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Prevalence of hepatitis B virus and hepatitis C virus in patients with human immunodeficiency virus infection in central China

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Abstract

Co-infection of hepatitis B virus (HBV) and/or hepatitis C virus (HCV) with human immunodeficiency virus (HIV) has an adverse effect on liver disease progression. This study investigated the prevalence of HBV and/or HCV co-infection in HIV-infected patients in Central China. A total of 978 HIV-infected patients from Hunan Province were enrolled. HBV serum markers, anti-hepatitis-C-virus antibody (anti-HCV), HBV DNA, and HBV genotypes were analyzed. The prevalence of hepatitis B surface antigen (HBsAg) and anti-HCV in HIV-infected patients was 19.4 % and 62.4 %, respectively. The prevalence of anti-HCV in HIV-positive intravenous drug users was 93.6 %. Among HBsAg-positive patients, 88.1 % were found to have at least one HBV serum marker. The rates of HIV mono-infection, HBV/HIV dual infection, HCV/HIV dual infection, and HBV/HCV/HIV triple infection were 30.4 %, 7.2 %, 50.2 %, and 12.2 %, respectively. Antibody to HBsAg (Anti-HBs) was more common in anti-HCV-positive than anti-HCV-negative patients (53.3 % vs 40.2 %, P = 0.000), but isolated hepatitis B core antibody (anti-HBc) was more common in anti-HCV-negative than anti-HCV-positive patients (24.2 % vs 12.3 %, P = 0.000). Hepatitis B e antigen (HBeAg) and sexual transmission were independent risk factors for active HBV replication. Intravenous drug use and male sex were independent risk factors, but old age and presence of HBeAg were independent protective factors for anti-HCV. Co-infection of HBV and/or HCV with HIV infection is common in central China. HCV status is associated with anti-HBs and isolated anti-HBc in co-infected patients.

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References

  1. Thio CL (2003) Hepatitis B in the human immunodeficiency virus-infected patients: epidemiology, natural history, and treatment. Semin Liver Dis 23:125–136

    Article  PubMed  CAS  Google Scholar 

  2. Taylor LE, Swan T, Mayer KH (2012) HIV coinfection with hepatitis C virus: evolving epidemiology and treatment paradigms. Clin Infect Dis 55(suppl 1):S33–S42

    Article  PubMed  CAS  Google Scholar 

  3. Alter M (2006) Epidemiology of viral hepatitis and HIV co-infection. J Hepatol 44:S6–S9

    Article  PubMed  Google Scholar 

  4. Adewole OO, Anteyi E, Ajuwon Z, Wada I, Elegba F, Ahmed P, Betiku Y, Okpe A, Eze S, Ogbeche T, Erhabor GE (2009) Hepatitis B and C virus co-infection in Nigerian patients with HIV infection. J Infect Dev Ctries 3:369–375

    Article  PubMed  CAS  Google Scholar 

  5. Hoffman C, Thio C (2007) Clinial implications of HIV and hepatitis B co-infection in Asia and Africa. Lancet Infect Dis 7:402–409

    Article  Google Scholar 

  6. Soriano V, Barreiro P, Nunez M (2006) Management of chronic hepatitis B and C in HIV-coinfected patients. J Antimicrob Chemother 57:815–818

    Article  PubMed  CAS  Google Scholar 

  7. Lacombe K, Bottero J, Lemoine M, Boyd A, Girard PM (2010) HIV/hepatitis B virus co-infection: current challenges and new strategies. J Antimicrob Chemother 65:10–17

    Article  PubMed  CAS  Google Scholar 

  8. Chun HM, Roediger MP, Hullsiek KH, Thio CL, Agan BK, Bradley WP, Peel SA, Jagodzinski LL, Weintrob AC, Ganesan A, Wortmann G, Crum-Cianflone NF, Maguire JD, Landrum ML (2012) Infectious Disease Clinical Research Program HIV Working Group: Hepatitis B virus coinfection negatively impacts HIV outcomes in HIV seroconverters. Clin Infect Dis 205:185–193

    Google Scholar 

  9. Nikolopoulos GK, Paraskevis D, Hatzitheodorou E, Moschidis Z, Sypsa V, Zavitsanos X, Kalapothaki V, Hatzakis A (2009) Impact of hepatitis B virus infection on the progression of AIDS and mortality in HIV-infected individuals: a cohort study and meta-analysis. Clin Infect Dis 48:1763–1771

    Article  PubMed  Google Scholar 

  10. Okamoto H, Tsuda F, Sakugawa H, Sastrosoewignjo RI, Imai M, Miyakawa Y, Mayumi M (1988) Typing hepatitis B virus by homology in nucleotide sequences: comparison of surface antigen subtypes. J Gen Virol 69:2575–2583

    Article  PubMed  CAS  Google Scholar 

  11. Norder H, Courouse AM, Magnius LO (1994) Complete genomes, phylogenetic relatedness, and structural proteins of six strains of the hepatitis B virus, four of which represent two new genotypes. Virology 198:489–503

