Generic placeholder image

Current HIV Research

Editor-in-Chief

ISSN (Print): 1570-162X
ISSN (Online): 1873-4251

Research Article

Comparison of Demographic, Epidemiological, Immunological, and Clinical Characteristics of Patients with HIV Mono-infection Versus Patients Co-infected with HCV or/and HBV: A Serbian Cohort Study

Author(s): J. Ranin, D. Salemovic, B. Brmbolic, J. Marinkovic, I. Boricic, Pavlovic I. Pesic, S. Zerjav, M. Stanojevic* and D. Jevtovic

Volume 16, Issue 3, 2018

Page: [222 - 230] Pages: 9

DOI: 10.2174/1570162X16666180717115614

Open Access Journals Promotions 2
Abstract

Objective: The study aimed to correlate the status of hepatitis C (HCV) and hepatitis B virus (HBV) co-infection in patients with human immunodeficiency virus (HIV) infection with clinical and demographic data prior to starting highly active antiretroviral therapy (HAART) and assess the impact of HCV and HBV co-infection on the natural history of HIV infection.

Patients and Methods: The study involved a total of 836 treatment-naive patients with available serological status for HBV and HCV at the point of therapy initiation. Patients were stratified into four groups: HIV mono-infection, HIV/HCV, HIV/HBV, and HIV/HCV/HBV co-infection. Demographic, epidemiological, immunological and clinical characteristics were analyzed in order to assess the possible impact of HCV and HBV co-infection on HIV - related immunodeficiency and progression to AIDS.

Results: The prevalence of HCV and HBV co-infection in our cohort was 25.7% and 6.3%, respectively. Triple HIV/HCV/HBV infection was recorded in 1.7% of the patients. In comparison with those co-infected with HCV, patients with HIV mono-infection had lower levels of serum liver enzymes activity and higher CD4 cell counts, and were less likely to have CD4 cell counts below100 cells/µL and clinical AIDS, with OR 0.556 and 0.561, respectively. No difference in the development of advanced immunodeficiency and/or AIDS was recorded between patients with HIV monoinfection and those co-infected with HBV, or both HCV/HBV.

Conclusion: HIV/HCV co-infection was found to be more prevalent than HIV/HBV co-infection in a Serbian cohort. Co-infection with HCV was related to more profound immunodeficiency prior to therapy initiation, reflecting a possible unfavorable impact of HCV on the natural history of HIV infection.

Keywords: Viral hepatitis, HIV co-infection, therapy-naive patients, immunodeficiency, HIV mono-infection, HAART.

