Seroprevalence of HBV,HCV,and HIV and Associated Risk Factors Among Apparently Healthy Pregnant Women in Anyigba,Nigeria

Abstract

Globally, infection of pregnant women by human immunodeficiency virus (HIV), hepatitis C virus (HCV), and hepatitis B virus (HBV) pose a significant health challenge for not just the mothers but also the newborn infant. This study was undertaken to assess the prevalence of HIV, HCV, and HBV among pregnant women attending antenatal clinic in Kogi State University Teaching Hospital (KSUTH), Anyigba, Nigeria. Sera samples obtained from 200 consented pregnant women were screened for hepatitis B surface antigen (HBsAg), anti-HCV, and anti-HIV antibodies using commercially available immunoassay test kit. Demographic variables and obstetric characteristic were obtained using structured questionnaire. Of the 200 sera tested, the seroprevalence rates were 1.0%, 0.5%, and 8.5% for HBsAg, anti-HCV, and anti-HIV antibodies, respectively. Although 0.5% were coinfected with HIV/HCV, none was simultaneously infected by the three viruses. Age, marital status, trimester, and educational and occupational status did not significantly affect the prevalence of HIV, HCV, and HBV infections. However, factors such as history of abortion/miscarriage (p = 0.04), intravenous drug use (p = 0.001), and history of other sexually transmitted infection (p = 0.01) were significantly higher in relation to HIV seropositivity. In conclusion, findings from this study revealed high HIV seroprevalence and a clear decline of hepatitis C and B infection prevalence compared with previous epidemiological data. Reason for the latter could be attributed to the current efforts to reduce mother-to-child transmission and possible HBV vaccination programs. High burden of HIV infection in our study suggests the needs to strengthen the national prevention programs including education of the people on the risk factors of HIV transmission.

Introduction

Nigeria with a national human immunodeficiency virus (HIV) seroprevalence of 3.4% and an estimated population of 195 million (14) reportedly has the highest burden of mother-to-child transmission globally (8). Population at risk for HIV is also at risk for hepatitis B virus (HBV) and/or hepatitis C virus (HCV) because both viruses share transmission routes and hence, the increased frequency for coinfection by both viruses (26). Viral hepatitis during pregnancy is associated with high risk of maternal, fetal, and neonatal complications (27). According to the world health report in 2003, acute hepatitis in pregnancy induces premature labor and adverse perinatal outcomes.

Coinfection of HBV and HCV with HIV is a major health problem and occurs frequently because of common routes of transmission (5,29). Both HBV and HCV are responsible for acute and chronic liver disease with significant mortality in the mother–child pair (21). Globally, ∼360 million people are chronic carriers of HBV (26) and risk of progression to liver disease is highest when infection occurs at the early stage of life (25).

Vertical transmission of HBV from carrier mother to her infant is one of the principal routes of acquisition of HBV infection in developing countries (4). Unlike in the developed countries where most cases of HBV infection occurs in adults, in a resource poor settings, infants and children are mostly affected, with >90% of the cases occurring at birth (13). HCV infection, on the contrary, results in chronic condition in ∼60–80% of patients following resolution of acute infection (24). About 7–8% of HCV seropositive women transmit the virus to their offspring and rates of transmission is higher for women concomitantly infected with HIV (1).

The epidemiology of HIV, HBV, and HCV has been widely studied in Nigeria. However, there is paucity of information on this subject among pregnant women in Anyigba, Kogi State, Nigeria. This study was therefore undertaken to assess the seroprevalence and potential risk factors of HIV, HBV, and HCV infections singly and concomitantly within an obstetric population attending the Kogi State University Teaching Hospital (KSUTH), Anyigba.

