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HIV–HBV and HIV–HCV Coinfection and Liver Cancer Development

  • Jianming Hu
  • Kuancheng Liu
  • Jun Luo
Chapter
Part of the Cancer Treatment and Research book series (CTAR, volume 177)

Abstract

Liver diseases that are caused by the hepatitis B virus (HBV) and hepatitis C virus (HCV), including cirrhosis and hepatocellular carcinoma (HCC), have become increasingly important in patients infected with the human immunodeficiency virus (HIV) as their life expectancy is getting longer with successful anti-HIV therapy. Due to their shared transmission routes, dual infection by HIV and HBV or HIV and HCV, and triple infection by all three viruses are fairly common and affect millions of people worldwide. Whereas the immunodeficiency caused by HIV enhances the likelihood of HBV and HCV persistence, hepatotoxicity associated with anti-HIV therapy can worsen the liver diseases associated with HBV or HCV persistence. Evidence suggests HIV infection increases the risk of HBV- or HCV-associated HCC risk although the precise mechanisms of enhanced hepatocarcinogenesis remain to be fully elucidated. Recent success in curing HCV infection, and the availability of therapeutic options effective in long-term suppression of both HIV and HBV replication, bring hope, fortunately, to those who are coinfected but also highlight the need for judicious selection of antiviral therapies.

Keywords

Hepatitis B virus Hepatitis C virus Human immunodeficiency virus HBV HCV HIV Hepatocellular carcinoma HCC Coinfection 

References

  1. 1.
    Thomas DL (2006) Growing importance of liver disease in HIV-infected persons. Hepatology 43(2 Suppl 1):S221–S229CrossRefGoogle Scholar
  2. 2.
    Cacoub P, Geffray L, Rosenthal E, Perronne C, Veyssier P, Raguin G (2001) Mortality among human immunodeficiency virus-infected patients with cirrhosis or hepatocellular carcinoma due to hepatitis C virus in French departments of internal medicine/Infectious diseases, in 1995 and 1997. Clin Infect Dis 32(8):1207–1214CrossRefGoogle Scholar
  3. 3.
    Cooper CL, Mills E, Wabwire BO, Ford N, Olupot-Olupot P (2009) Chronic viral hepatitis may diminish the gains of HIV antiretroviral therapy in sub-Saharan Africa. Int J Infect Dis. 13(3):302–306CrossRefGoogle Scholar
  4. 4.
    Koziel MJ, Peters MG (2007) Viral hepatitis in HIV infection. N Engl J Med 356(14):1445–1454PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    WHO (2017) Global hepatitis report, 2017Google Scholar
  6. 6.
    Hu J (2016) Hepatitis B virus virology and replication. In: Liaw Y-F, Zoulim F (eds) Hepatitis B virus in human diseases. Humana Press, Springer Cham Heidelberg New York Dordrecht London, pp 1–34Google Scholar
  7. 7.
    Ganem D, Prince AM (2004) Hepatitis B virus infection–natural history and clinical consequences. N Engl J Med 350(11):1118–1129CrossRefGoogle Scholar
  8. 8.
    Slagle BL, Andrisani OM, Bouchard MJ, Lee CG, Ou JH, Siddiqui A (2015) Technical standards for hepatitis B virus X protein (HBx) research. Hepatology 61(4):1416−1424PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Decorsiere A, Mueller H, van Breugel PC, Abdul F, Gerossier L, Beran RK et al (2016) Hepatitis B virus X protein identifies the Smc5/6 complex as a host restriction factor. Nature 531(7594):386–389CrossRefGoogle Scholar
  10. 10.
    Yim HJ, Lok AS (2006) Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology 43(2 Suppl 1):S173–S181CrossRefGoogle Scholar
  11. 11.
    Wright TL (2006) Introduction to chronic hepatitis B infection. Am J Gastroenterol 101(Suppl 1):S1–S6CrossRefGoogle Scholar
  12. 12.
    Ott JJ, Stevens GA, Groeger J, Wiersma ST (2012) Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine 30(12):2212–2219PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ (2015) Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 386(10003):1546–1555CrossRefGoogle Scholar
  14. 14.
