Multiple Sexual Partners as Major Predictor of Human Immunodeficiency Virus Seropositivity Among Pregnant Women,Osun State,Nigeria

Abstract

Concerning human immunodeficiency virus (HIV) epidemiology, pregnant women (PW) are particularly vulnerable and severely affected. Nigeria has over 40 years of HIV epidemiology and enlightenments; to suggest control hub, we sought to know extant variables predicting HIV positivity among PW in selected towns in Osun State. Our hypothesis: none of the study PW's variables predicts HIV seropositivity. With ethics approval from UNIOSUN Health Research Ethics Committee, 900 consecutively selected consenting PW attending antenatal care (ANC) facilities in four towns (capital city inclusive) provided relevant sociodemographic/behavioral data with questionnaire forms; each participant was aseptically bled and plasma screened with the Alere Determine^® Rapid HIV-1/2 Kit. The presumptive reactive plasma samples (and some randomly selected nonreactive samples) were confirmed with Genscreen^® ULTRA HIV-1/2 P²⁴ antigen/antibody ELISA. Microsoft Excel and SPSS 16.0 were used for result analysis using t-test, CHI² test, and binary logistic regression. The PW were 15–50 years of age (n = 900; mean: 26.6 years [95% CI: 26.1–26.9 years]); they were predominantly 15–29 years (71.1%), married (90.8%), with one lifetime sexual partner (86.4%). Seropositive PW by screening and confirmatory tests were, respectively, 14 (1.6% [95% CI: 0.9–2.6%]) and 15 (1.7% [95% CI: 0.9–2.7%]). The latter were predominantly 20–30 years (80.0%), married (93.3%), with ≤ secondary school education (86.7%), reportedly never screened for HIV (60.0%), with 86.7% aware HIV is sexually transmitted. Analysis showed only ≥ three lifetime sexual partners was independently associated with HIV seropositivity (p = 0.03; odds ratio (OR) = 17.0). Although educational status was not associated with seropositivity, PW having primary school education had about 6 times higher likelihood of seropositivity (p = 0.06; OR = 5.7 [95% CI: 0.94–35.1]). Also, primigravida had about twice higher likelihood of seropositivity (p = 0.44; OR = 1.5 [95% CI: 0.54–4.17]). HIV seropositivity was relatively low and majorly predicted by ≥ three lifetime sexual partners; suggesting this as prime focus of HIV counseling among PW attending ANC in Osun State, Nigeria.

Introduction

Pregnant women (PW) are central to epidemiological assessment of human immunodeficiency virus (HIV) in Nigeria (21) and sub-Saharan Africa; this is due to the fact that antenatal clinic (ANC) attendees are used for estimation of national and state-level HIV prevalence rate (33). ANC attendees of 15–49 years are veritable group for HIV epidemiology because they are sexually active; in addition, the act of human procreation commonly involves unprotected heterosexual intercourse that allows for HIV transmission when involved persons are infected (2). Therefore, since 1986 when the first case of HIV was reported in Nigeria, data generated from ANC attendees had been used to monitor the trends of HIV epidemic (1) before the recent largest ever national survey by NAIIS Consortium (9).

The virus, which consists of two types (HIV-1 and -2) belonging to Lentivirus genus in the Retroviridae family, is commonly transmitted and acquired through unprotected heterosexual intercourse. Other modes of HIV-1/2 transmission include blood transfusion; breast feeding; in utero mother-to-child or perinatal spread during child labor (32). Although both types can cause acquired immunodeficiency syndrome (AIDS), HIV-1 is the major cause of global AIDS pandemic (14). HIV-1 weakens the immune system of infected humans such that in the absence of adequate retroviral therapy, the victim progresses toward virus-mediated immunodeficiency and death (4).

In developing countries, women are central to and harder hit by HIV-1 pandemic. The reason is they are at higher risk of contracting HIV infection than men for biological and sociocultural reasons (32). Langerhans cells of the cervix of female genitalia have higher affinity for some strains of HIV-1, hence the female urogenital tract is more efficient in the heterosexual transmission. Consequently, the rate of HIV transmission from male to female is two to three times higher than vice versa (25,29). Other biological factors facilitating higher HIV infection rate among females include inflammation/ulceration of vulva and vagina; and presence of sexually transmitted infections/diseases (13,15).