Graphical Abstract
[1]
Matthews PC, Geretti AM, Goulder PJ, Klenerman P. Epidemiology and impact of HIV co-infection with hepatitis B and hepatitis C viruses in Sub-Saharan Africa. J Clin Virol 2014; 61: 20-33.
[2]
Petty LA, Steinbeck JL, Pursell K, Jensen DM. Human immunodeficiency virus and co-infection with hepatitis B and C. Infect Dis Clin North Am 2014; 28: 477-99.
[3]
Konstantinou D, Deutsch M. The spectrum of HBV/HCV co-infection: epidemiology, clinical characteristics, viral interactions and management. Ann Gastroenterol 2015; 28: 221-8.
[4]
Peters L, Mocroft A, Lundgren J, Grint D, Kirk O, Rockstroh J. HIV and hepatitis C co-infection in Europe, Israel and Argentina: a EuroSIDA perspective. BMC Infect Dis 2014; 14(Suppl. 6): S6-S13.
[5]
Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol 2006; 44(Suppl. 1): S6-9.
[6]
Zhou YH, Yao ZH, Liu FL, et al. High prevalence of HIV, HCV, HBV and co-infection and associated risk factors among injecting drug users in Yunnan province, China. PLoS One 2012; 7: e42937.
[7]
Alberti A, Clumeck N, Collins S, et al. Short statement of the first European consensus conference on the treatment of chronic hepatitis B and C in HIV co-infected patients. J Hepatol 2005; 42: 615-24.
[8]
Nyrenda M, Beadsworth MB, Stephany P, et al. Prevalence of infection with hepatitis B and C virus and coinfection with HIV in medical inpatients in Malawi. J Infect 2008; 57: 72-7.
[9]
Parvez MK. HBV and HIV co-infection impact on liver pathobiology and therapeutic approaches. World J Hepatol 2015; 7: 121-6.
[10]
Ingliz P, Rockstroh JK. Natural history of liver disease and effect of hepatitis C virus on HIV disease progression. Curr Opin HIV AIDS 2015; 10: 303-8.
[11]
Lin W, Weinberg EM, Tai AW, et al. HIV increases HCV replication in a TGF-beta1-dependent manner. Gastroenterology 2008; 134: 803-11.
[12]
Balasubramanian A, Ganju RK, Groopman JE. Signal transducer and activator of transcriptor factor 1 mediates apoptosis induced by hepatitis c virus and HIV envelope proteins in hepatocytes. J Infect Dis 2006; 194: 670-81.
[13]
Kim JH, Psevdos G Jr, Sharp V. Five-year review of HIV-hepatitis B virus (HBV) co-infected patients in a New York City AIDS center. J Korean Med Sci 2012; 27: 830-3.
[14]
Mastroianni CM, Lichtner M, Moscia C, Zuccalo P, Vullo V. Molecular mechanisms of liver fibrosis in HIV/HCV co-infection. Int J Mol Sci 2014; 15: 9184-208.
[15]
Soriano V, Puoti M, Sulkowski M, et al. Care of patients with hepatitis C and HIV co-infection. AIDS 2004; 18: 1-12.
[16]
Kourtis AP, Bulterys M, Hu DJ, Jamieson DJ. HIV-HBV co-infection-a global challenge. N Engl J Med 2012; 366: 1749-52.
[17]
Sulkowski MS, Mehta SH, Torbenson MS, et al. Rapid fibrosis progression among HIV/hepatitis C virus-co-infected adults. AIDS 2007; 21: 2209-16.
[18]
Lincoln D, Petoumenos K, Dore GJ. HIV/HBV and HIV/HCV co-infection, and outcomes following highly active antiretroviral therapy. HIV Med 2003; 4: 241-9.
[19]
Bonacini M, Louie S, Bzowej N, Wohl AR. Survival in patients with HIV infection and viral hepatitis B or C: a cohort study. AIDS 2004; 18: 2039-45.
[20]
Rotman Y, Liang J. Co-infection with hepatitis C virus and human immunodeficiency virus: virological, immunological and clinical outcomes. J Virol 2009; 83: 7366-74.
[21]
Taye S, Lakew M. Impact of hepatitis C viruses co-infection on HIV patients before and after highly active antiretroviral therapy: an immunological and clinical chemistry observation, Addis Ababa, Ethiopia. BMC Immunol 2013; 14: 23.
[22]
Greub G, Ledergerber B, Battegay M, et al. Clinical progression, survival, and immune recovery during antiretroviral therapy in patients with HIV-1 and hepatitis C virus co-infection: the Swiss HIV Cohort Study. Lancet 2000; 356: 1800-5.
[23]
