Seroprevalence,seroconversion,and mother-to-child transmission of dual and triplex infections of HIV,HBV,and HCV among Nigerian obstetric population: A national multicentre prospective cohort study

Abstract

Objectives

To determine seroprevalence, seroconversion, and mother-to-child transmission (MTCT) rates for dual and triplex infections of human immunodeficiency virus (HIV), hepatitis B virus (HBV), and hepatitis C virus (HCV) among pregnant women.

Methods

A multicentre prospective cohort study was conducted in six randomly selected tertiary hospitals from six geopolitical zones of Nigeria. Consenting participants were tested at recruitment for triplex infections and followed-up till delivery. Retests were performed at delivery for those who tested negative for all three infections/positive for only one. Polymerase chain reaction was used for validation while rapid test kits were employed for initial screening.

Results

Of the 2775 participants recruited, 13 (0.47%; 95% CI: 0.25%–0.80%) and 4 (0.14%; 95% CI: 0.04%–0.37%) were seropositive for dual and triplex infections, respectively. Dual infections revealed seroprevalences of 0.22% for HIV-HBV (6/2775; 95% CI: 0.08%–0.47%), 0.14% for HIV-HCV (4/2775; 95% CI: 0.04%–0.37%), and 0.11% for HBV-HCV (3/2775; 95% CI: 0.02%–0.32%). Multivariable analysis highlighted significant associations between HIV/HBV co-infection and religion (adjusted odds ratio (aOR): 0.068, 95% CI: 0.006–0.757) and house ownership (aOR): 1.65 × 10^–9, 95% CI: 1.60 × 10^–9–1.70 × 10⁻⁹). Continuing our follow-up until delivery for 2403 initial participants, 2386 did not have dual or triplex infections at the start. Upon retesting at delivery, three of these women were seropositive for a dual infection of HIV and HBV, giving a seroconversion rate of 0.12% (95% CI: 0.03% to 0.37%). MTCT rate stood at 0% at 6-week post-delivery.

Conclusion

We observed a relatively low seroprevalence and seroconversion rates for dual and triplex infections of HIV, HBV, and HCV among pregnant women in Nigeria and no MTCT.

Keywords

antenatal women HIV infection HBV HCV stillbirth triple infection

Introduction

Hepatitis B virus (HBV), hepatitis C virus (HCV), and human immunodeficiency virus (HIV), along with their dual or triplex combinations, continues to be a significant global public health concern, primarily impacting women.¹ In 2022, there were about 39 million HIV-positive individuals in the world.² Of these, 53% were women and girls, 37.5 million were adults, and 1.5 million were children under 15 years.² Currently, 257 million individuals are afflicted with chronic hepatitis B, and another 71 million with chronic hepatitis C. Should the current rate of spread remain unchanged, it is forecasted that both hepatitis B and C will lead to 20 million deaths from 2020 to 2030.³

There is evidence that co-infections with HIV, HBV, and HCV are common in sub-Saharan Africa.⁴ A recent study in Northwest Ethiopia reported that the co-infection rate of HBV and HCV among HIV-positive pregnant women was 0.4% for each.⁴ According to another recent study conducted in South Africa, 12.2% of those living with HIV/AIDS are also co-infected with HBV.⁵ The high rate of co-infections of HBV or HCV among HIV-positive population could be attributed to common routes of transmission such as sharing of sharps, sexual intercourse or mother-to-child transmission. Concerning dual and triple infections during pregnancy, a recent study by Tesfaye et al. revealed that a history of abortion (AOR = 11.028, 95% CI = 1.671–72.776, p = .013) and prior blood transfusion (AOR = 11.298, 95% CI = 1.066–119.777, p = .044) were significantly linked to an increased risk of HBV infection.⁴ However, multiple sexual partners (AOR = 18.819, 95% CI = 1.074–329.680, p = .045) and a history of abortion (AOR = 12.550, 95% CI = 1.174–134.202, p = .036) were the only significant predictors of HCV and HIV infections, respectively.⁴ Compared to any of these single infections, coinfection can result in more rapid disease progression, a variety of liver-related disorders, dysfunction of non-hepatic organs, and ultimately death.^5–9 Antiviral drug adverse effects, such as hepatotoxicity, drug resistance, and a lack of necessary responses, make treating coinfected individuals more difficult.⁵ Conversely, coinfected persons need to receive various pharmacological treatments concurrently, for the treatment of HIV in addition to HBV and/or HCV.^5–7

UNAIDS and WHO warn that there has been uneven progress in reducing new HIV, HBV, and HCV infections, increasing access to treatment, and ending AIDS and chronic hepatitis B and C-related deaths.^3,4,10 This is because many vulnerable people and populations have been left behind, despite the availability of an expanding range of effective HIV and hepatitis prevention tools and methods and a massive scale-up of HIV and hepatitis B and C screening and treatment in recent years.^3,4,10 Persistent financial constraints, along with stigma, discrimination, and social marginalisation, continue to hinder HIV and hepatitis B and C screening, treatment, and prevention efforts. These challenges remain significant barriers to addressing dual and triple infections effectively. Sustained commitment and ongoing epidemiological research are essential to strengthening global responses and ensuring the success of screening and treatment programmes.² There is currently a paucity of information regarding the seroprevalence, seroconversion, and transmission of dual and triplex infections from mother-to child during pregnancy in Nigeria. While some small-scale research has been done on dual and triplex infections in Nigerian cities, it has only been done at the state or city level and with a small sample size.^11–13

However, a significant gap in large-scale research is needed to determine the nationwide seroprevalence, seroconversion, and risk factors associated with dual and triplex infections. Furthermore, prior studies on the seroprevalence and mother-to-child transmission of triplex infections during pregnancy were inconsistent in the period for assessments and methods of assay for HIV and HBV viruses. Therefore, the authors suggested conducting more extensive and detailed prospective studies on dual and triple infections, given their clinical and epidemiological importance in co-infected individuals. They also highlighted the need to utilise Polymerase Chain Reaction (PCR) technology for accurate diagnosis.^14,15 Therefore, this study focuses on assessing the seroprevalence, seroconversion rates, and mother-to-child transmission rates of dual and triplex infections of HIV, hepatitis B, and hepatitis C viruses among pregnant women in Nigeria.

Methods

Study design and setting

This prospective cohort study was carried out between December 2020 and December 2021 at six tertiary hospitals each from a region of the countries six geopolitical zones. Apart from the lead institution for the TETFund National Research Fund 2019 (Nnamdi Azikiwe University Teaching Hospital, Nnewi (South- East), the other five institutions were randomly selected and included: University of Abuja Teaching Hospital, Gwagwalada (North-Central), University of Port Harcourt Teaching Hospital, Port Harcourt (South-South), Obafemi Awolowo University Teaching Hospital Complex, Ile-Ife (South-West), University of Maiduguri Teaching Hospital, Maiduguri (North East) and Aminu Kano Teaching Hospital, Kano (North West) from which we got representative participants. The full description of the study protocol¹⁶ as well as findings from the pilot study had been published elsewhere.^17,18

Participants

The study participants were drawn from pregnant women receiving antenatal care (ANC) in the selected hospitals. These women were categorised into two groups based on their HIV, HCV, and HBV status. The exposed group included pregnant women with at least two infections of HIV, HCV, or HBV, while the unexposed group comprised pregnant women either without any of these infections or with only one infection. Both groups of pregnant women and their infant pairs were monitored prospectively through the delivery period and up to 6 weeks post-delivery.

Inclusion and exclusion criteria

Women who attended their first ANC visit at the six tertiary hospitals during the study period and consented to participate were included. However, those who were critically ill and unable to continue follow-up visits, as well as those who declined participation, were excluded. Additionally, pregnant women with an indeterminate HIV serostatus or uncertain gestational age were not included in the study.