    Lavanchy D, Kane M (2016) Global epidemiology of hepatitis B virus infection. In: Liaw Y-F, Zoulim F (eds) Hepatitis B virus in human diseases. Humana Press, Springer Cham Heidelberg New York Dordrecht London, pp 187–203CrossRefGoogle Scholar
  15. 15.
    Trepo C, Chan HL, Lok A (2014) Hepatitis B virus infection. Lancet 384(9959):2053–2063CrossRefGoogle Scholar
  16. 16.
    Lindenbach BD, Rice CM (2005) Unravelling hepatitis C virus replication from genome to function. Nature 436(7053):933–938CrossRefGoogle Scholar
  17. 17.
    Chen SL, Morgan TR (2006) The natural history of hepatitis C virus (HCV) infection. Int J Med Sci. 3(2):47–52PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Seeff LB (1999) Natural history of hepatitis C. Am J Med 107(6B):10S–15SCrossRefGoogle Scholar
  19. 19.
    Park JS, Saraf N, Dieterich DT (2006) HBV plus HCV, HCV plus HIV, HBV plus HIV. Curr Gastroenterol Rep 8(1):67–74CrossRefGoogle Scholar
  20. 20.
    Alter MJ (2006) Epidemiology of viral hepatitis and HIV co-infection. J Hepatol 44(1 Suppl):S6–S9CrossRefGoogle Scholar
  21. 21.
    Spradling PR, Richardson JT, Buchacz K, Moorman AC, Brooks JT, Investigators HIVOS (2010) Prevalence of chronic hepatitis B virus infection among patients in the HIV outpatient study, 1996–2007. J Viral Hepat 17(12):879-86CrossRefGoogle Scholar
  22. 22.
    Alexiev I, Alexandrova M, Golkocheva-Markova E, Teoharov P, Gancheva A, Kostadinova A et al (2017) High rate of hepatitis B and C coinfections among people living with HIV-1 in Bulgaria: 2010–2014. AIDS Res Hum Retroviruses 33(3):228–229CrossRefGoogle Scholar
  23. 23.
    Martin-Carbonero L, Poveda E (2012) Hepatitis B virus and HIV infection. Semin Liver Dis 32(2):114–119CrossRefGoogle Scholar
  24. 24.
    Sulkowski MS (2008) Viral hepatitis and HIV coinfection. J Hepatol 48(2):353–367CrossRefGoogle Scholar
  25. 25.
    Lascar RM, Lopes AR, Gilson RJ, Dunn C, Johnstone R, Copas A et al (2005) Effect of HIV infection and antiretroviral therapy on hepatitis B virus (HBV)-specific T cell responses in patients who have resolved HBV infection. J Infect Dis 191(7):1169–1179CrossRefGoogle Scholar
  26. 26.
    Yeo W, Lam KC, Zee B, Chan PS, Mo FK, Ho WM et al (2004) Hepatitis B reactivation in patients with hepatocellular carcinoma undergoing systemic chemotherapy. Ann Oncol 15(11):1661–1666CrossRefGoogle Scholar
  27. 27.
    Gupta P, Hepatitis C (2013) Virus and HIV type 1 co-infection. Infect Dis Rep. 5(Suppl 1):e7PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Sterling RK, Sulkowski MS (2004) Hepatitis C virus in the setting of HIV or hepatitis B virus coinfection. Semin Liver Dis 24(Suppl 2):61–68CrossRefGoogle Scholar
  29. 29.
    Liu Z, Hou J (2006) Hepatitis B virus (HBV) and hepatitis C virus (HCV) dual infection. Int J Med Sci 3(2):57–62PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Chemin I, Trepo C (2005) Clinical impact of occult HBV infections. J Clin Virol 34(Suppl 1):S15–S21CrossRefGoogle Scholar
  31. 31.
    Tamori A, Nishiguchi S, Shiomi S, Hayashi T, Kobayashi S, Habu D et al (2005) Hepatitis B virus DNA integration in hepatocellular carcinoma after interferon-induced disappearance of hepatitis C virus. Am J Gastroenterol 100(8):1748–1753CrossRefGoogle Scholar
  32. 32.