Methodology

Study area

This study was conducted in Anyigba, a city under Dekina Local Government of Kogi State, Nigeria. Anyigba, which lies between latitude 7°15′–7°29′ north and longitude 7°11′–7°32′ east, has an average altitude of 420 m above sea level. The town has an estimated population of 130,000 comprising most ethnic groups in Nigeria (15). Behavioral practices such as early age at first sexual intercourse, use of unscreened blood and blood products, scarification marks, promiscuity, and intravenous drug use are common among the inhabitants (17).

Study population

The study was carried out among pregnant women, who were attendees of the antenatal clinic of KSUTH, Anyigba between September and November 2017. This hospital runs a weekly HIV/AIDS clinic and is a referral center for other health facilities in the study area. It has a record of ∼2,200 HIV patients per year. In a hospital-based cross-sectional study, a total number of 200 pregnant women were recruited using a nonprobability convenient sampling technique. Trained medical personnel in the hospital clearly explained the objectives/benefits of the study to the attendees and only those who gave consent by completing and endorsing filled-in questionnaire were consecutively recruited. Ethical approval for the study was obtained from the hospital management board on health issues in accordance with the Helsinki's code of conduct for biomedical research involving human subjects. Sample size (N) was determined using the formula N = Zα ² pq/d ² (3), where Zα = standard normal deviate set at 1.96, corresponding to 95% confidence interval (95% CI); p = proportion in the target population estimated to have a variable characteristic = 85% (0.85) from similar study (23); q = 1 − p = 15% (0.15); and d = degree of precision set at 0.05 (95% CI). Therefore, N = 196, which was approximated to the nearest 100 as 200.

Sample collection and storage

Four milliliters of blood sample was aseptically collected by vein puncture from each pregnant woman into a nonanticoagulant bottle after consent was sought and obtained. The participant's name, age, and time and date of collection were appended on the bottle for proper identification. Each of the samples was centrifuged at 3,000/rpm for 5 min and the serum portion was used on the test strip for antigen or antibody detection. Sera samples were stored at −20°C in line with the kit manufacturer's instruction until screened for HBsAg, anti-HIV, and anti-HCV antibodies. Sociodemographic variables and information considered as risk factor for contracting HBV, HCV, and HIV were collected using a structured questionnaire forms.

Serological analysis

Screening for antibodies to HIV type 1 and 2 antibodies in serum was carried out using two kits: Chembio HIV-1/2 Stat Pak (Combio Diagnostic Systems) and Unigold Determine HIV-1/2 test kit (Abbot Laboratories). Both kits have sensitivity and specificity of 100% each. Anti-HCV antibodies were detected using the ARIA HCV-Ab test kit (CTK Biotech, Inc., San Diego, CA). Test was double-antigen sandwich immunoassay for the qualitative detection of anti-hepatitis C antibodies in human serum. ARIA HCV-Ab kit utilizes purified recombinant antigens produced by Escherichia coli from clones selected in the nonstructural area of the hepatitis virus genome (NS3 and NS4), two peptides coded by capsid area of the HCV genome. The test has >99.55% sensitivity and 98.5% specificity. Test for HBsAg was carried out using Coschesic strips. This method is immunochromatographic and qualitatively detects HBV antigen in human blood. The test strip that is coated with monoclonal anti-HBs capture antibody has >99.9% sensitivity and 98.6% specificity when read. All the tests and interpretation of results were carried out in accordance with the guidelines of the kit's manufacturers.

Statistical analysis

Data entry and statistical analysis were performed with Statistical Packages for the Social Sciences, SPSS 16.0 for Windows (SPSS, Inc., Chicago, IL). Descriptive data were presented as simple summaries in tables. Logistic regression and chi-square test were used where appropriate to establish differences between participants' variables and prevalence rates. Probability values (p-values) ≤0.05 were considered significant.

