|
|
ORIGINAL ARTICLE |
|
Year : 2019 | Volume
: 3
| Issue : 1 | Page : 2-7 |
|
Seroepidemiology of hepatitis B virus among human immunodeficiency virus-infected patients in a tertiary hospital in Nigeria
Bankole Henry Oladeinde1, Richard Omoregie2
1 Department of Medical Laboratory Science, Edo University, Iyamho, Nigeria 2 School of Medical Laboratory Science University of Benin Teaching Hospital; Medical Microbiology Unit, University of Benin Teaching Hospital, Benin City, Edo State, Nigeria
Date of Web Publication | 26-Mar-2019 |
Correspondence Address: Dr. Bankole Henry Oladeinde Department of Medical Laboratory Science, Edo University, Iyamho, Edo State Nigeria
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/LJMS.LJMS_57_18
Aim: This study was aimed at determining the prevalence and associated risk factors for hepatitis B virus (HBV) infection among human immunodeficiency virus (HIV)-infected patients in a tertiary teaching hospital in Nigeria. Patients and Methods: Venous blood was collected from a total of 1680 (comprising of 1177 HIV infected and 503 non-HIV infected) patients and tested for the presence of HbsAg using immunochromatographic technique. Results: The seroprevalence of HBV among HIV and non-HIV-infected patients was 3.8% and 3.6%, respectively. HIV was not identified as a risk factor for HBV seropositivity (P = 0.919). A statistically significant association was found to exist between CD4 count <200 cells/mm3 and HBV seropositivity among highly active antiretroviral therapy-naïve HIV-infected patients (odds ratio [OR] = 10.085, 95% confidence interval [CI] = 1.314, 89.56, P = 0.008). HIV-infected males were observed to have a significantly higher prevalence of HBV infection (male vs. female: 6.1% vs. 3.1%; OR = 2.046, 95% CI = 1.103, 3.299, P = 0.029). Tribal mark was identified as a risk factor for HBV infection among HIV-infected male patients (P = 0.042). Conclusions: Male gender, presence of tribal marks, as well as CD4 count <200 cells/mm3 are risk factors for HBV infection among HIV-infected patients. Interventions by appropriate agencies are advocated.
Keywords: Hepatitis B virus, human immunodeficiency virus, Nigeria, seroprevalence
How to cite this article: Oladeinde BH, Omoregie R. Seroepidemiology of hepatitis B virus among human immunodeficiency virus-infected patients in a tertiary hospital in Nigeria. Libyan J Med Sci 2019;3:2-7 |
How to cite this URL: Oladeinde BH, Omoregie R. Seroepidemiology of hepatitis B virus among human immunodeficiency virus-infected patients in a tertiary hospital in Nigeria. Libyan J Med Sci [serial online] 2019 [cited 2023 Mar 28];3:2-7. Available from: https://www.ljmsonline.com/text.asp?2019/3/1/2/254958 |
Introduction | |  |
Human immunodeficiency virus (HIV) infection remains a major cause of morbidity and mortality worldwide.[1] Liver diseases are a major cause of morbidity and mortality among HIV-infected patients worldwide.[2] The global mortality from liver diseases is the second only to AIDS-related mortality, and most of these liver diseases are of viral etiology.[3] Hepatitis B virus (HBV) infection is a leading cause of chronic hepatitis, liver cirrhosis, and hepatocellular carcinoma worldwide.[4] Due to the shared modes of transmission, coinfection with HBV and HIV is not uncommon.[5] HBV and HIV have a mutually detrimental impact in that HIV infection accelerates HBV-related liver damage, leading to earlier cirrhosis and end-stage liver disease,[6],[7] and the presence of HBV infection has been reported to complicate the management of HIV infection, impairs CD4 recovery, accelerates immunologic progression, and increases the morbidity and mortality of HIV-infected patients.[7],[8]
Nigeria is Africa's most populous nation and is home to more people living with HIV than any other country in the world, except South Africa and India.[9] Investigators have reported varying prevalence rates of HBV infection among different groups in Nigeria. HBV rates between 4.6% and 16.3% have been documented among surgeons, infants, health-care workers, and pregnant women attending traditional birth homes in Nigeria.[10],[11],[12] However, few studies have evaluated the prevalence and associated risk factors for HBV infection among HIV-infected patients in Nigeria. The report indicates that HBV screening is not routinely conducted for HIV-infected patients in most Nigerian hospitals.[13] This is likely to result in missed diagnosis of HBV infection among HIV-infected patients, which over time could progress to other serious medical complications including death. Against this background, and the paucity of reports on the prevalence of HBV infection among HIV-infected patients in Nigeria, this study was undertaken.
