Cite this article:
Taiwo Modupe Balogun, Samuel Emmanuel, Emmanuel Folorunso Ojerinde. HIV, Hepatitis B and C virusesí coinfection among patients in a Nigerian tertiary hospital.
The Pan African Medical Journal. 2012;12:100
Key words: HIV, Hepatitis B, Hepatitis C, coinfections, Nigeria
Permanent link: http://www.panafrican-med-journal.com/content/article/12/100/full
Received: 15/08/2011 - Accepted: 09/03/2012 - Published: 08/08/2012
© Taiwo Modupe Balogun et al. The Pan African Medical Journal - ISSN 1937-8688. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
HIV, Hepatitis B and C virusesí coinfection among patients in a Nigerian tertiary hospital
Taiwo Modupe Balogun1, &, Samuel Emmanuel1, Emmanuel Folorunso Ojerinde1
1Lagos State University Teaching Hospital
& Corresponding author
Taiwo Modupe Balogun, P O Box 10315, G PO, Bank Anthony Way, Ikeja, Lagos, Nigeria
Hepatitis B virus (HBV) and hepatitis C virus (HCV) infections cause chronic hepatitis, cirrhosis and hepatocellular carcinoma, all of which are of serious public health concern . There is a heavy burden of HIV-HBV and HIV- HCV co infections in many regions of the developing world , Nigeria inclusive [3,4]. Available data suggest 15-60% of the normal population in many African countries may be positive for one or more of the serological markers of hepatitis B virus . The high prevalence of HBV infection in this region is thought to be due to horizontal transmission during childhood . Individuals co infected with HIV and HBV are more likely to develop chronic hepatitis B and are at increased risk for liver related mortality . Hepatitis C virus is the major cause of nonA, nonB hepatitis worldwide . Hepatitis C co infection has been found to be more common in HIV+ve individuals and is associated with an increased mortality and renal morbidity . In persons with HIV, HCV prevalence is estimated to be approximately 50% in the USA .
†Recently, co infection between hepatitis C virus and HIV have been associated with rapid decline in the CD4 count, rapid progression of HIV infection and with increased morbidity and mortality . Hepatitis co-infection with HIV accelerates disease progression in both HCV and HBV and also increases the risk of antiretroviral drug associated hepatotoxicity . With an increase use and accessibility of highly active antiretroviral therapy among HIV positive patients in sub Saharan Africa, co-infection with these viruses could contribute significantly to continuing morbidity and mortality among this group of patients over the coming years.
†The significant advancing in HIV management and survival have led to the recognition of chronic hepatitis as the pre eminent co morbid illness which now accounts for the majority of non AIDS related deaths in this population. To define the magnitude of this burden, we have examined the prevalence and risk of co infection with HBVand HCV among Nigerians with HIV infection. The result of this study would provide the baseline for future larger studies.
After obtaining ethical approval from the Lagos State University Teaching Hospital (LASUTH) health research ethics committee, a cross-sectional study was conducted in March - August 2006. The study population was adult Nigerian HIV infected patients attending the antiretroviral therapy clinics. Informed consent was obtained from study subjects before specific structured questionnaires were administered to capture demographic data and risk factors which predispose to acquisition of both HBV and HCV co infections.
†About 5millilitres of blood was collected from each patient and control subjects by venepuncture. The sera from the blood samples were separated and stored at -20oC until tested. Samples were brought to room temperature prior to testing and analyzed according to manufacturerís recommendations at the Blood Screening Centre of LASUTH.
†Each serum was analyzed for the presence of HBsAg and anti-HCV using commercially available 4th generation Enzyme Limited Immuno Assay (ELISA) kits (Dialab, Austria) with 99.87% specificity and100%sensitivity. The diagnosis of HIV was made in patients using WHO approved Determine1/2 very rapid kits with100% sensitivity and 99.6% specificity. Positive serostatus was confirmed with ELISA based Immunocomb I &II comb firm kits (Orgenics, Israel) The data were analyzed using a statistical package for social sciences (Version 9, SPSS). Chi-square test was used to assess the significance of differences among groups. A value of less than or equal to 0.001 was considered significant in all statistical comparisons.
