Download PDF
Semin Liver Dis 2012; 32(02): 103-113
DOI: 10.1055/s-0032-1316473
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

The Burden of Liver Disease in Human Immunodeficiency Virus-Infected Patients

Massimo Puoti
1   Department of Infectious Diseases, AO Ospedale Niguarda Ca' Granda, Milano, Italy
,
Maria Cristina Moioli
1   Department of Infectious Diseases, AO Ospedale Niguarda Ca' Granda, Milano, Italy
,
Giovanna Travi
1   Department of Infectious Diseases, AO Ospedale Niguarda Ca' Granda, Milano, Italy
,
Roberto Rossotti
1   Department of Infectious Diseases, AO Ospedale Niguarda Ca' Granda, Milano, Italy
› Author Affiliations
Further Information

Publication History

Publication Date:
03 July 2012 (online)

    Permissions and Reprints

Abstract

Introduction of effective combined antiretroviral therapy has made human immunodeficiency virus (HIV) infection a chronic illness. Substantial reductions in the number of acquired immunodeficiency syndrome- (AIDS-) related deaths have been accompanied by an increase in liver-related morbidity and mortality. Liver diseases rank in the first three most-common causes of death in HIV-infected persons. Mortality is mainly due to cirrhosis and hepatocellular carcinoma induced by hepatitis C virus and hepatitis B virus coinfection. However, antiretroviral drugs toxicity also plays a role. Nonalcoholic fatty liver disease is a common cause of liver injury as well. Nevertheless, alcohol consumption probably plays a pivotal role. Noncirrhotic portal hypertension, an uncommon condition observed in less than 1% of patients, is increasingly described. Finally, acute hepatitis A virus (HAV) and acute and even chronic hepatitis E virus infection have also been reported as causes of liver damage in HIV. Anti-HAV vaccination is thus recommended in persons at risk living with HIV.

Keywords

human immunodeficiency virus - hepatitis C virus - nonalcoholic fatty liver disease - alcoholic hepatitis - liver-related mortality - cirrhosis - noncirrhotic portal hypertension
 

  • References

  • 1 Joint UN Programme on HIV/AIDS 2010 Global report. Available at: http://www.unaids.org/globalreport/documents/20101123_GlobalReport_full_en.pdf Accessed April 1, 2012
    PubMedGoogle Scholar
  • 2 Mocroft A, Brettle R, Kirk O , et al; EuroSIDA study group. Changes in the cause of death among HIV positive subjects across Europe: results from the EuroSIDA study. AIDS 2002; 16 (12) 1663-1671
    CrossrefPubMedGoogle Scholar
  • 3 Weber R, Sabin CA, Friis-Møller N , et al. Liver-related deaths in persons infected with the human immunodeficiency virus: the D:A:D study. Arch Intern Med 2006; 166 (15) 1632-1641
    CrossrefPubMedGoogle Scholar
  • 4 Salmon-Ceron D, Lewden C, Morlat P , et al; Mortality 2000 study group. Liver disease as a major cause of death among HIV infected patients: role of hepatitis C and B viruses and alcohol. J Hepatol 2005; 42 (6) 799-805
    CrossrefPubMedGoogle Scholar
  • 5 Soriano V, Puoti M, Garcia-Gascó P , et al. Antiretroviral drugs and liver injury. AIDS 2008; 22 (1) 1-13
    CrossrefPubMedGoogle Scholar
  • 6 Ingiliz P, Valantin MA, Duvivier C , et al. Liver damage underlying unexplained transaminase elevation in human immunodeficiency virus-1 mono-infected patients on antiretroviral therapy. Hepatology 2009; 49 (2) 436-442
    CrossrefPubMedGoogle Scholar
  • 7 Vispo E, Morello J, Rodriguez-Novoa S, Soriano V. Noncirrhotic portal hypertension in HIV infection. Curr Opin Infect Dis 2011; 24 (1) 12-18
    CrossrefPubMedGoogle Scholar
  • 8 Fonquernie L, Meynard JL, Charrois A, Delamare C, Meyohas MC, Frottier J. Occurrence of acute hepatitis A in patients infected with human immunodeficiency virus. Clin Infect Dis 2001; 32 (2) 297-299