De Luca A, Bugarini R, Lepri AC, et al. Co-infection with hepatitis viruses and outcome of initial antiretroviral regimens in previously naive HIV-infected subjects. Arch Intern Med 2002; 162: 2125-32.
[24]
Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWRM Reccom Rep 1992; 41(RR-17): 1-19.
[25]
Prentice RL, Pyke R. Logistic disease incidence models and case-control studies. Biometrica 1979; 63: 403-11.
[26]
Batut MJ. Ministry of Health of Serbia and Institute of Public Health of Serbia. Overview of HIV epidemic in Serbia. 2016; 3-26.
[27]
EACS. ART of HIV positive persons. In: EACS Guidelines version 8.1, October 2016: 7-31.
[28]
Mills FP, Ford N, Nachega JB, et al. Earlier initialization of highly active antiretroviral therapy is associated with long-term survival and is cost-effective: findings from a deterministic model of a 10-year Ugandan cohort. J Acquir Immune Defic Syndr 2012; 61: 364-9.
[29]
Daw MA, Shabash A, El-Bouzedi A, Dau AA. Seroprevalence of HBV, HCV&HIV co-infection and risk factors analysis in Tripoli-Libya. PLoS One 2014; 9: e98793.
[30]
Muriuki BM, Gicheru MM, Wachira D, Nyamache AK, Khamadi SA. Prevalence of hepatitis B and C viral co-infections among HIV-1 infected individuals in Nairobi, Kenya. BMC Res Notes 2013; 6: 363-8.
[31]
Rosenthal E, Poiree M, Pradier C, et al. Mortality due to hepatitis C – related liver disease in HIV – infected patients in France (Mortavic 2001 study). AIDS 2003; 17: 1803-9.
[32]
Kim YA, Onofrey S, Church RD. An epidemiologic update on hepatitis C infection in persons living with or at risk of HIV infection. J Infect Dis 2013; 207(Suppl. 1): S1-6.
[33]
Butt Z, Grady S, Wilkins M, et al. Spatial epidemiology of HIV-hepatitis co-infection in the State of Michigan: a cohort study. Infect Dis (Lond) 2015; 47: 852-61.
[34]
Prussing C, Chan C, Pinchoff J, et al. HIV and viral hepatitis co-infection in New York City, 2000-2010: prevalence and case characteristics. Epidemiol Infect 2015; 143: 1408-16.
[35]
Ranjbar R, Davari A, Izadi M, Jonaidi N, Alovian SM. HIV/HBV co-infection: epidemiology, natural history and treatment. Iran Red Crescent Med J 2011; 13: 855-62.
[36]
Oliveira MP, Matos MA, Silva AM, et al. Prevalence, risk behaviors, and virological characteristics of hepatitis B virus infection in a group of men who have sex with men in Brazil: results from a respondent-driven sampling survey. PLoS One 2016; 11: e0160916.
[37]
Saravanan S, Velu V, Kumarasamy N, et al. Coinfection of hepatitis B and hepatitis C virus in HIV-infected patients in south India. World J Gastroenterol 2007; 13: 5015-20.
[38]
Melhem NM, Rahhal N, Charide R, Kreidieh K, El-Khatib R. Human immunodeficiency virus and viral hepatitis among high-risk groups: Understanding the knowledge gap in the Middle East and North Africa Region. World J Hepatol 2015; 7: 2619-30.
[39]
Mathers BM, Degenhardt L, Bucello C, Lemon J, Wiessing L, Hickman M. Mortality among people who inject drugs: A systematic review and meta-analysis. Bull World Health Organ 2013; 91: 102-23.
[40]
Robbins JL, Wenger L, Lorvick J, Shiboski C, Kral AH. Health and oral health care needs and health care-seeking behavior among homeless injection drug users in San Francisco. J Urban Health 2010; 87: 920-30.
[41]
Nambiar D, Stoove M, Hickman M, Dietze P. A prospective cohort study of hospital separations among people who inject drugs in Australia: 2008-2013. BMJ Open 2017; 7: e014854.
[42]
Jones DL, Waldrop-Valverde D, Gonzalez P, et al. Mental health in HIV seronegative and seropositive IDUs in South Florida. AIDS Care 2010; 22: 152-8.
[43]
Heath AJ, Kerr T, Ti L, et al. Healthcare avoidance by people who inject drugs in Bangkok, Thailand. J Public Health (Oxf) 2016; 38: e301-8.
[44]
Dorrucci M, Pezzoti P, Phillips AN, Lepri AC, Rezza G. Co-infection of hepatitis C virus with human immunodeficiency virus and progression to AIDS. Italian Seroconversion Study. J Infect Dis 1995; 172: 1503-8.