    Michalak TI, Mulrooney PM, Coffin CS (2004) Low doses of hepadnavirus induce infection of the lymphatic system that does not engage the liver. J Virol 78(4):1730–1738PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Pal S, Sullivan DG, Kim S, Lai KK, Kae J, Cotler SJ et al (2006) Productive replication of hepatitis C virus in perihepatic lymph nodes in vivo: implications of HCV lymphotropism. Gastroenterology 130(4):1107–1116CrossRefGoogle Scholar
  34. 34.
    Brechot C (2004) Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: old and new paradigms. Gastroenterology 127(5 Suppl 1):S56–S61CrossRefGoogle Scholar
  35. 35.
    Branda M, Wands JR (2006) Signal transduction cascades and hepatitis B and C related hepatocellular carcinoma. Hepatology 43(5):891–902CrossRefGoogle Scholar
  36. 36.
    Thorgeirsson SS, Grisham JW (2002) Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31(4):339–346CrossRefGoogle Scholar
  37. 37.
    Fattovich G, Stroffolini T, Zagni I, Donato F (2004) Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 127(5 Suppl 1):S35–S50CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Chen JG, Zhu J, Parkin DM, Zhang YH, Lu JH, Zhu YR, et al (2006) Trends in the incidence of cancer in Qidong, China, 1978–2002. Int J CancerGoogle Scholar
  39. 39.
    Davila JA, Morgan RO, Shaib Y, McGlynn KA, El-Serag HB (2004) Hepatitis C infection and the increasing incidence of hepatocellular carcinoma: a population-based study. Gastroenterology 127(5):1372–1380CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    El-Serag HB (2004) Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 127(5 Suppl 1):S27–S34CrossRefGoogle Scholar
  41. 41.
    White DL, Thrift AP, Kanwal F, Davila J, El-Serag HB (2017) Incidence of hepatocellular carcinoma in all 50 United States, from 2000 through 2012. Gastroenterology 152(4):812–20 e5CrossRefGoogle Scholar
  42. 42.
    Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118(12):3030–3044CrossRefGoogle Scholar
  43. 43.
    Tradati F, Colombo M, Mannucci PM, Rumi MG, De Fazio C, Gamba G, et al (1998) A prospective multicenter study of hepatocellular carcinoma in italian hemophiliacs with chronic hepatitis C. The study group of the association of Italian hemophilia centers. Blood 91(4):1173–7Google Scholar
  44. 44.
    Liang TJ, Heller T (2004) Pathogenesis of hepatitis C-associated hepatocellular carcinoma. Gastroenterology 127(5 Suppl 1):S62–S71CrossRefGoogle Scholar
  45. 45.
    Block TM, Mehta AS, Fimmel CJ, Jordan R (2003) Molecular viral oncology of hepatocellular carcinoma. Oncogene 22(33):5093–5107CrossRefGoogle Scholar
  46. 46.
    Anzola M (2004) Hepatocellular carcinoma: role of hepatitis B and hepatitis C viruses proteins in hepatocarcinogenesis. J Viral Hepat 11(5):383–393CrossRefGoogle Scholar
  47. 47.
    Guerrieri F, Belloni L, Pediconi N, Levrero M (2016) Pathobiology of Hepatitis B Virus-Induced Hepatocarcingenesis. In: Liaw Y-F, Zoulim F (eds) Hepatitis B virus in Human Diseases. Humana Press, Springer Cham Heidelberg New York Dordrecht London, pp 95–121CrossRefGoogle Scholar
  48. 48.
    Cougot D, Neuveut C, Buendia MA (2005) HBV induced carcinogenesis. J Clin Virol 34(Suppl 1):S75–S78CrossRefGoogle Scholar
  49. 49.
    Zhao LH, Liu X, Yan HX, Li WY, Zeng X, Yang Y et al (2016) Genomic and oncogenic preference of HBV integration in hepatocellular carcinoma. Nat Commun 7:12992PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Mason WS, Gill US, Litwin S, Zhou Y, Peri S, Pop O, et al (2016) HBV DNA integration and clonal hepatocyte expansion in chronic hepatitis B patients considered immune tolerant. Gastroenterology 151(5):986–98 e4CrossRefGoogle Scholar
  51. 51.
