Lipid metabolism alterations produced by hepatitis C virus in patients with chronic infection

e202005049

Authors

  • Ainara Muñoz-Cabrejas Adipocyte and Fat Biology Laboratory (AdipoFat). Unidad de Investigación Traslacional. Hospital Universitario Miguel Servet. Instituto Aragonés de Ciencias de la Salud (IACS). Instituto de Investigación Sanitaria de Aragón (IIS Aragón). Zaragoza. España.
  • Silvia Espina Cadena Adipocyte and Fat Biology Laboratory (AdipoFat). Unidad de Investigación Traslacional. Hospital Universitario Miguel Servet. Instituto Aragonés de Ciencias de la Salud (IACS). Instituto de Investigación Sanitaria de Aragón (IIS Aragón). Zaragoza. España.
  • José Miguel Arbonés-Mainar Adipocyte and Fat Biology Laboratory (AdipoFat). Unidad de Investigación Traslacional. Hospital Universitario Miguel Servet. Instituto Aragonés de Ciencias de la Salud (IACS). Instituto de Investigación Sanitaria de Aragón (IIS Aragón). Zaragoza. España. / CIBER Fisiopatología Obesidad y Nutrición (CIBERObn). Instituto Salud Carlos III. Madrid. España.
  • Belén Moreno-Franco Departamento de Microbiología, Medicina Preventiva y Salud Pública. Universidad de Zaragoza. Zaragoza. España. / Grupo de Prevención Cardiovascular. Hospital Universitario Miguel Servet. Instituto de Investigación Sanitaria de Aragón (IIS Aragón). Zaragoza. España.

Keywords:

Hepatitis C chronic, Cardiovascular diseases, Atherosclerosis, Lipid metabolism disorders, Cholesterol

Abstract

Background: Chronic infection with the hepatitis C virus (HCV) is known to generate an apparently favorable lipid profile. Paradoxically, these patients present an increase in concomitant cardiovascular events. The objectives of the present review were to analyze and synthesize studies that inquired into the changes produced by hepatitis C virus (HCV) in the lipid metabolism of patients with chronic infection, and about whether these modifications can be associated with subsequent episodes of cardiovascular diseases.
Methods: A bibliographic search was carried out in the Medline and Scopus databases of the articles published from January 2008 to February 2019. A total of 901 publications were identified, of which 10 studies that fulfilled the inclusion and exclusion criteria were reviewed.
Results: It was found that the levels of total cholesterol and its lipid fractions were decreased in patients with chronic HCV infection. There was no clear association with triglyceride levels. In addition, there seemed to be an association between chronic HCV infection and an increased risk of developing atherosclerosis and cardiovascular diseases.
Conclusions: Chronic HCV infection has a lipid-lowering effect and increases cardiovascular risk. Prospective studies are needed to analyze the effect of new therapies with direct-acting antivirals on lipid metabolism and cardiovascular risk.

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References

Bruggmann P, Berg T, Øvrehus ALH et al. Historical epidemiology of hepatitis C virus (HCV) in selected countries. J Viral Hepat. 2014;21:5–33.

World Health Organization. Global hepatitis report, 2017 [Internet]. WHO. 2017 [consultado el 01/11/2018]. p. 62. Disponible en: http://www.who.int/hepatitis.

Gobierno de España. 117.452 pacientes han recibido en España tratamiento de última generación para la Hepatitis C [Internet]. La Moncloa.gob.es. 2018 [consultado el 01/20/2019]. p. 4. Disponible en: http://www.lamoncloa.gob.es/serviciosdeprensa/notasprensa/sanidad/Paginas/2018/301018-hepatitis.aspx.

WHO. Guidelines for the screening, care and treatment of persons with hepatitis C infection [Internet]. Ginebra: World health Organization. 2016 [consultado el 02/02/2018]. p. 138. Disponible en: http://www.who.int/hepatitis/publications/hepatitis-c-guidelines-2016/en/.

Martínez-Rebollar M, Larrousse M, Calvo M et al. Estado actual de la hepatitis aguda C. Enferm Infecc Microbiol Clin. 2011;29(3):210–5.

WHO. Hepatitis C: Key facts [Internet]. Ginebra: World health Organization. 2017 [consultado el 05/05/2018]. p.9. Disponible en: http://www.who.int/en/news-room/fact-sheets/detail/hepatitis-c.

Centers for Disease Control and Prevention. Hepatitis C FAQs for Health Professionals [Internet]. CDC. 2018 [consultado el 04/25/2018]. p. 17. Disponible en: https://www.cdc.gov/hepatitis/hcv/hcvfaq.htm#section2.

Serfaty L. Metabolic Manifestations of Hepatitis C Virus: Diabetes Mellitus, Dyslipidemia. Clin Liver Dis. 2017;21(3):475–86.

Honda A, Matsuzaki Y. Cholesterol and chronic hepatitis C virus infection. Hepatol Res. 2011;41(8):697–710.