Sample size determination

The sample size for this study was calculated using Cochran’s formula for sample size determination, as outlined by Noordzij et al.,¹⁹ which is applicable when the population exceeds 10,000, as mentioned in the published protocol.¹⁶ The formula used was N = Z²αPQ/d². Here, ‘Z’ represents the standard normal deviation corresponding to a 95% confidence interval, ‘P’ denotes the issue prevalence (which, in this case, is the prevalence of health facility delivery rate among pregnant women in Nigeria, identified as 38.0% based on a recent study by Adedokun and Uthman utilising data from the 2013 Nigeria Demographic and Health Survey involving 20,192 women who had given birth within 5 years of the survey²⁰), ‘Q’ equals 1-P, and ‘d’ is the desired margin of error set at 0.05. The final figure was adjusted to accommodate a potential 10% attrition or nonresponse rate, resulting in a non-inferiority sample size of 363, which was then rounded up to 400. Consequently, a minimum of 400 pregnant women were enlisted from each of the six hospitals chosen, and a total of 2775 women were enrolled.

Sampling techniques

A tertiary hospital from each of Nigeria’s five geopolitical zones, in addition to the lead institution in the South-East geopolitical zone of the country, was selected through a simple random sampling method employing a lottery system. Every eligible pregnant woman who provided informed consent was enrolled progressively until each selected hospital’s allocated sample size was achieved.

Data collection procedure and quality assurance

A validated, pre-tested, structured, and interviewer-administered questionnaire was used to collect the data. The information was gathered using an interviewer-administered, structured, and standardized questionnaire. Individual interviews using a standardized questionnaire were used to gather clinical and sociodemographic data: numerous sexual partners, age, ethnicity, marital status, education, gravidity, and parity.

The tool was initially created in English, then translated into the mother tongues of Igbo, Yoruba, and Hausa to avoid communication problems, and lastly translated back into English to guarantee consistency with the assistance of linguists and public health specialists. Experts in infectious diseases, paediatricians, midwives, and obstetricians participated in face and content validity testing. Following delivery, information on the outcome variables – such as whether the newborn was born alive or stillborn, and other pertinent data were gathered from the mother and the infant. Additional information was gathered using a checklist from the pregnant women’s integrated prenatal, labour, delivery, and postnatal care records after delivery. Under the direction of the obstetricians who served as study site coordinators, data was gathered by skilled research assistants.

Supervisors and data collectors received training. Throughout the data-collecting period, daily supervision was provided by the supervisors, the lead investigator, or site coordinators. At the health facility where the pregnant women received their ANC follow-up, appropriate health information was given to them regarding the significance of consistent ANC attendance and, if feasible, institutional delivery.

Study variables

Operational definitions of study outcomes

The study’s outcome variables were the mother-to-child transmission rates, seroconversion rate, and seroprevalence rate. Seroprevalence for dual or triplex infections refers to the number of pregnant women who, at the start of the trial, tested positive for at least two illnesses – HCV, HBV, or HIV. Seroconversion for infections with multiple or triplex pregnant women who tested negative for any dual or triplex infection at the start of the study and tested positive for at least two or triplex infections during labour or delivery. When newborns exposed to at least two infections of HIV, HBV, or HCV become seropositive for at least two infections of HIV, HBV, or HCV at birth or within 6 weeks of life, it is implied that MTCT has occurred.

Exposure variable

The status of HIV, HBV, and HCV was taken into account as an exposure variable. As per the World Health Organisation, an individual who tests positive for HIV and has a second HIV antibody test or a positive virological test for HIV or its components confirmed by a second virological test acquired from a different determination is considered to be HIV positive.¹⁶ As part of the body’s normal immune response to infection, the body routinely develops antibodies to HBsAg.¹⁶ Hepatitis C virus infection is said to occur when a reactive or positive HCV antibody test is obtained. During the initial ANC follow-up, HIV, HBV, and HCV testing and diagnosis were carried out at the ANC clinics following Nigerian testing and counselling guidelines.

Independent variables

The independent variables include the study participants’ sociodemographic obstetric and medical factors.

Outcome ascertainment

Rigorous measures were employed during the data collection to ensure accurate outcome ascertainment. The gestational ages of the individuals were determined using the last menstrual period (LMP) and, when available, an ultrasound conducted before 20 weeks of gestation. We calculated the difference in days between the gestational age as determined by early ultrasound (before 20 weeks) and the date of the last menstrual period for pregnant women with a known LMP. If the discrepancy was less than 7 days, the LMP was utilised as the gestational age. Conversely, if the gestational age discrepancy exceeded 7 days, the age indicated by the ultrasound was adopted. In cases where an ultrasound before 20 weeks was not performed, the LMP was exclusively used to determine the gestational age.

Detection of dual and triplex infections

For serological testing, approximately 10 mL of peripheral blood were collected from each participant by trained medical professionals or laboratory scientists. The blood samples were briefly tested for HBV antigen and antibodies against HIV and HCV. Participants who initially tested negative for HIV, hepatitis B, and C viruses at the baseline were re-screened during labour or delivery.

For HIV testing, the Alere Determine HIV-1/2 test kit (Alere Medical Co. Ltd., Matsudo, Japan) was employed in a series, adhering to the Nigerian National HIV testing guidelines. In cases of positive results, confirmation was sought using the Uni-Gold Recombigen® HIV-1/2 (Trinity Biotech, Ireland) assay, followed by the HIV1/2 STAT-PAK (Chembio Diagnostic Systems, Inc., USA), as a tie breaker when the first two tests showed discordance results. According to the manufacturer, the HBsAg and anti-HCV were tested using the ELISA kit from LabACON (Hangzhou Biotest Biotech Company, Ltd., China), which boasts a 99.0% specificity and a 99.9% sensitivity. Each kit included controls to ensure accuracy. All procedures strictly followed the manufacturer’s guidelines, ensuring precise and reliable outcomes reporting.

Determination of viral load for HIV, hepatitis B, and C viruses

The Roche Cobas CTM/CAP real-time PCR technology was utilised to measure the viral loads of HIV, HBV, and HCV. After being separated at the collection sites, all blood samples designated for viral load testing and newborn status evaluation were stored in a freezer at minus 25°. These samples were then batched and transported under cold chain conditions to the Molecular Virology Laboratory at Nnamdi Azikiwe University Teaching Hospital (NAUTH) in Nnewi, Anambra State, Nigeria, and to other participating hospitals for analysis.

Diagnosis of infant HIV, HBV, and HCV

The HIV status of infants exposed to the virus was determined following the latest Nigerian National PMTCT (Prevention of Mother-To-Child Transmission) Guidelines.²¹ All newborns exposed to HIV, HBV, and HCV were screened using DNA PCR (Polymerase Chain Reaction). Dried blood samples (DBS) were collected from the infants at birth and again at 6 weeks old. These samples were then analysed using PCR at the Molecular Virology Laboratories to diagnose infections.

Data management and statistical analysis

Initially, the collected data were cleaned, coded, and entered into a Microsoft Excel spreadsheet. Subsequently, the data were transferred to SPSS version 23.0 (IBM, Armonk, NY, USA) for comprehensive analysis. The normality of continuous variables was evaluated using the Kolmogorov–Smirnov test. Continuous data were presented as means and standard deviations, while categorical data were expressed as frequencies and percentages. The independent sample t-test was utilised to compare continuous data with a normal distribution. Descriptive statistics, including frequencies, percentages, means, and standard deviations, were used to outline the characteristics of the study participants.

