Nonalcoholic fatty liver disease is an early predictor of metabolic diseases in a metabolically healthy population
Autoři:
Seokhun Yang aff001; Soongu Kwak aff001; Jeong-Hoon Lee aff002; Shinae Kang aff003; Seung-Pyo Lee aff001
Působiště autorů:
Division of Cardiology and Cardiovascular Institute, Department of Internal Medicine, Seoul National University Hospital, Seoul, South Korea
aff001; Division of Gastroenterology and Liver Research Institute, Department of Internal Medicine, Seoul National University Hospital, Seoul, South Korea
aff002; Division of Endocrinology, Department of Internal Medicine, Yonsei University, Seoul, South Korea
aff003
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224626
Souhrn
Aims
The relationship between nonalcoholic fatty liver disease and incident metabolic syndrome in metabolically healthy subjects is unknown. We aimed to investigate whether nonalcoholic fatty liver disease is a predictor of future metabolic syndrome in metabolically healthy subjects.
Materials and methods
Subjects who underwent health evaluation at least twice between 2009 and 2015 from the National Health Insurance Service-National Sample Cohort in South Korea were included. Patients without obesity who had no metabolic syndrome components were finally analyzed (n = 28,880). The definition of nonalcoholic fatty liver disease was based on both the hepatic steatosis and fatty liver indices. The incidence of metabolic syndrome, prediabetes/type 2 diabetes, hypertension, and dyslipidemia was compared between the subjects with and without nonalcoholic fatty liver disease.
Results
The presence of nonalcoholic fatty liver disease was associated with a higher risk of incident metabolic syndrome, prediabetes/type 2 diabetes, hypertension, and dyslipidemia in the entire cohort (metabolic syndrome: adjusted hazard ratio, 2.10; 95% confidence interval, 1.18–3.71; prediabetes/type 2 diabetes: adjusted hazard ratio, 1.42; 95% confidence interval, 1.06–1.90; hypertension: adjusted hazard ratio, 2.36; 95% confidence interval, 1.35–4.12; dyslipidemia: adjusted hazard ratio, 1.49; 95% confidence interval, 1.07–2.06). A similar finding was observed in the age-, sex-, smoking status-, and body mass index-based 1:5 propensity score-matched cohort of 1,092 subjects (metabolic syndrome: adjusted hazard ratio, 3.56; 95% confidence interval, 1.79–7.07; prediabetes/type 2 diabetes: adjusted hazard ratio, 1.97; 95% confidence interval, 1.04–3.73; hypertension: adjusted hazard ratio, 2.57; 95% confidence interval, 1.35–4.88; dyslipidemia: adjusted hazard ratio, 1.61; 95% confidence interval, 1.12–2.32).
Conclusions
Nonalcoholic fatty liver disease is an early predictor of metabolic dysfunction even in metabolically healthy populations.
Klíčová slova:
Fatty liver – Hypertension – Cholesterol – Metabolic disorders – Metabolic syndrome
Zdroje
1. 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(6):1138–1153. doi: 10.1136/gutjnl-2017-313884 28314735
2. Lonardo A, Nascimbeni F, Mantovani A, Targher G. Hypertension, diabetes, atherosclerosis and NASH: cause or consequence? J Hepatol. 2018;68(2):335–352. doi: 10.1016/j.jhep.2017.09.021 29122390
3. Italian Association for the Study of the Liver (AISF). AISF position paper on nonalcoholic fatty liver disease (NAFLD): Updates and future directions. Dig Liver Dis. 2017;49(5):471–483. doi: 10.1016/j.dld.2017.01.147 28215516
4. Vanni E1, Bugianesi E, Kotronen A, De Minicis S, Yki-Järvinen H, Svegliati-Baroni G. From the metabolic syndrome to NAFLD or vice versa? Dig Liver Dis. 2010;42(5):320–330. doi: 10.1016/j.dld.2010.01.016 20207596
5. Suzuki A1, Angulo P, Lymp J, St Sauver J, Muto A, Okada T, et al. Chronological development of elevated aminotransferases in a nonalcoholic population. Hepatology. 2005;41(1):64–71. doi: 10.1002/hep.20543 15690483
6. Meex RCR, Watt MJ. Hepatokines: linking nonalcoholic fatty liver disease and insulin resistance. Nat Rev Endocrinol. 2017;13(9):509–520. doi: 10.1038/nrendo.2017.56 28621339
7. Perry RJ, Samuel VT, Petersen KF, Shulman GI. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature. 2014;510(7503):84–91. doi: 10.1038/nature13478 24899308
8. Mantovani A, Byrne CD, Bonora E, Targher G. Nonalcoholic fatty liver disease and risk of incident type 2 diabetes: a meta-analysis. Diabetes Care. 2018;41(2):372–382. doi: 10.2337/dc17-1902 29358469
