Race/ethnicity-based temporal changes in prevalence of NAFLD-related advanced fibrosis in the United States, 2005–2016
Abstract
Background and aim
Advanced fibrosis associated with nonalcoholic fatty liver disease (NAFLD) has been reported to have a higher risk of hepatic and non-hepatic mortality. We aim to study the recent trends in the prevalence of NAFLD-related advanced fibrosis in a large population sample.
Methods
Cross-sectional data from 28,739 participants in the National Health and Nutrition Examination Survey (NHANES) from 2005 to 2016 were utilized. NAFLD was defined using the hepatic steatosis index (HSI) and the US fatty liver index (USFLI) in the absence of other causes of chronic liver disease. The presence and absence of advanced fibrosis in NAFLD was determined by the NAFLD fibrosis score, FIB-4 score, and aspartate aminotransferase-to-platelet ratio index.
Results
The prevalence of NAFLD-related advanced fibrosis increased from 2.6% [95% confidence interval (CI) 2.1–3.1] in 2005–2008 and 4.4% (95% CI 3.7–5.1) in 2009–2012, to 5.0% (95% CI 4.2–5.9) in 2013–2016 using HSI as the NAFLD prediction model; and from 3.3% (95% CI 2.5–4.5) in 2005–2008 and 6.4% (95% CI 3.7–5.1) in 2009–2012, to 6.8% (95% 5.3–8.7) in 2013–2016 using USFLI (p < 0.01). A similar trend was observed in entire NHANES cohort regardless of NAFLD status. While the prevalence of advanced fibrosis increased steadily in non-Hispanic whites through the duration of the study, it leveled off during 2013–2016 in non-Hispanic blacks.
Conclusions
Prevalence of advanced fibrosis associated with NAFLD increased steadily from 2005 to 2016. More importantly, race/ethnicity-based temporal differences were noted in the prevalence of NAFLD-related advanced fibrosis during the study.
Keywords
Hepatic steatosis National Health and Nutrition Examination Survey Nonalcoholic steatohepatitisAbbreviations
- NAFLD
Nonalcoholic fatty liver disease
- NFS
NAFLD fibrosis score
- APRI
Aspartate aminotransferase-to-platelet ratio index
- NHANES
National Health and Nutrition Examination Survey
- BMI
Body mass index
- HSI
Hepatic steatosis index
- USFLI
US fatty liver index
- ALT
Alanine aminotransferase
- AST
Aspartate aminotransferase
- CI
Confidence interval
Notes
Authors’ contributions
DK was involved in study concept and design, acquisition of data, analysis and interpretation of data, drafting of the manuscript. WK, ACA, GC, SPT, RJW, SAG, SAH and ZMY were involved in interpretation of data and critical revision of the manuscript for important intellectual content. AA was involved in study concept and design, analysis and interpretation of data, drafting of the manuscript, critical revision of the manuscript for important intellectual content, and study supervision.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Compliance with ethical standards
Conflict of interest
Donghee Kim, Won Kim, Adeyinka C. Adejumo, George Cholankeril, Sean P. Tighe, Robert J. Wong, Stevan A. Gonzalez, Stephen A. Harrison, Zobair M. Younossi and Aijaz Ahmed declare that they have no conflict of interest.