    Murakami Y, Saigo K, Takashima H, Minami M, Okanoue T, Brechot C et al (2005) Large scaled analysis of hepatitis B virus (HBV) DNA integration in HBV related hepatocellular carcinomas. Gut 54(8):1162–1168PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Minami M, Daimon Y, Mori K, Takashima H, Nakajima T, Itoh Y et al (2005) Hepatitis B virus-related insertional mutagenesis in chronic hepatitis B patients as an early drastic genetic change leading to hepatocarcinogenesis. Oncogene 24(27):4340–4348CrossRefGoogle Scholar
  53. 53.
    Hsu T, Moroy T, Etiemble J, Louise A, Trepo C, Tiollais P et al (1988) Activation of c-myc by woodchuck hepatitis virus insertion in hepatocellular carcinoma. Cell 55:627–635CrossRefGoogle Scholar
  54. 54.
    Moroy T, Marchio A, Etiemble J, Trepo C, Tiollais P, Buendia M (1986) Rearrangement and enhanced expression of c-myc in hepatocellular carcinoma of hepatitis virus infected woodchucks. Nature 324:276–279CrossRefGoogle Scholar
  55. 55.
    Fourel G, Trepo C, Bougueleret L, Henglein B, Ponzetto A, Tiollais P et al (1990) Frequent activation of N-myc genes by hepadnavirus insertion in woodchuck liver tumours. Nature 347(6290):294–298CrossRefGoogle Scholar
  56. 56.
    Dejean A, Bougueleret L, Grzeschik KH, Tiollais P (1986) Hepatitis B virus DNA integration in a sequence homologous to v-erb-A and steroid receptor genes in a hepatocellular carcinoma. Nature 322:70–72CrossRefGoogle Scholar
  57. 57.
    Wang J, Chenivesse X, Henglein B, Brechot C (1990) Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature 343(6258):555–557CrossRefGoogle Scholar
  58. 58.
    Benhamou Y, Bochet M, Di Martino V, Charlotte F, Azria F, Coutellier A et al (1999) Liver fibrosis progression in human immunodeficiency virus and hepatitis C virus coinfected patients. The multivirc group. Hepatology 30(4):1054–1058CrossRefGoogle Scholar
  59. 59.
    Colin JF, Cazals-Hatem D, Loriot MA, Martinot-Peignoux M, Pham BN, Auperin A et al (1999) Influence of human immunodeficiency virus infection on chronic hepatitis B in homosexual men. Hepatology 29(4):1306–1310CrossRefGoogle Scholar
  60. 60.
    Weinig M, Hakim JG, Gudza I, Tobaiwa O (1997) Hepatitis C virus and HIV antibodies in patients with hepatocellular carcinoma in Zimbabwe: a pilot study. Trans R Soc Trop Med Hyg 91(5):570–572CrossRefGoogle Scholar
  61. 61.
    Tswana SA, Moyo SR (1992) The interrelationship between HBV-markers and HIV antibodies in patients with hepatocellular carcinoma. J Med Virol 37(3):161–164CrossRefGoogle Scholar
  62. 62.
    Sherman M (2006) Optimizing management strategies in special patient populations. Am J Gastroenterology 101(Suppl 1):S26–S31CrossRefGoogle Scholar
  63. 63.
    Puoti M, Bruno R, Soriano V, Donato F, Gaeta GB, Quinzan GP et al (2004) Hepatocellular carcinoma in HIV-infected patients: epidemiological features, clinical presentation and outcome. AIDS 18(17):2285–2293CrossRefGoogle Scholar
  64. 64.
    Kramer JR, Giordano TP, Souchek J, Richardson P, Hwang LY, El-Serag HB (2005) The effect of HIV coinfection on the risk of cirrhosis and hepatocellular carcinoma in U.S. veterans with hepatitis C. Am J Gastroenterol 100(1):56–63CrossRefGoogle Scholar
  65. 65.
    Giordano TP, Kramer JR, Souchek J, Richardson P, El-Serag HB (2004) Cirrhosis and hepatocellular carcinoma in HIV-infected veterans with and without the hepatitis C virus: a cohort study, 1992–2001. Arch Intern Med 164(21):2349–2354CrossRefGoogle Scholar
  66. 66.
    Garcia-Samaniego J, Rodriguez M, Berenguer J, Rodriguez-Rosado R, Carbo J, Asensi V et al (2001) Hepatocellular carcinoma in HIV-infected patients with chronic hepatitis C. Am J Gastroenterol 96(1):179–183CrossRefGoogle Scholar
  67. 67.