9. Lau K, Lorbeer R, Haring R, Schmidt CO, Wallaschofski H, Nauck M, et al. The association between fatty liver disease and blood pressure in a population-based cohort study. J Hypertens. 2012;30(6):1260–1261. doi: 10.1097/HJH.0b013e3283536662 22573082
10. Speliotes EK, Massaro JM, Hoffmann U, Vasan RS, Meigs JB, Sahani DV, et al. Fatty liver is associated with dyslipidemia and dysglycemia independent of visceral fat: the Framingham Heart Study. Hepatology. 2010;51(6):1979–1987. doi: 10.1002/hep.23593 20336705
11. Hashimoto Y, Hamaguchi M, Fukuda T, Ohbora A, Kojima T, Fukui M. Fatty liver as a risk factor for progression from metabolically healthy to metabolically abnormal in non-overweight individuals. Endocrine. 2017;57(1):89–97. doi: 10.1007/s12020-017-1313-6 28508194
12. Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013;10(11):686–690. doi: 10.1038/nrgastro.2013.171 24042449
13. Park HE, Kwak MS, Kim D, Kim MK, Cha MJ, Choi SY. Nonalcoholic fatty liver disease is associated with coronary artery calcification development: a longitudinal study. J Clin Endocrinol Metab. 2016;101(8):3134–3143. doi: 10.1210/jc.2016-1525 27253666
14. Ma J, Hwang SJ, Pedley A, Massaro JM, Hoffmann U, Chung RT, et al. Bi-directional analysis between fatty liver and cardiovascular disease risk factors. J Hepatol. 2017;66(2):390–397. doi: 10.1016/j.jhep.2016.09.022 27729222
15. Lee JH, Kim D, Kim HJ, Lee CH, Yang JI, Kim W, et al Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis. 2010;42(7):503–508. doi: 10.1016/j.dld.2009.08.002 19766548
16. Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, et al. The Fatty Liver Index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;6:33. doi: 10.1186/1471-230X-6-33 17081293
17. Lee J, Lee JS, Park SH, Shin SA, Kim K. Cohort Profile: The National Health Insurance Service-National Sample Cohort (NHIS-NSC), South Korea. Int J Epidemiol. 2017;46(2):e15. doi: 10.1093/ije/dyv319 26822938
18. National Cholesterol Education Program Expert Panel on Detection E, Treatment of High Blood Cholesterol in A. Third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation. 2002;106(25):3143–3421. 12485966
19. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr., Spertus JA, Costa F, American Heart A, National Heart L, Blood I. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, lung, and blood institute scientific statement. Circulation. 2005;112(17):2735–2752. doi: 10.1161/CIRCULATIONAHA.105.169404 16157765
20. Adams LA, Waters OR, Knuiman MW, Elliott RR, Olynyk JK. NAFLD as a risk factor for the development of diabetes and the metabolic syndrome: an eleven-year follow-up study. Am J Gastroenterol. 2009;104(4):861–867. doi: 10.1038/ajg.2009.67 19293782
21. Ryoo JH, Choi JM, Moon SY, Suh YJ, Shin JY, Shin HC, et al. The clinical availability of non alcoholic fatty liver disease as an early predictor of the metabolic syndrome in Korean men: 5-year's prospective cohort study. Atherosclerosis. 2013;227(2):398–403. doi: 10.1016/j.atherosclerosis.2013.01.002 23390894
22. 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(5):936–944. doi: 10.1111/jgh.13264 26667191
23. Yki-Järvinen H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014;2(11):901–910. doi: 10.1016/S2213-8587(14)70032-4 24731669
24. 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(3):181–190. doi: 10.1016/j.dld.2014.09.020 25739820
25. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet. 2005;365(9468):1415–1428. doi: 10.1016/S0140-6736(05)66378-7 15836891
26. Kumashiro N, Erion DM, Zhang D, Kahn M, Beddow SA, Chu X, et al. Cellular mechanism of insulin resistance in nonalcoholic fatty liver disease. Proc Natl Acad Sci U S A. 2011;108(39):16381–16385. doi: 10.1073/pnas.1113359108 21930939
27. Ortiz-Lopez C, Lomonaco R, Orsak B, Finch J, Chang Z, Kochunov VG, et al. Prevalence of prediabetes and diabetes and metabolic profile of patients with nonalcoholic fatty liver disease (NAFLD). Diabetes Care. 2012;35(4):873–878. doi: 10.2337/dc11-1849 22374640
28. Liu M, Wang J, Zeng J, Cao X, He Y. Association of NAFLD with diabetes and the impact of BMI Changes: A 5-Year Cohort Study Based on 18,507 Elderly. J Clin Endocrinol Metab. 2017;102(4):1309–1316. doi: 10.1210/jc.2016-3440 28324002
29. 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(12):1861–1868. doi: 10.1038/ajg.2013.349 24100261
30. 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(9):1673–1679. doi: 10.2337/dc15-0140 26156527