In addition, there are sociocultural factors that predispose women to HIV infection more than men, these include, but not limited to, gender inequality; poverty; lesser access to formal education; lower employment opportunity; female circumcision; male resistance to condom use during sexual interaction and polygamy coupled with husbands' infidelity. Others are early sexual debut, unprotected sexual intercourse with multiple and concurrent sexual partners, or intergenerational and transactional sex (6,10,26 –28).

Another factor enhancing women's susceptibility to HIV infection is pregnancy, during which there is temporal immunosuppression in both HIV-infected and uninfected women, such as reduced immunoglobulins, complement levels, and cell-mediated immune response that make pregnant HIV-uninfected women more susceptible if exposed to the virus (16,18,24). Conversely, HIV infection also influences outcome of pregnancies; adverse outcomes such as spontaneous abortion (7), still birth (30), and preterm labor have been reported (5,19).

A major gateway to HIV/AIDS prevention, treatment, and care services is testing of citizens for exposure to the virus (8). Consequently, HIV Testing Services [HTS], which now replaces HIV Voluntary Counseling and Testing [HCT], is one of the five thematic areas of Nigeria National Strategic Framework for HIV and AIDS prevention and control interventions (20). The HTS currently adopted in Nigeria is voluntary and conforms with WHO's five C's, namely, consent, confidentiality, counseling, correct test results, and connections to care, treatment, and prevention services (8). The HTS algorithm used in Nigeria comprises screening of blood or plasma/serum for presence of HIV-specific antibodies using two Rapid HIV Test Kits (e.g., Determine^® and Stat-Pak^®) in serial or parallel algorithm; this is followed by testing of reactive samples with enzyme immunoassay (EIA) or indirect immunofluorescence assay.

Samples reactive to the EIA Kit are further confirmed by Western Blot assay. However, for epidemiologic purpose, initial screening and confirmation of blood samples using two different Rapid HIV Test Kits or use of EIA after initial screening with the Rapid Kit is sufficient to document HIV prevalence (8,12).

Undoubtedly, unprotected heterosexual intercourse remains the major route of HIV transmission among adults in sub-Saharan Africa and Nigeria; whereas more than 90% of HIV-infected children acquired it from infected mothers (3,32). PW living with HIV/AIDS therefore remain an important group to consider when building a picture of HIV epidemic. With over 40 years of HIV epidemic/epidemiology and enlightenments in Nigeria; it is important to continue to monitor HIV trend, risk factors among women and to suggest control hub. We hence sought to know current seroprevalence rate and the extant variables predicting HIV positivity among PW from four towns (Osogbo, the capital inclusive) in Osun State.

Materials and Methods

Study sites and population

The study conducted between March and October, 2019 involved four popular towns (including the capital city, Osogbo) in Osun State, a southwestern state in Nigeria. The towns were Osogbo, Ile-Ife, Ede, and Ikire, predominantly occupied by Yorubas. The study population were PW in the study locations. Selected health facilities with antenatal care sections were used for the study. The health care facilities in Ede, Ile-Ife, and Osogbo were government owned; whereas the one in Ikire was a private hospital.

Study design

This was a cross-sectional HIV-1 serosurvey that was antenatal care center-based. Ethics approval to conduct the study was obtained from UNIOSUN Health Research Ethics Committee (HREC). With permission of Managements of respective Health Care Facilities, PW were informed by health personnel on the objectives and protocols of the study; they were thereafter consecutively recruited in each study site as they presented for antenatal care. Each PW provided written consent and pertinent sociodemographic/behavioral data through interviewer-administered questionnaire form. Recommended serial testing algorithm was used for the serosurvey, with a fourth generation ELISA that detects HIV-1 P²⁴ antigen and antibody for confirmatory assay following initial presumptive Rapid HIV-1/2 test.

Sample collection

Each PW was aseptically bled by venipuncture into EDTA-treated blood sample tube. Plasma was prepared from the blood samples by centrifugation at 3,000 rpm for 10 min. The plasma samples were stored at −20°C until used for serological assays.