Depending on data suitability, categorical variables were analysed and compared based on participants’ exposure status using Pearson’s chi-square test or Fisher’s exact probability method. A generalised regression analysis was conducted to assess the influence of risk factors on the incidence of dual and triplex infections, revealing the likelihood ratios of predictor variables. For the multinomial regression analysis, variables were selected based on their significance in the bivariate analysis (p-value <.05) or their clinical relevance. This approach ensured that key predictors were appropriately considered in the multivariable model. The model’s goodness-of-fit was assessed using Pearson’s goodness-of-fit criterion, with a probability value greater than 0.05 indicating an acceptable model fit. Within the multivariable model, variables with a p-value less than 0.05 were considered statistically significant, maintaining a 95% confidence interval.

Ethics statement

The study was approved by the National Health Research Ethics Committee, Nigeria, on 23 January 2020, with ethical approval number NHREC/01/01/2007–23/01/2020. Written informed consent was obtained from all participants before their enrolment in the study, ensuring that they fully understood the study’s objectives, procedures, potential risks, and benefits. Participants were assured that their participation was entirely voluntary and that they had the right to withdraw from the study at any time without any consequences. To maintain confidentiality, all collected data were anonymised and securely stored, with access restricted to authorised research personnel only. Unique identification codes were used instead of personal identifiers to ensure privacy. For participants who tested positive for HIV, HBV, or HCV during the study, appropriate counselling and referral to designated healthcare facilities were provided in accordance with national treatment guidelines. Treatment costs for positive cases were not covered by the study, but participants were directed to available government and non-governmental programmes that provide free or subsidised treatment and care. The study was conducted in strict compliance with the ethical principles outlined in the Declaration of Helsinki and relevant national guidelines on human research ethics.

Results

Cohort profiles

In this study, 2775 pregnant women were enrolled in the antenatal clinics (ANC) of six tertiary hospitals across Nigeria’s six geopolitical zones. The distribution of participants was as follows: 400 from Nnamdi Azikiwe University Teaching Hospital, Nnewi (South-East); 529 from University of Abuja Teaching Hospital, Gwagwalada (North-Central); 445 from University of Port Harcourt Teaching Hospital, Port Harcourt (South-South); 401 from Obafemi Awolowo University Teaching Hospital Complex, Ile-Ife (South-West); 500 from University of Maiduguri Teaching Hospital, Maiduguri (North East); and 500 from Aminu Kano Teaching Hospital, Kano (North West).

These participants were monitored from their initial ANC visit through 6 weeks post-childbirth. Of the initial 2775, 2403 women (86.59%; 95% CI, 83.17% to 90.13%) were followed up until delivery. Among the 2403 followed, 2386 were initially free from dual or triplex infections at enrolment. However, at repeat testing during delivery, 3 of these 2386 participants tested seropositive for a dual infection of HIV and HBV, resulting in a seroconversion rate of 0.13% (95% CI, 0.03% to 0.36%). There were no recorded cases of seroconversion for HIV-HCV, HBV-HCV, or triplex infections among the participants.

Sociodemographic characteristics of the study participants

The mean age of the participants was 30.91 ± 5.54 years, and ages ranged from 18 to 49 years. The majority, 61.1%, identified as Christian, while 38.4% were Muslim. Up to 60.1% had completed postsecondary education, and 5.1% were unemployed. Regarding monthly income available for antenatal care (ANC), 37.5% had up to 2.2USD, 38.5% earned between USD 2.2 and USD 11.0, and a smaller portion, 4.0%, had over USD 55. Only 3.8% of the participants had access to the National Health Insurance Scheme (NHIS), either solely or combined with out-of-pocket options (refer to Table 1). As for housing, 31.3% owned their homes, while a significant majority, 53.7%, lived in rented accommodations. Regarding the type of dwelling, nearly half (49.9%) resided in 2- or 3-bedroom flats.

Table 1.

Sociodemographic distribution of respondents.

	Frequency	Percent
Religion
No religion	12	0.4
Christianity	1696	61.1
Islam	1065	38.4
Traditional	1	0
Other	1	0
Level of education
Less than postgraduate	940	33.9
Postsecondary	1669	60.1
Other	166	6
Occupation
Unemployed	142	5.1
Not in civil service	1897	68.4
Is/was in civil service	716	25.8
Other	20	0.7
Husband’s occupation
Unemployed	42	1.5
Student	1376	49.6
Formerly in private sector	1357	48.9
Income available for ANC (USD)
≤2.2	1040	37.5
>2.2 to 11	1064	38.3
>11 to 55	454	16.4
>55	112	4.0
NHIS and out-of-pocket	69	2.5
NHIS	36	1.3
Type of housing
Own house	869	31.3
Rented apartment	1489	53.7
Not given	417	15.0
Type of accommodation
Not given	420	15.1
One room	80	2.9
One room and palour	404	14.6
Self-contain	325	11.7
2–3 bed room flat	1386	49.9
Duplex	110	4.00
Bungalow	50	1.80
If yes to induced abortion, how many times?
0	1683	60.6
1	376	13.5
2	712	25.7
3	4	0.10
How many times have you been pregnant
Primiparous	552	19.9
2–5	1995	71.9
6–8	207	7.50
9–13	21	0.80
Have you ever received
Yes	329	11.9
Hepatitis B vaccination?
No	2446	88.1
What is the HIV status of your partner?
Positive	74	2.70
Negative	2701	97.3
What is the HBV status of your partner?
Positive	36	1.30
Negative	2739	98.7
What is the HCV status of your partner?
Positive	25	0.90
Negative	2750	99.1

ANC: antenatal care; HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus; NHIS: national health insurance scheme; 1 Nigeria Naira: 0.0011 United State Dollar.

Dual and triplex infections of HIV, HBV and HCV

Table 2 presents a summary of the study’s findings on the prevalence of HIV, HBV, and HCV, as well as dual and triplex infections during pregnancy, labour, at birth, and 6 weeks after delivery. Out of the 2775 participants enrolled, 13 (0.47%; 95% CI: 0.25% to 0.80%) and 4 (0.14%; 95% CI: 0.04% to 0.37%) tested seropositive for dual and triplex infections, respectively. The breakdown of dual infection seroprevalence was 0.22% for HIV-HBV (6/2775; 95% CI: 0.08% to 0.47%), 0.14% for HIV-HCV (4/2775; 95% CI: 0.04% to 0.37%), and 0.11% for HBV-HCV (3/2775; 95% CI: 0.02% to 0.32%). Multivariable analysis revealed significant associations of HIV and HBV co-infection with factors like religion (adjusted odds ratio: 0.068, 95% CI: 0.006 to 0.757) and house ownership (adjusted odds ratio: approximately 1.65 × 10⁻⁹, 95% CI: 1.60 × 10⁻⁹ to 1.70 × 10⁻⁹) among the women.

Table 2.

Prevalence of HIV, HBV, HCV, single, double, and triplex infections, during pregnancy, labour, at birth and at 6 weeks post-delivery.

Variables	Frequency	Prevalence, % (95% CI)
Pregnant woman during pregnancy
Single infection
HIV	125	4.50 (4.423 to 4.584)
HBV	126	4.54 (4.462 to 4.621)
HCV	21	0.76 (0.725 to 0.790)
Double infection
HIV & HCV	4	0.14 (0.0393 to 0.369)
HIV & HBV	6	0.22 (0.199 to 0.234)
HBV & HCV	3	0.11 (0.096 to 0.121)
Triplex infection	4	0.14 (0.0393 to 0.369)
No infection	2486	89.59 (89.234 to 89.938)
Pregnant woman during labour (n = 2403; seroconversion)
Double infection
HIV & HCV	0	0.00
HIV & HBV	3	0.12 (0.111 to 0.139)
HBV & HCV	0	0.00
Triplex infection	0	0.00
Baby at birth (N = 22)
Double infection
HIV & HCV	0	0.00
HIV & HBV	2	9.09 (7.785 to 10.442)
HBV & HCV	0	—
Triplex infection	0	0.00
Baby at 6 weeks (N = 19)
Double infection
HIV & HCV	0	0.00
HIV & HBV	0	0.00
HBV & HCV	0	0.00
Triplex infection	0	0.00

HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus.

