High Rate of Hepatitis B Virus Surface Antigenemia Among People Living with HIV/AIDS in Kakuri,Kaduna State,North West Nigeria

Abstract

Globally, increased incidence of liver disease caused by hepatitis B virus (HBV) is responsible for high morbidity and mortality among human immunodeficiency virus (HIV)-infected individuals. This is because both viruses share common routes of transmission. We determined prevalence of HBV-HIV coinfection and the influence of some risk factors on concomitant infection among people living with HIV in a treatment center in Kakuri, Kaduna State. Two hundred consenting individuals with HIV infection participated in the study. Fifty-seven males and 143 females were screened using commercial hepatitis B virus surface antigen (HBsAg) rapid membrane-based immunoassay kit (Fastep^™ HBV). Seventeen patients tested positive to HBsAg (8.5%). There were more males (14.0%) than females (6.3%). Patients within 40–49 years of age had more coinfection (20.6%) compared to those older than 50 years who had the least prevalence (2.7%). Age of HBV/HIV coinfection was statistically significant (p = 0.02). Risk factors include no knowledge of HBV infection, sharing sharp objects, history of sexually transmitted diseases, history of surgeries, and no HBV immunization. High infection rate observed in this study underscores the need for public awareness, to educate people on modes of transmission. Routine screening is advocated for early HBV identification, as this will facilitate reduction of comorbidity and mortality resulting from opportunistic infection. Findings from this study support introduction of HBV vaccination as part of the Expanded Programme on Immunization in Nigeria.

Introduction

Human Immunodeficiency virus (HIV) is responsible for an estimated 36.7 million infection in 2015, with sub-Saharan Africa being the most affected region. About 2.1 million new HIV infections occurred worldwide that year (50). The rate of infection is remarkably high in sub-Saharan Africa (49,51). Over 2 billion people are infected with Hepatitis B virus (HBV) globally (20,56), with approximately 350 million people being HBV carriers (46,54) and over 8% carriers in sub-Saharan Africa alone (53). HBV is highly endemic in Nigeria (13,24,32,40,47). The most common ways of transmission of both viruses are through unprotected sex, transfusion of unscreened blood, use of contaminated needles, and from mother to child during birth (54). Infants and young children have 90% and 30–50% risks, respectively, which may lead to chronic hepatitis (52). If infection is not treated, about 25% of the patients are likely to have liver cirrhosis and/or liver cancer (7). Early detection and prompt treatment with antiviral drugs are essential for breaking transmission (30,52).

HIV/HBV comorbidity has been identified as a major determinant that enhances progression of HIV/AIDS (18). Coinfected individuals are 17 times more likely to die of liver-related diseases than those infected with only HBV (44). HBV protein X enhances replication of HIV-1 (14), while HIV decreases rate of hepatitis B virus surface antigen (HBsAg) clearance in acute infection, thereby enhancing progression of liver disease (45). Also, coinfection with HBV increases risk of hepatotoxicity in people on HAART and enhances onset of AIDS, compared with HIV-1 monoinfection (11,15). This informs the need to determine proportion of people with HIV who are concurrently infected with HBV. Generally, in Nigeria, HIV rate in 2013 was 4.1% and an estimated 3.5 million people were living with HIV (27). Distribution of HIV/AIDS varies with location. In some states, infection is concentrated in certain groups and driven by high-risk behaviors, while other states have epidemics sustained primarily by multiple sexual partners. Kaduna State currently ranks third (9.2%) in the states with the highest rates of HIV/AIDS (28), but there is paucity of information on rate of HBV infection. We determined the rate of HBV infection among population of people living with HIV, to understand epidemiology of HIV-HBV comorbidity in the northern Nigeria State. This study is very important because of the security concerns in the far north and the difficulty in assessing some areas; the liberal nature of Kaduna and the fact that it is a converging point for most people from northern Nigeria will enable information obtained to be used to inform policy and educate the populace in infection control.

