Coinfection of Human Immunodeficiency Virus-Infected Patients with Hepatitis B Virus in Lokoja,North Central Nigeria

Abstract

Globally, coinfection of human immunodeficiency virus (HIV) patients with Hepatitis B Virus (HBV) is associated with an accelerated progression of HIV disease and higher mortality resulting from complications of liver-related disease. Despite the public health importance, data are lacking on this subject in the study area. Therefore, we evaluated the prevalence and risk factors for HIV/HBV coinfection among HIV patients accessing antiretroviral treatment in Lokoja, Nigeria. In a cross-sectional study, sera from randomly selected 200 consenting HIV patients were screened for hepatitis B surface antigen (HBsAg) using The Commercial Rapid Immunoassay Test Kit. Demographic variables and putative risk factors of HBV transmission were obtained using structured questionnaire. HBsAg prevalence was 8.0% in the sampled group with higher seropositivity rate in the age group, 40–49 years, followed by those 20–29 years of age, whereas the other age groups had zero positivity rates each. The difference between seroprevalence rates in relation to patients' age and sex was not statistically significant (p > 0.05). Patients with no formal education, who were married and were housewives, had higher rates of HBV infection compared with others in the group. Although not statistically significant (p > 0.05), the likelihood of exposure to HBV was higher among patients who were engaged in multiple sexual behaviors, alcoholism, smoking, sharing of sharps, ear piercing, and had history of blood transfusion. Conclusively, HIV/HBV coinfection rate in our study is comparable to other localities and thus, affirm the endemicity in the study area. The need to strengthen health education of the masses to desist from risky behaviors is recommended to reduce the morbidity and mortality arising from HIV/HBV comorbidity.

Introduction

Hepatitis B virus (HBV) has emerged as the leading cause of liver cancer globally (2). The principal routes of virus transmission are vertical, blood exposure and through unprotected sexual intercourse. Because of shared routes of transmission with Human immunodeficiency virus (HIV), a high proportion of patients with either infection are at greater risk for HIV/HBV coinfection (6). The rate of HBV infection in patients with HIV varies widely depending on the population and factors such as age at the time of infection and mode of acquisition, of which are determinants of chronic HBV infection (1).

Globally, ∼360 millions of people are infected with prolonged forms of hepatitis B, including active and inactive chronic forms (3) with annual deaths of about 600,000 (22). Although more than 90% of immune-competent individuals spontaneously clear HBV acquired in adulthood, persons infected with HIV are half as likely as HIV-uninfected persons to spontaneously clear the virus. Thus, chronic HBV infection occurs in 5%–10% of HIV-infected individuals who are exposed to HBV, a rate 10 times higher than seen in the general population (1). The chronic carrier states place HIV patients at a greater risk for progression to liver cirrhosis and/or hepatocellular carcinoma as well as transmitting HBV to others (8). A multicenter AIDS cohort study (20) showed that coinfected patients had about 13 times higher chances of developing liver-related mortality than those with HIV monoinfection. Also, HIV/HBV coinfection increases risk of hepatotoxicity of antiretroviral drugs and enhances onset of an AIDS-defining illnesses compared with HIV infection alone (7). Thus, for proper management of comorbid conditions, it is important to determine the proportion of HIV seropositive patients who are also infected with HBV.

Although studies on HIV/HBV coinfection have being reported from various parts of the country, there is paucity of information regarding the burden of the comorbidity in the study area. Therefore, this study became imperative to determine the rate of HBV infection and predisposing risk factors among the population of people living with HIV to generate information that could complement the epidemiological data on HIV/HBV comorbidity in Nigeria and which can also contribute to effective public health programs aimed at preventing/reducing the burden of the disease and associated sequelae.