Seroconversion rates for dual and triplex infections

Table 2 and Figure 1 show that 2403 of the 2775 participants (86.59%; 95% CI, 83.17% to 90.13%) were monitored until delivery. Among these 2403 women, 2386 were initially free from dual or triplex infections at enrolment. However, upon retesting during delivery, three of these 2386 individuals tested seropositive for a dual infection of HIV and HBV, resulting in a seroconversion rate of 0.12% (95% CI, 0.026% to 0.367%). There were no cases of seroconversion for HIV-HCV, HBV-HCV, or triplex infections among the participants.

Figure 1.

Flow chart of the study participants. pos + ve: positive; neg−ve: negative; HBV: hepatitis B virus; MTCT: mother-to-child transmission.

Mother-to-child transmission of dual and triplex infections

Table 2 outlines the MTCT rates for dual and triplex infections of HIV, HBV, and HCV. Among the mother-infant pairs that were positive for either dual or triplex infections, 20 mothers (17 with dual and triplex infections followed until labour or delivery, and three who seroconverted) had live births, resulting in 22 babies exposed to HIV, HBV, and HCV, which included two sets of twins. At birth, 2 of these 22 infants tested positive for both HIV and HBV, leading to a mother-to-child transmission (MTCT) rate for HIV-HBV at birth of 9.09% (95% CI: 7.785% to 10.442%). Notably, these two dual-positive infants were born to women who experienced seroconversion (as detailed in Figure 1). Subsequently, 19 infants (86.36%; 95% CI: 82.524 to 90.336%) were followed until 6 weeks post-birth. At this point, none of the infants, including those initially testing positive, were found to be HBV positive upon retesting. Thus, the MTCT rate for HBV at 6 weeks was determined to be 0.0%.

Risk factors for HIV-HBV dual infections

Table 3 demonstrates the use of univariate regression analysis to identify predictor variables for HIV-HBV dual infections. A generalised univariate regression analysis was conducted to examine the factors affecting the seroprevalence of HIV-HBV dual infections. Notably, the prevalence of HIV/HBV dual infections was significantly impacted by the participants’ religion and the type of house ownership. Specifically, HIV-HBV dual infection showed a significant correlation with both religion and house ownership among women. Table 4 details the results of the multinomial regression analysis for HIV/HBV dual infections, and Table 5 presents the findings based on the likelihood ratio for the same. Even after adjustments were made in the models, the significant association of HIV-HBV dual infection with religion and house ownership persisted among the participants.

Table 3.

Regression analysis showing chi-square and significance levels of likelihood ratios of predictor variables.

	HIV & HBV	HIV & HCV	HBV & HCV
	X² (p-value)	X² (p-value)	X² (p-value)
Intercept
BMI	0.69 (0.41)	0.93 (0.34)	6.09 (0.01)
Income for ANC per month	0.05 (0.83)	2.48 (0.12)	6.41 (0.01)
Number of pregnancies	0.11 (0.74)	5.36(0.02)	<0.01 (0.98)
Religion	8.17 (<0.01)	5.43(0.02)	<0.01 (1.00)
Level of education	0.49 (0.78)	1.03 (0.60)	5.42 (0.07)
Occupation	1.62 (0.45)	2.11 (0.35)	6.83 (0.03)
Husband’s occupation	0.02 (0.99)	1.80 (0.41)	5.88 (0.05)
Type of housing ownership	3.80 (0.04)	4.55 (0.03)	6.74 (0.01)
Type of accommodation	1.91 (0.86)	3.95 (0.56)	8.27 (0.14)
Ever used modern family planning method	0.89 (0.35)	4.64 (0.03)	7.70 (0.01)
Have you ever received hepatitis B vaccination	0.23 (0.64)	<0.01 (0.96)	6.2(0.01)
HIV status of partner	1.53 (0.22)	0.03 (0.86)	<0.01 (0.98)
HBV status of partner	0.31 (0.58)	0.01 (0.94)	<0.01 (1.00)
HCV status of partner	0.01 (0.93)	<0.01 (0.98)	<0.01 (1.00)
Sexual activity during pregnancy	0.53 (0.77)	2.81 (0.25)	<0.01 (1.00)

ANC: antenatal care; HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus; X²: Chisquare; predictor variable with p < .05 were put in a second table. Significant of p-values in bold.

Table 4.

Multinomial regression analysis for HIV and HBV dual infections.

	p-value	Exp(B)	LowerCI	UpperCI
Intercept	0.993
BMI
Continuous variable	0.395	0.74	0.37	1.48
Income for ANC per month
Continuous variable	0.264	1	1	1
Number of pregnancies
Continuous variable	0.214	32.225	0.134	7721.863
Religion
Christian	0.986	3.75 × 10⁻¹⁰	0	.b
Islam
Education
<Postsecondary	0.995	1.14 × 10⁻⁸²	<0.01	.b
Postsecondary	0.995	1.15 × 10⁻⁸¹	<0.01	.b
No formal
Occupation
Unemployed	0.998	1,529,260	0	.b
Not civil servant	0.299	67.902	0.024	195,171
Is/was civil servant
Husband’s occupation
Unemployed		0.048	0.048	0.048
Not civil servant	0.308	0.029	3.05 × 10⁻⁰⁵	26.78
Is/was civil servant
Housing ownership
Own	0.198	0.001	1.70 × 10⁻⁰⁸	40.332
Rented
House type
One room	0.999	7.47 × 10⁻⁰⁵	<0.01	.b
One room and palour	1	1.259	<0.01	.b
House type
Self-contain	1	0.078	<0.01	.b
2–3 bed room flat	0.997	1.58 × 10⁻⁰⁹	<0.01	.b
Duplex	1	1.507	<0.01	.b
Bungalow
Used modern family planning
Yes	0.177	0	3.18 × 10⁻⁰⁹	36.452
No
HBV vaccination
Yes	0.997	9515.304	<0.01	.b
No
Partner HIV status
Positive	0.999	4.72 × 10⁺⁰⁹	<0.01	.b
Negative
Partner HBV status
Positive	0.998	68,748.09	<0.01	.b
Negative
Partner HCV status
Positive	0.998	8470.482	<0.01	.b
Negative
Sexual activity with partner
Active	0.997	4.52 × 10⁻⁰⁷	<0.01	.b
Inactive	0.998	9599.06	<0.01	.b
None

HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus; ANC: antenatal clinic; BMI:body mass index.

Note. .b means number too long to be displayed; E = ×10.

Table 5.

Multinomial regression table for HIV and HBV dual infections based on likelihood ratio.

	p-value	Exp (B)	Lower CI	Upper CI
Intercept	<0.01
Religion
Christian	0.029	0.068	0.006	0.757
Islam
House ownership
Own	<0.05	1.65 × 10⁻⁰⁹	1.60 × 10⁻⁰⁹	1.70 × 10⁻⁰⁹
Rented

E = ×10. Signifiacnt of p-values in bold.

Risk factors for HIV-HCV dual infections

Table 3 shows the regression analysis showing significance levels of likelihood ratios of predictor variables for the HIV-HCV dual infections. Table 6 shows the multinomial regression analysis for HIV-HCV dual infections. Unfortunately, no model is fitted for further adjusted analysis for HIV-HCV dual infections based on the likelihood ratio p-values.

Table 6.