    CrossrefPubMedGoogle Scholar
  • 9 Jardi R, Crespo M, Homs M , et al. HIV, HEV and cirrhosis: evidence of a possible link from eastern Spain. HIV Med 2012; ; Jan 18 [Epub ahead of print]
    PubMedGoogle Scholar
  • 10 Smith C, Sabin CA, Lundgren JD , et al; Data Collection on Adverse Events of Anti-HIV drugs (D:A:D) Study Group. Factors associated with specific causes of death amongst HIV-positive individuals in the D:A:D Study. AIDS 2010; 24: 1537-1548
    PubMedGoogle Scholar
  • 11 Lifson AR, Belloso WH, Carey C , et al; INSIGHT Cause of Death Writing Group. Determination of the underlying cause of death in three multicenter international HIV clinical trials. HIV Clin Trials 2008; 9 (3) 177-185
    CrossrefPubMedGoogle Scholar
  • 12 Ruppik M, Ledergerber B, Rickenbach M , et al. Changing patterns of causes of death: SHCS, 2005 to 2009. Paper presented at: 18th Conference on Retroviruses and Opportunistic Infections; February 27–March 2, 2011; Boston, MA
    PubMedGoogle Scholar
  • 13 Salmon-Ceron D, Rosenthal E, Lewden C , et al; ANRS EN19 Mortalité Study Group and Mortavic. Emerging role of hepatocellular carcinoma among liver-related causes of deaths in HIV-infected patients: The French National Mortalité 2005 Study. J Hepatol 2009; 50 (4) 736-745
    CrossrefPubMedGoogle Scholar
  • 14 Leone S, Gregis G, Quinzan G , et al. Causes of death and risk factors among HIV-infected persons in the HAART era: analysis of a large urban cohort. Infection 2011; 39 (1) 13-20
    CrossrefPubMedGoogle Scholar
  • 15 Mocroft A, Soriano V, Rockstroh J , et al; EuroSIDA Study Group. Is there evidence for an increase in the death rate from liver-related disease in patients with HIV?. AIDS 2005; 19 (18) 2117-2125
    CrossrefPubMedGoogle Scholar
  • 16 Núñez-Fernández C, Martín-Carbonero L, Valencia ME , et al. Liver complications have reached a plateau as cause of hospital admission and death in HIV patients in Madrid. AIDS Res Hum Retroviruses 2009; 25 (4) 383-385
    CrossrefPubMedGoogle Scholar
  • 17 Tuma P, Medrano J, Resino S , et al. Incidence of liver cirrhosis in HIV-infected patients with chronic hepatitis B or C in the era of highly active antiretroviral therapy. Antivir Ther 2010; 15 (6) 881-886
    CrossrefPubMedGoogle Scholar
  • 18 Phillips AA, Justman JE. Screening HIV-infected patients for non-AIDS-defining malignancies. Curr HIV/AIDS Rep 2009; 6 (2) 83-92
    CrossrefPubMedGoogle Scholar
  • 19 Ocama P, Nambooze S, Opio CK, Shiels MS, Wabinga HR, Kirk GD. Trends in the incidence of primary liver cancer in Central Uganda, 1960-1980 and 1991-2005. Br J Cancer 2009; 100 (5) 799-802
    CrossrefPubMedGoogle Scholar
  • 20 Williams JH, Grubb JA, Davis JW , et al. HIV and hepatocellular and esophageal carcinomas related to consumption of mycotoxin-prone foods in sub-Saharan Africa. Am J Clin Nutr 2010; 92 (1) 154-160
    CrossrefPubMedGoogle Scholar
  • 21 Petoumenos K, Hui E, Kumarasamy N , et al; TREAT Asia HIV Observational Database. Cancers in the TREAT Asia HIV Observational Database (TAHOD): a retrospective analysis of risk factors. J Int AIDS Soc 2010; 13: 51
    PubMedGoogle Scholar
  • 22 Bierhoff E, Fischer HP, Willsch E , et al. Liver histopathology in patients with concurrent chronic hepatitis C and HIV infection. Virchows Arch 1997; 430 (4) 271-277
    CrossrefPubMedGoogle Scholar
  • 23 Soto B, Sánchez-Quijano A, Rodrigo L , et al. Human immunodeficiency virus infection modifies the natural history of chronic parenterally-acquired hepatitis C with an unusually rapid progression to cirrhosis. J Hepatol 1997; 26 (1) 1-5
    PubMedGoogle Scholar
  • 24 Pol S, Fontaine H, Carnot F , et al. Predictive factors for development of cirrhosis in parenterally acquired chronic hepatitis C: a comparison between immunocompetent and immunocompromised patients. J Hepatol 1998; 29 (1) 12-19
    CrossrefPubMedGoogle Scholar
  • 25 Pol S, Lamorthe B, Thi NT , et al. Retrospective analysis of the impact of HIV infection and alcohol use on chronic hepatitis C in a large cohort of drug users. J Hepatol 1998; 28 (6) 945-950
    CrossrefPubMedGoogle Scholar
  • 26 Benhamou Y, Bochet M, Di Martino V , et al; The Multivirc Group. Liver fibrosis progression in human immunodeficiency virus and hepatitis C virus coinfected patients. Hepatology 1999; 30 (4) 1054-1058
    CrossrefPubMedGoogle Scholar
  • 27 Puoti M, Bonacini M, Spinetti A , et al; HIV-HCV Coinfection Study Group. Liver fibrosis progression is related to CD4 cell depletion in patients coinfected with hepatitis C virus and human immunodeficiency virus. J Infect Dis 2001; 183 (1) 134-137
    CrossrefPubMedGoogle Scholar
  • 28 Serfaty L, Costagliola D, Wendum D , et al. Impact of early-untreated HIV infection on chronic hepatitis C in intravenous drug users: a case-control study. AIDS 2001; 15 (15) 2011-2016
    CrossrefPubMedGoogle Scholar
  • 29 Di Martino V, Rufat P, Boyer N , et al. The influence of human immunodeficiency virus coinfection on chronic hepatitis C in injection drug users: a long-term retrospective cohort study. Hepatology 2001; 34 (6) 1193-1199
    CrossrefPubMedGoogle Scholar
  • 30 Mohsen AH, Easterbrook PJ, Taylor C , et al. Impact of human immunodeficiency virus (HIV) infection on the progression of liver fibrosis in hepatitis C virus infected patients. Gut 2003; 52 (7) 1035-1040
    CrossrefPubMedGoogle Scholar
  • 31 Tural C, Fuster D, Tor J , et al. Time on antiretroviral therapy is a protective factor for liver fibrosis in HIV and hepatitis C virus (HCV) co-infected patients. J Viral Hepat 2003; 10 (2) 118-125
    CrossrefPubMedGoogle Scholar
  • 32 Martinez-Sierra C, Arizcorreta A, Díaz F , et al. Progression of chronic hepatitis C to liver fibrosis and cirrhosis in patients coinfected with hepatitis C virus and human immunodeficiency virus. Clin Infect Dis 2003; 36 (4) 491-498
    CrossrefPubMedGoogle Scholar
  • 33 Sterling RK, Contos MJ, Sanyal AJ , et al. The clinical spectrum of hepatitis C virus in HIV coinfection. J Acquir Immune Defic Syndr 2003; 32 (1) 30-37
    CrossrefPubMedGoogle Scholar
  • 34 Martín-Carbonero L, Benhamou Y, Puoti M , et al. Incidence and predictors of severe liver fibrosis in human immunodeficiency virus-infected patients with chronic hepatitis C: a European collaborative study. Clin Infect Dis 2004; 38 (1) 128-133
    CrossrefPubMedGoogle Scholar
  • 35 Mariné-Barjoan E, Saint-Paul MC, Pradier C , et al; Registre des Ponctions-Biopsies Hépatiques. Impact of antiretroviral treatment on progression of hepatic fibrosis in HIV/hepatitis C virus co-infected patients. AIDS 2004; 18 (16) 2163-2170
    CrossrefPubMedGoogle Scholar
  • 36 Macías J, Castellano V, Merchante N , et al. Effect of antiretroviral drugs on liver fibrosis in HIV-infected patients with chronic hepatitis C: harmful impact of nevirapine. AIDS 2004; 18 (5) 767-774
    CrossrefPubMedGoogle Scholar
  • 37 Fuster D, Planas R, Muga R , et al. Advanced liver fibrosis in HIV/HCV-coinfected patients on antiretroviral therapy. AIDS Res Hum Retroviruses 2004; 20 (12) 1293-1297
    CrossrefPubMedGoogle Scholar
  • 38 Arribas JR, González-García JJ, Lorenzo A , et al. Single (B or C), dual (BC or BD) and triple (BCD) viral hepatitis in HIV-infected patients in Madrid, Spain. AIDS 2005; 19 (13) 1361-1365
    CrossrefPubMedGoogle Scholar