[45]
Wright TL, Hollander H, Pu X, et al. Hepatitis C in HIV-infected patients with and without AIDS: prevalence and relationship to patient survival. Hepatology 1994; 20: 1152-5.
[46]
Sulkowski MS, Moore RD, Mehta SH, Chaisson RE, Thomas DL. Hepatitis C and progression of HIV disease. JAMA 2002; 288: 199-206.
[47]
Potter M, Odneyungbo A, Yang H, Saeed S, Klein MB. Impact of hepatitis C viral replication on CD4 T-lymphocyte progression in HIV-HCV co-infection before and after antiretroviral therapy. AIDS 2010; 24: 1857-65.
[48]
Haydon GH, Flegg PJ, Blair CS, Brettle RP, Burns SM, Hayes PC. The impact of chronic hepatitis C virus infection on HIV diseases and progression in intravenous drug users. Eur J Gastroenterol Hepatol 1998; 10: 495-9.
[49]
Operskalski EA, Kovacs A. HIV/HCV co-infection: pathogenesis, clinical complications, treatment, and new therapeutic technologies. Curr HIV/AIDS Rep 2011; 8: 12-22.
[50]
Zhang X, Xu J, Peng H, et al. HCV co-infection associated with slower disease progression in hiv-infected former plasma donors naive to art. PloS One 3 2008; 12: e3992.
[51]
Daar E, Lynn H, Donfield S. HCV load is associated with HIV-1 disease progression in hemophiliacs. J Infect Dis 2001; 183: 589-95.
[52]
Sansonno D, Lotesoriere C, Cornacchiuolo V, et al. Hepatitis C virus infection involves CD34+ hematopoetic progenitor cells in hepatitis C virus chronic carriers. Blood 1998; 92: 3328-37.
[53]
Lerat H, Shimizu YK, Lemon SM. Cell type-specific enhancement of hepatitis C virus internal ribosome entry site-directed translation due to 5′ non-translated region substitutions selected during passage of virus in lymphoblastoid cells. J Virol 2000; 74: 7024-31.
[54]
Taya N, Torimoto Y, Shindo M, Hirai K, Hasebe C, Kohgo Y. Fas-mediated apoptosis of peripheral blood mononuclear cells in patients with hepatitis C. Br J Haematol 2000; 110: 89-97.
[55]
Alhetheel A, Albarrag A, Shakoor Z, et al. Increased spontaneous programmed cell death is associated with impaired cytokine secretion in Peripheral Blood Mononuclear Cells from Hepatitis C Virus-Positive Patients. Viral Immunol 2017; 30: 283-7.
[56]
El-Bendary M, Hawas S, El-Hammady D, Al-Hadidy AH, Eldegla H. Profile of expression of certain markers of apoptosis in chronic hepatitis C and hepatitis B patients in an Egyptian population. Arch Virol 2016; 161: 2369-78.
[57]
Nikolopoulos GK, Paraskevis D, Hatzitheodoron E, et al. Impact of hepatitis B infection on the progression of AIDS and mortality in HIV-infected individuals: a cohort study and meta-analysis. Clin Infect Dis 2009; 48: 1763-71.
[58]
Tsuchiya N, Pathipovanich PA, Rojana W, Wichukchinda N, Kogo I. Chronic hepatitis B and C co-infection increased all cause mortality in HAART-naive HIV patients in nothern Thailand. Epidemiol Infect 2013; 141: 1840-8.
[59]
Petty LA, Steinbeck JL, Pursell K, Jensen DM. Human immunodeficiency virus and co-infection with hepatitis B and C. Infect Dis Clin North Am 2014; 28: 477-99.
[60]
Yan Q, Lan YH, Huang YX, et al. Hepatitis B virus replication is upregulated in proliferated peripheral blood lymphocytes. Mol Med Rep 2016; 13: 3581-7.
[61]
Xu CL, Hao YH, Lu YP, et al. Upregulation of toll-like receptor 4 on T cells in PBMCs is associated with disease aggravation of HBV-related acute-on-chronic liver failure. J Huazhong Univ Sci Technolog Med Sci 2015; 35: 910-5.
[62]
Lee Z, Nishikawa S, Goa S, et al. Detection of hepatitis B virus (HBV) genomes and HBV drug resistant variants by deep sequencing analysis of HBV genomes in immune cell subsets of HBV mono-infected and/or human immunodeficiency virus type-1 (HIV-1) and HBV co-infected individuals. PLoS One 2015; 10: e0137568.
[63]