One hundred and two HIV infected patients comprising 32 (31.4%) males and 70 (68.6%) females with M: F ratio of 1:2.2 was enrolled for this study. Table 1 shows the dual presence of HBsAg and anti-HCV in 4(3.9%)study patients while 29 (28.4%) tested positive for HBsAg and 15 (14.7%) for anti HCV. The control subjects have a much lower prevalence of 22(6.0%) and 3(0.8%) for HBsAg and anti-HCV respectively while dual presence of HBsAg and ant-HCV was 0% prevalence. The difference in prevalence of hepatitis between the control and subjects is statistically significant p< 0.001 In Figure 1, there are more female patients in the younger age group with a peak at 30-34years while the males are older with a peak in the 55- 59 years age group. The age range of the patients is 20-79 with a mean of 38years. More male patients 16(50%) have hepatitis co infection than the female32 (45.7%). The difference is however not statistically significant p>0.001 HIV/HBV co infected patients were more likely to be male12 (75%) while HIV/HCV co infected patients were more likely to be female12 (37.5%). In Table 2, triple infection with HIV/HBV/HCV was higher among the female 3 (9.4%) than the male patients 1 (6.3%).The difference is not statistically significant p>0.001.
Our study examined the prevalence of HBsAg and anti-HCV among HIV infected patients and healthy HIV negative blood donors. We observed HBsAg and anti-HCV positivity of 29 (28.4%) and 15(14.7%) respectively among HIV infected patients. Among healthy HIV negative blood donor controls, we observed HBsAg and anti-HCV prevalence of 22(6.0%) and 3(0.8%) respectively. The high prevalence of HBsAg 29(28.4%) and anti- HCV 15 (14.7%) among HIV infected patients in this study is comparable with reports by Forbi et al in North Central Nigeria , South Africa cohort , Senegal  and France . The prevalence of HBsAg 3(6.0%) among the control blood donors in this study is comparable with reported figures from previous studies in Lagos 6.9 %  Ile-Ife7.3 % , Nigeria. The observed HIV/HBV co infection prevalence(28.4%) in this study is comparable with previous reported high figures in different parts of Nigeria; (Keffi 20.6% , Jos28.7% , Ilorin30.4% , Kano70.5% ) and India 33.8% . Some previous reports of HIV/HBV co infection from South Africa 6% , Nigeria (Maiduguri15% , Lagos 9.2% , Niger Delta9.7%  and Thailand 8.7%  are however lower than observed figures in this study. Varying sample size, test kit sensitivity and specificity may be responsible for the differences in prevalence figures in this group of patients.
†The prevalence of HBV/HIV co infection was found to be higher among male study subjects12 (37.5%) than females 17(24.3%) in this study p=0.001. The difference is not statistically significant. This finding is compatible with previous reports from Jos, North Central Nigeria  and India . This observation may have been accounted for by the fact that men are more likely to have multiple sex partners and also practice unprotected sex in our polygamous setting. We also observed a significantly higher prevalence of HCV antibody among HIV infected patients as compared to HIV negative blood donors (14.7%vs0.8%respectively), p< 0.001 . The difference is statistically significant. The reason in difference may be due to shared modes of transmission of both viruses in the study patients. This observed high prevalence (14.7%) of HCV/HIVcoinfection among study patients is comparable with reports of previous studies in Nigeria (Keffi11.1%  Abuja 8.2% ), South Africa 13.4% , France 17% , and San Francisco 11.7% . We also found that the prevalence of HIV/HCV co infection was higher among the female patients 12 (37.5%) than the male 3 (18.8%), p>0.001. The difference is however not statistically significant. This observation is at par with a previous study by Lesi et al , but at variance with other reports [4, 25] with findings of older males being more co- infected in Nigeria. This higher rate of HIV/HCV co infection among females may have been accounted for by the fact that women of all ages are more likely than men to become infected with HIV and HCV during unprotected vaginal intercourse. We have observed that 4(3.9%) of the study patients have triple co infection with HIV/HBV/HCV in this study. Previous prevalence reports of triple co infection in this group of study subjects vary from Keffi7.2% , Ibadan 1%  in Nigeria, Kenya 0.3%  and France 1.6% . The results in this study show that the prevalence of HBV and HCV in the population of persons living with HIV in Nigeria is higher than found in the HIV negative population. In conclusion, there is therefore a higher risk of HBV and HCV co-infections among HIV infected patients compared to HIV negative blood donors in this study p<0.001. This high co infection rates among the study subjects demonstrate a correlation between these viral infections which could influence evolution of HIV, HBV and HCV diseases.