  • 39 González-García JJ, Mahillo B, Hernández S , et al. [Prevalences of hepatitis virus coinfection and indications for chronic hepatitis C virus treatment and liver transplantation in Spanish HIV-infected patients. The GESIDA 29/02 and FIPSE 12185/01 Multicenter Study]. Enferm Infecc Microbiol Clin 2005; 23 (6) 340-348
    CrossrefPubMedGoogle Scholar
  • 40 Marks KM, Petrovic LM, Talal AH, Murray MP, Gulick RM, Glesby MJ. Histological findings and clinical characteristics associated with hepatic steatosis in patients coinfected with HIV and hepatitis C virus. J Infect Dis 2005; 192 (11) 1943-1949
    CrossrefPubMedGoogle Scholar
  • 41 Bräu N, Salvatore M, Ríos-Bedoya CF , et al. Slower fibrosis progression in HIV/HCV-coinfected patients with successful HIV suppression using antiretroviral therapy. J Hepatol 2006; 44 (1) 47-55
    CrossrefPubMedGoogle Scholar
  • 42 Rockstroh JK, Mocroft A, Soriano V , et al; EuroSIDA Study Group. Influence of hepatitis C virus infection on HIV-1 disease progression and response to highly active antiretroviral therapy. J Infect Dis 2005; 192 (6) 992-1002
    CrossrefPubMedGoogle Scholar
  • 43 Soriano V, Grint D, d'Arminio Monforte A , et al. Hepatitis delta in HIV-infected individuals in Europe. AIDS 2011; 25 (16) 1987-1992
    CrossrefPubMedGoogle Scholar
  • 44 Aranzabal L, Casado JL, Moya J , et al. Influence of liver fibrosis on highly active antiretroviral therapy-associated hepatotoxicity in patients with HIV and hepatitis C virus coinfection. Clin Infect Dis 2005; 40 (4) 588-593
    CrossrefPubMedGoogle Scholar
  • 45 McGovern BH, Ditelberg JS, Taylor LE , et al. Hepatic steatosis is associated with fibrosis, nucleoside analogue use, and hepatitis C virus genotype 3 infection in HIV-seropositive patients. Clin Infect Dis 2006; 43 (3) 365-372
    CrossrefPubMedGoogle Scholar
  • 46 Food and Drug Administration. Aptivus (package insert). Available at: http://www.accessdata.fda.gov/drugsatfda_docs/label/2011/021814s011lbl.pdf . Accessed March 26, 2012
    PubMedGoogle Scholar
  • 47 Portilla J. [Safety and tolerability of etravirine]. Enferm Infecc Microbiol Clin 2009; 27 (Suppl 2) 21-26
    CrossrefPubMedGoogle Scholar
  • 48 Macías J, Neukam K, Portilla J , et al; HEPRAL study team. Liver tolerance of raltegravir-containing antiretroviral therapy in HIV-infected patients with chronic hepatitis C. J Antimicrob Chemother 2011; 66 (6) 1346-1350
    CrossrefPubMedGoogle Scholar
  • 49 Genebat M, Ruiz-Mateos E, Pulido I , et al. Long-term immunovirogical effect and tolerability of a maraviroc-containing regimen in routine clinical practice. Curr HIV Res 2010; 8 (6) 482-486
    CrossrefPubMedGoogle Scholar
  • 50 Crum-Cianflone N, Dilay A, Collins G , et al. Nonalcoholic fatty liver disease among HIV-infected persons. J Acquir Immune Defic Syndr 2009; 50 (5) 464-473
    CrossrefPubMedGoogle Scholar
  • 51 Crum-Cianflone N, Collins G, Medina S , et al. Prevalence and factors associated with liver test abnormalities among human immunodeficiency virus-infected persons. Clin Gastroenterol Hepatol 2010; 8 (2) 183-191
    CrossrefPubMedGoogle Scholar
  • 52 Borghi V, Puoti M, Mussini C , et al. HIV coinfection and antiretroviral therapy enhances liver steatosis in patients with hepatitis C, but only in those infected by HCV genotype other than 3. Antivir Ther 2008; 13 (8) 1057-1065
    PubMedGoogle Scholar
  • 53 López-Diéguez M, Montes ML, Pascual-Pareja JF , et al; GESIDA 37/03-FIPSE 36465/03-NEAT IG5 Study Group. The natural history of liver cirrhosis in HIV-hepatitis C virus-coinfected patients. AIDS 2011; 25 (7) 899-904
    CrossrefPubMedGoogle Scholar
  • 54 Ingiliz P, Valantin MA, Duvivier C , et al. Liver damage underlying unexplained transaminase elevation in human immunodeficiency virus-1 mono-infected patients on antiretroviral therapy. Hepatology 2009; 49 (2) 436-442