Marzouk D, Sass J, Bakr I et al. Metabolic and cardiovascular risk profiles and hepatitis C virus infection in rural Egypt. Gut. 2007;56(8):1105–10.

Hsu C-S, Liu C-J, Liu C-H et al. Metabolic profiles in patients with chronic hepatitis C: a case-control study. Hepatol Int. 2008;2(2):250–7.

Butt AA, Xiaoqiang W, Budoff M et al. Hepatitis C Virus Infection and the Risk of Coronary Disease. Clin Infect Dis. 2009;49(2):225–32.

Corey KE, Kane E, Munroe C et al. Hepatitis C virus infection and its clearance alter circulating lipids: Implications for long-term follow-up. Hepatology. 2009;50(4):1030–7.

Siagris D, Christofidou M, Theocharis GJ et al. Serum lipid pattern in chronic hepatitis C: histological and virological correlations. J Viral Hepat. 2006;13(1):56–61.

Miyazaki T, Honda A, Ikegami T et al. Hepatitis C virus infection causes hypolipidemia regardless of hepatic damage or nutritional state: An epidemiological survey of a large Japanese cohort. Hepatol Res. 2011;41(6):530–41.

Chang M-L. Metabolic alterations and hepatitis C: From bench to bedside. World J Gastroenterol. 2016;22(4):1461–77.

Aizawa Y, Seki N, Nagano T et al. Chronic hepatitis C virus infection and lipoprotein metabolism. World J Gastroenterol. 2015;21(36):10299–313.

Gershon AS, Margulies M, Gorczynski RM et al. Serum cytokine values and fatigue in chronic hepatitis C infection. J Viral Hepat. 2000;7(6):397–402.

Hansson GK. Inflammation, Atherosclerosis, and Coronary Artery Disease. N Engl J Med. 2005;352(16):1685–95.

Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6(7):508–19.

Libby P. Inflammation in atherosclerosis. Nature. 2002;420(6917):868–74.

Mehta SH, Brancati FL, Sulkowski MS et al. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med. 2000;133(8):592–9.

Mehta S, Brancati FL, Strathdee SA et al. Hepatitis C virus infection and incident type 2 diabetes. Hepatology. 2003;38(1):50–6.

Butt AA, Fultz SL, Kwoh CK et al. Risk of diabetes in HIV infected veterans pre- and post-HAART and the role of HCV coinfection. Hepatology. 2004;40(1):115–9.

Shaheen M, Echeverry D, Oblad MG et al. Hepatitis C, metabolic syndrome, and inflammatory markers: results from the Third National Health and Nutrition Examination Survey [NHANES III]. Diabetes Res Clin Pract. 2007;75(3):320–6.

Koike K. Hepatitis C as a metabolic disease: Implication for the pathogenesis of NASH. Hepatol Res. 2005;33(2):145–50.

Forde KA, Haynes K, Troxel AB et al. Risk of myocardial infarction associated with chronic hepatitis C virus infection: a population-based cohort study. J Viral Hepat. 2012;19(4):271–7.

Higgins J, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [Internet]. The Cochrane Collaboration; 2011. Disponible en: www.cochrane-handbook.org.

Moher D, Liberati A, Tetzlaff J et al. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med [Internet]. 2009 [consultado el 03/07/2018];6(7). Disponible en: http://www.ncbi.nlm.nih.gov/pubmed/19621072.

Scottish Intercollegiate Guidelines Network. Sign Grading System 1999 – 2012 [Internet]. Edimburgo: SIGN. 2012 [consultado el 06/20/2018]. p. 2. Disponible en: http://www.sign.ac.uk/sign-50.html.

Marzo-Castillejo M, Viana-Zulaica C. Calidad de la evidencia y grado de recomendación. Guias Clílnicas. 2007;7(1:6):1–14.

Petta S, Maida M, Macaluso FS et al. Hepatitis C Virus Infection Is Associated with Increased Cardiovascular Mortality: A Meta-Analysis of Observational Studies. Gastroenterology. 2016;150(1):145–55.

Olubamwo OO, Onyeka IN, Miettola J, et al. Hepatitis C as a risk factor for carotid atherosclerosis - a systematic review. Clin Physiol Funct Imaging. 2015;36(4):249–60.

Olubamwo OO, Aregbesola AO, Miettola J et al. Hepatitis C and risk of coronary atherosclerosis – A systematic review. Public Health. 2016;138:12–25.

Pateria P, Jeffrey GP, Macquillan G et al. The association between chronic hepatitis C infection and cardiovascular risk. Intern Med J. 2016;46(1):63–70.

Butt AA, Yan P, Simon TG et al. Changes in circulating lipids level over time after acquiring HCV infection: Results from ERCHIVES. BMC Infect Dis. 2015;15(1):1–9.

Butt AA, Yan P, Chew KW et al. Risk of Acute Myocardial Infarction among Hepatitis C Virus (HCV)-Positive and HCV-Negative Men at Various Lipid Levels: Results from ERCHIVES. Clin Infect Dis. 2017;65(4):557–65.