Patients and Methods | |  |
Study area
This study was conducted among patients attending different clinics of the University of Benin Teaching Hospital (UBTH), Benin City, Edo State Nigeria. The UBTH is a tertiary teaching hospital with a referral status, located in the South-South geopolitical zone of Nigeria.
Study population
A total of 1680 patients (comprising of 1177 HIV-infected and 503 non-HIV-infected patients) were recruited for this study using the random sampling technique. The age range of the study participants was 4–78 years. Verbal informed consent was obtained from all participating patients and their parents/guardians in the case of children before collection of specimen. The study was approved by the Ethical Committee of the UBTH, Benin City, Nigeria. A structured questionnaire was used to obtained relevant data from all patients.
Specimen collection and processing
A volume of 5 mL of blood was collected from each consenting patient and dispensed in a plain container and allowed to clot. The resulting serum was used for the serological detection of HIV using a previously described method.[14] Briefly, each patient's serum was screened for the presence of HIV antibodies using Determine™ (Abbott Laboratories, Tokyo, Japan) and HIV ½ STAT-PAK (Chembio Diagnostic Systems, New York, NY, USA). When both kits showed positivity, the patient was regarded as positive for HIV infection and vice versa. However, when test results were discordant, a third kit Genie II HIV-1/HIV-2 (Bio-rad, Marnes-la-Coquette, France) was used. The HIV serostatus of the patient was taken as the result of either of the first two kits that agree with that of the third kit. Sera of all consenting patients were screened for the presence of HbsAg using Determine™ HBsAg immunochromatographic test kit (Abbott Laboratories, Tokyo Japan) following the manufacturer's instruction.
Statistical analysis
The data obtained were analyzed using Chi-square test or Fisher's exact test as appropriate and odds ratio (OR) analysis using the statistical software INSTAT® (GraphPad Software Inc., La Jolla, CA, USA). Statistical significance was set at P < 0.05.
Results | |  |
A total of 45 (3.8%) out of the 1177 HIV-infected patients were found to be HBV seropositive. The seroprevalence of HBV among non-HIV-infected patients was 3.6%. There was no significant difference in seroprevalence of HBV between HIV and non-HIV-infected patients (P = 0.919). The prevalence of HBV did not differ significantly between highly active antiretroviral therapy (HAART) exposed and HAART-naïve HIV-infected patients (P = 0.885). A statistically significant association was found to exist between CD4 <200 cells/mm3 and HBV seropositivity among HAART-naïve HIV-infected patients (OR = 10.085, 95% confidence interval [CI] = 1.314, 89.56, P = 0.008) [Table 1]. | Table 1: Prevalence of hepatitis B virus among human immunodeficiency virus-infected patients
Click here to view |
HIV-infected males were observed to be two times significantly more likely to be HBV seropositive than female counterparts (male vs. female: 6.1% vs. 3.1%; OR = 2.046, 95% CI = 1.103, 3.299, P = 0.029). The seroprevalence of HBV was not found to be significantly affected by age (P = 0.153), history of blood transfusion (P = 0.695), history of surgery (P = 1.000), educational status (P = 0.061), place of residence (P = 0.502), circumcision status (female) (P = 0.759), and presence of body marks (P = 0.481) [Table 2]. | Table 2: Risk factors for hepatitis B virus infection among human immunodeficiency virus-infected patients
Click here to view |