Loustaud-Ratti V, Wagner A, Carrier P, et al. Distribution of total DNA and cccDNA in serum and PBMCs may reflect the HBV immune status in HBsAg+ and HBsAg- patients co-infected or not with HIV or HCV. Clin Res Hepatol Gastroenterol 2013; 37: 373-83.
[64]
Gomez-Gonzalo M, Carretero M, Rullas J, et al. The hepatitis B virus X protein induces HIV-1 replication and transcription in synergy with T-cell activation signals. J Biol Chem 2006; 38: 35435-43.
[65]
Chun HM, Roediger PM, Hullsiek HK, Chloe LT, Agon KB, et al. Hepatitis B virus co-infection negatively impacts HIV outcomes in HIV seroconverters. J Infect Dis 2012; 205: 185-93.
[66]
Tsai MS, Chang SY, Lo YC, Yang CJ. Sun Hy et al. Hepatitis B virus (HBV) co-infection accelerates immunologic progression in patients with primary HIV infection in an area of hyperendemicity for HBV infection. J Infect Dis 2013; 208: 1184-6.
[67]
Ockenga J, Tillmann H, Trautwein C, et al. Hepatitis B and C in HIV-infected patients. Prevalence and prognostic value. J Hepatol 1997; 27: 18-24.
[68]
Konopnicki D, Mocroft A, de Wit S, et al. Hepatitis B and HIV: prevalence, AIDS progression, response to highly active antiretroviral therapy and increased mortality in the EuroSIDA cohort. AIDS 2005; 19: 593-601.
[69]
Sinicco A, Raiteri R, Sciandra M, et al. Co-infected and superinfection of hepatitis B virus in patients infected with immunodeficiency virus: no evidence of faster progression to AIDS. Scand J Infect Dis 1997; 29: 111-5.
[70]
Ogwu-Richard SO, Ojo DA, Akingbade OA, Okonko IO. Triple positivity of HBsAg, anti-HCV antibody, and HIV and their influence on CD4+ lymphocyte levels in the highly HIV infected population of Abeokuta, Nigeria. Afr Health Sci 2015; 15: 719-27.
[71]
Adekunle AE, Oladimeji AA, Temi AP, Adeseye AI, Akinyeye OA, Taiwo RH. Baseline CD4+ T lymphocyte cell counts, hepatitis B and C viruses seropositivity in adults with human immunodeficiency virus infection at a tertiary hospital in Nigeria. Pan Afr Med J 2011; 9: 6-11.
[72]
Kallas E, Huik K, Turk S, et al. T cell distribution in relation to hiv/hbv/hcv co-infections and intravenous drug use. Viral Immunol 2016; 29: 464-70.
[73]
Chu CJ, Lee SD. Hepatitis B virus/hepatitis C virus co-infection: epidemiology, clinical features, viral interactions and treatment. J Gastroenterol Hepatol 2008; 23: 512-20.
[74]
Sagnelli E, Pasquale G, Coppola N, et al. Influence of chronic HBV-HCV concurrent infection on liver histology. Infection 2004; 32: 144-8.
[75]
Filippini P, Coppola N, Pisapia R, et al. Virological and clinical aspects of hbv-hcv co-infection in hiv positive patients. J Med Virol 2007; 79: 1679-85.
[76]
Siljic M, Salemovic D, Jevtovic Dj, et al. Molecular typing of the local HIV-1 epidemic in Serbia. Infect Genet Evol 2013; 19: 378-85.
[77]
Stanojevic M, Alexiev I, Beshkov D, et al. HIV‑1 molecular epidemiology in the Balkans: a melting pot for high genetic diversity. AIDS Rev 2012; 14: 28-36.
[78]
Jevtovic Dj, Salemovic D, Ranin J, Pesic I, Zerjav S, Djurkovic-Djakovic O. Long-term survival of HIV-infected patients treated with highly active antiretroviral therapy in Serbia and Montenegro. HIV Med 2007; 8: 75-9.
[79]
Jevtovic Dj, Dragovic G, Salemovic D, et al. Treatment outcome of HAART-treated patients in a resource-limited setting: the Belgrade Cohort Study. Biomed Pharmacother 2014; 68: 391-5.
[80]
Jevtovic Dj, Ranin J, Salemovic D, et al. The prevalence and risk of hepatitis flares in a Serbian cohort of HIV and HCV co-infected patients treated with HAART. Biomed Pharmacother 2008; 62: 21-5.
[81]
Salemovic D, Pesic-Pavlovic I, Jevtovic Dj, et al. Intravenous drug use – an independent predictor for HCV genotypes 3 and 4 infection among HIV/HCV co-infected patients. Arch Med Sci 2017; 13: 652-8.

© 2024 Bentham Science Publishers | Privacy Policy