Serological assays

Each frozen plasma sample was allowed to completely thaw at room temperature prior testing. With serial testing algorithm, each sample was first screened with the Alere Determine HIV-1/2 Kit (sensitivity 100% and specificity 99.6%) according to the manufacturer's instructions. The samples reactive to the Rapid Test Kit were subjected to confirmatory assay using the Genscreen^® ULTRA HIV-1/2 P²⁴ antigen/antibody ELISA (sensitivity 100% and specificity 99.75%) as per instructions of the manufacturer. Since only 14 of the 900 plasma samples were reactive to the Determine Rapid Kit, randomly selected unreactive samples were included in the ELISA to complete the 96 microtiter wells (including wells for controls). As the fourth generation ELISA used for confirmation of reactive samples is very sensitive and specific, those positive to the ELISA were considered HIV-1 seropositive and the other plasma samples seronegative.

Data analysis

Results of the study are presented with descriptive statistics (mean; median; percentage, 95% confidence interval). To establish existence of statistical associations between participants' variables and seropositivity of HIV antibody, Chi-square test, Student's t-test, and binary logistic regression were used as appropriate. Microsoft Excel and SPSS version 16.0 for Windows were used for statistical analysis. A p-Value ≤0.05 was used as indicator of statistical significance.

Results

Demography of the PW

The total participants (ANC attendees) were 900; age range was 15–50 years (mean age: 26.6 years [95% CI: 26.1–26.9 years]); 71.1% (640) of them were young adults. The level of literacy of the PW could be described as low, as 622 (69.1%) of them had ≤ secondary school education (4 of these had no formal education); 817 (90.8%) of them reported being married. Among them were 330 (36.7%) primigravida (those carrying their first pregnancies). Understandably, 69.2% (202) of the 292 who responded “no” to “Ever attended antenatal before?” were primigravida. While 82.9% reported having one lifetime sexual partner, 14 (1.6%) reportedly had ≥3 sexual partners; other demographic data are shown in Table 1.

Table 1.

Group-Specific Human Immunodeficiency Virus Seroprevalence Rates for the Pregnant Women and Associated Factor, Osun State, Nigeria

Variables	No. tested (%)	No. positive (%)	Odds ratio (95% CI)	p-value
Town/Location
Ikire	150 (16.7)	2 (1.3)	1^b
Ede	150 (16.7)	2 (1.3)	1.0 (0.14–7.19)	1.00
Osogbo	300 (33.3)	4 (1.3)	1.0 (0.18–5.52)	1.00
Ile-Ife	300 (33.3)	7 (2.3)	1.8 (0.34–8.62)	0.48
Age (years)
15–29	640 (71.1)	11 (1.7)	1.1 (0.35–3.55)	0.85
30–50	260 (28.9)	4 (1.5)	1^b
Educational status^a
Primary	75 (8.4)	3 (4.0)	5.6 (0.94–35.10)	0.06
Secondary	543 (60.6)	10 (1.8)	2.6 (0.56–11.9)	0.22
Tertiary	278 (31.0)	2 (0.8)	1^b
Marital status
Single	83 (9.2)	1 (1.2)	1^b
Married	817 (90.8)	14 (1.7)	1.4 (0.19–11.01)	0.73
Ever screened for HIV?
No	484 (53.8)	9 (1.9)	1.3 (0.46–3.66)	0.63
Yes	416 (46.2)	6 (1.4)	1^b
Gravidity^c
Primigravida	330 (37.0)	7 (2.1)	1.5 (0.54–4.20)	0.44
Multigravida	561 (63.0)	8 (1.4)	1^b
Ever attended ANC before?^d
No	292 (32.8)	8 (2.7)	2.4 (0.85–6.62)	0.09
Yes	598 (67.2)	7 (1.2)	1^b
Ever received blood transfusion?^e
Yes	63 (7.1)	1 (1.6)	1b
No	823 (92.9)	14 (1.7)	1.1 (0.14–8.29)	0.95
Ever donated blood?^f
No	846 (97.4)	14 (1.7)	—
Yes	23 (2.6)	0 (0.0)		Invalid
Ever shared razor blade?^g
No	654 (73.3)	9 (1.4)	1^b
Yes	238 (26.7)	6 (2.5)	1.9 (0.65–5.26)	0.24
Ever shared needle?^h
No	691 (77.5)	12 (1.7)	1.2 (0.33–4.17)	0.81
Yes	201 (22.5)	3 (1.5)	1^b
No. of lifetime sexual partnersⁱ
1	746 (86.4)	12 (1.6)	1.7 (0.23–12.96)	0.63
2	103 (11.9)	1 (0.97)	1^b
≥3	14 (1.6)	2 (14.3)	17 (1.43–201.76)	0.03
Ever heard of HIV?^j
No	84 (9.5)	2 (2.4)	1.5 (0.33–6.67)	0.61
Yes	802 (90.5)	13 (1.6)	1^b
Knowledge of sexual spread of HIV^k
No	76 (8.7)	2 (2.6)	1.6 (0.35–7.29)	0.53
Yes	793 (91.3)	13 (1.6)	1^b