31. Sung KC, Wild SH, Byrne CD. Development of new fatty liver, or resolution of existing fatty liver, over five years of follow-up, and risk of incident hypertension. J Hepatol. 2014;60(5):1040–1045. doi: 10.1016/j.jhep.2014.01.009 24445219
32. Ryoo JH, Suh YJ, Shin HC, Cho YK, Choi JM, Park SK. Clinical association between non-alcoholic fatty liver disease and the development of hypertension. J Gastroenterol Hepatol. 2014;29(11):1926–1931. doi: 10.1111/jgh.12643 24910023
33. Artunc F, Schleicher E, Weigert C, Fritsche A, Stefan N, Haring HU. The impact of insulin resistance on the kidney and vasculature. Nat Rev Nephrol. 2016;12(12):721–737. doi: 10.1038/nrneph.2016.145 27748389
34. Bonnet F, Gastaldelli A, Pihan-Le Bars F, Natali A, Roussel R, Petrie J, et al. Gamma-glutamyltransferase, fatty liver index and hepatic insulin resistance are associated with incident hypertension in two longitudinal studies. J Hypertens. 2017;35(3):493–500. doi: 10.1097/HJH.0000000000001204 27984413
35. Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010;363(14):1341–1350. doi: 10.1056/NEJMra0912063 20879883
36. Kantartzis K, Rittig K, Cegan A, Machann J, Schick F, Balletshofer B, et al. Fatty liver is independently associated with alterations in circulating HDL2 and HDL3 subfractions. Diabetes Care. 2008;31(2):366–368. doi: 10.2337/dc07-1558 18000185
37. Cali AM, Zern TL, Taksali SE, de Oliveira AM, Dufour S, Otvos JD, et al. Intrahepatic fat accumulation and alterations in lipoprotein composition in obese adolescents: a perfect proatherogenic state. Diabetes Care. 2007;30(12):3093–3098. doi: 10.2337/dc07-1088 17717283
38. Kikkawa K, Nakajima K, Shimomura Y, Tokita Y, Machida T, Sumino H, et al. Small dense LDL cholesterol measured by homogeneous assay in Japanese healthy controls, metabolic syndrome and diabetes patients with or without a fatty liver. Clin Chim Acta. 2015;438:70–79. doi: 10.1016/j.cca.2014.07.017 25050800
39. Yamada T, Fukatsu M, Suzuki S, Wada T, Yoshida T, Joh T. Fatty liver predicts impaired fasting glucose and type 2 diabetes mellitus in Japanese undergoing a health checkup. J Gastroenterol Hepatol. 2010;25(2):352–356. doi: 10.1111/j.1440-1746.2009.05998.x 19817963
40. Brown AE, Walker M. Genetics of insulin resistance and the metabolic syndrome. Curr Cardiol Rep. 2016;18(8):75. doi: 10.1007/s11886-016-0755-4 27312935
41. Lonardo A, Ballestri S, Targher G. "Not all forms of NAFLD were created equal". Do metabolic syndrome-related NAFLD and PNPLA3-related NAFLD exert a variable impact on the risk of early carotid atherosclerosis? Atherosclerosis. 2017;257:253–255. doi: 10.1016/j.atherosclerosis.2017.01.008 28126321
42. Fedchuk L, Nascimbeni F, Pais R, Charlotte F, Housset C, Ratziu V. Performance and limitations of steatosis biomarkers in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2014;40(10):1209–1222. doi: 10.1111/apt.12963 25267215
43. Lee E, Choi EK, Han KD, Lee H, Choe WS, Lee SR, et al. Mortality and causes of death in patients with atrial fibrillation: A nationwide population-based study. PLoS One. 2018;13(12): e0209687. doi: 10.1371/journal.pone.0209687 30586468
44. Choi YJ, Lee DH, Han KD, Yoon H, Shin CM, Park YS, et al. Is nonalcoholic fatty liver disease associated with the development of prostate cancer? A nationwide study with 10,516,985 Korean men. PLoS One. 2018;13(9): e0201308. doi: 10.1371/journal.pone.0201308 30231041
45. Lonardo A, Nascimbeni F, Ballestri S, Fairweather D, Win S, Than TA, et al. Sex differences in NAFLD: State of the art and identification of research gaps. Hepatology. 2019; [Epub ahead of print].
46. Yang JD, Abdelmalek MF, Guy CD, Gill RM, Lavine JE, Yates K, et al. Patient sex, reproductive status, and synthetic hormone use associate with histologic severity of nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol. 2017;15(1):127–131.e2. doi: 10.1016/j.cgh.2016.07.034 27523635
Článek vyšel v časopise
PLOS One
2019 Číslo 11
- Tisícileté topoly, mokří psi, stárnoucí kočky a ospalé octomilky – „jednohubky“ z výzkumu 2024/41
- Jaké jsou aktuální trendy v léčbě karcinomu slinivky?
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Menstruační krev má značný diagnostický potenciál, mimo jiné u diabetu
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
Nejčtenější v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy