Download PDF
Semin Liver Dis 2012; 32(02): 147-157
DOI: 10.1055/s-0032-1316476
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Challenges and Priorities in the Management of HIV/HBV and HIV/HCV Coinfection in Resource-Limited Settings

Philippa Easterbrook
1   Department of HIV/AIDS, World Health Organisation, Geneva, Switzerland
,
Anita Sands
2   Department of Essential Medicines and Health Products
,
Hande Harmanci
3   Global Hepatitis Programme, World Health Organisation, Geneva, Switzerland
› Author Affiliations
Further Information

Publication History

Publication Date:
03 July 2012 (online)

    Permissions and Reprints

Abstract

Liver disease due to chronic hepatitis B virus (HBV) and hepatitis C virus (HCV) infection is now emerging as an increasing cause of morbidity and mortality in human immunodeficiency virus- (HIV-) infected persons in resource-limited settings (RLS). Existing management guidelines have generally focused on care in tertiary level facilities in developed countries. Less than half of low-income countries have guidance, and in those that do, there are important omissions or disparities in recommendations. There are multiple challenges to delivery of effective hepatitis care in RLS, but the most important remains the limited access to antiviral drugs and diagnostic tests. In 2010, the World Health Assembly adopted a resolution calling for a comprehensive approach for the prevention, control, and management of viral hepatitis. We describe activities at the World Health Organization (WHO) in three key areas: the establishment of a global hepatitis Program and interim strategy; steps toward the development of global guidance on management of coinfection for RLS; and the WHO prequalification program of HBV and HCV diagnostic assays. We highlight key research gaps and the importance of applying the lessons learned from the public health scale-up of ART to hepatitis care.

Keywords

HIV-hepatitis B coinfection - HIV-hepatitis C coinfection - resource-limited settings
 

  • References

  • 1 Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine 2012; 30 (12) 2212-2219
    CrossrefPubMedGoogle Scholar
  • 2 Lavanchy D. Chronic viral hepatitis as a public health issue in the world. Best Pract Res Clin Gastroenterol 2008; 22 (6) 991-1008
    CrossrefPubMedGoogle Scholar
  • 3 Madhava V, Burgess C, Drucker E. Epidemiology of chronic hepatitis C virus infection in sub-Saharan Africa. Lancet Infect Dis 2002; 2 (5) 293-302
    CrossrefPubMedGoogle Scholar
  • 4 Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 2005; 5 (9) 558-567
    CrossrefPubMedGoogle Scholar
  • 5 Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 2006; 45 (4) 529-538
    CrossrefPubMedGoogle Scholar
  • 6 Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol 2006; 44 (1, Suppl) S6-S9
    PubMedGoogle Scholar
  • 7 Hoffmann CJ, Thio CL. Clinical implications of HIV and hepatitis B co-infection in Asia and Africa. Lancet Infect Dis 2007; 7 (6) 402-409
    CrossrefPubMedGoogle Scholar
  • 8 Modi AA, Feld JJ. Viral hepatitis and HIV in Africa. AIDS Rev 2007; 9 (1) 25-39
    PubMedGoogle Scholar
  • 9 Scharschmidt BF, Held MJ, Hollander HH , et al. Hepatitis B in patients with HIV infection: relationship to AIDS and patient survival. Ann Intern Med 1992; 117 (10) 837-838
    CrossrefPubMedGoogle Scholar
  • 10 Sinicco A, Raiteri R, Sciandra M , et al. Coinfection and superinfection of hepatitis B virus in patients infected with human immunodeficiency virus: no evidence of faster progression to AIDS. Scand J Infect Dis 1997; 29 (2) 111-115
    CrossrefPubMedGoogle Scholar
  • 11 El-Serag HB, Giordano TP, Kramer J, Richardson P, Souchek J. Survival in hepatitis C and HIV co-infection: a cohort study of hospitalized veterans. Clin Gastroenterol Hepatol 2005; 3 (2) 175-183
    CrossrefPubMedGoogle Scholar
  • 12 Sulkowski MS, Moore RD, Mehta SH, Chaisson RE, Thomas DL. Hepatitis C and progression of HIV disease. JAMA 2002; 288 (2) 199-206
    CrossrefPubMedGoogle Scholar
  • 13 Thio CL, Seaberg EC, Skolasky Jr R , et al; Multicenter AIDS Cohort Study. HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet 2002; 360 (9349) 1921-1926
    CrossrefPubMedGoogle Scholar
  • 14 Hadigan C, Kottilil S. Hepatitis C virus infection and coinfection with human immunodeficiency virus: challenges and advancements in management. JAMA 2011; 306 (3) 294-301
    CrossrefPubMedGoogle Scholar
  • 15 Bodsworth N, Donovan B, Nightingale BN. The effect of concurrent human immunodeficiency virus infection on chronic hepatitis B: a study of 150 homosexual men. J Infect Dis 1989; 160 (4) 577-582
    CrossrefPubMedGoogle Scholar
  • 16 Colin JF, Cazals-Hatem D, Loriot MA , et al. Influence of human immunodeficiency virus infection on chronic hepatitis B in homosexual men. Hepatology 1999; 29 (4) 1306-1310
    CrossrefPubMedGoogle Scholar
  • 17 Gilson RJ, Hawkins AE, Beecham MR , et al. Interactions between HIV and hepatitis B virus in homosexual men: effects on the natural history of infection. AIDS 1997; 11 (5) 597-606
    CrossrefPubMedGoogle Scholar
  • 18 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
  • 19 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
  • 20 Graham CS, Baden LR, Yu E , et al. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. Clin Infect Dis 2001; 33 (4) 562-569
    CrossrefPubMedGoogle Scholar
  • 21 Konopnicki D, Mocroft A, de Wit S , et al; EuroSIDA Group. Hepatitis B and HIV: prevalence, AIDS progression, response to highly active antiretroviral therapy and increased mortality in the EuroSIDA cohort. AIDS 2005; 19 (6) 593-601
    CrossrefPubMedGoogle Scholar
  • 22 Puoti M, Spinetti A, Ghezzi A , et al. Mortality for liver disease in patients with HIV infection: a cohort study. J Acquir Immune Defic Syndr 2000; 24 (3) 211-217
    PubMedGoogle Scholar
  • 23 Núñez M. Clinical syndromes and consequences of antiretroviral-related hepatotoxicity. Hepatology 2010; 52 (3) 1143-1155
    CrossrefPubMedGoogle Scholar
  • 24 Labarga P, Soriano V, Vispo ME , et al. Hepatotoxicity of antiretroviral drugs is reduced after successful treatment of chronic hepatitis C in HIV-infected patients. J Infect Dis 2007; 196 (5) 670-676
    CrossrefPubMedGoogle Scholar
  • 25 Zöllner B, Petersen J, Puchhammer-Stöckl E , et al. Viral features of lamivudine resistant hepatitis B genotypes A and D. Hepatology 2004; 39 (1) 42-50
    CrossrefPubMedGoogle Scholar
  • 26 Benhamou Y, Bochet M, Thibault V , et al. Long-term incidence of hepatitis B virus resistance to lamivudine in human immunodeficiency virus-infected patients. Hepatology 1999; 30 (5) 1302-1306
    CrossrefPubMedGoogle Scholar
  • 27 DeSimone J, Pomerantz R, Babinchak T. Inflammatory reactions in HIV-1 infected persons after initiation of highly active antiretroviral therapy. Ann Intern Med 2000; 133: 447-454
    CrossrefPubMedGoogle Scholar
  • 28 Shelburne S, Hamill R, Rodriguez-Barradas M , et al. Immune reconstitution inflammatory syndrome: emergence of a unique syndrome during highly active antiretroviral therapy. Medicine (Baltimore) 2002; 81 (3) 213-227
    CrossrefPubMedGoogle Scholar
  • 29 Weber R, Sabin C, 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
  • 30 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
  • 31 Ford N, Kirby C, Singh K , et al. Chronic hepatitis C treatment outcomes in low- and middle-income countries: a systematic review and meta-analysis. Bulletin of the World Health Organisation 2012. Available at: http://www.who.int/bulletin/online_first/11-097147.pdf . Accessed January 12, 2012
    PubMedGoogle Scholar
  • 32 Viral hepatitis: global policy. London: World Hepatitis Alliance; 2011. . Available at: http://www.worldhepatitisalliance.org/Policy/2010PolicyReport.aspx . Accessed January 12, 2012
    Google Scholar
  • 33 Viral hepatitis. WHA63.18. Sixty-third World Health Assembly. Agenda item 11.12. Geneva: World Health Organization; 2010. . Available at: http://apps.who.int/gb/ebwha/pdf_files/WHA63/A63_R18-en.pdf . Accessed January 12, 2012
    Google Scholar
  • 34 European Association For The Study Of The Liver. EASL Clinical Practice Guidelines: management of chronic hepatitis B. J Hepatol 2009; 50 (2) 227-242
    CrossrefPubMedGoogle Scholar
  • 35 Liaw YF, Leung N, Kao JH , et al; Chronic Hepatitis B Guideline Working Party of the Asian-Pacific Association for the Study of the Liver. Asian-Pacific consensus statement on the management of chronic hepatitis B: a 2008 update. Hepatol Int 2008; 2 (3) 263-283
    CrossrefPubMedGoogle Scholar
  • 36 Rockstroh JK, Bhagani S, Benhamou Y , et al; EACS Executive Committee. European AIDS Clinical Society (EACS) guidelines for the clinical management and treatment of chronic hepatitis B and C coinfection in HIV-infected adults. HIV Med 2008; 9 (2) 82-88
    CrossrefPubMedGoogle Scholar
  • 37 Soriano V, Puoti M, Sulkowski M , et al. Care of patients coinfected with HIV and hepatitis C virus: 2007 updated recommendations from the HCV-HIV International Panel. AIDS 2007; 21 (9) 1073-1089
    CrossrefPubMedGoogle Scholar
  • 38 Thursz M, Cooke GS, Hall AJ. Hepatitis B treatment in resource poor settings: time for action. Trop Med Int Health 2010; 15 (1) 2-4
    PubMedGoogle Scholar
  • 39 Wiersma ST, McMahon B, Pawlotsky JM , et al; World Health Organization Department of Immunization, Vaccines and Biologicals. Treatment of chronic hepatitis B virus infection in resource-constrained settings: expert panel consensus. Liver Int 2011; 31 (6) 755-761
    CrossrefPubMedGoogle Scholar
  • 40 Ford N, Singh K, Cooke GS , et al. Expanding access to treatment for hepatitis C in resource-limited settings: lessons from HIV/AIDS. Clin Infect Dis 2012; 54 (10) 1465-1472
    CrossrefPubMedGoogle Scholar
  • 41 Heenan R, Wiersma S, Vitori M, Cheung A, Easterbrook P. Significant variation in recommendations for management of HIV-Hepatitis B and C (HIV-HBV and HIV-HCV) co-infection: A Survey of National Guidelines from Resource Limited Settings. Abstract presented at: International Aids Conference; July 22–27, 2012; Washington, DC
    Google Scholar
  • 42 Davis LG, Weber DJ, Lemon SM. Horizontal transmission of hepatitis B virus. Lancet 1989; 1 (8643) 889-893
    PubMedGoogle Scholar
  • 43 Kew MC. Progress towards the comprehensive control of hepatitis B in Africa: a view from South Africa. Gut 1996; 38 (Suppl 2) S31-S36
    CrossrefPubMedGoogle Scholar
  • 44 Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan Africa: a view from tropical and subtropical Africa. Gut 1996; 38 (Suppl 2) S5-S12
    CrossrefPubMedGoogle Scholar
  • 45 Custer B, Sullivan SD, Hazlet TK , et al. Global Epidemiology of Hepatitis B Virus. J Clin Gastroenterol 2004; 38 (3) S158-S168
    CrossrefPubMedGoogle Scholar
  • 46 Nur YA, Groen J, Elmi AM, Ott A, Osterhaus AD. Prevalence of serum antibodies against bloodborne and sexually transmitted agents in selected groups in Somalia. Epidemiol Infect 2000; 124 (1) 137-141
    CrossrefPubMedGoogle Scholar
  • 47 Herrero Martínez E. Hepatitis B and hepatitis C co-infection in patients with HIV. Rev Med Virol 2001; 11 (4) 253-270
    CrossrefPubMedGoogle Scholar
  • 48 Candotti D, Mundy C, Kadewele G, Nkhoma W, Bates I, Allain JP. Serological and molecular screening for viruses in blood donors from Ntcheu, Malawi: high prevalence of HIV-1 subtype C and of markers of hepatitis B and C viruses. J Med Virol 2001; 65 (1) 1-5
    CrossrefPubMedGoogle Scholar
  • 49 Matee MI, Lyamuya EF, Mbena EC , et al. Prevalence of transfusion-associated viral infections and syphilis among blood donors in Muhimbili Medical Centre, Dar es Salaam, Tanzania. East Afr Med J 1999; 76 (3) 167-171
    PubMedGoogle Scholar
  • 50 Ansa VO, Udoma EJ, Umoh MS, Anah MU. Occupational risk of infection by human immunodeficiency and hepatitis B viruses among health workers in south-eastern Nigeria. East Afr Med J 2002; 79 (5) 254-256
    PubMedGoogle Scholar
  • 51 Hauri AM, Armstrong GL, Hutin YJ. The global burden of disease attributable to contaminated injections given in health care settings. Int J STD AIDS 2004; 15 (1) 7-16
    CrossrefPubMedGoogle Scholar
  • 52 Njouom R, Pasquier C, Ayouba A , et al. Low risk of mother-to-child transmission of hepatitis C virus in Yaounde, Cameroon: the ANRS 1262 study. Am J Trop Med Hyg 2005; 73 (2) 460-466
    PubMedGoogle Scholar
  • 53 Broderick AL, Jonas MM. Hepatitis B in children. Sem Liver Dis 2003; 23 (1) 59-68
    Article in Thieme ConnectPubMedGoogle Scholar
  • 54 Pasquier C, Njouom R, Ayouba A , et al. Distribution and heterogeneity of hepatitis C genotypes in hepatitis patients in Cameroon. J Med Virol 2005; 77 (3) 390-398
    CrossrefPubMedGoogle Scholar
  • 55 Scheiblauer H, El-Nageh M, Diaz S , et al. Performance evaluation of 70 hepatitis B virus (HBV) surface antigent (HBsAg) assays from around the world by a geographically diverse panel with an array of HBV genotypes and HBsAg subtypes. Vox Sang 2010; 98: 581
    PubMedGoogle Scholar
  • 56 Allain JP, Candotti D, Soldan K , et al. The risk of hepatitis B virus infection by transfusion in Kumasi, Ghana. Blood 2003; 101 (6) 2419-2425
    CrossrefPubMedGoogle Scholar
  • 57 Callahan JD, Constantine NT, Kataaha P, Zhang X, Hyams KC, Bansal J. Second generation hepatitis C virus assays: performance when testing African sera. J Med Virol 1993; 41 (1) 35-38
    CrossrefPubMedGoogle Scholar
  • 58 Castera L. Non-invasive assessment of liver fibrosis in chronic hepatitis C. Hepatol Int 2011; 5 (2) 625-634
    CrossrefPubMedGoogle Scholar
  • 59 Baranova A, Lal P, Birerdinc A, Younossi ZM. Non-invasive markers for hepatic fibrosis. BMC Gastroenterol 2011; 11: 91
    CrossrefPubMedGoogle Scholar
  • 60 Degos F, Perez P, Roche B , et al; FIBROSTIC study group. Diagnostic accuracy of FibroScan and comparison to liver fibrosis biomarkers in chronic viral hepatitis: a multicenter prospective study (the FIBROSTIC study). J Hepatol 2010; 53 (6) 1013-1021
    CrossrefPubMedGoogle Scholar
  • 61 Nunes D, Fleming C, Offner G , et al. HIV infection does not affect the performance of non-invasive markers of fibrosis for the diagnosis of hepatitis C virus-related liver disease. J Acquir Immune Defic Syndr 2005; 40 (5) 538-544
    CrossrefPubMedGoogle Scholar
  • 62 Cacoub P, Carrat F, Bédosa P , et al. Comparison of non-invasive liver fibrosis biomarkers in HIV/HCV co-infected patients: The fibrovic study—ANRS HCO2. J Hepatol 2008; 48 (5) 765-773
    CrossrefPubMedGoogle Scholar
  • 63 World Health Organization.. Antiretroviral therapy for HIV infection in adults and adolescents: recommendations for a public health approach - 2010 revision. Available at: http://whqlibdoc.who.int/publications/2010/9789241599764_eng.pdf. Accessed January 12, 2012
    PubMedGoogle Scholar
  • 64 Bessesen M, Ives D, Condreay L, Lawrence S, Sherman KE. Chronic active hepatitis B exacerbations in human immunodeficiency virus-infected patients following development of resistance to or withdrawal of lamivudine. Clin Infect Dis 1999; 28 (5) 1032-1035
    CrossrefPubMedGoogle Scholar
  • 65 Diagnostics and Laboratory Technology. Geneva:: World Health Organization;; 2011. . Available at: http://www.who.int/diagnostics_laboratory/evaluations/110322_pqdx_007_pq_overview_document_v4.pdf Accessed January 12, 2012
    Google Scholar
  • 66 Diagnostics and Laboratory Technology. Geneva:: World Health Organization;; 2012 . Available at: http://www.who.int/diagnostics_laboratory/pq_status/en/index.html. Accessed January 12, 2012
    PubMedGoogle Scholar
  • 67 Easterbrook PJ. HIV immune reconstitution syndrome in sub-Saharan Africa. AIDS 2008; 22 (5) 643-645
    CrossrefPubMedGoogle Scholar
  • 68 Viljoen J, Gampini S, Danaviah S , et al; World Health Organization/ANRS 1289 Kesho Bora Study Group. Dried blood spot HIV-1 RNA quantification using open real-time systems in South Africa and Burkina Faso. J Acquir Immune Defic Syndr 2010; 55 (3) 290-298
    CrossrefPubMedGoogle Scholar