: An Epidemiological Perspective

Affiliations
  • 1Department of Endocrinology and Metabolism, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea. hongsiri@hanmail.net

Abstract

Nonalcoholic fatty liver disease (NAFLD) is thought to stem from the body's inability to store excess energy in adipocytes; as such, it is commonly viewed as the hepatic manifestation of metabolic syndrome. The pathogenesis of NAFLD involves ectopic fat accumulation, which also takes place in the liver, muscle and visceral fat. NAFLD is rapidly becoming more widespread in Korea, with an estimated prevalence of 30% in adults. Type 2 diabetes mellitus (T2DM) and NAFLD share insulin resistance as a common pathophysiological mechanism, and each of these two diseases affects the development of the other. Recent studies have suggested that NAFLD is often present as a comorbidity in T2DM patients. The mutual interrelationship between these conditions is shown by findings suggesting that T2DM can exacerbate NAFLD by promoting progression to nonalcoholic hepatosteatosis or fibrosis, while NAFLD causes the natural course of diabetic complications to worsen in T2DM patients. It remains unknown whether one disease is the cause of the other or vice versa. In this review, I would like to discuss current epidemiological data on the associations between NAFLD and T2DM, and how each disease affects the course of the other.

Keyword

Non-alcoholic fatty liver disease; Diabetes mellitus, type 2; Insulin resistance; Epidemiology

MeSH Terms

Adipocytes
Adult
Comorbidity
Diabetes Complications
Diabetes Mellitus, Type 2
Epidemiology
Fibrosis
Humans
Insulin Resistance
Intra-Abdominal Fat
Korea
Liver
Non-alcoholic Fatty Liver Disease*
Prevalence

Figure

  • Fig. 1 Relationships between diabetes, nonalcoholic fatty liver disease and their consequences. NASH, nonalcoholic steatohepatitis; NAFLD, nonalcoholic fatty liver disease.