Illiterate were 4 in number with zero positivity (hence excluded from the analysis).

Reference group.

9 PW did not respond to this.

10 PW did not respond to this.

14 PW did not respond to this.

31 PW, one of which was seropositive, did not respond to this.

8 PW did not respond to this.

37 PW did not respond to this.

14 PW did not respond to this.

31 PW did not respond to this.

Crossmatching the young PW (15–29 years) with some of these data, we found out that 71.7% of this category had a lower level of formal education (≤ secondary school education), were mostly married (87.8%), and constituted more than half (50.6%) of the primigravida. Of the 627 PW in this group that provided information on “ever heard of HIV?” 89.1% responded “yes”; however, almost 60.0% (59.7%) of this group never screened for HIV. It was good to know that 90.5% of this category of the PW knew HIV is sexually transmitted. Of the total 14 participants that reported having ≥3 lifetime sexual partners, 64.3% were young PW.

HIV-1 seroprevalence rate of the PW

Of the 900 PW studied, 14 (1.6% [95% CI: 95% CI: 0.9–2.6%]) were initially reactive to the Determine Rapid Kit; whereas 15 (1.7% [95% CI: 0.9–2.7%]) tested positive to the confirmatory ELISA. It was noted that 11 of the 14 samples reactive to presumptive rapid test were also seropositive with the ELISA to show 78.6% concordance with the presumptive test. The remaining four samples seropositive to the ELISA were initially nonreactive (i.e., false-negative results) to the Rapid Kit and were considered missed (4/15 [26.7%]) by the Rapid Kit. It was also observed that three samples reactive to the Rapid Kit (i.e., false positive results) were negative to ELISA.

It was noticeable that the 15 seropositive PW were predominantly 20–30 years in age (80.0%), married (93.3%), with ≤ secondary school education (86.7%); reportedly never screened for HIV (60.0%); with 86.7% aware that HIV is sexually transmitted.

As shown in Table 1, group-specific prevalence rates ranged from 0.0% for those that responded “yes” to “Ever donated blood” to 14.3% for those having ≥3 lifetime sexual partners (median: 1.6% seroprevalence rate [i.e. the distribution was right-skewed]). The younger PW (15–29 years) had slightly higher seropositivity compared with the older ones (1.7% vs. 1.5%; p = 0.85). Although the PW with primary school educational status were just 75 (8.3%) in number, this group had the highest seroprevalence rate with respect to educational status (4.0%; p = 0.06). Other groups with insignificant but relatively high seroprevalence rates include PW from Ile-Ife; secondary educational status; primigravida; “no” to “Ever attended ANC before?”; “yes” to “Ever shared razor blade?”; “no” to “Ever heard of HIV?”; and “no” to “Knowledge of sexual spread of HIV” (Table 1).