    Bruno R, Puoti M, Sacchi P, Filice C, Carosi G, Filice G (2006) Management of hepatocellular carcinoma in human immunodeficiency virus-infected patients. J Hepatol 44(1 Suppl):S146–S150CrossRefGoogle Scholar
  68. 68.
    Smukler AJ, Ratner L (2002) Hepatitis viruses and hepatocellular carcinoma in HIV-infected patients. Curr Opin Oncol 14(5):538–542CrossRefGoogle Scholar
  69. 69.
    Goeser F, Glassner A, Kokordelis P, Wolter F, Lutz P, Kaczmarek DJ et al (2016) HIV mono-infection is associated with an impaired anti-hepatitis C virus activity of natural killer cells. AIDS 30(3):355–363Google Scholar
  70. 70.
    Hyun CB, Coyle WJ (2004) Hepatocellular carcinoma in a patient with human immunodeficiency virus and hepatitis B virus coinfection: an emerging problem? South Med J 97(4):401–406CrossRefGoogle Scholar
  71. 71.
    Chew KW, Bhattacharya D (2016) Virologic and immunologic aspects of HIV-hepatitis C virus coinfection. AIDS 30(16):2395–2404PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Kew MC, Smuts H, Stewart A (2010) Does HIV infection enhance the hepatocarcinogenic potential of chronic hepatitis B virus infection? J Acquir Immune Defic Syndr 53(3):413–414CrossRefGoogle Scholar
  73. 73.
    Soriano V, Puoti M, Peters M, Benhamou Y, Sulkowski M, Zoulim F et al (2008) Care of HIV patients with chronic hepatitis B: updated recommendations from the HIV-Hepatitis B Virus International Panel. AIDS 22(12):1399–1410CrossRefGoogle Scholar
  74. 74.
    Puoti M, Torti C, Bruno R, Filice G, Carosi G (2006) Natural history of chronic hepatitis B in co-infected patients. J Hepatol 44(1 Suppl):S65–S70CrossRefGoogle Scholar
  75. 75.
    Brau N, Fox RK, Xiao P, Marks K, Naqvi Z, Taylor LE, et al (2007) Presentation and outcome of hepatocellular carcinoma in HIV-infected patients: a U.S.-Canadian multicenter study. J Hepatol 47(4):527–37CrossRefGoogle Scholar
  76. 76.
    Dharel N, Sterling RK (2014) Hepatitis B virus-HIV coinfection: forgotten but not gone. Gastroenterol Hepatol (N Y). 10(12):780–788PubMedCentralPubMedGoogle Scholar
  77. 77.
    Iser DM, Lewin SR (2009) The pathogenesis of liver disease in the setting of HIV-hepatitis B virus coinfection. Antivir Ther 14(2):155–164Google Scholar
  78. 78.
    Tanaka T, Imamura A, Masuda G, Ajisawa A, Negishi M, Tanaka S et al (1996) A case of hepatocellular carcinoma in HIV-infected patient. Hepatogastroenterology 43(10):1067–1072Google Scholar
  79. 79.
    Chen CJ, Yang HI, Su J, Jen CL, You SL, Lu SN et al (2006) Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 295(1):65–73CrossRefGoogle Scholar
  80. 80.
    Ohata K, Hamasaki K, Toriyama K, Ishikawa H, Nakao K, Eguchi K (2004) High viral load is a risk factor for hepatocellular carcinoma in patients with chronic hepatitis B virus infection. J Gastroenterol Hepatol 19(6):670–675CrossRefGoogle Scholar
  81. 81.
    Hu J, Nguyen D (2004) Therapy for chronic hepatitis B: the earlier, the better? Trends Microbiol 12(10):431–433CrossRefGoogle Scholar
  82. 82.
    van Zonneveld M, Honkoop P, Hansen BE, Niesters HG, Murad SD, de Man RA et al (2004) Long-term follow-up of alpha-interferon treatment of patients with chronic hepatitis B. Hepatology 39(3):804–810CrossRefGoogle Scholar
  83. 83.
    Akuta N, Suzuki F, Suzuki Y, Sezaki H, Hosaka T, Someya T et al (2005) Favorable efficacy of long-term lamivudine therapy in patients with chronic hepatitis B: an 8-year follow-up study. J Med Virol 75(4):491–498CrossRefGoogle Scholar
  84. 84.