    Article  PubMed  CAS  Google Scholar 

  12. Stuyver L, De Gendt S, Van Geyt C, Zoulim F, Fried M, Schinazi RF, Rossau R (2000) A new genotype of hepatitis B virus: complete genome and phylogenetic relatedness. J Gen Virol 81:67–74

    PubMed  CAS  Google Scholar 

  13. Arauz-ruiz P, Norder H, Robertson BH, Magnius LO (2002) Genotype H: a new Amerindian genotype of hepatitis B virus revealed in Central America. J Gen Virol 83:2059–2073

    PubMed  CAS  Google Scholar 

  14. Olinger CM, Jutavijittum P, Hubschen JM, Yousukh A, Samountry B, Thammavong T, Toriyama K, Muller CP (2008) Possible new hepatitis B virus genotype, southeast Asia. Emerg Infect Dis 14:1777–1780

    Article  PubMed  Google Scholar 

  15. Tatematsu K, Tanaka Y, Kurbanov F, Sugauchi F, Mano S, Maeshiro T, Nakayoshi T, Wakuka M, Miyakawa Y, Mizokami M (2009) A genetic variant of hepatitis B virus divergent from known human and ape genotypes isolated from a Japanese patient and provisionally assigned to new genotype J. J Virol 83:10538–10547

    Article  PubMed  CAS  Google Scholar 

  16. Norder H, Courouce AM, Coursaget P, Echevarria JM, Lee SD, Mushahwar IK, Robertson BH, Locarnini S, Magnius LQ (2004) Genetic diversity of hepatitis B virus strains derived worldwide: genotypes, subgenotypes, and HBsAg subtypes. Intervirology 47:289–309

    Article  PubMed  Google Scholar 

  17. Pourkarim MR, Lemey P, Amini-Bavil-Olyaee S, Houspie L, Verbeeck J, Rahman M, Maes P, Vanwijingaerden E, Nevens F, Van Ranst M (2011) Molecular characterization of hepatitis B virus strains circulating in Belgian patients co-infected with HIV and HBV: overt and occult infection. J Med Virol 83:1876–1884

    Article  PubMed  CAS  Google Scholar 

  18. Shibayama T, Masuda G, Ajisawa A, Hiruma K, Tsuda F, Nishizawa T, Takahashi M, Okamoto H (2005) Characterization of seven genotypes (A to E, G and H) of hepatitis B virus recovered from Japanese patients infected with human immunodeficiency virus type 1. J Med Virol 76:24–32

    Article  PubMed  Google Scholar 

  19. Fujisaki S, Ykomaku Y, Shiino T, Koibuchhi T, Hattori J, Ibe S, Iwatani Y, Iwamoto A, Shirasaka T, Hamaguchi M, Sugiura W (2011) Outbreak of infections by hepatitis B virus genotype A and transmission of genetic drug resistance in patients coinfected with HIV-1 in Japan. J Clin Microbiol 49:1017–1024

    Article  PubMed  CAS  Google Scholar 

  20. Ramos B, Nunez M, Martin-Carbonero L, Sheldon J, Rios P, Labarga P, Romero M, Barreiro P, Garcia-Samaniego J, Soriano V (2007) Hepatitis B virus genotypes and lamivudine resistance mutations in HIV/hepatitis B virus-coinfected patients. J Acquir Immune Defic Syndr 44:557–561

    Article  PubMed  Google Scholar 

  21. Quarleri J, Moretti F, Bouzas MB, Laufer N, Carrillo MG (2007) giuliano SF, Perez H, Cahn P, Salomo H. Hepatitis B virus genotype distribution and its lamivudine-resistant mutants in HIV-coinfected patients with chronic occult hepatitis B. AIDS Res Hum Retroviruses 23:525–531

    Article  PubMed  CAS  Google Scholar 

  22. Damerow H, Yuen L, Wiegand J, Walker C, Bock CT, Locarnini S, Tillmann HL (2010) Mutation pattern of lamivudine resistance in relation to hepatitis B genotypes: hepatitis B genotypes differ in their lamivudine resistance associated mutation pattern. J Med Virol 82:1850–1858

    Article  PubMed  CAS  Google Scholar 

  23. Sheng WH, Hung CC, Chang SY, Liu CJ, Chen MY, Hsieh SM, Kao JH, Chen PJ, Chang SC (2012) Differential clinical and virologic impact of hepatitis B virus genotypes B and C on HIV-coinfected patients receiving lamivudine-containing highy active antiretroviral therapy. Clin Infec Dis 54:548–555

    Article  CAS  Google Scholar 

  24. Lada O, Gervais A, Branger M, Peytavin G, Roquebert B, Collin G, Fraqueiro G, Moucari R, Hamet G, Martinot-Peignoux M, Matheron S, Marcellin P (2012) Long-term outcome of primary non-responders to tenofovir therapy in HIV/HBV-co-infected patients: impact of HBV genotype G. Liver Int 32:93–101

    Article  PubMed  CAS  Google Scholar 

  25. Dao DY, Balko J, Attar N, Neak E, Yuan HJ, Lee WM, Jain MK (2011) Hepatitis B virus genotype G: prevalence and impact in patients co-infected with human immunodeficiency virus. J Med Virol 83:1551–1558