Association between HIV-1 seroprevalence and variables of the PW

We observed that the seropositive (n = 15; mean age: 27.7 years) and seronegative (n = 885; mean age: 26.6 years) PW were statistically comparable (p = 0.45) in mean age. Only the number of lifetime sexual partner had significant association (p = 0.03) with HIV-1 seropositivity with those reporting ≥3 lifetime sexual partners having 17 times higher likelihood of being so when compared with those having two sexual partners. We also observed that the PW who reported having one lifetime sexual partner recorded higher HIV seroprevalence rate (1.6%) compared with those having two (0.97%). While other variables showed no significant association with HIV seropositivity, many of the groups manifested higher likelihood of seropositivity compared with respective reference groups, and these include Ile-Ife (OR: 1.8); others are primary and secondary educational status; primigravida; those reporting “no” to “Ever attended ANC before?” and “yes” to “Ever shared razor blade?”; “no” to “Ever heard of HIV?”; and “no” to “Knowledge of sexual spread of HIV” (Table 1).

Discussion

This study aimed at assessing HIV seroprevalence among PW presenting for antenatal care in four selected towns in Osun State with the view to identifying prime risk factor(s) for the infection. As previously observed, PW constitute a critical group in HIV epidemiology; they are particularly vulnerable due to temporal compromised state of their immunity, they could transmit HIV to their recent sexual partners and unborn children, and in sub-Saharan Africa, they have significantly higher probability of maternal/child death (23). Having had more than 40 years of HIV epidemic and enlightenments in Nigeria, we need to identify the prime factor(s) exposing PW to HIV for the purpose of protecting this critical population.

The study showed that most of the PW were young adults (71%); but married (90.8%) with more than 80% reporting having one lifetime sexual partner, both suggesting high level of sexual fidelity. As previously shown, young people are still very relevant to HIV epidemiology in Nigeria (22).

Reports have it that females in sub-Saharan Africa had less access to formal education (31); since we did not compare the PW with their male counterparts, this study could not really say the 69.1% having ≤ secondary school education connote lesser access to formal education. However, their level of formal education could be described as low because about 70% of them had ≤ secondary school education. The latter might connote low level of enlightenment regarding HIV infection prevention/control, corroborated by more than 50% that had never screened for HIV; conversely, about 90% of them reported having heard about HIV and that the virus is sexually transmitted. Their high level of knowledge about mode of HIV transmission might explain the reason for their low proportion (13.6%) having more than one sexual partner.

Advancing age may correspond with level of exposure/enlightenment, the young PW (15–29 years) manifested inverse relationships with basic information on HIV infection prevention/control, as about 90% of this category reported having heard about the virus and its sexual mode of transmission. However, concerning their sexual behaviors, the younger age probably dictated the contribution of higher proportion (64.3%) of those having ≥3 lifetime sexual partners and reason about 60% of the young PW had never screened for HIV before this study.

Regarding HIV seroprevalence, the PW recorded overall rate of 1.7%. This rate could be described as low vis-à-vis the sample size (n = 900); this was lower than Osun State's HIV prevalence rate of 2.6% reported by Nigeria FMoH (11) among ANC women. It was rather comparable to national HIV prevalence rate of 1.9% (among 15–49 year olds) reported by NAIIS Consortium (9) that conducted the largest ever household-based national HIV survey in Nigeria. The 1.7% was however, higher than 1.2% reported by the same Consortium for the entire south-west zone of Nigeria. A possible reason for the difference could be that this study was antenatal care center based and restricted to only four towns in Osun State (a Nigerian southwestern state).

Among the PW, group-specific prevalence rates ranged from 0.0% to 14.3%, the upper limit was due to the highest value recorded among the 14 PW that reported having ≥3 lifetime sexual partners. The lower limit occurred among women with history of blood donation; the zero rate was therefore expected as blood donation requires that blood donors are HIV negative. The observation that the 15 seropositive women were predominantly young adults with ≤ secondary school education suggests we need to increase HIV enlightenment/awareness among young PW as they attend ANC.

Analysis of HIV seroprevalence rate vis-à-vis some variables of the PW was done. This showed that, with respect to age, the 15 seropositive women were truly a subset of the 900 PW as they were comparable in mean age with the remaining seronegative women. We observed that, of all the variables studied, only the number of lifetime sexual partner significantly associated with HIV seropositivity among the PW; in addition, this factor showed that those having ≥3 lifetime sexual partners were about 17 times more likely to be HIV seropositive. This clearly showed that PW visiting ANC centers in Osun State need to be counseled against having more than one lifetime sexual partner to reduce their exposure to HIV. In addition, by extension, having only one sexual partner would reduce spread of the virus to unborn child and also reduce maternal/child mortality. The observation that those having one lifetime sexual partner had higher, although not statistically significant, HIV seroprevalence rate compared with those having two sexual partners indicated that the virus transmission is not restricted to sexual mode alone.