Materials and Methods

Study area

A study was carried out at Lokoja, the state capital of Kogi State, Nigeria. Lokoja, which is located on latitude 7.80^oN and longitude 6.74^oE, is situated at an elevation of 53 m above sea level. The city is the converging point of river Niger and Benue with a population of 195,261 at the 2006 census and an area of 3,180 km². It is bounded by the Niger in the north and east upstream from the capital until the border with Kwara State, and includes the city of Lokoja. The town is situated in the tropical Wet and Dry savanna climate zone of Nigeria, and temperature remains hot all year round.

Study population/design

HIV-positive patients accessing the antiretroviral treatment center at the Kogi State Specialist Hospital (KSSH) Lokoja were enrolled in the study. The hospital runs a weekly HIV/AIDS clinic and is a referral hospital and one of the most utilized health facilities in Kogi State. Participants in the study were counseled and only those who provided consent were enrolled in the study. Participants 18 years of age and above provided oral and written informed consent while for those between 5 and 17 years, parents, or legal guardian provided oral consent. Ethical approval for the study was obtained from the Ethics Review Committee of the KSSH in line with the Helsinki Declaration on ethics for biomedical research involving human subjects (Institutional Review Board approval number: 120). A sample size of 200 was determined using the formula prescribed by Bartlett et al. (4) and a prevalence of 8.5% from a similar study in Nigeria (13).

Sample collection, preparation, and storage

Five milliliters of venous blood was obtained from each of the 200 consented HIV-seropositive patients into a well-labeled EDTA tube. At the same time, structured questionnaire was administered to collect data on patients' sociodemographics and information considered as potential risk factors on HBV transmission. Sera were separated from the blood samples by centrifugation at 3,000 revolutions per minute for 10 min. Afterward, the labeled sera were stored at −20°C in line with the manufacturer's specification until tested for hepatitis B surface antigen (HBsAg).

Assays for HBsAg

A one-step test was carried out to detect HBsAg in serum using Coschesic strips^®. This method is immunochromatographic and qualitative in nature and detects HBV antigen in human blood. The test strip which is coated with monoclonal anti-HBs capture antibody has more than 99.9% sensitivity and 98.6% specificity when read in vitro. The test and interpretation of the results were done in accordance with the kit's manufacturer's specification.

Statistical analysis

The data generated in the study were presented using descriptive statistics. Analysis of the data was done using the Statistical Packages for Social Sciences (SPSS) version 16 for windows. Chi-square or Fisher's exact test was used where appropriate to assess the difference between variables and seroprevalence rates. A p < 0.05 was considered as the level of statistical significance.

Results

Sixteen (8.0%) out of the total of 200 HIV patients enrolled in the study were seropositive for HBsAg. The hepatitis B surface antigenemia rate was higher in the age group 40–49 years at 14.29% followed by those 20–29 years of age at 10.27%, while those that were 5–20, 30–39, and 50–59 years of age had zero prevalence rates each. The difference in seroprevalence rates in relation to patients age was not significant (p > 0.05). Even though more females than males participated in the study, both of them were equally comparable in exposure to HBV infection (p > 0.05) with seroprevalence rates of 8.0% each. Married patients in the study were more predisposed to HBV infection than the single participants as the former had prevalence of 9.52% higher than 7.30% of the latter. With the exception of those who had primary education as highest level of qualification, patients' level of education was inversely correlated with HBV infection, as seropositivity rate generally decreased with higher educational attainment. However, difference in positivity rates in relation to patients level of education was not statistically significant (p > 0.05). HBV infection was observed in all the occupational groups, but those who were housewives were more predisposed to infection compared with the other occupational groups (Table 1). Patient factors, such as multiple sexual partnerships, alcoholism, smoking, sharing of sharps, ear piercing, history of blood donation/reception, history of jaundice, or family history of HBV infection, were associated with higher hepatitis B surface antigenemia. However, the difference between each variable and seropositivity rate was not statistically significant (p > 0.05). Patients in the study with history of HBV vaccination were least infected (5.7%) than the vaccine-naive subjects (8.48%) (Table 2).

Table 1.