    CrossrefPubMedGoogle Scholar
  • 55 Samet JH, Phillips SJ, Horton NJ, Traphagen ET, Freedberg KA. Detecting alcohol problems in HIV-infected patients: use of the CAGE questionnaire. AIDS Res Hum Retroviruses 2004; 20 (2) 151-155
    CrossrefPubMedGoogle Scholar
  • 56 Bertholet N, Cheng DM, Samet JH, Quinn E, Saitz R. Alcohol consumption patterns in HIV-infected adults with alcohol problems. Drug Alcohol Depend 2010; 112 (1-2) 160-163
    CrossrefPubMedGoogle Scholar
  • 57 Galvan FH, Bing EG, Fleishman JA , et al. The prevalence of alcohol consumption and heavy drinking among people with HIV in the United States: results from the HIV Cost and Services Utilization Study. J Stud Alcohol 2002; 63 (2) 179-186
    PubMedGoogle Scholar
  • 58 Szabo G, Zakhari S. Mechanisms of alcohol-mediated hepatotoxicity in human-immunodeficiency-virus-infected patients. World J Gastroenterol 2011; 17 (20) 2500-2506
    CrossrefPubMedGoogle Scholar
  • 59 Maida I, Garcia-Gasco P, Sotgiu G , et al. Antiretroviral-associated portal hypertension: a new clinical condition? Prevalence, predictors and outcome. Antivir Ther 2008; 13 (1) 103-107
    PubMedGoogle Scholar
  • 60 Vispo E, Morello J, Rodriguez-Novoa S, Soriano V. Noncirrhotic portal hypertension in HIV infection. Curr Opin Infect Dis 2011; 24 (1) 12-18
    CrossrefPubMedGoogle Scholar
  • 61 Franco E, Giambi C, Ialacci R, Coppola RC, Zanetti AR. Risk groups for hepatitis A virus infection. Vaccine 2003; 21 (19-20) 2224-2233
    CrossrefPubMedGoogle Scholar
  • 62 Urbanus AT, van Houdt R, van de Laar TJ, Coutinho RA. Viral hepatitis among men who have sex with men, epidemiology and public health consequences. Euro Surveill 2009; 14 (47) 19421
    PubMedGoogle Scholar
  • 63 Pini A, Tomasoni LR, Cristini G , et al. Hepatitis A in men having sex with men (MSMs) in northern Italy. Infez Med 2010; 18 (2) 113-114
    PubMedGoogle Scholar
  • 64 Bordia L, Rozeraa G, Scognamiglio P , et al. Monophyletic outbreak of hepatitis A involving HIV-infected men who have sex with men, Rome, Italy 2008–2009. J Clin Virol 2012; 54: 26-29
    CrossrefPubMedGoogle Scholar
  • 65 Ridolfo AL, Rusconi S, Antinori S, Balotta C, Galli M. Persisting HIV-1 replication triggered by acute hepatitis A virus infection. Antivir Ther 2000; 5 (1) 15-17
    PubMedGoogle Scholar
  • 66 Wallace MR, Hill HE, Tasker SA, Miller LK. Hepatitis A in human immunodeficiency virus-infected patients. Clin Infect Dis 1998; 27 (3) 651-653
    CrossrefPubMedGoogle Scholar
  • 67 Vento S, Garofano T, Renzini C , et al. Fulminant hepatitis associated with hepatitis A virus superinfection in patients with chronic hepatitis C. N Engl J Med 1998; 338 (5) 286-290
    CrossrefPubMedGoogle Scholar
  • 68 Bodsworth NJ, Neilsen GA, Donovan B. The effect of immunization with inactivated hepatitis A vaccine on the clinical course of HIV-1 infection: 1-year follow-up. AIDS 1997; 11 (6) 747-749
    CrossrefPubMedGoogle Scholar
  • 69 Laurence JC. Hepatitis A and B immunizations of individuals infected with human immunodeficiency virus. Am J Med 2005; 118 (Suppl 10A) 75S-83S
    CrossrefPubMedGoogle Scholar
  • 70 Kemper CA, Haubrich R, Frank I , et al; California Collaborative Treatment Group. Safety and immunogenicity of hepatitis A vaccine in human immunodeficiency virus-infected patients: a double-blind, randomized, placebo-controlled trial. J Infect Dis 2003; 187 (8) 1327-1331
    CrossrefPubMedGoogle Scholar
  • 71 Shire NJ, Welge JA, Sherman KE. Efficacy of inactivated hepatitis A vaccine in HIV-infected patients: a hierarchical bayesian meta-analysis. Vaccine 2006; 24 (3) 272-279