Multinomial regression analysis for HIV and HCV dual infections.

	p-value	Exp (B)	Lower CI	Upper CI
Intercept	0.993
BMI
Continuous variable	0.395	0.74	0.37	1.48
Income for ANC per month
Continuous variable	0.264	1	1	1
Number of pregnancies
Continuous variable	0.214	32.225	0.134	7721.863
Religion
Christian	0.986	3.75 × 10⁻¹⁰	0	.b
Islam
Education
<Postsecondary	0.995	1.14 × 10⁻⁸²	<0.01	.b
Postsecondary	0.995	1.15 × 10⁻⁸¹	<0.01	.b
No formal
Occupation
Unemployed	0.998	1,529,260.208	0	.b
Not civil servant	0.299	67.902	0.024	195,171.005
Is/was civil servant
Husband’s occupation
Unemployed		0.048	0.048	0.048
Not civil servant	0.308	0.029	3.05 × 10^-05	26.78
Is/was civil servant
Housing ownership
Own	0.198	0.001	1.70 × 10^-08	40.332
Rented
House type
One room	0.999	7.47 × 10⁻⁰⁵	<0.01	.b
One room and palour	1	1.259	<0.01	.b
House type
Self-contain	1	0.078	<0.01	.b
2–3 bed room flat	0.997	1.58 × 10⁻⁰⁹	<0.01	.b
Duplex	1	1.507	<0.01	.b
Bungalow
Used modern family planning
Yes	0.177	0	3.18 × 10⁻⁰⁹	36.452
No
HBV vaccination
Yes	0.997	9515.304	<0.01	.b
No
Partner HIV status
Positive	0.999	4,718,515,683	<0.01	.b
Negative
Partner HBV status
Positive	0.998	68,748.089	<0.01	.b
Negative
Partner HCV status
Positive	0.998	8470.482	<0.01	.b
Negative
Sexual activity with partner
Active	0.997	4.52 × 10⁻⁰⁷	<0.01	.b
Inactive	0.998	9599.06	<0.01	.b
None

BMI: body mass index; HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus.

Note. No model fitted based on the likelihood ratio p-values; b means number too long to be displayed; E = ×10.

Risk factors for HBV-HCV dual infections

Table 3 shows the regression analysis showing significance levels of likelihood ratios of predictor variables for the HBV-HCV dual infections. Table 7 shows the multinomial regression analysis for HBV-HCV dual infections. Unfortunately, no model is fitted for further adjusted analysis for HBV-HCV dual infections based on the likelihood ratio p-values.

Table 7.

Multinomial regression table for HBV & HCV dual infections.

	p-value	Exp (B)	Lower CI	Upper CI
Intercept	0.879
BMI
	0.871	66,362.812	6.94 × 10⁻⁵⁴	6.34 × 10⁺⁶²
Income for ANC per month
	0.869	0.995	0.936	1.057
Number of pregnancies
	0.904	0.002	1.07 × 10⁻⁴⁵	5.50 × 10⁺³⁹
Religion
Christian	0.959	1.63 × 10⁺¹⁰⁶	0	.b
Islam
Education
<Postsecondary	0.876	<0.01	<0.01	.b
Postsecondary	0.875	<0.01	<0.01	.b
No formal
Occupation
Unemployed	0.996	3.00897 × 10⁺¹²	0	.b
Not civil servant	0.956	4.23 × 10⁻¹¹¹	0	.b
Is/was civil servant
Husband’s occupation
Unemployed		5.42 × 10⁻¹⁶¹	5.42 × 10^-161	5.42 × 10^-161
Not civil servant	0.976	1.78 × 10⁻⁶⁰	0	.b
Is/was civil servant
Housing ownership
Own	0.913	1.42 × 10⁺⁴⁶	<0.01	.b
Rented
House type
One room	0.975	1.07 × 10⁺¹²⁵	<0.01	.b
One room and palour	0.992	1.42 × 10⁺³⁹	<0.01	.b
House type
Self-contain	0.973	1.73 × 10⁺¹⁴⁹	<0.01	.b
2–3 bed room flat	0.963	3.86 × 10⁺¹⁸¹	<0.01	.b
Duplex	0.985	3.18 × 10⁺⁸⁷	<0.01	.b
Bungalow
Used modern family planning
Yes	0.882	1.40 × 10⁺⁹⁹	<0.01	.b
No
HBV vaccination
Yes	0.986	7.91 × 10⁺⁴⁶	<0.01	.b
No
Partner HIV status
Positive	0.96	.b	<0.01	.b
Negative
Partner HBV status
Positive	0.992	1.26 × 10⁻⁴⁸	<0.01	.b
Negative
Partner HCV status
Positive	0.987	2.12 × 10⁻⁸⁷	<0.01	.b
Negative
Sexual activity with partner
Active	0.987	6.26 × 10⁻³⁴	<0.01	.b
Inactive	0.992	1.79 × 10⁺³⁶	<0.01	.b
None

ANC: antenatal care HIV: human immuno deficiency virus; HBV: hepatitis B virus; HCV: hepatitis C virus; BMI: body mass index.

Note. No model fitted based on the likelihood ratio p-values; b means number too long to be displayed; E = ×10.

Discussion

The impetus for this study stemmed from the absence of comprehensive national and hospital-based data on the seroprevalence, seroconversion, and mother-to-child transmission of triplex infections during pregnancy in Nigeria. Key findings of the study included a seroprevalence of 0.22% for HIV-HBV, 0.14% for HIV-HCV, 0.11% for HBV-HCV, and 0.14% for triplex infections. A notable correlation was observed between the occurrence of HIV/HBV co-infection and factors such as the individuals’ property ownership and religious affiliation. The study also found that the seroconversion rate for HIV-HBV dual infections was 0.12%, and remarkably, the mother-to-child transmission rate for these infections was 0% at 6 weeks post-birth, indicating no transmission from the mothers to their newborns during this period.

The frequency of dual infection with HIV and HBV among pregnant women in Nigeria has been documented in several studies and reviews.^12–15 In this study, the rate of HIV/HBV coinfection was 0.22%. Comparatively, higher rates of HIV-HBV coinfection have been reported in Angola,²² Northwest Ethiopia,⁴ Dar es Salaam, Tanzania,²³ Addis Ababa, Ethiopia,²⁴ and Rwanda,²⁵ with prevalence rates of 0.4%, 0.4%, 2.8%, 3.4%, and 4.1%, respectively. While differences in prevalence may be attributed to variations in healthcare infrastructure, screening programmes, and access to preventive measures, direct comparative studies evaluating awareness and public health initiatives between Nigeria and these East African countries and Angola are limited.^{6,7,11–15,17} However, Nigeria has implemented several national policies and programmes focused on viral hepatitis and HIV prevention, including routine screening during antenatal care, increased access to antiretroviral therapy, and integration of HBV vaccination into childhood immunisation programmes.^11–15,17 Additionally, factors such as population differences, genetic susceptibility, cultural practices, and healthcare-seeking behaviour may contribute to the observed variations in HIV-HBV coinfection rates across regions.⁴ Also, it could be due to the high proportion of women who are educated in the current study and they may have a tendency to observe safe practices that could prevent dual and triplex infections. Further research is needed to comprehensively assess the impact of public health interventions on infection prevalence in different settings.

There was a strong association between women’s simultaneous HIV/HBV infections and their house property ownership and religion. The tendency is that persons who own property may be of higher socioeconomic status and HIV, HBV, and HCV are conditions that are more associated with lower socio economic status. In a previous study in Uganda, HIV/HBV co-infections were independently associated with having lived in an internally displaced persons’ camp and having shared housing with HBV-infected people during childhood.²⁶ Another previous Ugandan study did not find any correlation between HIV/HBV co-infection and religion.²⁷ Our findings have clinical significance, and more research focused on HIV-HBV cohorts is required to see whether changing one’s lifestyle might enhance these associations.