Results

Two hundred pregnant women attending the antenatal clinic of the KSUTH were screened for HBV, HCV, and HIV, of which 1.0%, 0.5%, and 8.5% were positive for HBsAg, anti-HCV, and anti-HIV antibodies, respectively. Dual seropositivity of anti-HCV/anti-HIV accounted for 0.5% and none of the participants was concomitantly infected with the three viruses. Age groups with peak seropositivity for anti-HIV antibodies, HBsAg, and anti-HCV antibodies were 36–40, 31–35, and 21–25 years, respectively. However, the difference between women's age of acquiring both infections and the seropositivity rate was not statistically significant (p > 0.05). Divorced and widowed women with seroprevalence of 16.67% each were more exposed to HIV infection than married (8.24%) and single (0.00%) women. With regard to hepatitis viruses, married women in the study were the only marital group seropositive for HBsAg (1.18%) and anti-HCV antibodies (0.50%). However, there was no statistical significant difference between each marital group and HIV (p = 0.31), HBV (p = 0.93), or HCV (p = 1.0) positivity. Although there was no statistical association between educational levels and seropositivity rates, there was generally a decreasing trend in HIV, HCV, and HBsAg seropositivity as level of education increases. Women who were engaged in one form of business or the other were more infected with HIV (13.64%) and HCV (0.91%), whereas housewives had higher hepatitis B surface antigenemia rate (2.17%) in comparison with the other occupational groups (Table 1). Pregnant women with history of abortion/miscarriage (p = 0.04), intravenous drug use (p = 0.001), and sexually transmitted diseases (p = 0.01) were significantly seropositive for anti-HIV antibody (Table 2).

Table 1.

Sociodemographic and Obstetric Characteristics of Pregnant Participants and Serologic Outcomes of the Three Assays in Anyigba, Kogi State, Nigeria, 2017

Variable	No. tested	HIV⁺, n ( %)	HBV⁺, n (%)	HCV⁺, n (%)
Age range, years
15–20	25	0 (0.0)	0	0 (0.0)
21–25	47	4 (8.510)	0	1 (2.13)
26–30	57	5 (8.77)	1 (1.75)	0 (0.0)
31–35	46	4 (8.69)	1 (2.17)	0 (0.0)
36–40	22	4 (18.18)	0	0 (0.0)
>40	3	0 (0.0)	0	0 (0.0)
Total	200	17 (8.5)	2 (1.0)	1 (0.5)
p-value		0.21	0.77	0.72
Marital status
Single	12	0 (0.0)	0	0 (0.0)
Married	170	14 (8.24)	2 (1.18)	1 (0.59)
Divorced	12	2 (16.67)	0	0 (0.0)
Widowed	6	1 (16.67)	0	0 (0.0)
Total	200	17 (8.5)	2 (2.0)	1 (0.5)
p-value		0.31	0.93	1.0
Level of education
None	31	3 (9.68)	0	0 (0.0)
Primary	39	5 (12.82)	1 (2.56)	1 (2.56)
Secondary	89	7 (9.82)	1 (1.12)	0 (0.0)
Tertiary	41	2 (4.89)	0	0 (0.0)
Total	200	17 (8.5)	2 (2.0)	1 (0.5)
p-value		0.84	0.58	0.43
Occupational status
Housewives	46	0 (0.0)	1 (2.17)	0 (0.0)
Business	110	15 (13.64)	1 (0.91)	1 (0.91)
Farming	8	1 (12.5)	0	0 (0.0)
Civil servant	15	1 (6.67)	0	0 (0.0)
Student	21	0 (0.0)	0	0 (0.0)
Total	200	17 (8.5)	2 (2.0)	1 (0.5)
p-value		0.01	0.60	1.0
Trimester
First	34	1 (2.94)	0	0 (0.0)
Second	123	12 (9.76)	2 (1.63)	1 (0.81)
Third	43	4 (9.30)	0	0 (0.0)
Total	200	17 (8.5)	2 (2.0)	1 (0.0)
p-value		0.49	0.44	0.66

Table 2.