Materials and Methods

Study design

This is a prospective cross-sectional study carried out for a period of 4 months spanning from March to June, 2016. A total of 200 people with HIV infection participated in the study; selection was by random sampling. There were 57 males and 143 females, with a male to female ratio of 1:2.5. Participants were enrolled at Gwamna Awan General Hospital, Kakuri, Southern Kaduna, located in northwestern Nigeria on latitude 10°20’N and longitude 7°45’E (29). Kaduna has a population of 6,113,503 according to the 2006 population census. Ethics approval for the study was obtained from Kaduna State Ministry of Health and Human Services in line with the Helsinki declaration on ethics for biomedical research involving human subjects. Sample size (N) was calculated using formula N = Zα²pq/d², where Zα = standard normal deviate set at 1.96, corresponding to 95% confidence level; P = Proportion in the target population estimated to have a variable characteristic = 85% (0.85); q = 1-p = 15% (0.15); and d = degree of precision set at 0.05 (95% confidence interval). Therefore, N = 196, which was approximated to the nearest hundred as 200.

Specimen collection and preparation

Approximately 4 mL of blood was aseptically collected from each participant by venipuncture, into a sterile plain tube. After 10 min, it was spun at 200 rpm for 10 min to separate sera from clotted blood. Sera and test strips were stored at −15°C until screening was to be carried out. Demographic data and information on risk factors were collected using a structured questionnaire. Before questionnaire administration, participants were informed about the study and their consent to participate obtained. Consent forms were signed and confidentiality maintained.

Assay for HIV and HBsAg

Anti-HBsAg antibodies were immobilized unto a strip. During testing, sera migrate through membrane by capillary action, reacting with reagents on the membrane. HBsAg in sera reacts with anti-HBsAg conjugated to color particles and precoated on the strip. If there is enough HBsAg in specimen, a colored band will form at the test (T) region of membrane; presence of colored band indicates a positive result, while absence indicates a negative result. Appearance of colored band at another region serves as procedural control, indicating that adequate volume of specimen was added and membrane wicking occurred. Screening for HIV-1 and -2 antibodies in serum was carried out using two kits: Unigold Determine HIV1/2 test strips (Inverness medical) and HIV1/2 Stat Pak (Combio Diagnostic Systems). These are qualitative rapid immunoassay techniques for detection of antibodies specific for HIV 1/2. Limitation of the study is that results in this study cannot be generalizable to the entire country, bearing in mind that they are at variance with some published studies from other parts of Nigeria.

Data analysis

Data was analyzed with Statistical Package for Social Sciences (SPSS version 16.0). Descriptive data were summarized in statistical tables. Chi-square and Fisher's exact tests were used to test for association between variables. The level of statistical significance was set at p ≤ 0.05. Logistic regression was used to determine risk factors independently associated with HBV infection using odds ratio (OR), which was calculated at 95% confidence interval (CI) for data that satisfy 2 by 2 contingency table.

Results

A total of 200 people living with HIV participated in this study. Table 1 shows 17 (8.5%) were positive for HBsAg. Highest prevalence of 20.6% was found among individuals between 40–49 years of age, while participants who were ≥50 years of age had the least prevalence (2.7%). The association between age and HBV infection in HIV patients was statistically significant (p = 0.02) (Table 2). Gender distribution of infection showed 8 (14.0%) males and 9 (6.9%) females tested positive to HBsAg. There were more males with HBV compared to females; however, the association was not statistically significant (p > 0.05). Married people had higher HBsAg antigenemia (10.3%) compared to single and divorced, who had 6.3% and 0% prevalence rates respectively. Risk factors such as sharing of sharp objects, lack/occasional use of condom, history of surgery, knowledge of HBV infection, immunization against HBV, and history of sexually transmitted infections were associated with higher prevalence rates. However, only immunization against HBV was statistically significant with HBsAg seropositivity (p = 0.00).

Table 1.

Distribution of HBsAg Outcome Among HIV-Positive Participants

HBV status	Frequency	Percentage
Positive	17	8.5
Negative	183	91.5
Total	200	100

HBV, hepatitis B virus; HIV, human immunodeficiency virus; HBsAg, hepatitis B virus surface antigen.

Table 2.

Distribution of HBV Infection According to Sociodemographic Factors

Variable	No. tested	No. positive (%)	p-Value
Age (years)
≤19	6	1 (16.7)
20–29	33	4 (12.1)
30–39	53	3 (5.7)	0.02
40–49	34	7 (20.6)
≥50	74	2 (2.7)
Gender
Male	57	8 (14.0)
Female	143	9 (6.3)	0.08
Marital status
Single	79	5 (6.3)
Married	116	12 (10.3)	0.48
Divorced	5	0 (0.00)
Occupation
Business woman	61	4 (6.6)
Students	41	3 (7.3)
Housewives	26	0 (0.0)	0.26
Civil servants	42	7 (16.7)
Farmers	8	1 (12.5)
Unemployed	22	2 (9.1)

Discussion

In this study, 8.5% HIV-positive patients had HBV (Table 1), which is consistent with seroprevalence rates of 7.95% previously reported in Kano (55), 8.2% in Yola (36), and 8.3% in Nnewi (8). However, the prevalence rate in this study is lower than two reports in Jos where 28.7% was reported by Irisena et al., (19) and 25% by Uneke et al., (48). It is also lower than 26.5% reported in a study in Gombe (25), 15% in Maiduguri (4), 70.5% in Kano (31), 20.6% in Keffi (12), 30.4% in Ilorin (35), 11% in Nasarawa (2), and 30.6% in Abeokuta (33). A study in Cote d'Ivoire reported 12.1% (38), while a meta-analysis found that 1 in 7 HIV patients in Ghana suffer from chronic HBV infection (1).

A study among blood donors reported 5.4% in Benin City (37), 2.7% in Benue state (21), 0.3% in Ibadan (34), 0.5% in Yenegoa (6), and 1.14% in Ebonyi (17). In Tanzania, 1.2% was reported (43), 4% in Kenya (16), and 3.6% in Netherlands (41). Variations observed in HBV-HIV coinfection in different geographical settings may be attributed to genetic disparity. According to Blumberg (5), individuals homozygous for T allele at the vitamin D receptor locus (VDR) are more likely to become carriers of HBV. Higher level of HBV DNA is associated with low level of 25-hydroxyl vitamin D (10). Although, this was not sought in this study, it could be a possible explanation.

Gender-related seroprevalence of HBV-HIV coinfection (Table 2) showed males were more infected than females, despite the fact that there were more females. This observation agrees with reports in rural and urban areas of southeastern Turkey (22). Findings in this study agree with Baba et al., (4) who reported high HBsAg seroprevalence in males than females. However, another group of researchers found higher rates of coinfection in females (28.2%) than males (24.7%) (25). Although the reason for this disparity is not clear, it has been found that males are less likely to clear HBsAg and have higher risk of progression to cirrhosis (4). Differences in gender distribution of infection in this study (Table 2) suggest that both genders are not equally susceptible and gender may be an important epidemiological determinant for HBV-HIV coinfection.

Motta-Castro et al. (23), reported that age was significantly associated with HBsAg seropositivity among Afro-descendant communities in Brazil. This is in agreement with findings in this study. It correlates with previous studies that observed a significant increase in seroprevalence of HBV among older adults (42). Age of acquiring infection is the major determinant of incidence and prevalence rates (9).

Civil servants had high HBV seropositivity followed by farmers and housewives who had no antigenemia. However, this difference was not statistically significant. The reason for high antigenemia among civil servants is not clear. While this may be an observation by chance, a larger study will properly explain this phenomenon. Determining occupational groups at high risk is important as it will help to take measures to prevent infections in these groups.