    CrossrefPubMedGoogle Scholar
  • 72 Crum-Cianflone NF, Wilkins K, Lee AW , et al; Infectious Disease Clinical Research Program HIV Working Group. Long-term durability of immune responses after hepatitis A vaccination among HIV-infected adults. J Infect Dis 2011; 203 (12) 1815-1823
    CrossrefPubMedGoogle Scholar
  • 73 Neilsen GA, Bodsworth NJ, Watts N. Response to hepatitis A vaccination in human immunodeficiency virus-infected and -uninfected homosexual men. J Infect Dis 1997; 176 (4) 1064-1067
    CrossrefPubMedGoogle Scholar
  • 74 Santagostino E, Gringeri A, Rocino A, Zanetti A, de Biasi R, Mannucci PM. Patterns of immunogenicity of an inactivated hepatitis A vaccine in anti-HIV positive and negative hemophilic patients. Thromb Haemost 1994; 72 (4) 508-510
    PubMedGoogle Scholar
  • 75 Wallace MR, Brandt CJ, Earhart KC , et al. Safety and immunogenicity of an inactivated hepatitis A vaccine among HIV-infected subjects. Clin Infect Dis 2004; 39 (8) 1207-1213
    CrossrefPubMedGoogle Scholar
  • 76 Saksawad R, Likitnukul S, Warachit B, Hanvivatvong O, Poovorawan Y, Puripokai P. Immunogenicity and safety of a pediatric dose virosomal hepatitis A vaccine in Thai HIV-infected children. Vaccine 2011; 29 (29-30) 4735-4738
    CrossrefPubMedGoogle Scholar
  • 77 Weinberg A, Gona P, Nachman SA , et al; Pediatric AIDS Clinical Trials Group 1008 Team. Antibody responses to hepatitis A virus vaccine in HIV-infected children with evidence of immunologic reconstitution while receiving highly active antiretroviral therapy. J Infect Dis 2006; 193 (2) 302-311
    CrossrefPubMedGoogle Scholar
  • 78 Siberry GK, Coller RJ, Henkle E , et al. Antibody response to hepatitis A immunization among human immunodeficiency virus-infected children and adolescents. Pediatr Infect Dis J 2008; 27 (5) 465-468
    PubMedGoogle Scholar
  • 79 Weinberg A, Huang S, Fenton T , et al; IMPAACT P1008 Team. Virologic and immunologic correlates with the magnitude of antibody responses to the hepatitis A vaccine in HIV-infected children on highly active antiretroviral treatment. J Acquir Immune Defic Syndr 2009; 52 (1) 17-24
    CrossrefPubMedGoogle Scholar
  • 80 Spada E, Genovese D, Tosti ME , et al. An outbreak of hepatitis A virus infection with a high case-fatality rate among injecting drug users. J Hepatol 2005; 43 (6) 958-964
    CrossrefPubMedGoogle Scholar
  • 81 Viral Hepatitis Statement WHO A62/22. Available at: http://apps.who.int/gb/ebwhal/pdf_files/A62/A62_22-en.pdf . Accessed March 26, 2012
    PubMedGoogle Scholar
  • 82 Mushahwar IK. Hepatitis E virus: molecular virology, clinical features, diagnosis, transmission, epidemiology, and prevention. J Med Virol 2008; 80 (4) 646-658
    CrossrefPubMedGoogle Scholar
  • 83 Viswanathan R. Epidemiology. Indian J Med Res 1957; 45 (Suppl.) 1-29
    PubMedGoogle Scholar
  • 84 Lewis HC, Boisson S, Ijaz S , et al. Hepatitis E in England and Wales. Emerg Infect Dis 2008; 14 (1) 165-167
    CrossrefPubMedGoogle Scholar
  • 85 Amon JJ, Drobeniuc J, Bower WA , et al. Locally acquired hepatitis E virus infection, El Paso, Texas. J Med Virol 2006; 78 (6) 741-746
    CrossrefPubMedGoogle Scholar
  • 86 Balayan MS, Andjaparidze AG, Savinskaya SS , et al. Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 1983; 20 (1) 23-31
    CrossrefPubMedGoogle Scholar
  • 87 Mushahwar IK. Hepatitis E virus: molecular virology, clinical features, diagnosis, transmission, epidemiology, and prevention. J Med Virol 2008; 80 (4) 646-658
    CrossrefPubMedGoogle Scholar
  • 88 Lu L, Li C, Hagedorn CH. Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis. Rev Med Virol 2006; 16 (1) 5-36
    CrossrefPubMedGoogle Scholar