Ramcharran D, Wahed AS, Conjeevaram HS et al. Serum lipids and their associations with viral levels and liver disease severity in a treatment-naïve chronic hepatitis C type 1-infected cohort. J Viral Hepat. 2011;18(4):144–52.

Miyajima I, Kawaguchi T, Fukami A et al. Chronic HCV infection was associated with severe insulin resistance and mild atherosclerosis: A population-based study in an HCV hyperendemic area. J Gastroenterol. 2013;48(1):93–100.

Kakinami L, Block RC, Adams MJ et al. Risk of cardiovascular disease in HIV, Hepatitis C, or HIV/Hepatitis C patients compared to the general population. Int J Clin Pr. 2013;67(1):6–13.

Roed T, Kristoffersen US, Knudsen A et al. Increased prevalence of coronary artery disease risk markers in patients with chronic hepatitis C--a cross-sectional study. Vasc Health Risk Manag. 2014;10:55–62.

Cicognani C, Malavolti M, Morselli-Labate AM et al. Serum lipid and lipoprotein patterns in patients with liver cirrhosis and chronic active hepatitis. Arch Intern Med. 1997;157(7):792–6.

Wang C, Kao J. Hepatitis C virus infection, lipids, and coronary heart disease: a Pandora’s box. Hepatology. 2010;51:343.

Maggi G, Bottelli R, Gola D et al. Serum cholesterol and chronic hepatitis C. Ital J Gastroenterol. 28(8):436–40.

Serfaty L, Andreani T, Giral P et al. Hepatitis C virus induced hypobetalipoproteinemia : a possible mechanism for steatosis in chronic hepatitis C. J Hepatol. 2001;34:428–34.

Moriya K, Shintani Y, Fujie H et al. Serum lipid profile of patients with genotype 1b hepatitis C viral infection in Japan. Hepatol Res. 2003;25(4):371—6.

Babiker A, Jeudy J, Kligerman S et al. Risk of Cardiovascular Disease Due to Chronic Hepatitis C Infection: A Review. J Clin Transl Hepatol. 2017;5(4):1–20.

Shah P. Link between infection and atherosclerosis: who are the culprits: viruses, bacteria, both, or neither? Circulation. 2001;103:5–6.

Zampino R, Marrone A, Restivo L et al. Chronic HCV infection and inflammation: Clinical impact on hepatic and extra-hepatic manifestations. World J Hepatol. 2013;5(10):528–40.

Leandro G, Mangia A, Hui J et al. Relationship Between Steatosis, Inflammation, and Fibrosis in Chronic Hepatitis C: A Meta-Analysis of Individual Patient Data. Gastroenterology. 2006;130(6):1636–42.

Alyan O, Kacmaz F, Ozdemir O et al. Hepatitis C infection is associated with increased coronary artery atherosclerosis defined by modified Reardon severity score system. Circ J Off J Japanese Circ Soc. 2008;72(12):1960–5.

Tsui JI, Whooley MA, Monto A et al. Association of Hepatitis C Virus Seropositivity With Inflammatory Markers and Heart Failure in Persons With Coronary Heart Disease: Data From the Heart and Soul Study. J Card Fail. 2009;15(5):451–6.

Riordan SM, Skinner NA, Kurtovic J et al. Toll-like receptor expression in chronic hepatitis C: Correlation with pro-inflammatory cytokine levels and liver injury. Inflamm Res. 2006;55(7):279–85.

Oliveira CPMS, Kappel CR, Siqueira ER et al. Effects of Hepatitis C virus on cardiovascular risk in infected patients: A comparative study. Int J Cardiol. 2013;164(2):221–6.

Negro F. Facts and fictions of HCV and comorbidities: Steatosis, diabetes mellitus, and cardiovascular diseases. J Hepatol. 2014;61(1):69–78.

Adinolfi LE, Restivo L, Zampino R et al. Chronic HCV infection is a risk of atherosclerosis. Role of HCV and HCV-related steatosis. Atherosclerosis. 2012;221(2):496–502.

Petta S, Torres D, Fazio G et al. Carotid atherosclerosis and chronic hepatitis C: A prospective study of risk associations. Hepatology. 2012;55(5):1317–23.

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Published

2020-05-18

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1.
Muñoz-Cabrejas A, Espina Cadena S, Arbonés-Mainar JM, Moreno-Franco B. Lipid metabolism alterations produced by hepatitis C virus in patients with chronic infection: e202005049. Rev Esp Salud Pública [Internet]. 2020 May 18 [cited 2024 Nov. 16];94:15 páginas. Available from: https://ojs.sanidad.gob.es/index.php/resp/article/view/891

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Copyright (c) 2020 Ainara Muñoz-Cabrejas, Silvia Espina Cadena, José Miguel Arbonés-Mainar, Belén Moreno-Franco

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