There were other variables of the PW that, although not significantly associated with the seropositivity, showed higher likelihood of making the participants seropositive for HIV. These include being from Ile-Ife; having primary and secondary educational status; primigravida; never attending ANC before; sharing razor blade; never heard of HIV; and not knowing HIV can be sexually transmitted (Table 1). Since Ile-Ife is comparable to Osogbo (the capital of Osun State) with respect to urbanization, tertiary institutes of education and health (OAU and OAUTHC), the reason for higher HIV prevalence rate among those attending ANC in Ile-Ife compared with those from Osogbo, could not be easily discerned. However, the fact that Ede and Ikire are not as urban as Ile-Ife coupled with higher sample size from the latter, might explain the reason for lower prevalence rates in the two former towns.

We also observed that 6 (42.9%) of the 14 women reporting ≥3 lifetime sexual partners happened to be from ANC in Ile-Ife. These implies that HIV counseling efforts would need to be intensified in Ile-Ife among PW. Understandably, low level of formal education might mean low level of public enlightenment regarding infectious diseases, such as HIV. This was evidenced by the observation that PW having primary school education that constituted as low as 8.3% of the PW had highest HIV seroprevalence rate with four times higher likelihood of being so compared with those with tertiary educational status. In addition, not attending ANC where counseling regarding HIV spread and control could be provided and sharing sharp objects like razor blades could increase exposure to HIV, hence the increased likelihood of seropositivity observed in this study. Therefore, public enlightenments in Osun State (and Nigeria) on HIV transmission/acquisition, as well as, prevention strategies would also need to target PW having less than tertiary education and young women (primigravida) attending ANC for the first time. They would also need to be counseled against sharing sharp objects like razor blades that can transmit blood-borne infectious agents like HIV.

Regarding Rapid diagnostic tests (RDTs) in epidemiological study of HIV infection, RDTs have been reported to be a matter of concern (17); as performed in their study, nationally approved serial algorithm was used with intriguing results from the presumptive and confirmatory assays (8,12). As a resource-limited country, retesting all the 900 samples with ELISA was financially prohibitive, hence the use of serial algorithm; however, from an epidemiological point of view, the Rapid Kit performed poorly as it missed 26.7% of positive samples. As once observed (17), missing positive samples is possible when HIV infection is recent with antibody below the detection limit by the Rapid Kit (Determine in our case), which implies that, the 4 HIV-reactive patients might receive negative report with the attendant possibility of spreading the virus. In the same vein, it was ethically inappropriate to say the 3 false-positive patients were HIV reactive. From all these, as once recommended, a Rapid Kit that detects HIV-1 p²⁴ antigen that can detect recent HIV infection would be appropriate for resource-limited settings for epidemiological study, and when possible, Western Blot should be employed to confirm samples tested by Rapid and ELISA Kits.

Conclusively, the PW manifested relatively low HIV seropositivity; the number of lifetime sexual partners could be a prime focus for HIV counseling and testing among PW attending ANC in Osun State, Nigeria to reduce their exposure to HIV.

Footnotes

Acknowledgments

The authors appreciate the Managements of the various ANC centers/Health facilities used for this study. They thank the health care personnel that assisted in one way or the other in the course of this study; they also thank the PW for participating in the study. Efforts of the laboratory technologists and Olaniyan Olabode that assisted in conducting the ELISA did not go unappreciated.

Author Disclosure Statement

The authors declare no conflicts of interest.

Authors' Contribution

G.O., B.T., A.A., M.A., S.A., and A.A. collected the samples, prepared proposal for ethics review and contributed to sample serologic analysis. W.F. conceived the research, designed the study, participated in serologic assay, analyzed and interpreted the data, and prepared the article. All authors approved of the final article for publication.

Funding Information

The study received no external funding other than the fund provided by the authors.

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