Skip to main content

Advertisement

SpringerLink
Log in

Assessment of the Association of HIV Infection with Hepatic Steatosis or Fibrosis: a Cross-sectional Case–Control Study

  • Original Paper
  • Published:
SN Comprehensive Clinical Medicine Aims and scope Submit manuscript

Abstract

Human immunodeficiency virus (HIV) infection and antiretroviral therapy have been associated with non-alcoholic fatty liver disease (NAFLD), but few studies have evaluated whether HIV infection is an independent risk factor for the development of hepatic steatosis and advanced liver fibrosis. To study the prevalence and severity of hepatic steatosis and advanced fibrosis in people living with HIV and control outpatients. We conducted a cross-sectional analysis of relevant data from 875 pairs of individuals belonging to an HIV-dedicated outpatient clinic and an adult primary care clinic of an inner-city hospital. Hepatic Steatosis Index (HSI) and FIB-4 index were calculated as non-invasive measures of steatosis and fibrosis, respectively. A multivariate logistic regression analysis was performed to assess predictors of steatosis and advanced fibrosis. The prevalence of hepatic steatosis, determined by HSI ≥ 36, was higher in HIV-negative subjects (71.5% vs. 65.4%, p = 0.006). The prevalence of advanced fibrosis, determined by FIB-4 index ≥ 3.25, was higher in the HIV-positive group (7% vs. 1.7%, p < 0.001). Multivariable analysis did not identify HIV infection to be an independent risk factor for hepatic steatosis (p = 0.068) and advanced fibrosis. In this cohort, hepatic steatosis was more prevalent in non-HIV infected patients, while advanced fibrosis had a higher prevalence in people living with HIV. HIV infection was not found to be an independent risk factor for either hepatic steatosis or fibrosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data availability

The dataset can be provided after data use agreement among Jacobi Medical Center, and the requester’s institution is requested and approved.

Code Availability

Not applicable.

References

  1. Palella FJ Jr, et al. Mortality in the highly active antiretroviral therapy era: changing causes of death and disease in the HIV outpatient study. J Acquir Immune Defic Syndr. 2006;43(1):27–34.

    Article  CAS  Google Scholar 

  2. Maurice, J.B., et al., Prevalence and risk factors of nonalcoholic fatty liver disease in HIV-monoinfection. AIDS, 2017. 31(11).

  3. Kapoor N, et al. A gathering storm: HIV infection and nonalcoholic fatty liver disease in low and middle-income countries. AIDS. 2019;33(7):1105–15.

    Article  Google Scholar 

  4. Lake, J.E., et al., Expert panel review on non-alcoholic fatty liver disease in persons with HIV. Clin Gastroenterol Hepatol, 2020.

  5. Price JC, et al. Risk factors for fatty liver in the multicenter AIDS cohort study. Am J Gastroenterol. 2014;109(5):695–704.

    Article  CAS  Google Scholar 

  6. Mohammed SS, et al. HIV-positive patients with nonalcoholic fatty liver disease have a lower body mass index and are more physically active than HIV-negative patients. J Acquir Immune Defic Syndr. 2007;45(4):432–8.

    Article  CAS  Google Scholar 

  7. Morse CG, et al. Nonalcoholic steatohepatitis and hepatic fibrosis in HIV-1-monoinfected adults with elevated aminotransferase levels on antiretroviral therapy. Clin Infect Dis. 2015;60(10):1569–78.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Crum-Cianflone N, et al. Nonalcoholic fatty liver disease among HIV-infected persons. J Acquir Immune Defic Syndr. 2009;50(5):464–73.

    Article  Google Scholar 

  9. Guaraldi G, et al. Nonalcoholic fatty liver disease in HIV-infected patients referred to a metabolic clinic: prevalence, characteristics, and predictors. Clin Infect Dis. 2008;47(2):250–7.

    Article  Google Scholar 

  10. Nishijima T, et al. Traditional but not HIV-related factors are associated with nonalcoholic fatty liver disease in Asian patients with HIV-1 infection. PLoS ONE. 2014;9(1):e87596–e87596.

