J Korean Diabetes.  2017 Jun;18(2):81-87. 10.4093/jkd.2017.18.2.81.

Clinical Characteristics of Non-Alcoholic Fatty Liver Disease Based on Analyses from the Kangbuk Samsung Health Study

• Rhee EJ

• KMID: 2385569
• DOI: http://doi.org/10.4093/jkd.2017.18.2.81

Abstract

Non-alcoholic fatty liver disease (NAFLD) is the hepatic manifestation of metabolic syndrome, indicating that the body can no longer effectively store excess energy in adipose tissue. This phenomenon is called "˜ectopic fat accumulation,' and the most common ectopic organs in which excess energy can accumulate in the form of triglyceride are the liver, visceral fat and muscle. The prevalence of NAFLD is rapidly increasing in Korean populations and is estimated to reach 30% in adults. NAFLD is one of the strongest risk factors of type 2 diabetes mellitus (T2DM), and the presence of NAFLD in T2DM patients is known to deteriorate the natural course of diabetic complications. Recent studies suggest that NAFLD is not only a sign of insulin resistance, but also a cardiovascular risk factor. In this review, I discuss the current knowledge regarding the prevalence, risk factors, and consequences of NAFLD based on results published in the Kangbuk Samsung Health Study, which is one of the largest health screening databases in the world.

Keyword

Clinical; Kangbuk Samsung Health Study; Non-alcoholic fatty liver disease

MeSH Terms

Adipose Tissue
Adult
Diabetes Complications
Diabetes Mellitus, Type 2
Humans
Insulin Resistance
Intra-Abdominal Fat
Liver
Mass Screening
Non-alcoholic Fatty Liver Disease*
Prevalence
Risk Factors
Triglycerides

Reference

References

1. Adams LA, Anstee QM, Tilg H, Targher G. Nonalcoholic fatty liver disease and its relationship with cardiovascular disease and other extrahepatic diseases. Gut. 2017; 66:1138–53.

2. Loria P, Lonardo A, Targher G. Is liver fat detrimental to vessels?: intersections in the pathogenesis of NAFLD and atherosclerosis. Clin Sci (Lond). 2008; 115:1–12.

3. Kitade H, Chen G, Ni Y, Ota T. Nonalcoholic fatty liver disease and insulin resistance: new insights and potential new treatments. Nutrients. 2017; 9:doi: 10.3390/nu9040387.

4. Park SH, Jeon WK, Kim SH, Kim HJ, Park DI, Cho YK, Sung IK, Sohn CI, Keum DK, Kim BI. Prevalence and risk factors of nonalcoholic fatty liver disease among Korean adults. J Gastroenterol Hepatol. 2006; 21:138–43.

5. Jeong EH, Jun DW, Cho YK, Choe YG, Ryu S, Lee SM, Jang EC. Regional prevalence of nonalcoholic fatty liver disease in Seoul and Gyeonggi-do, Korea. Clin Mol Hepatol. 2013; 19:266–72.

6. Park SH, Kim BI, Yun JW, Kim JW, Park DI, Cho YK, Sung IK, Park CY, Sohn CI, Jeon WK, Kim H, Rhee EJ, Lee WY, Kim SW. Insulin resistance and C-reactive protein as independent risk factors for nonalcoholic fatty liver disease in non-obese Asian men. J Gastroenterol Hepatol. 2004; 19:694–8.

7. 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.

8. Yun KE, Nam GE, Lim J, Park HS, Chang Y, Jung HS, Kim CW, Ko BJ, Chung EC, Shin H, Ryu S. Waist gain is associated with a higher incidence of nonalcoholic fatty liver disease in Korean adults: a cohort study. PLoS One. 2016; 11:e0158710.

9. Choe YG, Jin W, Cho YK, Chung WG, Kim HJ, Jeon WK, Kim BI. Apolipoprotein B/AI ratio is independently associated with nonalcoholic fatty liver disease in nondiabetic subjects. J Gastroenterol Hepatol. 2013; 28:678–83.

10. Seo YY, Cho YK, Bae JC, Seo MH, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Lee WY. 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; 28:41–5.

11. Jeon WS, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Lee WY. 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; 28:283–7.

12. 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; 65:791–7.

13. Bae JC, Suh S, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Kim SW, Hur KY, Kim JH, Lee MS, Lee MK, Kim KW, Lee WY. 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.

14. Kim CW, Yun KE, Jung HS, Chang Y, Choi ES, Kwon MJ, Lee EH, Woo EJ, Kim NH, Shin H, Ryu S. Sleep duration and quality in relation to nonalcoholic fatty liver disease in middle-aged workers and their spouses. J Hepatol. 2013; 59:351–7.

15. Ryu S, Chang Y, Jung HS, Yun KE, Kwon MJ, Choi Y, Kim CW, Cho J, Suh BS, Cho YK, Chung EC, Shin H, Kim YS. Relationship of sitting time and physical activity with nonalcoholic fatty liver disease. J Hepatol. 2015; 63:1229–37.

16. Tilg H, Moschen AR, Roden M. NAFLD and diabetes mellitus. Nat Rev Gastroenterol Hepatol. 2017; 14:32–42.

17. Yu TY, Wang CY. Impact of nonalcoholic fatty pancreas disease on glucose metabolism. J Diabetes Investig 2017. doi: 10.1111/jdi.12665. [Epub ahead of print].