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Reference

1. Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol. 2015; 62(1 Suppl):S47–S64.
Article
2. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004; 40:1387–1395.
Article
3. Bugianesi E, Gastaldelli A, Vanni E, Gambino R, Cassader M, Baldi S, et al. Insulin resistance in non-diabetic patients with non-alcoholic fatty liver disease: sites and mechanisms. Diabetologia. 2005; 48:634–642.
Article
4. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Bugianesi E, Lenzi M, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001; 50:1844–1850.
Article
5. Lee YH, Cho Y, Lee BW, Park CY, Lee DH, Cha BS, et al. Nonalcoholic fatty liver disease in diabetes. Part I: epidemiology and diagnosis. Diabetes Metab J. 2019; 43:31–45.
Article
6. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology. 2012; 142:1592–1609.
Article
7. 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; 51:1593–1602.
Article
8. Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013; 10:686–690.
Article
9. Park SH, Jeon WK, Kim SH, Kim HJ, Park DI, Cho YK, et al. Prevalence and risk factors of non-alcoholic fatty liver disease among Korean adults. J Gastroenterol Hepatol. 2006; 21(1 Pt 1):138–143.
Article
10. Jeong EH, Jun DW, Cho YK, Choe YG, Ryu S, Lee SM, et al. Regional prevalence of non-alcoholic fatty liver disease in Seoul and Gyeonggi-do, Korea. Clin Mol Hepatol. 2013; 19:266–272.
Article
11. Park SH, Kim BI, Yun JW, Kim JW, Park DI, Cho YK, et al. Insulin resistance and C-reactive protein as independent risk factors for non-alcoholic fatty liver disease in non-obese Asian men. J Gastroenterol Hepatol. 2004; 19:694–698.
Article
12. Rhee EJ, Lee WY, Cho YK, Kim BI, Sung KC. Hyperinsulinemia and the development of nonalcoholic fatty liver disease in nondiabetic adults. Am J Med. 2011; 124:69–76.
Article
13. Yun KE, Nam GE, Lim J, Park HS, Chang Y, Jung HS, et al. Waist gain is associated with a higher incidence of nonalcoholic fatty liver disease in Korean adults: a cohort study. PLoS One. 2016; 11:e0158710.
Article
14. Choe YG, Jin W, Cho YK, Chung WG, Kim HJ, Jeon WK, et al. Apolipoprotein B/AI ratio is independently associated with non-alcoholic fatty liver disease in nondiabetic subjects. J Gastroenterol Hepatol. 2013; 28:678–683.
Article
15. Seo YY, Cho YK, Bae JC, Seo MH, Park SE, Rhee EJ, et al. Tumor necrosis factor-α as a predictor for the development of nonalcoholic fatty liver disease: a 4-year follow-up study. Endocrinol Metab (Seoul). 2013; 28:41–45.
Article
16. Jeon WS, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, et al. Association of serum adipocyte-specific fatty acid binding protein with fatty liver index as a predictive indicator of nonalcoholic fatty liver disease. Endocrinol Metab (Seoul). 2013; 28:283–287.
Article
17. Sung KC, Ryu S, Lee JY, Kim JY, Wild SH, Byrne CD. Effect of exercise on the development of new fatty liver and the resolution of existing fatty liver. J Hepatol. 2016; 65:791–797.
Article
18. Bae JC, Suh S, Park SE, Rhee EJ, Park CY, Oh KW, et al. Regular exercise is associated with a reduction in the risk of NAFLD and decreased liver enzymes in individuals with NAFLD independent of obesity in Korean adults. PLoS One. 2012; 7:e46819.
Article
19. Kim CW, Yun KE, Jung HS, Chang Y, Choi ES, Kwon MJ, et al. Sleep duration and quality in relation to non-alcoholic fatty liver disease in middle-aged workers and their spouses. J Hepatol. 2013; 59:351–357.
Article
20. Ryu S, Chang Y, Jung HS, Yun KE, Kwon MJ, Choi Y, et al. Relationship of sitting time and physical activity with non-alcoholic fatty liver disease. J Hepatol. 2015; 63:1229–1237.
Article
21. Lonardo A, Ballestri S, Marchesini G, Angulo P, Loria P. Nonalcoholic fatty liver disease: a precursor of the metabolic syndrome. Dig Liver Dis. 2015; 47:181–190.
Article
22. Bril F, Cusi K. Management of nonalcoholic fatty liver disease in patients with type 2 diabetes: a call to action. Diabetes Care. 2017; 40:419–430.
Article
23. Portillo-Sanchez P, Bril F, Maximos M, Lomonaco R, Biernacki D, Orsak B, et al. High prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus and normal plasma aminotransferase levels. J Clin Endocrinol Metab. 2015; 100:2231–2238.
Article
24. Kim BY, Jung CH, Mok JO, Kang SK, Kim CH. Prevalences of diabetic retinopathy and nephropathy are lower in Korean type 2 diabetic patients with non-alcoholic fatty liver disease. J Diabetes Investig. 2014; 5:170–175.
Article
25. Eguchi Y, Hyogo H, Ono M, Mizuta T, Ono N, Fujimoto K, 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; 47:586–595.
Article
26. Anstee QM, Targher G, Day CP. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol. 2013; 10:330–344.
Article
27. Tilg H, Moschen AR, Roden M. NAFLD and diabetes mellitus. Nat Rev Gastroenterol Hepatol. 2017; 14:32–42.
Article
28. Adams LA, Anstee QM, Tilg H, Targher G. Non-alcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut. 2017; 66:1138–1153.