Analysis of Collected Risk Factors Vis-a-Vis Seropositivity of Anti-HIV, HBsAg, and Anti-HCV to Establish Statistical Association Among the Variables

S/N	Risk factor history	Responses sought	No. of responders	No. of HIV⁺ (%)	p-value	No. of HBV⁺ (%)	p-value	No. of HCV⁺ (%)	p-value
1	Transfusion	Yes	49	7 (14.29)	0.10	1 (2.04)	0.44	0 (0.0)	0.57
1	Transfusion	No	151	10 (6.62)		1 (0.66)		1 (0.66)
2	Surgery	Yes	30	4 (13.33)	0.30	0	0.55	0 (0.0)	0.67
2	Surgery	No	170	13 (7.65)		2 (1.18)		1 (0.59)
3	Tattooing	Yes	12	0 (0.0)	0.28	0	0.72	0 (0.0)	0.80
3	Tattooing	No	188	17 (9.04)		2 (1.06)		1 (0.53)
4	Ear piercing	Yes	50	3 (6)	0.46	0	0.41	0 (0.0)	0.56
4	Ear piercing	No	150	14 (9.33)		2 (1.33)		1 (0.67)
5	Liver problem/jaundice	Yes	1	0 (0.0)	0.76	0	0.92	0 (0.0)	0.94
5	Liver problem/jaundice	No	199	17 (8.59)		2 (1.0)		1 (0.50)
6	Liver problem/jaundice in family members	Yes	2	0 (0.0)	0.67	0	0.89	0 (0.0)	0.92
6	Liver problem/jaundice in family members	No	198	17 (8.59)		2 (1.01)		1 (0.50)
7	Abortion/miscarriage	Yes	43	7 (16.28)	0.04	0	0.46	0 (0.0)	0.60
7	Abortion/miscarriage	No	157	10 (6.37)		2 (1.27)		1 (0.63)
8	Shared sharp object	Yes	114	10 (8.77)	0.87	0	0.10	1 (0.88)	0.38
8	Shared sharp object	No	86	7 (8.14)		2 (2.33)		0 (0.0)
9	Tribal mark	Yes	110	13 (11.82)	0.06	0	0.12	0 (0.0)	0.37
9	Tribal mark	No	90	4 (4.44)		2 (2.22)		1 (1.11)
10	History of STDs	Yes	16	4 (25)	0.01	0	0.68	0 (0.0)	0.77
10	History of STDs	No	184	13 (7.07)		2 (1.09)		1 (0.54)
11	IDU	Yes	7	3 (42.86)	0.001	0	0.79	0 (0.0)	0.85
11	IDU	No	193	14 (7.25)		2 (1.04)		1 (0.51)
12	Smoking	Yes	10	2 (20)	0.18	0	0.74	0 (00)	0.82
12	Smoking	No	190	15 (7.89)		2 (1.05)		1 (0.53)
13	Alcoholism	Yes	14	2 (14.29)	0.42	0	0.70	0 (00)	0.78
13	Alcoholism	No	186	15 (8.06)		2 (1.08)		1 (6.67)
14	Peptic ulcer	Yes	9	1 (11.11)	0.77	0	0.76	0 (00)	0.83
14	Peptic ulcer	No	191	16 (8.38)		2 (1.05)		1 (0.52)
15	Vaccination	Yes	15			0	0.69
15	Vaccination	No	185	NA		2 (1.08)	NA

IDU, intravenous drug use; HBsAg, hepatitis B surface antigen; HCV, hepatitis C virus; HIV, human immunodeficiency virus; NA, nonapplicable; STDs, sexually transmitted diseases.