    Liaw YF, Sung JJ, Chow WC, Farrell G, Lee CZ, Yuen H et al (2004) Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 351(15):1521–1531CrossRefGoogle Scholar
  85. 85.
    Matsumoto A, Tanaka E, Rokuhara A, Kiyosawa K, Kumada H, Omata M, et al (2005) Efficacy of lamivudine for preventing hepatocellular carcinoma in chronic hepatitis B: a multicenter retrospective study of 2795 patients. Hepatol Res 32(3):173–184CrossRefGoogle Scholar
  86. 86.
    Shindo M, Hamada K, Oda Y, Okuno T (2001) Long-term follow-up study of sustained biochemical responders with interferon therapy. Hepatology 33(5):1299–1302CrossRefGoogle Scholar
  87. 87.
    Tsuda N, Yuki N, Mochizuki K, Nagaoka T, Yamashiro M, Omura M et al (2004) Long-term clinical and virological outcomes of chronic hepatitis C after successful interferon therapy. J Med Virol 74(3):406–413CrossRefGoogle Scholar
  88. 88.
    Meuleman P, Libbrecht L, Wieland S, De Vos R, Habib N, Kramvis A et al (2006) Immune suppression uncovers endogenous cytopathic effects of the hepatitis B virus. J Virol 80(6):2797–2807PubMedCentralCrossRefPubMedGoogle Scholar
  89. 89.
    Yoon EJ, Hu KQ (2006) Hepatitis C virus (HCV) infection and hepatic steatosis. Int J Med Sci 3(2):53–56PubMedCentralCrossRefPubMedGoogle Scholar
  90. 90.
    Gaslightwala I, Bini EJ (2006) Impact of human immunodeficiency virus infection on the prevalence and severity of steatosis in patients with chronic hepatitis C virus infection. J Hepatol 44(6):1026–1032CrossRefGoogle Scholar
  91. 91.
    Shmagel KV, Saidakova EV, Shmagel NG, Korolevskaya LB, Chereshnev VA, Robinson J et al (2016) Systemic inflammation and liver damage in HIV/hepatitis C virus coinfection. HIV Med 17(8):581–589PubMedCentralCrossRefPubMedGoogle Scholar
  92. 92.
    Rivera MM, Soza A, Jazwinski A, Mi L, Kleiner DE, Zhao X et al (2015) HIV through the looking glass: insights derived from Hepatitis B. J Acquir Immune Defic Syndr 68(2):123–127PubMedCentralCrossRefPubMedGoogle Scholar
  93. 93.
    Page EE, Nelson M, Kelleher P (2011) HIV and hepatitis C coinfection: pathogenesis and microbial translocation. Curr Opin HIV AIDS 6(6):472–477CrossRefGoogle Scholar
  94. 94.
    Li KW, Kramvis A, Liang S, He X, Chen QY, Wang C et al (2017) Higher prevalence of cancer related mutations 1762T/1764A and PreS deletions in hepatitis B virus (HBV) isolated from HBV/HIV co-infected compared to HBV-mono-infected Chinese adults. Virus Res 227:88–95CrossRefGoogle Scholar
  95. 95.
    Sung FY, Lan CY, Huang CJ, Lin CL, Liu CJ, Chen PJ et al (2016) Progressive accumulation of mutations in the hepatitis B virus genome and its impact on time to diagnosis of hepatocellular carcinoma. Hepatology 64(3):720–731CrossRefGoogle Scholar
  96. 96.
    Altavilla G, Caputo A, Lanfredi M, Piola C, Barbanti-Brodano G, Corallini A (2000) Enhancement of chemical hepatocarcinogenesis by the HIV-1 tat gene. Am J Pathol 157(4):1081–1089PubMedCentralCrossRefPubMedGoogle Scholar
  97. 97.
    Pol S, Lebray P, Vallet-Pichard A (2004) HIV infection and hepatic enzyme abnormalities: intricacies of the pathogenic mechanisms. Clin Infect Dis 38(Suppl 2):S65–S72CrossRefGoogle Scholar
  98. 98.