  • 89 Chandra V, Kalia M, Hajela K, Jameel S. The ORF3 protein of hepatitis E virus delays degradation of activated growth factor receptors by interacting with CIN85 and blocking formation of the Cbl-CIN85 complex. J Virol 2010; 84 (8) 3857-3867
    CrossrefPubMedGoogle Scholar
  • 90 Teo CG. Much meat, much malady: changing perceptions of the epidemiology of hepatitis E. Clin Microbiol Infect 2010; 16 (1) 24-32
    CrossrefPubMedGoogle Scholar
  • 91 Purcell RH, Emerson SU. Hepatitis E: an emerging awareness of an old disease. J Hepatol 2008; 48 (3) 494-503
    CrossrefPubMedGoogle Scholar
  • 92 Dalton HR, Hazeldine S, Banks M, Ijaz S, Bendall R. Locally acquired hepatitis E in chronic liver disease. Lancet 2007; 369 (9569) 1260
    PubMedGoogle Scholar
  • 93 Feagins AR, Opriessnig T, Guenette DK, Halbur PG, Meng XJ. Detection and characterization of infectious Hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J Gen Virol 2007; 88 (Pt 3) 912-917
    CrossrefPubMedGoogle Scholar
  • 94 Kuniholm MH, Purcell RH, McQuillan GM, Engle RE, Wasley A, Nelson KE. Epidemiology of hepatitis E virus in the United States: results from the Third National Health and Nutrition Examination Survey, 1988-1994. J Infect Dis 2009; 200 (1) 48-56
    CrossrefPubMedGoogle Scholar
  • 95 Said B, Ijaz S, Kafatos G , et al; Hepatitis E Incident Investigation Team. Hepatitis E outbreak on cruise ship. Emerg Infect Dis 2009; 15 (11) 1738-1744
    CrossrefPubMedGoogle Scholar
  • 96 Matsubayashi K, Kang JH, Sakata H , et al. A case of transfusion-transmitted hepatitis E caused by blood from a donor infected with hepatitis E virus via zoonotic food-borne route. Transfusion 2008; 48 (7) 1368-1375
    CrossrefPubMedGoogle Scholar
  • 97 Bihl F, Castelli D, Marincola F, Dodd RY, Brander C. Transfusion-transmitted infections. J Transl Med 2007; 5: 25
    CrossrefPubMedGoogle Scholar
  • 98 Montella F, Rezza G, Di Sora F, Pezzotti P, Recchia O. Association between hepatitis E virus and HIV infection in homosexual men. Lancet 1994; 344 (8934) 1433
    CrossrefPubMedGoogle Scholar
  • 99 Mansuy JM, Abravanel F, Miedouge M , et al. Acute hepatitis E in south-west France over a 5-year period. J Clin Virol 2009; 44 (1) 74-77
    CrossrefPubMedGoogle Scholar
  • 100 Balayan MS, Fedorova OE, Mikhailov MI , et al. Antibody to hepatitis E virus in HIV-infected individuals and AIDS patients. J Viral Hepat 1997; 4 (4) 279-283
    CrossrefPubMedGoogle Scholar
  • 101 Crum-Cianflone NF, Curry J, Drobeniuc J , et al; Infectious Disease Clinical Research Program HIV Working Group. Hepatitis E virus infection in HIV-infected persons. Emerg Infect Dis 2012; 18 (3) 502-506
    CrossrefPubMedGoogle Scholar
  • 102 Fainboim H, González J, Fassio E , et al. Prevalence of hepatitis viruses in an anti-human immunodeficiency virus-positive population from Argentina. A multicentre study. J Viral Hepat 1999; 6 (1) 53-57
    CrossrefPubMedGoogle Scholar
  • 103 Jardi R, Crespo M, Homs M , et al. HIV, HEV and cirrhosis: evidence of a possible link from eastern Spain. HIV Med 2012; ; In press
    PubMedGoogle Scholar
  • 104 Kaba M, Richet H, Ravaux I , et al. Hepatitis E virus infection in patients infected with the human immunodeficiency virus. J Med Virol 2011; 83 (10) 1704-1716
    CrossrefPubMedGoogle Scholar
  • 105 Keane F, Gompels M, Bendall R , et al. Hepatitis E virus coinfection in patients with HIV infection. HIV Med 2012; 13 (1) 83-88
    PubMedGoogle Scholar
  • 106 Kenfak-Foguena A, Schöni-Affolter F, Bürgisser P , et al; Data Center of the Swiss HIV Cohort Study, Lausanne, Switzerland. Hepatitis E virus seroprevalence and chronic infections in patients with HIV, Switzerland. Emerg Infect Dis 2011; 17 (6) 1074-1078