We recommend that HIV positive patients should be routinely screened for HBV&HCV markers before initiation of highly active antiretroviral therapy as this practice would guide correct choice of drug combination. This would in turn reduce morbidity and mortality from antiretroviral drug associated hepatotoxicity among these patients.
T M Balogun-Lead author with the following contributions: Physician in charge of study subjects and controls, Selection of study participants, Supervision of sample collection, transportation, storage and screening, literature search, Preparation and proofreading of manuscript, data analysis Samuel Emmanuel: supervision of sample separation, storage and screening, presentation of screening results/data. EF Ojerinde-co author: statistical analysis. All the authors have read and approved the final version of the manuscript.
There is no monetary reward or gratification of any sort involved in the conduct and reporting of this research work.
We thank the management of Strides Vital Nigeria Limited for funding this study. We also appreciate the resident doctors and nurses of the Haematology Department, LASUTH for their support when blood samples were collected.
Table 1: The prevalence and risk of HBsAg and Anti- HCV among HIV Patients and Controls
Table 2: The gender prevalence of HBsAg and Anti-HCV among study subjects
Figure 1: illustrates age and sex distribution of patients
- Shaw TA, Stiffel L, Chronic hepatitis. In; Mandell GL Bennett JE, Dolin R, eds. Principles and Practice of infectious Disease. 5th ed.
- Cooper CL, Mills E, WabwireBO, Ford N, Olupot-Olupot P. Chronic viral hepatitis may diminish the gains of HIV antiretroviral therapy in Sub-Saharan Africa. Int J Infect Dis. 2009 May; 13(3):302-6. This article on PubMed
- Ola SO, OtegbayoGN, Odaibo OD, Olaleye OD, Olubuyide O. Serum Hepatitis C virus and hepatitis B surface antigenaemia in Nigerian patients with acute Icteric hepatitis. West Afr J Med. 2002 Jul-Sep; 21(3):215-7. This article on PubMed
- Forbi JC, Gabadi S, Alabi R, Iperepolu HO, Pam CR, Entonu PE, Agwale SM. The role of triple infection with hepatitis Bvirus, hepatitis C virus, and human immunodeficiency virus(HIV) type -1 on CD4+ lymphocyte levels in the highly HIV infected population of North Central Nigeria. Mem Inst Oswaldo Cruz. 2007 Jun; 102(4):535-7. This article on PubMed
- Bojuwoye BJ. The burden of viral hepatitis in Africa. West Afr J Med. 1997 Oct-Dec; 16(4):198-203. This article on PubMed
- ThioCL, Sea berg EC, Skolasky R Jr et al. HIV-1 hepatitis B virus and risk of liver related mortality in Multicentre Cohort Study (MACS). Lancet. 2002; 360:1921-1926. This article on PubMed
- Centers for Disease Control and Prevention (CDC). Recommendations for the Prevention and Control of Hepatitis C virus (HCV) infection and HCV related chronic disease. MMWR Recomm Rep. 1998 Oct 16; 47(RR-19):1-39. This article on PubMed
- Parboosing R, Paruk I, Lalloo UG. Hepatitis C virus seropositivity in a South African cohort of HIVinfected, ARV naive patients is associated with renal insufficiency and increased mortality. J Med Virol. 2008 Sep; 80(9):1530-6. This article on PubMed
- Dodig M. Hepatitis C and human immunodeficiency virus confections. J Clin Gastroenterol. 2001 Nov-Dec; 33(5):367-74. This article on PubMed
- Thomas DL. Hepatitis C and human immunodeficiency virus infection. Hepatology. 2002 Nov; 36(5 Suppl 1):S201-9. This article on PubMed
- Greub G. Clinical progression, survival and immune recovery during antiretroviral therapy in patients with HIV-1 and hepatitis C co infection, Swiss HIV cohort study. Lancet. 2000; 356:1800-1805. This article on PubMed
- Diop-Ndiaye H, Toure-Kane C, Etard JF, Lo G, Diaw P, Ngom-Gueye NF, Gueye NF et al. Hepatitis B, C seroprevalence and delta viruses in HIV-1 Senegalese patients at HAART initiation. J Med Virol. 2008 Aug; 80(8):1332-6. This article on PubMed
- Larsen C, Pialoux G, Salmon D, Antona D, Le Strat Y, Piroth L et al. Prevalence of hepatitis C and hepatitis B infection in the HIV-infected population of France. Euro Surveill. 2008; 13 (22):18888. This article on PubMed
- Akanmu AS, Esan OA, Adewuyi JO, DaviesAO, OkanyC C, Olatunji RO, Babalola T. Evaluation of a rapid test kit for detection of HBsAg/eAg in whole blood: a possible method for pre-donation testing. Afr J Med med Sci. 2006; 35: 5-8. This article on PubMed
- Durosinmi MA, Ndububa DA, Alabi OA, et al. Prevalence of HIV-1 and HBsAg in normal blood donors in Ile-lfe, Nigeria. Nig Med J. 1992; 21(13):138-140
- irisena ND, Njoku MD, Idoko JA. Hepatitis surface antigenaemia in patients with human immunodeficiency virus -1(HIV-1) infection in Jos, Nigeria. Nig Med Pract. 2002; 41(12):18-20.