Although research on pregnant individuals with HIV/HCV co-infection remains relatively limited, several studies have been conducted in Nigeria and other parts of Africa, providing valuable insights into the prevalence, risk factors, and potential maternal and neonatal complications associated with co-infection.^{6,7,11–15,17,28} However, there is still a need for more comprehensive studies focussing on longitudinal pregnancy outcomes, access to treatment, and the impact of co-infection on both maternal and neonatal health. In this study, 0.14% of participants were identified as co-infected with HIV/HCV, reinforcing the need for continued surveillance and targeted interventions to mitigate potential adverse effects. In contrast, a study conducted in France reported an HIV/HCV dual infection prevalence of 1.7% (95% CI: 1.3–2.1) among pregnant women within the HIV-positive cohort.²⁹ This prevalence remains higher than the 0.14% observed in our study, highlighting potential regional differences in risk factors, healthcare access, and harm reduction strategies.^13,29 The variation may be influenced by differences in intravenous drug use rates, blood transfusion practices, and HCV screening policies between France and Nigeria.^3,12,13,29 Nevertheless, the study’s binomial regression analysis highlighted that factors such as parity, religion, house ownership, and the use of family planning methods significantly influenced the prevalence of HIV/HCV dual infection among women. However, an adjusted analysis could not be conducted due to the absence of a model based on the likelihood ratio p-values.

Previous reports on the prevalence of HBV-HCV dual infections among pregnant women in Nigeria remain limited, with many studies being regionally focused and lacking national representation.^{12,13,30–33} While some studies^12,13,30 have involved relatively small sample sizes (e.g. 102 participants), others, such as those with 2439 pregnant women,^31,33 were more comparable to our study in scale. However, a key limitation of these studies was the lack of comparisons to a reference group, limiting their ability to establish broader epidemiological trends and risk factor associations.^30,31 Additionally, only a handful of national studies are conducted in hospital settings. In Ethiopia, the prevalence rates for pregnancy-related HBV-HCV infections were reported as 1.1% in one study²⁴ and 0.0% in a more recent one.³² While our results support these earlier findings,^24,32 it is worth noting that differences in regional practices and testing methods may contribute to variations in the reported prevalence rates.

The HBV and HCV statuses were ascertained in the current investigation using PCR. Some authorities may argue that the use of PCR alone could cause an underestimation of the percentage of HBV or HCV status since the presence of HBsAg or an HCV antibody test alone may indicate a temporary infection rather than a transformative infection where the HBV or HCV genome has integrated into the human genome. However, according to the 2020 revision of the World Health Organisation’s HCV categorisation, verified molecular methods like PCR should ideally be used to confirm the existence of HCV.^3,14,17 PCR rules out the false positives including those who continue to have circulating antibodies but no active disease. These antibodies are actually evidence of previous disease or immunity. Our data which uses the gold standard of the PCR are giving the actual true values while other studies which may have used only antibody detection may actually have inflated values. This is because PCR was used for confirmatory testing, while initial screening was performed using rapid test kits.

Regression analysis revealed that several factors, such as employment, home ownership, use of family planning methods, and HBV vaccination status, appeared to affect the women’s HBV-HCV dual positive status. However, no model was fitted based on the likelihood ratio p-values, so we could not perform an adjusted analysis.

There is little research on triplex infections during pregnancy in Nigeria,^14,33,34 as most of the information was derived from non-obstetric population data. But a recent meta-analysis of triplex infection in Nigeria by Eleje et al. found that the pooled prevalence of triplex infection in pregnancy was 0.03% (95% CI: 0.02–0.04%), with a higher prevalence in the HIV-positive group (0.08%) than in the general obstetric group (0.00%).¹⁴ Furthermore, compared to certain other nations, this study’s overall prevalence of triplex infection during pregnancy was lower. For example, in Ethiopia,²⁴ it was 0%, while in a systematic review conducted in Africa,³⁵ it was 0.7% in the non-obstetric population.

In this study, we observed a seroconversion rate of 0.12%. Before this research, there was a lack of detailed data on the seroconversion rates for dual and triplex infections during pregnancy in Nigeria, which is one of the aims addressed by our investigation. The significance of our findings lies in the possibility that widespread antiretroviral therapy, routine HBV vaccinations, and comprehensive prenatal care could help maintain low seroconversion rates for dual and triplex infections. The observed minimal seroconversion rate in Nigeria might also be attributed to the adoption of universal precautions, safer sex practices, extensive use of antiretroviral drugs, and regular immunization.^12–14,18 However, to provide a comparative perspective, studies conducted in other African countries, such as Ethiopia and Rwanda, have reported higher rates of HBV and HCV seroconversion among pregnant women.^4,25 Similarly, studies in Angola and Tanzania have documented greater HIV-HBV co-infection rates compared to our findings.^22,23 These differences may reflect variations in healthcare infrastructure, public health interventions, and screening coverage. Further comparative studies are needed to assess the long-term impact of preventive measures on seroconversion rates across different settings.

There is a notable lack of comprehensive data on the MTCT rates for dual and triplex infections of HIV, HBV, and HCV in the obstetric population. While MTCT is a recognized concern in obstetrics, indicating potential shortcomings in PMTCT programs for HIV, HBV, and HCV, the infants in this study exhibited zero MTCT rates for these infections at 6 weeks of age. Our findings align with those from a recent Nigerian meta-analysis aiming to assess MTCT rates of hepatitis B, hepatitis C, and HIV among pregnant women with one, two, or all three infections.¹⁵ Additionally, the review highlighted a lack of data on MTCT rates of hepatitis C in mono-infections, as well as the combined mother-to-child transmission rates of HIV, hepatitis B, and hepatitis C among mother-infant pairs with dual or triplex infections in Nigeria.¹⁵

The mother-to-child transmission (MTCT) rate for HBV in this study was 0%. This finding aligned with a Chinese study where only 2 out of 1544 subjects experienced MTCT of HBV.³⁶ To provide a more contextually relevant justification, national data from Nigeria would be ideal. However, limited studies specifically report the MTCT rate of HBV in Nigeria. Some reports suggest that Nigeria has made progress in hepatitis B vaccination coverage, with increasing uptake of the birth dose and routine immunization.^18,37,38 Nevertheless, further studies are needed to evaluate the effectiveness of these preventive measures in eliminating MTCT of HBV in the Nigerian population. If national data remain unavailable, the observed 0% MTCT rate in this study should be interpreted cautiously, considering potential factors such as sample size and healthcare interventions received by participants. Nevertheless, the discrepancy in infant test results may be attributed to passive transfer of maternal antibodies at birth, which waned over time.