    CrossrefPubMedGoogle Scholar
  • 107 Madejón A, Vispo E, Bottecchia M, Sánchez-Carrillo M, García-Samaniego J, Soriano V. Lack of hepatitis E virus infection in HIV patients with advanced immunodeficiency or idiopathic liver enzyme elevations. J Viral Hepat 2009; 16 (12) 895-896
    CrossrefPubMedGoogle Scholar
  • 108 Ng KP, He J, Saw TL, Lyles CM. A seroprevalence study of viral hepatitis E infection in human immunodeficiency virus type 1 infected subjects in Malaysia. Med J Malaysia 2000; 55 (1) 58-64
    PubMedGoogle Scholar
  • 109 Maylin S, Stephan R, Molina JM , et al. Prevalence of antibodies and RNA genome of hepatitis E virus in a cohort of French immunocompromised. J Clin Virol 2012; 53 (4) 346-349
    CrossrefPubMedGoogle Scholar
  • 110 Pischke S, Heim A, Bremer B , et al. Hepatitis E: an emerging infectious disease in Germany?. Z Gastroenterol 2011; 49 (9) 1255-1257
    Article in Thieme ConnectPubMedGoogle Scholar
  • 111 Gérolami R, Moal V, Colson P. Chronic hepatitis E with cirrhosis in a kidney-transplant recipient. N Engl J Med 2008; 358 (8) 859-860
    CrossrefPubMedGoogle Scholar
  • 112 Haagsma EB, van den Berg AP, Porte RJ , et al. Chronic hepatitis E virus infection in liver transplant recipients. Liver Transpl 2008; 14 (4) 547-553
    CrossrefPubMedGoogle Scholar
  • 113 Kamar N, Selves J, Mansuy JM , et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med 2008; 358 (8) 811-817
    CrossrefPubMedGoogle Scholar
  • 114 Ollier L, Tieulie N, Sanderson F , et al. Chronic hepatitis after hepatitis E virus infection in a patient with non-Hodgkin lymphoma taking rituximab. Ann Intern Med 2009; 150 (6) 430-431
    PubMedGoogle Scholar
  • 115 le Coutre P, Meisel H, Hofmann J , et al. Reactivation of hepatitis E infection in a patient with acute lymphoblastic leukaemia after allogeneic stem cell transplantation. Gut 2009; 58 (5) 699-702
    CrossrefPubMedGoogle Scholar
  • 116 Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. Persistent carriage of hepatitis E virus in patients with HIV infection. N Engl J Med 2009; 361 (10) 1025-1027
    CrossrefPubMedGoogle Scholar
  • 117 Colson P, Gérolami R, Moreau J, Borentain P, Brouqui P. Concurrent autochthonous acute hepatitis E and hepatitis B reverse seroconversion in an HIV-1-infected patient: one virus may hide another. Int J Infect Dis 2010; 14 (4) e357
    PubMedGoogle Scholar
  • 118 Takahashi M, Kusakai S, Mizuo H , et al. Simultaneous detection of immunoglobulin A (IgA) and IgM antibodies against hepatitis E virus (HEV) is highly specific for diagnosis of acute HEV infection. J Clin Microbiol 2005; 43 (1) 49-56
    CrossrefPubMedGoogle Scholar
  • 119 Kamar N, Garrouste C, Haagsma EB , et al. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants. Gastroenterology 2011; 140 (5) 1481-1489
    CrossrefPubMedGoogle Scholar
  • 120 Dalton HR, Keane FE, Bendall R, Mathew J, Ijaz S. Treatment of chronic hepatitis E in a patient with HIV infection. Ann Intern Med 2011; 155 (7) 479-480
    CrossrefPubMedGoogle Scholar
  • 121 Kamar N, Abravanel F, Garrouste C , et al. Three-month pegylated interferon-alpha-2a therapy for chronic hepatitis E virus infection in a haemodialysis patient. Nephrol Dial Transplant 2010; 25 (8) 2792-2795
    CrossrefPubMedGoogle Scholar
  • 122 Jagjit Singh GK, Ijaz S, Rockwood N , et al. Chronic hepatitis E as a cause for cryptogenic cirrhosis in HIV. J Infect 2011; ; Dec 06 [Epub ahead of print]
    PubMedGoogle Scholar
  • 123 Kamar N, Rostaing L, Abravanel F , et al. Ribavirin therapy inhibits viral replication on patients with chronic hepatitis e virus infection. Gastroenterology 2010; 139 (5) 1612-1618
    CrossrefPubMedGoogle Scholar