    Article  Google Scholar 

  11. Sterling RK, Smith PG, Brunt EM. Hepatic steatosis in human immunodeficiency virus: a prospective study in patients without viral hepatitis, diabetes, or alcohol abuse. J Clin Gastroenterol. 2013;47(2):182–7.

    Article  CAS  Google Scholar 

  12. Vodkin I, et al. Clinical, biochemical and histological differences between HIV-associated NAFLD and primary NAFLD: a case-control study. Aliment Pharmacol Ther. 2015;41(4):368–78.

    Article  CAS  Google Scholar 

  13. Macías J, et al. Prevalence and factors associated with liver steatosis as measured by transient elastography with controlled attenuation parameter in HIV-infected patients. AIDS. 2014;28(9):1279–87.

    Article  Google Scholar 

  14. Lombardi R, et al. Liver test abnormalities in patients with HIV mono-infection: assessment with simple noninvasive fibrosis markers. Ann Gastroenterol. 2017;30(3):349–56.

    PubMed  PubMed Central  Google Scholar 

  15. Ong, J.P. and Z.M. Younossi, Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis, 2007. 11(1): p. 1–16, vii.

  16. Aguilar, E., Obesity and Diabetes. Wellness Newsletter, 2017.

  17. Maurice, J.B., et al., Increased BMI and type 2 diabetes are the main predictors of NAFLD and advanced fibrosis in liver biopsies of patients with HIV mono-infection. Clin Infect Dis, 2020.

  18. Observational studies: getting clear about transparency. PLoS Med, 2014. 11(8): p. e1001711.

  19. Classification and Diagnosis of Diabetes. Diabetes Care. 2017;40(Supplement 1):S11–24.

    Article  Google Scholar 

  20. Sebastiani, G., et al., Incidence and predictors of hepatic steatosis and fibrosis by serum biomarkers in a large cohort of human immunodeficiency virus mono-infected patients. Open forum infectious diseases, 2015. 2(1): p. ofv015-ofv015.

  21. Lee JH, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis. 2010;42(7):503–8.

    Article  CAS  Google Scholar 

  22. Vallet-Pichard A, et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection Comparison with liver biopsy and fibrotest. Hepatology. 2007;46(1):32–6.

    Article  CAS  Google Scholar 

  23. Després JP, et al. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol. 2008;28(6):1039–49.

    Article  Google Scholar 

  24. Gholam PM, et al. Nonalcoholic fatty liver disease in severely obese subjects. Am J Gastroenterol. 2007;102(2):399–408.

    Article  CAS  Google Scholar 

  25. He Q, et al. Insulin resistance, hepatic lipid and adipose tissue distribution in HIV-infected men. Antivir Ther. 2008;13(3):423–8.

    PubMed  PubMed Central  Google Scholar 

  26. Sulkowski MS, Benhamou Y. Therapeutic issues in HIV/HCV-coinfected patients. J Viral Hepatitis. 2007;14(6):371–86.

    Article  CAS  Google Scholar 

  27. Woreta TA, et al. Incidence and risk factors for steatosis progression in adults coinfected with HIV and hepatitis C virus. Gastroenterology. 2011;140(3):809–17.

    Article  Google Scholar 

  28. Macias J, et al. Impact of genetic polymorphisms associated with nonalcoholic fatty liver disease on HIV-infected individuals. AIDS. 2015;29(15):1927–35.

    Article  CAS  Google Scholar 

  29. Li Vecchi V, et al. Prospective evaluation of hepatic steatosis in HIV-infected patients with or without hepatitis C virus co-infection. Int J Infect Dis. 2012;16(5):e397-402.

    Article  Google Scholar 

  30. Siddiqui MS, et al. Validation of noninvasive methods for detecting hepatic steatosis in patients with human immunodeficiency virus infection. Clin Gastroenterol Hepatol. 2015;13(2):402–5.