The discussion persists on how strengthening interventions for maternal and infant HIV, HBV, and HCV during pregnancy could impact Nigeria’s progress toward achieving the WHO 2030 target for global hepatitis elimination. This discussion is distinct from our study’s focus, which was confined to examining the epidemiology of dual and triplex infections during pregnancy, including their prevalence, seroconversion rates, and mother-to-child transmission (MTCT) rates, without considering the non-obstetric population. Additionally, there remains a notable gap in knowledge about the prevalence of triplex infections in this vital demographic despite concerns that it may impact pregnancy outcomes and increase the risk of perinatal transmission.²⁸

Even without the non-obstetric population, we were nevertheless able to detect a significant trend in the elimination of HIV, HBV, and HCV during pregnancy thanks to the design of our study. The implementation of the PMTCT package, the WHO ‘treat all approach’, birth dose hepatitis B vaccination, and the Sustainable Development Goals (SDG) of ending HIV/AIDS and hepatitis B by 2030 are just a few of the significant efforts made over the last two to three decades to make ART, HBV vaccination, and related interventions accessible and affordable for all people living with HIV/AIDS and HBV.^39–41

Since antiretroviral therapy and HBV antivirals effectively suppress the HIV and HBV viral load and eventually reduce the likelihood of unfavourable birth outcomes among HIV and HBV-positive women to a certain extent, these therapies have, in turn, improved the health and welfare of women living with HIV and HBV.^42,43 We do not fully understand why women with dual or triplex infections have a better prognosis in terms of zero MTCT rates. In addition to a better response to treatment, younger age, comprehensive knowledge of MTCT, a lower presentation stage, and male partner involvement in sustaining interventions for preventing MTCT are proposed as factors for these better prognosis.^44,45

Strengths and limitations of the study

The study has several strengths. Our study’s primary strength is its evaluation of MTCT, seroconversion, and seroprevalence rates of triplex infections at the national population level across an observational period of up to 6 weeks after birth. The study’s external validity is reinforced by the fact that it was a multisite, nationwide, data-based investigation that enabled us to extrapolate the findings to state and federal levels. This study represents the most comprehensive investigation of dual and triplex infections among pregnant Nigerian women to date, yielding robust findings. Additionally, the inclusion of the husband’s results allowed for an assessment of potential household transmission dynamics. Certain limitations to our study are worthy of being discussed. This study has a restriction about institutional settings, whereby only pregnant women who underwent ANC follow-up were included in the analysis, notwithstanding its strengths. For several reasons, some expectant women in the community did not receive PMTCT services in addition to ANC follow-up. Regretfully, the study’s findings may be reported too little if pregnant women who did not receive PMTCT services or ANC follow-up were excluded.

Conclusion

Pregnant women in Nigeria showed comparatively low rates of seroprevalence and seroconversion for dual and triplex infections of HIV, HBV, and HCV, but low or nonexistent rates of MTCT. Considering this is necessary while offering maternal health services, especially prenatal care and delivery services, which are primarily for women who have dual and triplex infections. Current efforts at preventing increasing rates of HIV/HBV/HCV dual or triplex infections in Nigeria among pregnant populations should be sustained with further enhancement of policies and practices for prevention of MTCT.

Footnotes

Authors’ note

GUE presented the preliminary Result of this work as an oral presentation at the State General Meeting/Scientific Conference/4^th Late Emeritus Prof FA Nwakor Memorial Lecture organised by Nigerian Medical Association Conference, Anambra State Branch held in Awka, Anambra State, Nigeria on 23 July 2022.

Acknowledgments

We are grateful to the six tertiary hospitals for allowing us to conduct this research. We want to thank data collectors and supervisors for their dedication and cooperation throughout the data collection process. We would also like to thank everyone who participated in the tool validation and language translation process. Finally, we would like to express our appreciation to the study participants without whom the study could not be realised.

ORCID iDs

George Uchenna Eleje

Chinyere Ukamaka Onubogu

Preye Owen Fiebai

Ayyuba Rabiu

Ikechukwu Innocent Mbachu

Osita Samuel Umeononihu

Rebecca Chinyelu Chukwuanukwu

Ngozi Nneka Joe-Ikechebelu

Emeka Philip Igbodike

Chike Henry Nwankwo

Chisom God’swill Chigbo

Shirley Nneka Chukwurah

Chinwe Elizabeth Uzochukwu

Samuel Oluwagbenga Inuyomi

Odion Emmanuel Igue

Harrison Chiro Ugwuoroko

Lydia Ijeoma Eleje

Angela Ogechukwu Ugwu

Uzoamaka Rufina Ebubedike

Chiamaka Henrietta Jibuaku

Nnaedozie Paul Obiegbu

Amaka Elizabeth Agbata

Kingsley Chukwuebuka Agu

Statements and declarations

Author contributions

GUE is the principal investigator. GUE and OCE conceived the study. Data assessment was performed by HAU, POF, OML, IIM, GOA, AR, CUO, MTC, RCC, NNI, CHN, SOK, CNO, SNC, CEU, ICO, AA, ROE, HCU, CHJ, SOI, BAA, UIA, UCO, EAE, OEI, ODO, POA, CPC, HIS, FEA, AIN, SAO, OSU, CCO, IKN, AAO, EOU, SIN, ICA, DCI, EPI, URE, NPO, COE, IAY, CCN, AEA, KCA, CGO, OKN, KCN, RKY, IAE, MOI, EAO, CCN, and JII. Calculations and data interpretation were performed by GUE, CHN, CGC, LIE, CSG, and MDE. Statistical analysis was performed by CGC and MDE. CGC, LIE, MDE, and CSG prepared tables and figures. The first draft of the paper was written by GUE and EPI, CUO EOU, AOU, JII, and COE critically revised the paper. All authors reviewed and edited the final draft. All authors critically reviewed the article, gave final approval of the version to be published, agreed on the journal to which the article has been submitted, and agreed to be accountable for all aspects of the work.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was funded by the TETFund National Research Fund 2019 (Grant number TETFund/DR&D/CE/NRF/STI/33).

Conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

We can share the data if there are reasonable requests. Data can be shared by the corresponding author.*

Appendix

References

Shahriar

Araf

Ahmad

, et al. Insights into the coinfections of human immunodeficiency virus-hepatitis B virus, human immunodeficiency virus-hepatitis C virus, and hepatitis B virus-hepatitis C virus: prevalence, risk factors, pathogenesis, diagnosis, and treatment. Front Microbiol 2022; 12: 780887.

The global HIV and AIDS epidemic. https://www.hiv.gov/hiv-basics/overview/data-and-trends/global-statistics/. Accessed on 27th December, 2023.

Ejaz

Abdullah

Malik

, et al. Screening of hepatitis B and C viral infection, recognition of risk factors, and immunization of patients against hepatitis B virus: a module developed for effective hepatitis control. Front Public Health 2023; 11: 1269209.

Tesfaye

Abebaw

Bizualem

, et al. Seroprevalence of hepatitis B and C and HIV infections and associated risk factors among pregnant women attending antenatal care unit at simada hospital, south Gondar zone, northwest Ethiopia. BioMed Res Int 2025; 2025: 6895237.

Kaswa

de Villiers

. Prevalence of hepatitis-B virus co-infection among people living with HIV in Mthatha region of South Africa. Afr Health Sci 2023; 23(1): 149–156.

Frempong

Ntiamoah

Annani-Akollor

, et al. Hepatitis B and C infections in HIV-1 and non-HIV infected pregnant women in the Brong-Ahafo region, Ghana. PLoS One 2019; 14(7): e0219922.

Ugwu

Eleje

Ugwu

, et al. Antivirals for prevention of hepatitis B virus mother-to-child transmission in human immunodeficiency virus positive pregnant women co-infected with hepatitis B virus. Cochrane Database Syst Rev 2023; 6(6): CD013653.

Eke

Eleje

Eke

, et al. Hepatitis B immunoglobulin during pregnancy for prevention of mother-to-child transmission of hepatitis B virus. Cochrane Database Syst Rev 2017; 2(2): CD008545.

Cao

Zhang

, et al. Effects of hepatitis B virus infection and strategies for preventing mother-to-child transmission on maternal and fetal T-cell immunity. Front Immunol 2023; 14: 1122048.

10.

Bekker

Alleyne

Baral

, et al. Advancing global health and strengthening the HIV response in the era of the sustainable development goals: the international AIDS society-lancet commission. Lancet 2018; 392(10144): 312–358.

11.

Magaji

Okolo

Hassan

, et al. Prevalence of hepatitis B virus infection among pregnant women in Jos, Nigeria. Ann Afr Med 2020; 19(3): 176–181.

12.

Ojiegbe

Eleje

Nduka

, et al. Hepatitis B virus infection and infectivity status among pregnant women in Nigeria. Hong Kong J Obstetrics Gynaecol 2018; 1(1): 6–13.