Discussion

In this study, 8.5% of the apparently healthy 200 women attending the antenatal clinic of the KSUTH recruited using a nonprobability convenient sampling technique were positive for HIV. This rate is above the national HIV seroprevalence rate of 3.0% reported among antenatal women in 2014 (6), the 1% global prevalence rate (10), and the overall prevalence of 3.3% reported for Kogi State during the 2014 national sentinel survey (6). It is also higher than the seroprevalence rates of 4.9%, 5.25%, and 7.2% earlier reported among pregnant women in Osogbo, Bayelsa, and Benin City by Opaleye et al. (20), Buseri et al. (4) and Oladeinde et al. (16), respectively. In other countries, Mathur et al. (12) in India and Kabinda et al. (11) in Democratic Republic of Congo also reported lower seroprevalence rates. Our finding is comparable with the 8.9% reported in Jos, Plateau State, Nigeria (7). The seroprevalence rate in this study is suggestive of high burden of HIV infection in the study area. This calls for concern as HIV infection of mothers during pregnancy is associated with high risk of mother-to-child transmission and may also contribute to increase in the number of orphaned children in the study area.

Our observation of 1.0% for HBsAg in this study is comparable with the 2.2% reported by Oladeinde et al. (16) among pregnant women in Southern Nigeria but lower than 8.5% reported by Omatola et al. (19) among pregnant women in the Northwestern Nigeria. The seroprevalence of anti-HCV antibodies of 0.5% in this study is similar to the 0.3% reported by Parveen et al. (22) in an antenatal population in India. However, this rate is lower than findings of other epidemiological studies (2–4%) (11,18,20). The disparities in seroprevalence rates for HBsAg, HCV, and HIV in our study compared with findings from other similar epidemiological studies might be attributable to differences in sexual practices and behaviors, awareness of sexually transmitted infections (STIs), sociocultural practices, and accessibility to health care.

Pregnant women in the age range of 21–40 years had higher seroprevalence rates for the three viruses. As was previously opined by Parveen et al. (22), the reason for the peak infection in this age group could be attributed to greater probability of exposure of the women to risk factors of transmission. This finding was corroborated by assertions of Stevens et al. (28) that seropositivity of these viral infections increases until age 40 years but declines afterward.

Analysis by marital status revealed that only married women were infected by either HBV (1.18%) or HCV (0.59%). Although difference in seropositivity rates and marital status were not statistically significant, this observation points to the role of sexual intercourse in the transmission of these viruses. Marriage provides a means of unprotected sex and unfaithfulness on the part of any of the partners by way of being involved in unprotected extramarital relationship could increase the chances of exposure and transmission of HBV and/or HCV.

The higher rates of HBV, HCV, and HIV infection among women with lower level of education in this study might be because of the fact that those with higher educational attainment are probably more informed and consequently could implement prevention and control strategies. A significant proportion of pregnant women seropositive to HIV, HCV, or HBV were either business women or housewives. This finding lends credence to the role of education in disease prevention and equally justifies the assertion of Zeba et al. (30) that these occupational groups, which are usually less enlightened, still believe in traditional rituals such as tribal marks/scarification that can expose them to infection.

This study observed a significantly higher HIV seropositivity (p = 0.04) among pregnant women with history of abortion/miscarriage, thus corroborating earlier reports by Alarcon et al. (2) that history of abortion is a significant predictor of HIV seropositivity. The finding of significant HIV positivity in relation to history of STI is in conformity with previous reports of Fissehatsion et al. (9) among pregnant women in Addis Ababa.

In conclusion, the overall anti-HIV prevalence rate of 8.5% in our study confirms its endemicity in the study area. The HIV/HCV coinfection rate of 0.5% and the hepatitis B surface antigenemia rate calls for a comprehensive screening of all pregnant women for anti-HIV, anti-HCV, and HBsAg for early interventions to curb mother-to-child transmission of these viral infections and associated sequelae. It is also important to keep educating the masses on mode of spread of these viruses, implementation of universal precautions, and avoidance of high-risk sexual behavior.

Footnotes

Acknowledgments

The authors acknowledge the support and cooperation of staffs of Kogi State University Teaching Hospital, Anyigba. The authors also appreciate the pregnant women for their participation. The research was solely funded by authors.

Author Disclosure Statement

No competing financial interests exist.

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