18. Bae JC, Cho YK, Lee WY, Seo HI, Rhee EJ, Park SE, Park CY, Oh KW, Sung KC, Kim BI. Impact of nonalcoholic fatty liver disease on insulin resistance in relation to HbA1c levels in nondiabetic subjects. Am J Gastroenterol. 2010; 105:2389–95.

19. Bae JC, Rhee EJ, Lee WY, Park SE, Park CY, Oh KW, Park SW, Kim SW. 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; 34:727–9.

20. Chon CW, Kim BS, Cho YK, Sung KC, Bae JC, Kim TW, Won HS, Joo KJ. Effect of nonalcoholic fatty liver disease on the development of type 2 diabetes in nonobese, nondiabetic Korean men. Gut Liver. 2012; 6:368–73.

21. Choi JH, Rhee EJ, Bae JC, Park SE, Park CY, Cho YK, Oh KW, Park SW, Lee WY. 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; 44:115–20.

22. Chang Y, Jung HS, Yun KE, Cho J, Cho YK, Ryu S. Cohort study of nonalcoholic fatty liver disease, NAFLD fibrosis score, and the risk of incident diabetes in a Korean population. Am J Gastroenterol. 2013; 108:1861–8.

23. Seo MH, Rhee EJ. Metabolic and cardiovascular implications of a metabolically healthy obesity phenotype. Endocrinol Metab (Seoul). 2014; 29:427–34.

24. Lee MK, Rhee EJ, Kim MC, Moon BS, Lee JI, Song YS, Han EN, Lee HS, Son Y, Park SE, Park CY, Oh KW, Park SW, Lee WY. Metabolic health is more important than obesity in the development of nonalcoholic fatty liver disease: a 4-year retrospective study. Endocrinol Metab (Seoul). 2015; 30:522–30.

25. Chang Y, Jung HS, Cho J, Zhang Y, Yun KE, Lazo M, Pastor-Barriuso R, Ahn J, Kim CW, Rampal S, Cainzos-Achirica M, Zhao D, Chung EC, Shin H, Guallar E, Ryu S. Metabolically healthy obesity and the development of nonalcoholic fatty liver disease. Am J Gastroenterol. 2016; 111:1133–40.

26. Chang Y, Jung HS, Yun KE, Cho J, Ahn J, Chung EC, Shin H, Ryu S. Metabolically healthy obesity is associated with an increased risk of diabetes independently of nonalcoholic fatty liver disease. Obesity (Silver Spring). 2016; 24:1996–2003.

27. Bhatia LS, Curzen NP, Calder PC, Byrne CD. Nonalcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur Heart J. 2012; 33:1190–200.

28. Kim BJ, Kim NH, Kim BS, Kang JH. The association between nonalcoholic fatty liver disease, metabolic syndrome and arterial stiffness in nondiabetic, nonhypertensive individuals. Cardiology. 2012; 123:54–61.

29. Sung KC, Cha SC, Sung JW, So MS, Byrne CD. Metabolically healthy obese subjects are at risk of fatty liver but not of preclinical atherosclerosis. Nutr Metab Cardiovasc Dis. 2014; 24:256–62.

30. Lee MK, Park HJ, Jeon WS, Park SE, Park CY, Lee WY, Oh KW, Park SW, Rhee EJ. Higher association of coronary artery calcification with nonalcoholic fatty liver disease than with abdominal obesity in middle-aged Korean men: the Kangbuk Samsung Health Study. Cardiovasc Diabetol. 2015; 14:88.

31. Lee JI, Kim MC, Moon BS, Song YS, Han EN, Lee HS, Son Y, Kim J, Han EJ, Park HJ, Park SE, Park CY, Lee WY, Oh KW, Park SW, Rhee EJ. The relationship between 10-year cardiovascular risk calculated using the pooled cohort equation and the severity of nonalcoholic fatty liver disease. Endocrinol Metab (Seoul). 2016; 31:86–92.

32. Kim BJ, Cheong ES, Kang JG, Kim BS, Kang JH. Relationship of epicardial fat thickness and nonalcoholic fatty liver disease to coronary artery calcification: from the CAESAR study. J Clin Lipidol. 2016; 10:619–26.e1.

33. Ryu S, Suh BS, Chang Y, Kwon MJ, Yun KE, Jung HS, Kim CW, Kim BK, Kim YJ, Choi Y, Ahn J, Cho YK, Kim KH, Ahn Y, Park HY, Chung EC, Shin H, Cho J. Menopausal stages and nonalcoholic fatty liver disease in middle-aged women. Eur J Obstet Gynecol Reprod Biol. 2015; 190:65–70.

34. Ryu S, Chang Y, Choi Y, Kwon MJ, Kim CW, Yun KE, Jung HS, Kim BK, Kim YJ, Ahn J, Cho YK, Kim KH, Chung EC, Shin H, Cho J. Age at menarche and nonalcoholic fatty liver disease. J Hepatol. 2015; 62:1164–70.

35. Rhee EJ, Kim MK, Park SE, Park CY, Baek KH, Lee WY, Kang MI, Park SW, Kim SW, Oh KW. High serum vitamin D levels reduce the risk for nonalcoholic fatty liver disease in healthy men independent of metabolic syndrome. Endocr J. 2013; 60:743–52.