Abstract
To assess the prevalence of hepatitis B virus (HBV) and hepatitis C virus (HCV) infection and to investigate their mutual influences on infection status among human immunodeficiency virus type 1 (HIV-1)-seropositive injection drug users (IDUs). A cross-sectional study was conducted among HIV infected IDUs in Dali, China. The participants were tested for serological markers of HBV and HCV infection, alanine transaminase (ALT) activity and CD4+ T cell count. HCV genotype was determined by sequencing. Of 529 patients, 498 (94.1 %) HIV infected IDUs agreed to participate. The overall prevalence of HCV infection (anti-HCV antibody positive) and spontaneous HCV clearance were 90.8 % (452/498) and 21.5 % (97/452), respectively. Of 411 subjects who had not received HBV vaccine, 296 (72.0 %) were positive for antibody against HBV core antigen (HBcAb), while 274 (66.7 %) were positive for both HCV antibody and HBcAb. HBV antigens were detected in 52 of the HBV-infected subjects (17.6 %). HCV clearance was associated with HBV antigenemia (p = 0.0002) and higher CD4+ T cell count (p = 0.0294). Resolved HBV infection was associated with HCV genotype 3 (p = 0.0365). HBV and HCV infection are highly prevalent and mutually influence infection status in HIV-1 infected IDUs in Dali, China.
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Anderson KB, Guest JL, Rimland D (2004) Hepatitis C virus coinfection increases mortality in HIV-infected patients in the highly active antiretroviral therapy era: data from the HIV Atlanta VA Cohort Study. Clin Infect Dis 39:1507–1513
Chen SY, Kao CF, Chen CM, Shih CM, Hsu MJ, Chao CH, Wang SH, You LR, Lee YH (2003) Mechanisms for inhibition of hepatitis B virus gene expression and replication by hepatitis C virus core protein. J Biol Chem 278:591–607
Gebo KA, Diener-West M, Moore RD (2003) Hospitalization rates differ by hepatitis C status in an urban HIV cohort. J Acquir Immune Defic Syndr 34:165–173
Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, Hoffmann R, Schirren CA, Santantonio T, Pape GR (1999) Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 117:933–941
Graham CS, Baden LR, Yu E, Mrus JM, Carnie J, Heeren T, Koziel MJ (2001) Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. Clin Infect Dis 33:562–569
Greub G, Ledergerber B, Battegay M, Grob P, Perrin L, Furrer H, Burgisser P, Erb P, Boggian K, Piffaretti JC, Hirschel B, Janin P, Francioli P, Flepp M, Telenti A (2000) Clinical progression, survival, and immune recovery during antiretroviral therapy in patients with HIV-1 and hepatitis C virus coinfection: the Swiss HIV Cohort Study. Lancet 356:1800–1805
Guidotti LG, Chisari FV (2001) Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19:65–91
Hoffmann CJ, Thio CL (2007) Clinical implications of HIV and hepatitis B co-infection in Asia and Africa. Lancet Infect Dis 7:402–409
Kobayashi Y, Kawaguchi Y, Mizuta T, Kuwashiro T, Oeda S, Oza N, Takahashi H, Iwane S, Eguchi Y, Anzai K, Ozaki I, Fujimoto K (2011) Metabolic factors are associated with serum alanine aminotransferase levels in patients with chronic hepatitis C. J Gastroenterol 46:529–535
Liaw YF (1995) Role of hepatitis C virus in dual and triple hepatitis virus infection. Hepatology (Baltimore, Md) 22:1101–1108
Lu L, Nakano T, He Y, Fu Y, Hagedorn CH, Robertson BH (2005) Hepatitis C virus genotype distribution in China: predominance of closely related subtype 1b isolates and existence of new genotype 6 variants. J Med Virol 75:538–549
Maio G, d’Argenio P, Stroffolini T, Bozza A, Sacco L, Tosti ME, Intorcia M, Fossi E, d’Alessio G, Kondili LA, Rapicetta M, Mele A (2000) Hepatitis C virus infection and alanine transaminase levels in the general population: a survey in a southern Italian town. J Hepatol 33:116–120
Morsica G, Bagaglio S, Cicconi P, Capobianchi MR, Pellizzer G, Caramello P, Orani A, Moioli C, Rizzardini G, Uberti-Foppa C, Puoti M, Monforte AD (2009) Viral interference between hepatitis B, C, and D viruses in dual and triple infections in HIV-positive patients. J Acquir Immune Defic Syndr 51:574–581
Nelson PK, Mathers BM, Cowie B, Hagan H, Des Jarlais D, Horyniak D, Degenhardt L (2011) Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: results of systematic reviews. Lancet 378:571–583
Pontisso P, Ruvoletto MG, Fattovich G, Chemello L, Gallorini A, Ruol A, Alberti A (1993) Clinical and virological profiles in patients with multiple hepatitis virus infections. Gastroenterology 105:1529–1533
Pratt DS, Kaplan MM (2000) Evaluation of abnormal liver-enzyme results in asymptomatic patients. N Engl J Med 342:1266–1271
Ruan YH, Hong KX, Liu SZ, He YX, Zhou F, Qin GM, Chen KL, Xing H, Chen JP, Shao YM (2004) Community-based survey of HCV and HIV coinfection in injection drug abusers in Sichuan Province of China. World J Gastroenterol 10:1589–1593
Sagnelli E, Coppola N, Marrocco C, Onofrio M, Sagnelli C, Coviello G, Scolastico C, Filippini P (2006) Hepatitis C virus superinfection in hepatitis B virus chronic carriers: a reciprocal viral interaction and a variable clinical course. J Clin Virol 35:317–320
