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Awareness of Nonalcoholic Fatty Liver Disease Is Increasing but Remains Very Low in a Representative US Cohort

  • Amandeep SinghEmail author
  • Amaninder S. Dhaliwal
  • Shailainder Singh
  • Atul Kumar
  • Rocio Lopez
  • Mohit Gupta
  • Mazen Noureddin
  • William Carey
  • Arthur McCullough
  • Naim Alkhouri
Original Article

Abstract

Background

Nonalcoholic fatty liver disease (NAFLD) has become the most common form of chronic liver disease in the USA. Interestingly, most patients with NAFLD are unaware of having any liver disease (LD). We aimed to assess the awareness of suspected NAFLD and factors associated with being aware of LD.

Methods

Adult subjects with suspected NAFLD (BMI > 25) with elevated ALT in the absence of secondary causes of LD who participated in the continuous national health and nutrition examination survey (NHANES) during 2001–2016 were identified and analyzed. Trends of NAFLD awareness were then assessed in periods of 4 years each. Multivariable logistic regression analysis was performed to assess factors associated with LD awareness.

Results

A total of 7033 subjects were included in the final analysis (1731, 1757, 1711, and 1834 subjects for the periods of 2001–2004, 2005–2008, 2009–2012, and 2013–2016, respectively). Over the study duration, an increase in BMI, waist circumference, diabetes, and HbA1c; and a decrease in the number of smokers, platelets count, bilirubin, total cholesterol, and LDL level were noticed (p < 0.001). Awareness of having LD across study periods has increased over time from 1.5% in the 2001–2004 periods to 3.1% in the 2013–2016 periods. Multivariable logistic regression analysis showed that older age, ethnicity (non-black), having fewer drinks/week, metabolic syndrome, higher ALT, ALP, and GGT were associated with being aware of having LD.

Conclusions

Awareness of having LD among subjects with suspected NAFLD has increased over the last two decades, but more than 95% of these patients are still unaware of having LD. Educational programs to increase awareness of LD and risk factors for NAFLD should be implemented on a large scale.

Clinical Trial Registration Number

Not required, as we used de-identified NHANES data.

Keywords

Nonalcoholic fatty liver disease (NAFLD) Noninvasive scores Awareness Liver disease 