In this study, marital status-specific prevalence showed that coinfection of HIV-HBV was higher among patients who were married (10.3%) (Table 2). This is contrary to an earlier study that reported higher coinfection rates among unmarried or separated/widowed (25).

National Agency for the Control of AIDS identified drivers of HIV/AIDS in Nigeria to include high illiteracy, high rate of sexually transmitted diseases, and low condom use (26). This study supports these findings (Table 3). Similarly, Mbaawuaga et al. (21) and Amuta et al. (3) in Makurdi, Benue State, highlighted that lack of knowledge of HBV infection, occasional use of condom, history of STDs, history of surgery, and no vaccination against HBV as risk factors that predispose individuals to HBsAg infection. In this study, participants who shared sharp objects had more coinfection. The odds ratio (OR = 2.36, 95% CI = 0.74–7.52) shows that they are twice more likely to be at risk of becoming infected with HBV. These findings corroborate previously documented evidence in Nigeria of important risk factors such as circumcision, ear piercing, and parenteral injections (39).

Table 3.

Risk Factors for HBV Transmission

Variables	No. tested	No. positive (%)	OR	Confidence interval	p-Value
Knowledge of HBV
Yes	110	8 (7.3)	0.71	0.24–1.66	0.35
No	90	9 (10.0)
Mouth-to-mouth kissing
Yes	124	10 (8.1)	0.86	0.32–2.38	0.78
No	76	7 (9.2)
Shared sharp object(s)
Yes	119	13 (10.9)	2.36	0.74–7.52	0.14
No	81	4 (4.9)
No of sexual partners
None	39	2 (5.1)
One	111	11 (9.9)	—	—	0.82
Two	35	3 (8.6)
More	15	1 (6.7)
History of STDs
Yes	69	6 (8.7)	1.04	0.37–2.94	0.94
No	131	11 (8.4)
Use of condom
Regular	60	5 (8.3)
Occasional	140	12 (8.6)	0.97	0.33–2.88	0.96
Never
Had blood transfusion
Yes	57	3 (5.3)	0.51	0.14–1.85	0.28
No	143	14 (9.8)
History of surgery
Yes	63	6 (9.5)	1.21	0.43–3.42	0.73
No	137	11 (8.0)
History of IDU
Yes	72	4 (5.6)	0.52	0.23–1.93	0.44
No	128	13 (10.2)
Immunized for HBV
Yes	91	2 (2.2)	0.14	0.03–0.63	0.00
No	109	15 (13.8)
Tribal marks
Yes	83	6 (7.2)	0.75	0.27–2.12	0.59
No	117	11 (9.4)
Alcohol consumption rate
Low	140	10 (7.1)
Moderate	42	5 (11.9)	—	—	0.57
High	18	2 (11.1)

STDs, sexually transmitted diseases; IDU, intravenous drug use; OR, odds ratio, for only data that satisfied 2 × 2 contingency table.

In conclusion, the HBV/HIV comorbidity rate observed in this study is high compared to previous reports in Nigeria. The seroprevalence rate of concomitant infection in this study may be an indication of high burden of sexually transmitted diseases in the general population. This observation calls for more surveillance and public health education to enlighten the general populace about risk factors and routes of transmission. In addition, routine HBV screening is advocated to ensure early detection and facilitate prompt intervention. In this study, the low rate of HBV antigenemia was found to be highly statistically related to the patient's HBV immunization status (p = 0.00). In view of this, routine HBV immunization program should be strengthened to curb spread of HBV and its sequelae.

Footnotes

Acknowledgments

We thank the management and staff of Gwamna Awan General Hospital, Kakuri, Kaduna. We sincerely appreciate the participation and cooperation of the patients who enrolled in the study. Research was funded by the authors and no competing interest was declared.

Author Disclosure Statement

The authors declare that there are no actual or potential conflicts of interest.

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