Hepatitis B Surface Antigen Distribution in Relation to Sociodemographic Characteristics of Human Immunodeficiency Virus Patients Studied in Lokoja

Variable	Number tested	Number positive (%)	X²-value	p
Age group
<20	17	0	6.07	0.19
20–29	136	14 (10.27)
30–39	28	0
40–49	14	2 (14.29)
50–59	5	0
Total	200	16 (8.00)
Marital status
Single	138	10 (7.30)	0.290	0.59
Married	63	6 (9.52)
Divorced/widowed	0	—
Total	200	16 (8.00)
Gender
Male	75	6 (8.00)
Female	125	10 (8.00)	0.00	1.00
Total	200	16 (8.00)
Educational level
Tertiary	137	11 (8.03)	1.31	0.73
Secondary	49	4 (8.16)
Primary	8	0
None	6	1 (16.67)
Total	200	16 (8.00)
Marital status
Housewife	4	1 (25.0)	5.87	0.21
Business	40	6 (15.0)
Farming	8	1 (12.5)
Civil servant	24	1 (4.17)
Student	124	7 (5.65)
Total	200	16 (8.00)

Table 2.

Probable Risk Factors and Outcome of Hepatitis B Surface Antigen Tested Among Human Immunodeficiency Virus Seropositive Patients Studied in Lokoja

	Variable	HBsAg positive (%)	HBsAg negative (%)	X²-value	p
1	History of blood transfusion
	Yes (n = 54)	5 (9.26)	49 (90.74)	0.16	0.69
	No (n = 146)	11 (7.53)	135 (92.47)
2	Surgery
	Yes (n = 75)	6 (8.00)	69 (92.0)	0.00	1.0
	No (n = 125)	10 (8.00)	155 (92.0)
3	Tattooing
	Yes (n = 29)	2 (6.70)	27 (93.10)	0.06	0.81
	No (n = 171)	14 (8.19)	157 (91.81)
4	Ear piercing
	Yes (n = 44)	5 (11.36)	39 (88.64)	0.87	0.35
	No (n = 156)	11 (7.05)	145 (92.92)
5	History of jaundice
	Yes (n = 23)	2 (8.70)	21 (91.30)	0.02	0.90
	No (n = 177)	14 (68.36)	163 (92.09)
6	Sharing of sharps
	Yes (n = 136)	12 (8.82)	124 (91.18)	0.39	0.53
	No (n = 64)	4 (6.25)	60 (93.75)
7	Tribal marks
	Yes (n = 85)	6 (7.06)	79 (92.94)	0.18	0.67
	No (n = 115)	10 (8.70)	105 (91.30)
8	Family history of HBV
	Yes (n = 36)	5 (13.89)	31 (86.11)	2.07	0.15
	No (n = 164)	11 (6.71)	153 (93.29)
9	Intravenous drug use
	Yes (n = 26)	2 (7.69)	24 (92.31)	0.004	0.95
	No (n = 174)	14 (8.05)	160 (91.95)
10	Smoking
	Yes (n = 37)	6 (16.22)	42 (91.30)	0.04	0.84
	No (n = 163)	10 (6.13)	142 (86.59)
11	Alcoholism
	Yes (n = 46)	4 (8.70)	42 (91.30)	0.04	0.84
	No (n = 164)	12 (7.32)	142 (86.59)
12	Consistent condom use
	Yes (n = 26)	3 (11.54)	23 (88.46)	0.51	0.48
	No (n = 174)	13 (7.47)	163 (92.53)
13	Multiple sexual partners
	Yes (n = 94)	8 (8.51)	86 (91.46)	0.063	0.80
	No (n = 106)	8 (7.55)	98 (92.45)
14	Immunized
	Yes (n = 35)	2 (5.7)	33 (94.29)	0.30	0.58
	No (n = 165)	14 (8.48)	157 (91.52)

HBsAg, hepatitis B surface antigen; HBV, hepatitis B virus.