13.

Uyoh

Eleje

Onyegbule

, et al. Correlates and prevalence of human immuno-deficiency virus and hepatitis B virus co-infection in pregnancy. International J Adv Medical Sci 2018; 3(7): 1–12.

14.

Eleje

Loto

Usman

, et al. A systematic review and meta-analysis of the prevalence of triplex infections (combined human immunodeficiency virus, hepatitis B virus, and hepatitis C virus) among pregnant women in Nigeria. Obstet Gynecol Int 2023; 2023: 3551297.

15.

Eleje

Onubogu

Fiebai

, et al. Mother-to-child transmission of human immunodeficiency virus, hepatitis B virus and hepatitis C virus among pregnant women with single, dual or triplex infections of human immunodeficiency virus, hepatitis B virus and hepatitis C virus in Nigeria: a systematic review and meta-analysis. Sage Open Med 2022; 10: 20503121221095411.

16.

Eleje

Mbachu

Ogwaluonye

, et al. Prevalence, seroconversion and mother-to-child transmission of dual and triplex infections of HIV, hepatitis B and C viruses among pregnant women in Nigeria: study protocol. Reprod Health 2020; 17(1): 144.

17.

Eleje

Rabiu

Mbachu

, et al. Awareness and prevalence of hepatitis C virus infection among pregnant women in Nigeria: a national pilot cross-sectional study. Womens Health 2021; 17: 17455065211031718.

18.

Eleje

Akaba

Mbachu

, et al. Pregnant women's hepatitis B vaccination coverage in Nigeria: a national pilot cross-sectional study. Ther Adv Vaccines Immunother 2021; 9: 25151355211032595.

19.

Noordzij

Tripepi

Dekker

, et al. Sample size calculations: basic principles and common pitfalls. Nephrol Dial Transplant 2010; 25(5): 1388–1393.

20.

Adedokun

Uthman

. Women who have not utilized health service for delivery in Nigeria: who are they and where do they live? BMC Pregnancy Childbirth 2019; 19(1): 93.

21.

Nigeria guidelines for HIV prevention, treatment and care, 2023. https://www.prepwatch.org/resources/nigeria-guidelines-for-hiv-prevention-treatment-and-care-2023/

22.

Oliveira

Martins

MDR

Castro

, et al. Seropositivity rate and sociodemographic factors associated to HIV, HBV, HCV and syphilis among parturients from Irene Neto maternity of Lubango city, Angola. Sex Transm Infect 2020; 96(8): 587–589.

23.

Manyahi

Msigwa

Mhimbira

, et al. High sero-prevalence of hepatitis B virus and human immunodeficiency virus infections among pregnant women attending antenatal clinic at Temeke municipal health facilities, Dar es Salaam, Tanzania: a cross sectional study. BMC Pregnancy Childbirth 2017; 17(1): 109.

24.

Tesfu

Belay

Habtemariam

. Co-infection of HIV or HCV among HBsAg positive delivering mothers and its associated factors in governmental hospitals in Addis Ababa, Ethiopia: a cross-sectional study. PLoS One 2022; 17(8): e0273300.

25.

Mutagoma

Balisanga

Malamba

, et al. Hepatitis B virus and HIV co-infection among pregnant women in Rwanda. BMC Infect Dis 2017; 17(1): 618.

26.

Chiesa

Ochola

Oreni

, et al.

Hepatitis B and HIV coinfection in Northern Uganda: is a decline in HBV prevalence on the horizon?

PLoS One 2020; 15(11): e0242278.

27.

Drazidio

Kirabira

Atuhairwe

, et al. Factors influencing hepatitis B virus co-infection among HIV patients attending health care services in mungula health centre IV Adjumani district, west Nile region Uganda. Hospital-based cross-sectional study. Health Sci J 2022; 16(5): 94.

28.

Curtis

Chappell

. Evidence for implementation: HIV/HCV coinfection and pregnancy. Curr HIV AIDS Rep 2023; 20(1): 1–8.

29.

Benhammou

Tubiana

Matheron

, et al. HBV or HCV coinfection in HIV-1-infected pregnant women in France: prevalence and pregnancy outcomes. J Acquir Immune Defic Syndr 2018; 77(5): 439–450.

30.

Balogun

Emmanuel

Ojerinde

. HIV, hepatitis B and C viruses’ co-infection among patients in a Nigerian tertiary hospital. Pan Afr Med J 2012; 12: 100.

31.

Ugbebor

Aigbirior

Osazuwa

, et al. The prevalence of hepatitis B and C viral infections among pregnant women. N Am J Med Sci 2011; 3(5): 238–241.

32.

Assefa

Kiros

Delelegn

. Seroprevalence and associated factors of HBV and HCV among pregnant women attending antenatal care at debre tabor comprehensive specialized hospital, northwest Ethiopia: a cross-sectional study. Internet J Microbiol 2023; 2023: 2282673.

33.

Ezechi

Kalejaiye

Gab-Okafor

, et al. Sero-prevalence and factors associated with hepatitis B and C co-infection in pregnant Nigerian women living with HIV infection. Pan Afr Med J 2014; 17: 197.

34.

Okeke

Obi

Okezie

, et al. Coinfection with hepatitis B and C viruses among HIV positive pregnant women in Enugu south east, Nigeria. Niger J Med 2012; 21(1): 57–60.

35.

Kenfack-Momo

Kenmoe

Takuissu

, et al. Epidemiology of hepatitis B virus and/or hepatitis C virus infections among people living with human immunodeficiency virus in Africa: a systematic review and meta-analysis. PLoS One 2022; 17(5): e0269250.

36.

Han

Zhang

, et al. Staging and clinical characteristics of pregnant women with chronic hepatitis B virus infection: a retrospective cohort study from Nanjing, China. J Obstet Gynaecol Res 2023; 49(10): 2427–2435.

37.

Eke

Okafor

, et al. Prevalence, correlates and pattern of hepatitis B surface antigen in a low resource setting. Virol J 2011; 8: 12.

38.

Olaleye

Kuti

Makinde

, et al. Perinatal transmission of hepatitis B virus infection in Ile-Ife, south western, Nigeria. J Neonatal Perinat Med 2013; 6(3): 231–236.

39.

Vo-Quang

Lemoine

. Global elimination of HBV: Is it really achievable? J Viral Hepat. 2024; 31(Suppl 2): 4–12. doi:10.1111/jvh.1395538797984.

40.

Damayanti

Yanti

Mulyanti

, et al. The implementation of government regulation on the administration of immunization. J Infras Policy Dev 2024; 8(8): 5728.

41.

Eleje

Emmanuel

Akinsolu

, et al. Assessment of the acceptability and detection rate of HIV self-testing in Nigeria: a systematic review and meta-analysis. Discov Epidemics 2024; 1(1): 1–18.

42.

Eke

Ramaiyer

Eleje

, et al. A systematic review and meta-analysis of maternal weight changes and pregnancy outcomes associated with integrase inhibitors and tenofovir alafenamide in pregnant women with HIV. Am J Obstet Gynecol MFM 2024; 6(8): 101406.

43.

Eke

Brummel

Aliyu

, et al. Lipid and glucose profiles in pregnant women with HIV on tenofovir-based antiretroviral therapy. Clin Infect Dis 2024; 80: 594–601.

44.

Terefe

Jembere

Liyew

. Comprehensive knowledge of mother-to-child HIV/AIDS transmission, prevention, and associated factors among reproductive-age women in East Africa: insights from recent demographic and national health surveys. BMC Womens Health 2024; 24(1): 318.

45.

Malindi

Maputle

. Involvement of male partners in sustaining interventions for preventing mother-to-child transmission of HIV among women with HIV. Int J MCH AIDS 2024; 13: e023.