    Article  Google Scholar 

  31. Younossi ZM, et al. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64(1):73–84.

    Article  Google Scholar 

  32. Ryan P, et al. Predictors of severe hepatic steatosis using abdominal ultrasound in HIV-infected patients. HIV Med. 2009;10(1):53–9.

    Article  CAS  Google Scholar 

  33. Kim PS, et al. A1C underestimates glycemia in HIV infection. Diabetes Care. 2009;32(9):1591–3.

    Article  CAS  Google Scholar 

Download references

Funding

Dr. Donald Kotler has received funding for work outside of the submitted manuscript: Abbvie, for research grants. None of the other authors has any relationships to disclose.

Author information

Author notes

  1.  Paula Debroy, Sanjana Nagraj and Natalia Chamorro-Pareja contributed equally.

Authors and Affiliations

  1. Jacobi Medical Center, Bronx, NY, USA

    Paula Debroy, Sanjana Nagraj, Natalia Chamorro-Pareja, Neva Castro, Arcelia Guerson-Gil, Orlando Quintero, Isaac Laniado, Dimpi Desai, Priyanka Mathias, Jason Leider, Preeti Kishore, Leonidas Palaiodimos & Donald P. Kotler

  2. University of Texas Health Sciences Center, Houston, TX, USA

    Paula Debroy

  3. Albert Einstein College of Medicine, Bronx, NY, USA

    Sanjana Nagraj, Natalia Chamorro-Pareja, Arcelia Guerson-Gil, Orlando Quintero, Isaac Laniado, Dimpi Desai, Priyanka Mathias, Jason Leider, Preeti Kishore, Leonidas Palaiodimos & Donald P. Kotler

  4. Montefiore Medical Center, Bronx, NY, USA

    Sanjana Nagraj, Natalia Chamorro-Pareja, Arcelia Guerson-Gil, Orlando Quintero, Isaac Laniado, Priyanka Mathias, Jason Leider, Preeti Kishore, Leonidas Palaiodimos & Donald P. Kotler

  5. Stony Brook University Hospital, Stony Brook, NY, USA

    Neva Castro

  6. Baylor College of Medicine, Houston, TX, USA

    Alejandro de Leon

  7. North Central Bronx Hospital, Bronx, NY, USA

    Michail Kladas

Authors
  1. Paula Debroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanjana Nagraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Chamorro-Pareja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Neva Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alejandro de Leon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arcelia Guerson-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Orlando Quintero
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Isaac Laniado
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michail Kladas
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dimpi Desai
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Priyanka Mathias
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jason Leider
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Preeti Kishore
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Leonidas Palaiodimos
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Donald P. Kotler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Drs. Debroy, Leider, and Kotler contributed to the conception of this project. Drs. Nagraj, Chamorro-Pareja, Palaiodimos, and de Leon designed the study. Drs. Debroy, Nagraj, Chamorro-Pareja, Palaiodimos, Castro, Quintero, Mathias, Laniado, Guerson-Gil, Kladas, and Desai performed the data collection. Drs. Palaiodimos, Leider, and Kotler performed the statistical analysis. All authors evaluated the results of the analysis and substantially contributed to the interpretation of results and drafting of the article. Drs. Debroy, Kotler, Nagraj, Chamorro Pareja, and Palaiodimos critically revised the manuscript. All authors approved the final version.

Corresponding author

Correspondence to Sanjana Nagraj.

Ethics declarations

Ethics Approval

This project was approved by the Albert Einstein College of Medicine Institutional Review Board. A consent waiver was provided.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Medicine

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 14 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Debroy, P., Nagraj, S., Chamorro-Pareja, N. et al. Assessment of the Association of HIV Infection with Hepatic Steatosis or Fibrosis: a Cross-sectional Case–Control Study. SN Compr. Clin. Med. 3, 2504–2510 (2021). https://doi.org/10.1007/s42399-021-01054-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42399-021-01054-4

Keywords

Search

Navigation