    Revill P, Locarnini S (2016) The basis for antiviral therapy: drug targets, cross-resistance, and novel small nolecule inhibitors. In: Liaw Y-F, Zoulim F (eds) Hepatitis B virus in human diseases. Humana Press, Springer Cham Heidelberg New York Dordrecht London, pp 303–324CrossRefGoogle Scholar
  99. 99.
    Soriano V, de Mendoza C, Pena JM, Barreiro P (2015) Advances in treating drug-resistant hepatitis B virus in HIV-infected patients. Expert Opin Pharmacother 16(2):179–186CrossRefGoogle Scholar
  100. 100.
    Soriano V, Labarga P, de Mendoza C, Pena JM, Fernandez-Montero JV, Benitez L et al (2015) Emerging challenges in managing hepatitis B in HIV patients. Curr HIV/AIDS Rep 12(3):344–352CrossRefGoogle Scholar
  101. 101.
    Sherman KE (2015) Management of the hepatitis B virus/HIV-coinfected patient. Top Antivir Med 23(3):111–114Google Scholar
  102. 102.
    Audsley J, Bent SJ, Littlejohn M, Avihingsanon A, Matthews G, Bowden S et al (2016) Effects of long-term tenofovir-based combination antiretroviral therapy in HIV-hepatitis B virus coinfection on persistent hepatitis B virus viremia and the role of hepatitis B virus quasispecies diversity. AIDS 30(10):1597–1606CrossRefGoogle Scholar
  103. 103.
    Piroth L, Wittkop L, Lacombe K, Rosenthal E, Gilbert C, Miailhes P, et al (2017) Efficacy and safety of direct-acting antiviral regimens in HIV/HCV-coinfected patients—French ANRS CO13 HEPAVIH cohort. J Hepatol 67(1):23–31CrossRefGoogle Scholar
  104. 104.
    Meissner EG (2017) Update in HIV-hepatitis C virus coinfection in the direct acting antiviral era. Curr Opin Gastroenterol 33(3):120–127PubMedCentralCrossRefPubMedGoogle Scholar
  105. 105.
    Mandorfer M, Schwabl P, Steiner S, Scheiner B, Chromy D, Bucsics T et al (2016) Interferon-free treatment with sofosbuvir/daclatasvir achieves sustained virologic response in 100% of HIV/hepatitis C virus-coinfected patients with advanced liver disease. AIDS 30(7):1039–1047CrossRefGoogle Scholar
  106. 106.
    Woreta TA, Sutcliffe CG, Mehta SH, Brown TT, Higgins Y, Thomas DL et al (2011) Incidence and risk factors for steatosis progression in adults coinfected with HIV and hepatitis C virus. Gastroenterology 140(3):809–817CrossRefGoogle Scholar
  107. 107.
    Macias J, Monge P, Mancebo M, Merchante N, Neukam K, Real LM, et al (2016) High frequency of potential interactions between direct-acting antivirals and concomitant therapy in HIV/hepatitis C virus-coinfected patients in clinical practice. HIV Med 18(7):445–451CrossRefGoogle Scholar
  108. 108.
    Khatri A, Dutta S, Dunbar M, Podsadecki T, Trinh R, Awni W et al (2016) Evaluation of Drug-Drug Interactions between Direct-Acting Anti-Hepatitis C Virus Combination Regimens and the HIV-1 Antiretroviral Agents Raltegravir, Tenofovir, Emtricitabine, Efavirenz, and Rilpivirine. Antimicrob Agents Chemother 60(5):2965–2971PubMedCentralCrossRefPubMedGoogle Scholar
  109. 109.
    Mehta N, Cunningham CK, Flynn P, Pepe J, Obaro S, Kapogiannis BG et al (2010) Impaired generation of hepatitis B virus-specific memory B cells in HIV infected individuals following vaccination. Vaccine 28(21):3672–3678PubMedCentralCrossRefPubMedGoogle Scholar
  110. 110.
    van den Berg R, van Hoogstraten I, van Agtmael M (2009) Non-responsiveness to hepatitis B vaccination in HIV seropositive patients; possible causes and solutions. AIDS Rev 11(3):157–164Google Scholar
  111. 111.
    Pollack TM, Trang le TT, Ngo L, Cuong do D, Thuy PT, Colby DJ (2016) Response to hepatitis B vaccination among HIV-infected adults in Vietnam. J Virus Erad 2(2):102–6Google Scholar
  112. 112.