    Article  PubMed  Google Scholar 

  26. Liang X, Bi S, Yang W, Wang L, Cui G, Cui F, Zhang Y, Liu J, Gong X, Chen Y, Wang F, Zheng H, Wang F, Guo J, Ma J, Wang H, Luo H, Li L, Jin S, Hadler SC, Wang Y (2009) Epidemiological serosurvey of hepatitis B in China—declining HBV prevalence due to hepatitis B vaccination. Vaccine 27:6550–6557

    Article  PubMed  Google Scholar 

  27. Zeng G, Wang Z, Wen S, Jiang J, Wang L, Cheng J, Tan D, Xiao F, Ma S, Li W, Luo K, Naoumov NV, Hou J (2005) Geographic distribution, virologic and clinical characteristics of hepatitis B virus genotypes in China. J Viral Hepatitis 12:609–617

    Article  CAS  Google Scholar 

  28. Wu Z, Sullivan SG, Wang Y, Rotheram-Borus MJ, Detels R (2007) Evolution of China’s response to HIV/AIDS. Lancet 369:679–690

    Article  PubMed  Google Scholar 

  29. He N, Chen L, Lin HJ, Zhang M, Wei J, Yang JH, Gabrio J, Rui BL, Zhang ZF, Fu ZH, Ding YY, Zhao GM, Jiang QW, Detels R (2011) Multiple viral coinfections among HIV/AIDS patients in China. Biosci Trends 5:1–9

    Article  PubMed  CAS  Google Scholar 

  30. Shen Y, Wang Z, Qi T, Jiang X, Song W, Tang J, Liu L, Zhang R, Zheng Y, Dai Z, Lu H (2013) Serological survey of viral hepatitis markers among newly diagnosed patients with HIV/AIDS in China. HIV Med 14:167–175

    Google Scholar 

  31. Spradling PR, Richardson JT, Buchacz K, Moorman AC, Brooks JT (2010) HIV Outpatient Study (HOPS) Investigators: prevalence of chronic hepatitis B virus infection among patients in the HIV outpatients study, 1996–2007. J Viral Hepat 17:879–886

    Article  PubMed  CAS  Google Scholar 

  32. Yang R, Gui X, Xiong Y, Gao S, Zhang Y, Deng L, Liang K, Yan Y, Rong Y (2011) Risk of liver-associated morbidity and mortality in a cohort of HIV and HBV coinfected Han Chinese. Infection 39:427–431

    Article  PubMed  CAS  Google Scholar 

  33. Winnock M, Bani-Sadr F, Pambrun E, Loko MA, Lascoux-Combe C, Garipuy D, Rosenthal E, Carrieri P, Dabis F, Salmon D (2011) Prevalence of immunity to hepatitis viruses A and B in a large cohort of HIV/HCV-coinfected patients, and factors associated with HAV and HBV vaccination. Vaccine 29:8656–8660

    Article  PubMed  CAS  Google Scholar 

  34. Gandhi RT, Wurcel A, Lee H, McGovern B, Boczanowski M, Gerwin R, Corcoran CP, Szczepiorkowski Z, Toner S, Cohen DE, Sax PE, Ukomadu C (2003) Isolated antibody to hepatitis B core antigen in human immunodeficiency virus type-1-infected individuals. Clin Infect Dis 36:1602–1605

    Article  PubMed  CAS  Google Scholar 

  35. French AL, Operskalski E, Peters M, Strickler HD, Tien PC, Sharp GB, Glesby MJ, Young M, Augenbraun M, Seaberg E, Kovacs A (2007) Isolated hepatitis B core antibody is associated with HIV and ongoing but not resolved hepatitis C virus infection in a cohort of US women. J Infect Dis 195:1437–1442

    Article  PubMed  CAS  Google Scholar 

  36. Garten RJ, Zhang J, Lai S, Liu W, Chen J, Yu XF (2005) Coinfection with HIV and hepatitis C virus among injection drug users in southern China. Clin Infect Dis 41(Suppl 1):S18–S24

    Article  PubMed  Google Scholar 

  37. Liu JY, Lin HH, Liu YC, Lee SS, Chen YL, Hung CC, Ko WC, Huang CK, Lai CH, Chen YS, Shih YL, Chung HC, Liang SH, Lin JN (2008) Extremely high prevalence and genetic diversity of hepatitis C virus infection among HIV-infected injection drug users in Taiwan. Clin Infect Dis 46:1761–1768

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by National Mega-project of Science Research (No. 2008ZX10001-003) and Hunan Provincial Project of Medical Science Research (No. B2010-091).

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Correspondence to Xi Chen.

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Chen, X., He, JM., Ding, LS. et al. Prevalence of hepatitis B virus and hepatitis C virus in patients with human immunodeficiency virus infection in central China. Arch Virol 158, 1889–1894 (2013). https://doi.org/10.1007/s00705-013-1681-z

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  • DOI: https://doi.org/10.1007/s00705-013-1681-z

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