Sagnelli E, Coppola N, Pisaturo M, Masiello A, Tonziello G, Sagnelli C, Messina V, Filippini P (2009) HBV superinfection in HCV chronic carriers: a disease that is frequently severe but associated with the eradication of HCV. Hepatology (Baltimore, Md) 49:1090–1097
Schuttler CG, Fiedler N, Schmidt K, Repp R, Gerlich WH, Schaefer S (2002) Suppression of hepatitis B virus enhancer 1 and 2 by hepatitis C virus core protein. J Hepatol 37:855–862
Sheen IS, Liaw YF, Chu CM, Pao CC (1992) Role of hepatitis C virus infection in spontaneous hepatitis B surface antigen clearance during chronic hepatitis B virus infection. J Infect Dis 165:831–834
Shih CM, Lo SJ, Miyamura T, Chen SY, Lee YH (1993) Suppression of hepatitis B virus expression and replication by hepatitis C virus core protein in HuH-7 cells. J Virol 67:5823–5832
Simmonds P (1995) Variability of hepatitis C virus. Hepatology (Baltimore, Md) 21:570–583
Simmonds P (2001) The origin and evolution of hepatitis viruses in humans. J Gen Virol 82:693–712
Soriano V, Mocroft A, Rockstroh J, Ledergerber B, Knysz B, Chaplinskas S, Peters L, Karlsson A, Katlama C, Toro C, Kupfer B, Vogel M, Lundgren J (2008) Spontaneous viral clearance, viral load, and genotype distribution of hepatitis C virus (HCV) in HIV-infected patients with anti-HCV antibodies in Europe. J Infect Dis 198:1337–1344
Squadrito G, Orlando ME, Pollicino T, Raffa G, Restuccia T, Cacciola I, Di Marco V, Picciotto A, Colucci G, Craxi A, Raimondo G (2002) Virological profiles in patients with chronic hepatitis C and overt or occult HBV infection. Am J Gastroenterol 97:1518–1523
Sterling RK, Sulkowski MS (2004) Hepatitis C virus in the setting of HIV or hepatitis B virus coinfection. Semin Liver Dis 24(Suppl 2):61–68
Strader DB, Wright T, Thomas DL, Seeff LB (2004) Diagnosis, management, and treatment of hepatitis C. Hepatology (Baltimore, Md) 39:1147–1171
Sulkowski MS, Moore RD, Mehta SH, Chaisson RE, Thomas DL (2002) Hepatitis C and progression of HIV disease. JAMA 288:199–206
Sulkowski MS, Thomas DL, Mehta SH, Chaisson RE, Moore RD (2002) Hepatotoxicity associated with nevirapine or efavirenz-containing antiretroviral therapy: role of hepatitis C and B infections. Hepatology (Baltimore, Md) 35:182–189
Thio CL, Seaberg EC, Skolasky R Jr, Phair J, Visscher B, Munoz A, Thomas DL (2002) HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet 360:1921–1926
Thomson EC, Fleming VM, Main J, Klenerman P, Weber J, Eliahoo J, Smith J, McClure MO, Karayiannis P (2011) Predicting spontaneous clearance of acute hepatitis C virus in a large cohort of HIV-1-infected men. Gut 60:837–845
Verucchi G, Calza L, Manfredi R, Chiodo F (2004) Human immunodeficiency virus and hepatitis C virus coinfection: epidemiology, natural history, therapeutic options and clinical management. Infection 32:33–46
Weber R, Sabin CA, Friis-Moller N, Reiss P, El-Sadr WM, Kirk O, Dabis F, Law MG, Pradier C, De Wit S, Akerlund B, Calvo G, Monforte A, Rickenbach M, Ledergerber B, Phillips AN, Lundgren JD (2006) Liver-related deaths in persons infected with the human immunodeficiency virus: the D:A:D study. Arch Intern Med 166:1632–1641
Wietzke P, Schott P, Braun F, Mihm S, Ramadori G (1999) Clearance of HCV RNA in a chronic hepatitis C virus-infected patient during acute hepatitis B virus superinfection. Liver 19:348–353
Xia X, Lu L, Tee KK, Zhao W, Wu J, Yu J, Li X, Lin Y, Mukhtar MM, Hagedorn CH, Takebe Y (2008) The unique HCV genotype distribution and the discovery of a novel subtype 6u among IDUs co-infected with HIV-1 in Yunnan, China. J Med Virol 80:1142–1152
Zarski JP, Bohn B, Bastie A, Pawlotsky JM, Baud M, Bost-Bezeaux F, Tran van Nhieu J, Seigneurin JM, Buffet C, Dhumeaux D (1998) Characteristics of patients with dual infection by hepatitis B and C viruses. J Hepatol 28:27–33
Zhang C, Yang R, Xia X, Qin S, Dai J, Zhang Z, Peng Z, Wei T, Liu H, Pu D, Luo J, Takebe Y, Ben K (2002) High prevalence of HIV-1 and hepatitis C virus coinfection among injection drug users in the southeastern region of Yunnan, China. J Acquir Immune Defic Syndr 29:191–196
Zhou YH, Liu FL, Yao ZH, Duo L, Li H, Sun Y, Zheng YT (2011) Comparison of HIV-, HBV-, HCV- and co-infection prevalence between Chinese and Burmese intravenous drug users of the China-Myanmar border region. PLoS ONE 6:e16349
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Y. Dong, C. Qiu and X. Xia equally contributed to this work.
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Dong, Y., Qiu, C., Xia, X. et al. Hepatitis B virus and hepatitis C virus infection among HIV-1-infected injection drug users in Dali, China: prevalence and infection status in a cross-sectional study. Arch Virol 160, 929–936 (2015). https://doi.org/10.1007/s00705-014-2311-0
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DOI: https://doi.org/10.1007/s00705-014-2311-0