Among HIV-infected male patients, the presence of tribal marks was associated with a significantly higher prevalence of HBV infection (tribal marks vs. no tribal marks: 9.9% vs. 3.6%; OR = 2.915, 95% CI = 1.045, 6.132, P = 0.042) [Table 3]. | Table 3: Prevalence of hepatitis b virus infection with respect to type of body marks
Click here to view |
Discussion | |  |
There is limited data on the prevalence of HBV among HIV infected patients in Nigeria. Against this background this study aimed at determining the sero-prevalence and associated risk factors for HBV infection among HIV infected subjects in Nigeria. In this study, the seroprevalence of HBV infection among HIV-infected patients was 3.8%. Other Nigerian studies have reported lower[13],[15] and higher[16],[17] values in the past. The prevalence of HBV infection is reported to vary from country to country and from time to time even within the same region.[18] The observed variation in seroprevalence of HBV infection may be due to differences in geographical location as the studies by Onwuliri et al., 2014,[17] were conducted in Southwest Nigeria, Egah et al., 2007[15] and Forbi et al., 2007[16] in North Central Nigeria, and Diwe et al., 2013,[13] in South Eastern Nigeria, in contrast to our study which was conducted in Mid-Western Nigeria. HIV was not found to significantly affect the seroprevalence of HBV in this study. Similar findings have been reported in another Nigerian study.[19]
The finding of a lower seroprevalence of HBV among HAART naïve HIV-infected patients in this study is in line with reports from other African studies.[20],[21] Direct interaction of HIV on HAART has been reported to reduce the efficacy of anti-HBV therapy including lamivudine resistance.[22] This may explain the observed pattern of the result. In general, the seroprevalence of HBV infection was not significantly affected by HAART status in this study, consistent with a report elsewhere.[23] The degree of immunodeficiency represents an important factor in the progression of hepatitis disease.[24] HAART-naïve HIV-infected patients with CD4 count <200 cells/mm3 had a significantly higher seroprevalence HBV infection than those with higher counts. The may be related to a poorer and/or slower rate of HBV resolution occasioned by severely depleted CD40-T lymphocyte count. It could also be attributed to higher reactivation rate, as reactivation of HBV infection has been reported to be associated with low CD4 count.[25] As HBV screening is not routinely conducted among HIV-infected patients in Nigeria,[13] this finding provides a strong basis for the inclusion of all HIV-infected patients with low CD4 count for HBV screening.
The age was not identified a risk factor for HBV infection in this study. However, an interesting find was that all patients aged 14 years and less were seronegative for HBV. This is contrasting to report from an earlier African study which showed that HIV-infected patients <20 years had the highest prevalence of HBV infection.[26] Nigeria commenced her universal HBV immunization program in 2004.[11] The study participants within the age group of 4–14 years are more likely to be beneficiaries of such a young program than older participants and thus may present with lower risk for HBV infection.
With respect to gender, HIV-infected males were observed to have a significantly higher seroprevalence of HBV infection than females. A Nigeria study has reported similar findings.[23] HIV-infected males were observed to have twice as much risk of being HBV seropositive than their female counterparts. Reports indicate that androgen and estrogen may play very different roles in the progression of HBV infection,[27] with serum estrogen shown to exert a protective effect against the development of HCC.[28] Thus, the observed higher seroprevalence recorded among males may be related to higher levels of androgen expressed among them.