Discussion

Eight percent of the HIV patients accessing the antiretroviral drugs at the KSSH, Lokoja were coinfected with HBV. Finding is comparable with previous reports in Nigeria (13,21), Thailand (19), and Brazil (17), but lower than rates (5,10) reported in other parts of Nigeria. The difference in HBV/HIV coinfection in different geographical areas could be attributed to variation in sexual behaviors, community-specific behaviors, such as scarification marks and sensitivity of diagnostic assays.

The comparable rates of HBV/HIV coinfection between males and females in our study had also been previously observed (12). Contrasting reports, however, suggest that males are more susceptible to HBV infection as compared with females (9,18). Reason for this inconsistency may be explained by gender differential in exposure to infection owing to sociocultural and behavioral practices such as sexual promiscuity and male circumcision. In conformity with the higher rate of HIV/HBV coinfection reported among the married HIV patients in Kaduna (13) and Kogi States (12), the current study also observed similar trend in HBsAg seropositivity and this lends credence to the role of sexual intercourse in disease transmission. Although, HBsAg statuses of patients' spouses are not known in this study, it may not be unconnected with sexual exposures

The finding of higher HBV infection among HIV patients with no formal education compared with the highly educated persons in the current study supports the positive role of education in disease prevention as the highly educated ones are likely more informed about the routes and risk factors of HBV transmission. Earlier, Sule et al. (18) in Ankpa, Kogi State and Mehmet et al. (9) in the Southeastern region of Turkey reported similar inverse relationships between HBV infection and patients' level of education. Thus, current efforts geared toward improving the level of education to reduce poverty and improve quality of life of these vulnerable communities should be strengthened to achieve a breakthrough in the fight against HIV/HBV comorbidity in Nigeria. Occupational distribution of HBsAg among the HIV patients revealed that, although infection occurred in all the occupational groups, the housewives in the study demonstrated higher exposure to HBV infection. Detection of high HBsAg seropositivity rates in all the occupational groups is a reflection of endemicity of HBV infection in the study area and with the housewives that are usually less educated in the study area, the higher rate of HBV/HIV coinfection is expected.

In this study, HIV patients that were 40–49 years of age demonstrated greater predisposition to HBV infection compared with the other age groups. This finding is consistent with previous reports (16) that observed higher hepatitis B surface antigenemia among the older HIV-positive patients in Brazil. It is also comparable with previous reports in Nigeria (13). Socioeconomic and unsafe sexual practices of polygamous men in Nigeria could be the reason for the peak age of infection in our study.

The high rate of HIV/HBV coinfection observed among patients who were engaged in risky behaviors, such as alcoholism, sharing of sharps, ear piercing, and multiple sexual partnerships, has also been reported in other parts of the state (11). Findings also corroborate previously documented evidence in Nigeria of some important risk factors, such as circumcision, ear piercing, and parenteral injections (15). Although not statistically significant, the lower hepatitis B surface antigenemia rate observed among patients with HBV vaccine history compared with the vaccine-naive subjects points to the protective role of HBV immunization.

In conclusion, the seroprevalence rate obtained in this study portends a substantial burden in this resource-poor setting and has a huge implication for management of the coinfected HIV patients. Thus, to ensure proper management of comorbid conditions, all persons diagnosed of HIV should be screened for HBV. Findings from this study support the assertions of Qadir (14) that there is the need for national policy programs on health to engage in continuous monitoring and evaluation as well as treatment of HIV coinfected patients with hepatitis to reduce the risks of liver-related complications. Even though the putative risk factors examined in the current study were not statistically significant to HIV/HBV coinfection, public health education is strongly needed to highlight the dangers of coinfections of HIV and HBV. This study has certain limitations. The true burden of the disease may be underestimated as the hospital-based study may not capture the community-based cases. A second limitation was the lack of follow-up data, which would help to predict the disease outcome. Despite these limitations, finding from current study is important as it would contribute to the current epidemiological data on the burden of the disease in the study area.

Footnotes

Acknowledgments

The authors acknowledge the support and cooperation of staffs of KSSH, Lokoja. They also thank the study participants for granting consent and for taking time to respond to their questionnaire.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

The research was solely funded by authors.

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