- Olatunji OP, Iseniyi JO. Hepatitis B and C virusesí co-infection with human immunodeficiency virus infected patients at UITH, IIorin. Nig Med Pract. 2008; 54(1):8-10.
- Nwokedi EE, Epopees MA, Dutse AI. Human immunodeficiency virus and hepatitis B virus co infection among patients in Kano, Nigeria. Niger J Med. 2006 Jul-Sep; 15(3):227-9. This article on PubMed
- Stud A, Singh J, Dhiman RK, Wanchu A, Singh S, Chawia Y. Hepatitis B virus co-infection in HIV infected patients. Trop Gastroenterol. 2001; 22(2):90-92. This article on PubMed
- Lodenyo H, Schoub B, Ally R, Kairu S, Segal I. Hepatitis B and C virus infections and liver function in AIDS patients at Chris Hani Baragwanath, Johannesburg. East African Medical Journal. 2000; 77(1): 13-15. This article on PubMed
- Baba MM, Gushau W, Hassan A W. Detection of hepatitis-B surface antigenaemia in patients with and without the manifestations of AIDS in Maiduguri, Nigeria. Postgrad Med J. 1998; 5 (3): 125-127.
- Lesi O A, Kehinde M O, Oguh DN, Amira CO. Hepatitis B and C virus infection in Nigerian patients with HIV/AIDS. Niger Postgrad Med J. 2007 Jun; 14(2):129-33. This article on PubMed
- Ejele OA, Nwauche C A, Erhabor O. The Prevalence of Hepatitis B surface Antigenaemia in HIV positive patients in the Niger Delta Nigeria. Niger J Med. 2004 Apr-Jun; 13(2):175-9. This article on PubMed
- Sungkanuparph S, Vibhagool A, Manosuthi W, Kiertiburanakul S, Atamasirikul K, Aumkhyan A, Thakkinstian A. Prevalence of hepatitis B virus and hepatitis C co infection with human immunodeficiency virus in Thai patients: a tertiary case based study. J Med Assoc Thai. 2004; 87 (11):1349-1354. This article on PubMed
- Agwale SM, TanimotoL, Womack C, Odama L, Leung K, DueyD et al. Prevalence of HCVcoinfection in HIV-infected individuals in Nigeria and characterization of HCV genotype. J Clin Virol. 2004 Dec; 31 Suppl 1:S3-6. This article on PubMed
- Wright TL, Honnander H, Pu X, Held M J, Lipson P, Quan S, et al. Hepatitis C in HIV infected patients with and without AIDS, prevalence and relationship to survival. Hepatology. 1994; 20:1152. This article on PubMed
- Otegbayo JA, Taiwo BO, AkingbolaTS, OdaiboGN, Adedapo KS, Penugonda S et al. Prevalence of hepatitis B and C seropositivity in a Nigerian cohort of HIV-infected patients. Ann Hepatol. 2008; 7(2):152-6. This article on PubMed
- Harania RS, Karuru J, Nelson M, Stebbing J. HIV, hepatitis B, and hepatitis C co infection in Kenya. AIDS. 2008; 22(10):1221-1222. This article on PubMed