HIV-infected patients with a history of blood transfusion were observed to have an insignificantly higher seroprevalence of HBV infection. This is consistent with a report elsewhere.[21] The finding of a lower seroprevalence of HBV among patients with a history of surgery in this study is at variance with reports from other African studies.[29],[30] The risk of contracting viral hepatitis infection is reported to vary with the type of surgery.[31] Thus, differences in the type and number of surgeries performed may explain the contrasting findings in these studies. However, the seroprevalence of HBV infection did not differ significantly with respect to the history of surgery in this study. This is in agreement with a previous report.[3]
HIV-infected patients with no formal education had the highest seroprevalence of HBV in this study. This concurs with findings from a Nigerian study[32] but disagrees with another.[33] Educated persons are often more aware of preventive measures against infectious diseases, and this may have accounted for the observed pattern of the result. The prevalence of HBV, however, was not significantly affected by educational status in this study. This is concurs with findings from an African study.[23]
The finding of a higher seroprevalence of HBV infection among HIV-infected patients in rural communities is in line with reports from other African studies.[32],[33] It is, however, at variance with one outside Africa.[34] Lack of hygiene and low socioeconomic status are risk factors for horizontal contagion of HBV disease.[35] Poverty and illiteracy are hallmarks of several rural communities in Nigeria,[36] and these factors have been reported to be driving forces for the acquisition of HBV.[37] Report indicates that the HBV immunization coverage is much poorer in rural than urban communities of Nigeria.[38] These may explain the result obtained in this study. In general, the seroprevalence of HBV did not differ with respect to location of the study participant. This agrees with findings from other African studies.[39],[40]
An insignificantly higher seroprevalence of HBV was observed among the female cohort of patients. This is in line with an earlier Ghanaian report.[41] It is common knowledge that the practice of female genital mutilation in Nigeria is done by traditional midwives who often work in unhygienic environment and use sharps in mutilating women. These sharps which may have been used repeatedly on different women could serve as a vehicle for the transmission of blood-borne viruses and be responsible for the observed higher seroprevalence of HBV among circumcised female patients in this study.
A statistically insignificant association was found to exist between the presence of scarification and HBV seropositivity among HIV-infected patients. Of all types of marks evaluated in this study, only tribal marks were found to be significantly associated with HBV seroinfection, and this was only observed among HIV-infected male patients. Although common in the past, the practice of tribal markings is fading and rapidly falling into disuse in Nigeria.[42] It is, therefore, likely that most persons with tribal markings in this study may have received them a long time ago and in an era when use and re-use of unsterilized sharps among person were rife. Other factors such as male hormone which has been reported to support HBV replication, and excessive alcohol common to males, may also contribute to the observed pattern of result.
Conclusion | |  |
Summarily, the seroprevalence of HBV infection among HIV-infected patients was high and significantly associated with male gender. HAART-naïve HIV-infected patients with CD4 count < 200 cells/mm3 had a significantly higher risk of acquiring HBV infection. The presence of tribal marks was significantly associated with HBV infection among HIV-infected males only. Intervention effort by relevant agencies at reducing HBV infection and associated sequelae among HIV-infected patients is advocated.
Acknowledgment