Abbreviations

AF

Advanced fibrosis

AST

Aspartate aminotransferase

ALT

Alanine aminotransferase

APRI

AST to platelet ration index

BMI

Body mass index

CDC

Centers for disease control and prevention

ESLD

End-stage liver disease

FIB-4

Fibrosis-4

GGT

γ-Glutamyl transpeptidase

HSI

Hepatic steatosis index

HDL

High-density lipoprotein

HbA1c

Hemoglobin A1c

IDF

International diabetes federation

LDL

Low-density lipoprotein

LD

Liver disease

MCQ

“Medical conditions” questionnaire

MetS

Metabolic syndrome

NHANES

National health and nutrition examination survey

NAFLD

Nonalcoholic fatty liver disease

NFS

NAFLD fibrosis score

NASH

Nonalcoholic steatohepatitis

NCHS

National center for health statistics

ULN

Upper limit of normal

Notes

Author’s contribution

AS, ASD, MG, and NA helped in study concept and design; AS contributed to acquisition of data; all authors helped in analysis and interpretation of data, drafting of the manuscript and critical revision of the manuscript for important intellectual content, and administrative, technical, or material support; RL, AS, and NA contributed to statistical analysis; ASD, SS, AK, AK, MN, WC, AM, and NA contributed to study supervision.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology (Baltimore, Md).. 2016;64:73–84.CrossRefGoogle Scholar
  2. 2.
    Wong RJ, Liu B, Bhuket T. Significant burden of nonalcoholic fatty liver disease with advanced fibrosis in the US: a cross-sectional analysis of 2011–2014 National Health and Nutrition Examination Survey. Aliment Pharmacol Ther. 2017;46:974–980.CrossRefGoogle Scholar
  3. 3.
    Kabbany MN, Conjeevaram Selvakumar PK, Watt K, 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;112:581–587.CrossRefGoogle Scholar
  4. 4.
    Noureddin M, Vipani A, Bresee C, et al. NASH leading cause of liver transplant in women: updated analysis of indications for liver transplant and ethnic and gender variances. Am J Gastroenterol. 2018;113:1649–1659.CrossRefGoogle Scholar
  5. 5.
    Marchesini G, Brizi M, Bianchi G, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50:1844–1850.CrossRefGoogle Scholar
  6. 6.
    Wieland AC, Mettler P, McDermott MT, Crane LA, Cicutto LC, Bambha KM. Low awareness of nonalcoholic fatty liver disease among patients at high metabolic risk. J Clin Gastroenterol. 2015;49:e6–e10.CrossRefGoogle Scholar
  7. 7.
    Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999–2006. Diabetes Care. 2011;34:216–219.CrossRefGoogle Scholar
  8. 8.
    Adams LA, Lymp JF, St Sauver J, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005;129:113–121.CrossRefGoogle Scholar
  9. 9.
    Sanna C, Rosso C, Marietti M, Bugianesi E. Nonalcoholic fatty liver disease and extra-hepatic cancers. Int J Mol Sci. 2016;17:717.CrossRefGoogle Scholar
  10. 10.
    Yasui K, Sumida Y, Mori Y, et al. Nonalcoholic steatohepatitis and increased risk of chronic kidney disease. Metab Clin Exp. 2011;60:735–739.CrossRefGoogle Scholar
  11. 11.
    Yan LH, Mu B, Guan Y, et al. Assessment of the relationship between nonalcoholic fatty liver disease and diabetic complications. J Diabetes Investig. 2016;7:889–894.CrossRefGoogle Scholar
  12. 12.
    Leung CM, Lai LS, Wong WH, et al. Nonalcoholic fatty liver disease: an expanding problem with low levels of awareness in Hong Kong. J Gastroenterol Hepatol. 2009;24:1786–1790.CrossRefGoogle Scholar
  13. 13.
    Federation ID. The IDF Consensus Worldwide Definition of the Metabolic Syndrome 2011. https://www.pitt.edu/~super1/Metabolic/IDF1.pdf. Accessed 30 Jan 2019.
  14. 14.
    Lee JH, Kim D, Kim HJ, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis: Off J Ital Soc Gastroenterol Ital Assoc Study Liver. 2010;42:503–508.CrossRefGoogle Scholar
  15. 15.
    Johnson CL, Paulose-Ram R, Ogden CL, et al. National health and nutrition examination survey: analytic guidelines, 1999–2010. Vital Health Stat. 2013;2:1–24.Google Scholar
  16. 16.
    Kim D, Kim WR. Nonobese Fatty Liver Disease. Clin Gastroenterol Hepatol: Off Clin Pract J Am Gastroenterol Assoc. 2017;15:474–485.CrossRefGoogle Scholar
  17. 17.
    Yilmaz Y. Is nonalcoholic fatty liver disease the hepatic expression of the metabolic syndrome? World J Hepatol. 2012;4:332–334.CrossRefGoogle Scholar