Article
29. Ballestri S, Zona S, Targher G, Romagnoli D, Baldelli E, Nascimbeni F, et al. Nonalcoholic fatty liver disease is associated with an almost twofold increased risk of incident type 2 diabetes and metabolic syndrome: evidence from a systematic review and meta-analysis. J Gastroenterol Hepatol. 2016; 31:936–944.
Article
30. Kim CH, Park JY, Lee KU, Kim JH, Kim HK. Fatty liver is an independent risk factor for the development of type 2 diabetes in Korean adults. Diabet Med. 2008; 25:476–481.
Article
31. Sung KC, Kim SH. Interrelationship between fatty liver and insulin resistance in the development of type 2 diabetes. J Clin Endocrinol Metab. 2011; 96:1093–1097.
Article
32. Sung KC, Wild SH, Byrne CD. Resolution of fatty liver and risk of incident diabetes. J Clin Endocrinol Metab. 2013; 98:3637–3643.
Article
33. Yamazaki H, Tsuboya T, Tsuji K, Dohke M, Maguchi H. Independent association between improvement of nonalcoholic fatty liver disease and reduced incidence of type 2 diabetes. Diabetes Care. 2015; 38:1673–1679.
Article
34. Bae JC, Han JM, Cho JH, Kwon H, Park SE, Park CY, et al. The persistence of fatty liver has a differential impact on the development of diabetes: the Kangbuk Samsung Health Study. Diabetes Res Clin Pract. 2018; 135:1–6.
Article
35. Sung KC, Jeong WS, Wild SH, Byrne CD. Combined influence of insulin resistance, overweight/obesity, and fatty liver as risk factors for type 2 diabetes. Diabetes Care. 2012; 35:717–722.
Article
36. Bae JC, Rhee EJ, Lee WY, Park SE, Park CY, Oh KW, et al. Combined effect of nonalcoholic fatty liver disease and impaired fasting glucose on the development of type 2 diabetes: a 4-year retrospective longitudinal study. Diabetes Care. 2011; 34:727–729.
Article
37. Bae JC, Kim SK, Han JM, Kwon S, Lee DY, Kim J, et al. Additive effect of non-alcoholic fatty liver disease on the development of diabetes in individuals with metabolic syndrome. Diabetes Res Clin Pract. 2017; 129:136–143.
Article
38. Choi JH, Rhee EJ, Bae JC, Park SE, Park CY, Cho YK, et al. Increased risk of type 2 diabetes in subjects with both elevated liver enzymes and ultrasonographically diagnosed nonalcoholic fatty liver disease: a 4-year longitudinal study. Arch Med Res. 2013; 44:115–120.
Article
39. Chang Y, Jung HS, Yun KE, Cho J, Cho YK, Ryu S. Cohort study of non-alcoholic fatty liver disease, NAFLD fibrosis score, and the risk of incident diabetes in a Korean population. Am J Gastroenterol. 2013; 108:1861–1868.
Article
40. Bhatia LS, Curzen NP, Calder PC, Byrne CD. Non-alcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur Heart J. 2012; 33:1190–1200.
Article
41. 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.
Article
42. Kwok R, Choi KC, Wong GL, Zhang Y, Chan HL, Luk AO, et al. Screening diabetic patients for non-alcoholic fatty liver disease with controlled attenuation parameter and liver stiffness measurements: a prospective cohort study. Gut. 2016; 65:1359–1368.
Article
43. Koehler EM, Plompen EP, Schouten JN, Hansen BE, Darwish Murad S, Taimr P, et al. Presence of diabetes mellitus and steatosis is associated with liver stiffness in a general population: the Rotterdam study. Hepatology. 2016; 63:138–147.
Article
44. McPherson S, Hardy T, Henderson E, Burt AD, Day CP, Anstee QM. Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: implications for prognosis and clinical management. J Hepatol. 2015; 62:1148–1155.
Article
45. Goh GB, Pagadala MR, Dasarathy J, Unalp-Arida A, Sargent R, Hawkins C, et al. Clinical spectrum of non-alcoholic fatty liver disease in diabetic and non-diabetic patients. BBA Clin. 2014; 3:141–145.
Article
46. Hossain N, Afendy A, Stepanova M, Nader F, Srishord M, Rafiq N, et al. Independent predictors of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2009; 7:1224–1229.
Article
47. Targher G, Bertolini L, Rodella S, Tessari R, Zenari L, Lippi G, et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care. 2007; 30:2119–2121.
Article
48. Targher G, Bertolini L, Rodella S, Zoppini G, Lippi G, Day C, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia. 2008; 51:444–450.
Article
49. Adams LA, Harmsen S, St Sauver JL, Charatcharoenwitthaya P, Enders FB, Therneau T, et al. Nonalcoholic fatty liver disease increases risk of death among patients with diabetes: a community-based cohort study. Am J Gastroenterol. 2010; 105:1567–1573.
Article
50. Targher G, Pichiri I, Zoppini G, Trombetta M, Bonora E. Increased prevalence of cardiovascular disease in type 1 diabetic patients with non-alcoholic fatty liver disease. J Endocrinol Invest. 2012; 35:535–540.
51. Targher G, Mantovani A, Pichiri I, Mingolla L, Cavalieri V, Mantovani W, et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of chronic kidney disease in patients with type 1 diabetes. Diabetes Care. 2014; 37:1729–1736.
Article
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