Authors would like to acknowledge with thanks all patients that participated in this study.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References | |  |
1. | Fokouo JV, Vokwely JE, Noubiap JJ, Nouthe BE, Zafack J, Minka Ngom ES, et al. Effect of HIV infection and highly active antiretroviral therapy on hearing function: A prospective case-control study from Cameroon. JAMA Otolaryngol Head Neck Surg 2015;141:436-41. |
2. | Palella FJ Jr., Baker RK, Moorman AC, Chmiel JS, Wood KC, Brooks JT, et al. Mortality in the highly active antiretroviral therapy era: Changing causes of death and disease in the HIV outpatient study. J Acquir Immune Defic Syndr 2006;43:27-34. |
3. | Luma HN, Eloumou SA, Ekaney DS, Lekpa FK, Donfack-Sontsa O, Ngahane BH, et al. Sero-prevalence and correlates of hepatitis B and C co-infection among HIV-infected individuals in two regional hospitals in Cameroon. Open AIDS J 2016;10:199-208. |
4. | Wong CH, Goh K. Chronic hepatitis B infection and liver cancer. Biomed Imaging Interv J 2006;2:e7. |
5. | Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: A review. World J Gastroenterol 2014;20:14598-614. |
6. | Konopnicki D, Mocroft A, de Wit S, Antunes F, Ledergerber B, Katlama C, 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. |
7. | Thio CL, Seaberg EC, Skolasky R Jr., Phair J, Visscher B, Muñoz A, et al. HIV-1, hepatitis B virus, and risk of liver-related mortality in the multicenter cohort study (MACS). Lancet 2002;360:1921-6. |
8. | Wandeler G, Gsponer T, Bihl F, Bernasconi E, Cavassini M, Kovari H, et al. Hepatitis B virus infection is associated with impaired immunological recovery during antiretroviral therapy in the Swiss HIV cohort study. J Infect Dis 2013;208:1454-8. |
9. | Joint United Nations Programme on HIV and AIDS. (UNAIDS 2014a). The Gap Report: Children and Pregnant Women Living with HIV. Geneva: UNAIDS; 2014. |
10. | Mello FC, Souto FJ, Nabuco LC, Villela-Nogueira CA, Coelho HS, Franz HC, et al. Hepatitis B virus genotypes circulating in Brazil: Molecular characterization of genotype F isolates. BMC Microbiol 2007;7:103. |
11. | Sadoh AE, Ofili A. Hepatitis B infection among Nigerian children admitted to a children's emergency room. Afr Health Sci 2014;14:377-83. |
12. | Oladeinde BH, Omoregie R, Oladeinde OB. Prevalence of HIV, HBV, and HCV infections among pregnant women receiving antenatal care in a traditional birth home in Benin city, Nigeria. Saudi J Health Sci2013;2:113-9. [Full text] |
13. | Diwe CK, Okwara EC, Enwere OO, Azike JE, Nwaimo NC. Sero-prevalence of hepatitis B virus and hepatitis C virus among HIV patients in a suburban university teaching hospital in South-East Nigeria. Pan Afr Med J 2013;16:7. |
14. | Omoregie R, Efam MO, Ihongbe JC, Ogefere HO, Omokaro EU. Seroprevalence of HIV infection among psychiatric patients in Benin city, Nigeria. Neurosciences (Riyadh) 2009;14:100-1. |
15. | Egah DZ, Banwat EB, Audu ES, Iya D, Mandong BM, Anele AA, et al. Hepatitis B surface antigen, hepatitis C and HIV antibodies in a low-risk blood donor group, Nigeria. East Mediterr Health J 2007;13:961-6. |
16. | Forbi JC, Gabadi S, Alabi R, Iperepolu HO, Pam CR, Entonu PE, et al. The role of triple infection with hepatitis B virus, 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;102:535-7. |
17. | Onwuliri EA, Ndako JA, Dimlong MY. Seroprevalence of hepatitis B surface antigen [HBsAg] co-infections among HIV positive individuals. Researcher 2014;6:74-8. |
18. | Gyar SD, Agbo P, Reuben CR. Assessment of hepatitis b co-infection among HIV/AIDS patients attending antiretroviral therapy (ART) clinic in Garaku, Central Nigeria. Res J Microbiol 2014;9:232-8. |
19. | Ikeako L, Ezegwui H, Ajah L, Dim C, Okeke T. Seroprevalence of human immunodeficiency virus, hepatitis B, hepatitis C, syphilis, and co-infections among antenatal women in a tertiary institution in South East, Nigeria. Ann Med Health Sci Res 2014;4:954-8. [Full text] |
20. | Adewumi MO, Donbraye E, Sule WF, Olarinde O. HBV infection among HIV-infected cohort and HIV-negative hospital attendees in South Western Nigeria. Afr J Infect Dis 2015;9:14-7. |