    Njom Nlend AE, Nguwoh PS, Ngounouh CT, Tchidjou HK, Pieme CA, Otele JM et al (2016) HIV-infected or -exposed children exhibit lower immunogenicity to hepatitis B vaccine in Yaounde, Cameroon: an appeal for revised policies in Tropical settings? PLoS ONE 11(9):e0161714PubMedCentralCrossRefPubMedGoogle Scholar
  113. 113.
    Lopes VB, Hassing RJ, de Vries-Sluijs TE, El Barzouhi A, Hansen BE, Schutten M et al (2013) Long-term response rates of successful hepatitis B vaccination in HIV-infected patients. Vaccine 31(7):1040–1044CrossRefGoogle Scholar
  114. 114.
    Whitaker JA, Rouphael NG, Edupuganti S, Lai L, Mulligan MJ (2012) Strategies to increase responsiveness to hepatitis B vaccination in adults with HIV-1. Lancet Infect Dis 12(12):966–976PubMedCentralCrossRefPubMedGoogle Scholar
  115. 115.
    Stapleton JT, Williams CF, Xiang J (2004) GB virus type C: a beneficial infection? J Clin Microbiol 42(9):3915–3919PubMedCentralCrossRefPubMedGoogle Scholar
  116. 116.
    Berzsenyi MD, Bowden DS, Roberts SK (2005) GB virus C: insights into co-infection. J Clin Virol 33(4):257–266CrossRefGoogle Scholar
  117. 117.
    Tenckhoff S, Kaiser T, Bredeek F, Donfield S, Menius E, Lail A et al (2012) Role of GB virus C in HIV-1-infected and hepatitis C virus-infected hemophiliac children and adolescents. J Acquir Immune Defic Syndr 61(2):243–248CrossRefGoogle Scholar
  118. 118.
    Xiang J, Wunschmann S, Diekema DJ, Klinzman D, Patrick KD, George SL et al (2001) Effect of coinfection with GB virus C on survival among patients with HIV infection. N Engl J Med 345(10):707–714CrossRefGoogle Scholar
  119. 119.
    Tillmann HL, Heiken H, Knapik-Botor A, Heringlake S, Ockenga J, Wilber JC et al (2001) Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345(10):715–724CrossRefGoogle Scholar
  120. 120.
    Xiang J, George SL, Wunschmann S, Chang Q, Klinzman D, Stapleton JT (2004) Inhibition of HIV-1 replication by GB virus C infection through increases in RANTES, MIP-1alpha, MIP-1beta, and SDF-1. Lancet 363(9426):2040–2046CrossRefGoogle Scholar
  121. 121.
    Revill P, Testoni B, Locarnini S, Zoulim F (2016) Global strategies are required to cure and eliminate HBV infection. Nat Rev Gastroenterol Hepatol 13(4):239–248CrossRefGoogle Scholar
  122. 122.
    Deeks SG, Lewin SR, Ross AL, Ananworanich J, Benkirane M, Cannon P et al (2016) International AIDS Society global scientific strategy: towards an HIV cure 2016. Nat Med 22(8):839–850PubMedCentralCrossRefPubMedGoogle Scholar
  123. 123.
    Gjaerde LI, Shepherd L, Jablonowska E, Lazzarin A, Rougemont M, Darling K et al (2016) Trends in incidences and risk factors for hepatocellular carcinoma and other liver events in HIV and hepatitis C virus-coinfected individuals from 2001 to 2014: a multicohort study. Clin Infect Dis 63(6):821–829PubMedCentralCrossRefPubMedGoogle Scholar
  124. 124.
    Peters L, Klein MB (2015) Epidemiology of hepatitis C virus in HIV-infected patients. Curr Opin HIV AIDS 10(5):297–302CrossRefGoogle Scholar
  125. 125.
    Klein MB, Althoff KN, Jing Y, Lau B, Kitahata M, Lo Re V, 3rd, et al (2016) Risk of end-stage liver disease in HIV-viral hepatitis coinfected persons in North America from the early to modern antiretroviral therapy Eras. Clin Infect Dis 63(9):1160–7Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyThe Pennsylvania State University College of MedicineHersheyUSA

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