Supplementary material
References
- 1.Klein S. The national obesity crisis: a call for action. Gastroenterology 2004;126:6CrossRefGoogle Scholar
- 2.Lim YS, Kim WR. The global impact of hepatic fibrosis and end-stage liver disease. Clin Liver Dis 2008;12:733–746CrossRefGoogle Scholar
- 3.Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 2007;11:1–16CrossRefGoogle Scholar
- 4.Kim D, Kim WR, Kim HJ, Therneau TM. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology 2013;57:1357–1365CrossRefGoogle Scholar
- 5.Dulai PS, Singh S, Patel J, Soni M, Prokop LJ, Younossi Z, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology 2017;65:1557–1565CrossRefGoogle Scholar
- 6.Heron M. Deaths: leading causes for 2014. Natl Vital Stat Rep 2016;65:1–96Google Scholar
- 7.Kim D, Li AA, Gadiparthi C, Khan MA, Cholankeril G, Glenn JS, et al. Changing trends in etiology-based annual mortality from chronic liver disease, from 2007 through 2016. Gastroenterology 2018;155:1154–1163CrossRefGoogle Scholar
- 8.McPherson S, Stewart SF, Henderson E, Burt AD, Day CP. Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease. Gut 2010;59:1265–1269CrossRefGoogle Scholar
- 9.Wong VW, Wong GL, Chim AM, Tse AM, Tsang SW, Hui AY, et al. Validation of the NAFLD fibrosis score in a Chinese population with low prevalence of advanced fibrosis. Am J Gastroenterol 2008;103:1682–1688CrossRefGoogle Scholar
- 10.Ruhl CE, Everhart JE. Joint effects of body weight and alcohol on elevated serum alanine aminotransferase in the United States population. Clin Gastroenterol Hepatol 2005;3:1260–1268CrossRefGoogle Scholar
- 11.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;42:503–508CrossRefGoogle Scholar
- 12.Meffert PJ, Baumeister SE, Lerch MM, Mayerle J, Kratzer W, Volzke H. Development, external validation, and comparative assessment of a new diagnostic score for hepatic steatosis. Am J Gastroenterol 2014;109:1404–1414CrossRefGoogle Scholar
- 13.Hajifathalian K, Torabi Sagvand B, McCullough AJ. Effect of alcohol consumption on survival in non-alcoholic fatty liver disease: a national prospective cohort study. Hepatology. 2018. https://doi.org/10.1002/hep.30226 Google Scholar
- 14.Ruhl CE, Everhart JE. Fatty liver indices in the multiethnic United States National Health and Nutrition Examination Survey. Aliment Pharmacol Ther 2015;41:65–76CrossRefGoogle Scholar
- 15.Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology 2007;45:846–854CrossRefGoogle Scholar
- 16.Shah AG, Lydecker A, Murray K, Tetri BN, Contos MJ, Sanyal AJ, et al. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2009;7:1104–1112CrossRefGoogle Scholar
- 17.Wai CT, Greenson JK, Fontana RJ, Kalbfleisch JD, Marrero JA, Conjeevaram HS, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 2003;38:518–526CrossRefGoogle Scholar
- 18.National Health and Nutrition Examination Survey: analytic guidelines, 1999–2010, Vital and health statistics. Series 10, Data from the National Health Survey; no. 161, DHHS publication, no. 2013-1361. https://stacks.cdc.gov/view/cdc/21305
- 19.Gu Q, Paulose-Ram R, Burt VL, Kit BK. Prescription cholesterol-lowering medication use in adults aged 40 and over: United States, 2003–2012. NCHS Data Brief 2014;177:1–8Google Scholar
- 20.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;66:1138–1153CrossRefGoogle Scholar
- 21.Ekstedt M, Hagstrom H, Nasr P, Fredrikson M, Stal P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology 2015;61:1547–1554CrossRefGoogle Scholar
- 22.Angulo P, Bugianesi E, Bjornsson ES, Charatcharoenwitthaya P, Mills PR, Barrera F, et al. Simple noninvasive systems predict long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 2013;145:782–789CrossRefGoogle Scholar
- 23.Hagstrom H, Nasr P, Ekstedt M, Hammar U, Stal P, Hultcrantz R, et al. Fibrosis stage but not NASH predicts mortality and time to development of severe liver disease in biopsy-proven NAFLD. J Hepatol 2017;67:1265–1273CrossRefGoogle Scholar
- 24.Vilar-Gomez E, Calzadilla-Bertot L, Wong VWS, Castellanos M, Aller-de-la Fuente R, Metwally M, et al. Fibrosis severity as a determinant of cause-specific mortality in patients with advanced nonalcoholic fatty liver disease: a multi-national cohort study. Gastroenterology 2018;155:443–457CrossRefGoogle Scholar
- 25.Armstrong MJ, Houlihan DD, Bentham L, Shaw JC, Cramb R, Olliff S, et al. Presence and severity of non-alcoholic fatty liver disease in a large prospective primary care cohort. J Hepatol 2012;56:234–240CrossRefGoogle Scholar
- 26.Kabbany MN, Conjeevaram Selvakumar PK, Watt K, Lopez R, Akras Z, Zein N, et al. Prevalence of nonalcoholic steatohepatitis-associated cirrhosis in the United States: an analysis of national health and nutrition examination survey data. Am J Gastroenterol 2017;112:581–587CrossRefGoogle Scholar
- 27.Unalp-Arida A, Ruhl CE. Liver fat scores predict liver disease mortality in the United States population. Aliment Pharmacol Therap 2018;48:1003–1016CrossRefGoogle Scholar