21. | Nwolisa E, Mbanefo F, Ezeogu J, Amadi P. Prevalence of hepatitis B co-infection amongst HIV infected children attending a care and treatment centre in Owerri, South-Eastern Nigeria. Pan Afr Med J 2013;14:89. |
22. | Peters MG. Diagnosis and management of hepatitis B virus and HIV coinfection. Top HIV Med 2007;15:163-6. |
23. | Ishaku A, Godwin O, Ishaleku D. Seroprevalence of hepatitis B and C co-infcetionamong cohort seropositive HIV patients accessing healthcare in Nassarawa state, North Central Nigeria. Br J Psychol Res 2013;1:15-24. |
24. | Gaeta GB, Stornaiuolo G, Precone DF, Lobello S, Chiaramonte M, Stroffolini T, et al. Epidemiological and clinical burden of chronic hepatitis B virus/hepatitis C virus infection. A multicenter Italian study. J Hepatol 2003;39:1036-41. |
25. | Okocha EC, Oguejiofor OC, Odenigbo CU, Okonkwo UC, Asomugha L. Prevalence of hepatitis B surface antigen seropositivity among HIV-infected and non-infected individuals in Nnewi, Nigeria. Niger Med J 2012;53:249-53.  [ PUBMED] [Full text] |
26. | Nakwagala FN, Kagimu MM. Hepatitis B virus and HIV infections among patients in Mulago hospital. East Afr Med J 2002;79:68-72. |
27. | Humphries C. Sex differences: Luck of the chromosomes. Nature 2014;516:S10-1. |
28. | Yu MW, Chang HC, Chang SC, Liaw YF, Lin SM, Liu CJ, et al. Role of reproductive factors in hepatocellular carcinoma: Impact on hepatitis B- and C-related risk. Hepatology 2003;38:1393-400. |
29. | Weldemhret L, Asmelash T, Belodu R, Gebreegziabiher D. Sero-prevalence of HBV and associated risk factors among HIV positive individuals attending ART clinic at Mekelle hospital, Tigray, Northern Ethiopia. AIDS Res Ther 2016;13:6. |
30. | Zenebe Y, Mulu W, Yimer M, Abera B. Sero-prevalence and risk factors of hepatitis B virus and human immunodeficiency virus infection among pregnant women in Bahir Dar city, Northwest Ethiopia: A cross sectional study. BMC Infect Dis 2014;14:118. |
31. | Asthana S, Kneteman N. Operating on a patient with hepatitis C. Can J Surg 2009;52:337-42. |
32. | Okoye FN, Anzaku AS, Ocheke AN, Musa J, Sagay AS. Burden and determinants of hepatitis B virus co-infection in a cohort of HIV positive pregnant women in Jos, Niger Inter J Trop Dis Health 2015;9:1-9. |
33. | Lar PM, Pam VK, Christopher PB, Gwamzhi L, Mawak J. Prevalence and immune status of HIV/HBV co-infected pregnant women. Afri J Clin Exper Microbiol 2013;14:120-6. |
34. | Altay T, Uskun E, Akcam FZ. Seroprevalence of hepatitis B surface antigen and its correlation with risk factors among new recruits in Turkey. Braz J Infect Dis 2012;16:339-44. |
35. | Akcam FZ. Infection of hepatitis B. STED 2003; 12:211-4. |
36. | Oladeinde BH, Phil RO, Olley M, Anunibe JA. Prevalence of HIV and anemia among pregnant women. N Am J Med Sci 2011;3:548-51. |
37. | Lemoine M, Nayagam S, Thursz M. Viral hepatitis in resource-limited countries and access to antiviral therapies: Current and future challenges. Future Virol 2013;8:371-80. |
38. | Ophori EA, Tula MY, Azih AV, Okojie R, Ikpo PE. Current trends of immunization in Nigeria: Prospect and challenges. Trop Med Health 2014;42:67-75. |
39. | Abongwa LE, Anye MC, Nantia AE, Ntonifor HN. Sero-prevalence of human immunodeficiency virus (HIV) and hepatitis b virus (HBV) co-infection among pregnant women residing in Bamenda health District, Cameroon Int J Curr Microbiol App Sci2015;4:473-83. |
40. | Abera B, Zenebe Y, Mulu W, Kibret M, Kahsu G. Seroprevalence of hepatitis B and C viruses and risk factors in HIV infected children at the felgehiwot referral hospital, ethiopia. BMC Res Notes 2014;7:838. |
41. | Kye-Duodu G, Nortey P, Malm K, Nyarko KM, Sackey SO, Ofori S, et al. Prevalence of hepatitis B virus co-infection among HIV-seropositive persons attending antiretroviral clinics in the eastern region of Ghana. Pan Afr Med J 2016;25:7. |
42. | Odunbaku JB. The use of tribal marks in archaeological and historical reconstruction: Isale abandoned settlement as a case study. Res Hum Soc Sci 2012;2:251-60. |
[Table 1], [Table 2], [Table 3]
|