  18. 18.
    Dyson JK, Anstee QM, McPherson S. Nonalcoholic fatty liver disease: a practical approach to diagnosis and staging. Frontline Gastroenterol. 2014;5:211–218.CrossRefGoogle Scholar
  19. 19.
    Lee MJ, Kim EH, Bae SJ, et al. Age-related decrease in skeletal muscle mass is an independent risk factor for incident nonalcoholic fatty liver disease: a 10-year retrospective cohort study. Gut Liver. 2019;13:67–76.CrossRefGoogle Scholar
  20. 20.
    Lazo M, Hernaez R, Eberhardt MS, et al. Prevalence of nonalcoholic fatty liver disease in the United States: the third national health and nutrition examination survey, 1988–1994. Am J Epidemiol. 2013;178:38–45.CrossRefGoogle Scholar
  21. 21.
    Coogan PE, Wise LA, Cozier YC, Palmer JR, Rosenberg L. Lifecourse educational status in relation to weight gain in African American women. Ethn Dis. 2012;22:198–206.Google Scholar
  22. 22.
    Bergqvist CJ, Skoien R, Horsfall L, Clouston AD, Jonsson JR, Powell EE. Awareness and opinions of nonalcoholic fatty liver disease by hospital specialists. Intern Med J. 2013;43:247–253.CrossRefGoogle Scholar
  23. 23.
    Grattagliano I, D’Ambrosio G, Palmieri VO, et al. Improving nonalcoholic fatty liver disease management by general practitioners: a critical evaluation and impact of an educational training program. J Gastrointestin Liver Dis. 2008;17:389–394.Google Scholar
  24. 24.
    Polanco-Briceno S, Glass D, Stuntz M, Caze A. Awareness of nonalcoholic steatohepatitis and associated practice patterns of primary care physicians and specialists. BMC Res Notes. 2016;9:157.CrossRefGoogle Scholar
  25. 25.
    Singh Sp MB, Misra D, Pati GK, et al. Awareness and opinion of nonalcoholic fatty liver disease (NAFLD) patients about obesity and its consequences. J Hepatol. 2014;60:S352.Google Scholar
  26. 26.
    Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, et al. Long term nutritional intake and the risk for nonalcoholic fatty liver disease (NAFLD): a population based study. J Hepatol. 2007;47:711–717.CrossRefGoogle Scholar
  27. 27.
    Singh SP, Singh A, Misra D, et al. Risk factors associated with nonalcoholic fatty liver disease in Indians: a case-control study. J Clin Exp Hepatol. 2015;5:295–302.CrossRefGoogle Scholar
  28. 28.
    Modi AA, Feld JJ, Park Y, et al. Increased caffeine consumption is associated with reduced hepatic fibrosis. Hepatology (Baltimore, Md).. 2010;51:201–209.CrossRefGoogle Scholar
  29. 29.
    Kistler KD, Brunt EM, Clark JM, et al. Physical activity recommendations, exercise intensity, and histological severity of nonalcoholic fatty liver disease. Am J Gastroenterol. 2011;106:460–468. quiz 469.CrossRefGoogle Scholar
  30. 30.
    Goldberg RB, Temprosa M, Haffner S, et al. Effect of progression from impaired glucose tolerance to diabetes on cardiovascular risk factors and its amelioration by lifestyle and metformin intervention: the Diabetes Prevention Program randomized trial by the Diabetes Prevention Program Research Group. Diabetes Care. 2009;32:726–732.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Amandeep Singh
    • 1
    • 2
    Email author
  • Amaninder S. Dhaliwal
    • 3
  • Shailainder Singh
    • 3
  • Atul Kumar
    • 4
  • Rocio Lopez
    • 5
  • Mohit Gupta
    • 6
  • Mazen Noureddin
    • 7
  • William Carey
    • 2
  • Arthur McCullough
    • 2
  • Naim Alkhouri
    • 8
  1. 1.Department of Gastroenterology, Hepatology and Nutrition, Center for Human Nutrition, A5 AnnexCleveland Clinic FoundationClevelandUSA
  2. 2.Department of Gastroenterology, Hepatology and Nutrition, Digestive Diseases and Surgery InstituteCleveland ClinicClevelandUSA
  3. 3.University of Nebraska Medical CenterOmahaUSA
  4. 4.Department of Gastroenterology and HepatologyStony Brook UniversityNew YorkUSA
  5. 5.Center for Populations Health Sciences and Quantitative Health SciencesCleveland Clinic FoundationClevelandUSA
  6. 6.Department of Hospital MedicineCleveland ClinicClevelandUSA
  7. 7.Cedar-Sinai Medical CenterLos AngelesUSA
  8. 8.Texas Liver InstituteUniversity of Texas (UT) HealthSan AntonioUSA

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