Determining the effectiveness of integrating hepatitis B, C, and HIV using an integrated care model to optimize uptake of screening among pregnant mothers attending antenatal clinics in West Nile Sub-Region, Uganda

¹Department of Family Medicine, Epidemiology and Community Health, School of Health Sciences, Kenyatta University, Nairobi, Kenya, ²School of Public Health, Clarke International University, Kampala, Uganda, ³Department of Paediatrics and Child Health, School of Medicine College of Health Sciences, Makerere University Kampala, Uganda

^&Corresponding author
John Bosco Alege, Department of Family Medicine, Epidemiology and Community Health, School of Health Sciences, Kenyatta University, Nairobi, Kenya

Introduction    

Infectious diseases such as viral hepatitis B (HBV), viral hepatitis C (HCV), and human immunodeficiency virus (HIV) create a high public health burden among pregnant women globally. Thus, it highlights the need to strengthen biomedical interventions, especially through integration, since all three diseases have a similar mode of transmission [1,2]. It is estimated that 36.9 million people are infected with HIV worldwide [3,4], while 248 million people have chronic viral hepatitis B, and 110 million have viral hepatitis C antibodies, out of which 80 million have viremic HCV [5,6]. Nevertheless, estimates often cited in the available literature vary substantially [7]. HBV and HCV infections are normally associated with considerable morbidity and mortality arising from chronic liver disease. They contribute to approximately 57% of cirrhosis and 78% of hepatocellular carcinoma (HCC) 57% of cirrhosis and 78% of hepatocellular carcinoma cases worldwide, and together account for approximately 1.4 million deaths annually [8]. The high burden of HBV and HCV is felt more in developing countries, especially in Asia and Africa.

Globally, the majority of people with chronic viral hepatitis were infected during the perinatal period and/or childhood. This normally happens way before they become infected with HBV, as opposed to HCV, which is usually acquired in adulthood. Similarly, perinatal or vertical transmission of HIV occurs predominantly in sub-Saharan Africa and Asia [2-9]. Thus, best practice requires that screening for vertically transmitted infections is mandatory and should be done during the first trimester during antenatal (ANC) visit. Moreover, women are more vulnerable and are affected by infection, especially those in the lowest socioeconomic level [5]. The World Health Organisation (WHO) highly recommends testing for HIV and HBV during pregnancy and childbirth to prevent vertical transmission [10]. The prevalence of HIV and HBV infections in the prenatal population is a clear indicator of prevalence in the general population and a determinant of a preventive strategy such as vaccination. Another study noted that the intrapartum period is likely to be the only clinical access point for the antenatal care clinic (ANC) population in resource-limited settings, as these successful measures to prevent vertical transmission include rapid birth tests demonstrated in several resource-constrained settings [11].

Evidence suggests that perinatal transmission of HBV from an infected mother to the baby is an important route of transmission in highly endemic regions [11,12]. HBV infection is transmissible from an infected mother to her baby during pregnancy, childbirth, or the postpartum period, and most transmission occurs during childbirth or during the perinatal period [13,14]. Therefore, there is an increased likelihood of vertical transmission and chronic infection from a mother carrying chronic hepatitis B (CHB) surface antigen (HBsAg) to her child. The risk of transmission is estimated to be 90% in pregnant women who are positive for (HBeAg) with high levels of HBV deoxyribonucleic acid (DNA) titers [13-15]. Moreover, the 2016 Uganda Population HIV Impact Assessment (UPHIA) report published by the Ministry of Health (MoH) noted that currently there is availability of cheap, easily administered and rapid diagnostic tests for HIV infection, however, opportunities have been missed to provide HBV and HCV prevention testing and counseling (C&T) within the ANC setting [16]. Consequently, providing such a package of services using the maternal, newborn, and child health (MNCH) platform is highly recommended.

The UPHIA report, which also considered HBV serology, estimated the prevalence of hepatitis B virus as 4.1% in the general population, with men at 5.4% and women at 3.0%, respectively, with no HCV prevalence established [8]. West Nile lies in the viral hepatitis high burden belt in Uganda, with prevalence of HBV as follows: Mid North 4.6%, North East 4.4% and West Nile 3.8% [8]. The two districts selected for the study have very low uptake of first ANC, particularly in the first trimester, with Koboko and Maracha districts at 33% and 27%, respectively. West Nile borders the Democratic Republic of Congo to the west and South Sudan in the north. Lastly, the West Nile Region is a host to about one million refugees residing in 12 refugee settlements and host communities [9]. Thus, Uganda and the study area lie in the intermediate range, based on the WHO classification of <2% mild, intermediate 2-8%, or high endemicity >8% of HBV infection [5].

The Uganda Ministry of Health (MoH) and WHO Afro highlighted integration as a key priority strategy for elimination of HBV and HCV by 2030 [10]. However, there is no evidence currently to demonstrate why integrating HBV and HCV services into maternal and newborn clinics in the West Nile Sub-Region, and Uganda in general. The WHO guidelines for the management of HBV and HCV recommend that HBV, HCV, HIV, and all other interventions targeting viral diseases should be incorporated into the present public health services and/or decentralized in order to increase screening, prevention, treatment, and better clinical outcomes [11-19]. Thus, screening for HBV, HCV, and HIV targeting risk groups such as pregnant women increases the chances of identifying undiagnosed infections, improving prognosis and reducing the risk of transmission to the unborn baby. Therefore, this study was set out to evaluate the effectiveness of an integrated viral hepatitis B, C and HIV care model to optimize screening among pregnant mothers attending antenatal care at health facilities in West Nile Region, Uganda.

Methods     

Study design and sites: in this study, we conducted a quasi-experimental study design. In this quasi-experimental study, we created a pseudo-population that mimicked randomization to enable us to achieve a balance in the distribution of confounders across the experimental and control groups [20-22].

Study participants: the study participants were pregnant mothers who accessed ANC services in their first trimester. The study enrolled 1,396 participants; 705 (50.5%) were in the intervention arm, from five health centre IIIs in Koboko District, and 691 (49.5%) in the control arm, also from five health centre IIIs in Maracha District. There are various types of quasi-experimental study designs with a variety of applications depending on the specific context [23]. Thus, in this study, a pretest-post-test non-equivalent groups design was used, which justifies the selection of study participants from two neighbouring districts. Also, this selection approach enhanced external validity (generalizability) and reduced selection bias through carefully selecting non-equivalent comparison groups [24].

Sample size determination: the formula used to compare two independent group means in quantitative studies was used in this study [25].

The required sample size per arm for this study was set at prespecified power 1 - β to detect a pre-specified difference of d = p₁ - p₂ is n₁ [25].

Where σ₁² = p₁ (1 - p₁) and similarly for σ₁² = p₁ (1 - p₁), n₁ is the sample size; z denotes the statistical certainty (critical value) selected at 95%; p₁ is the proportion of mothers screened for HBV, HCV, and HIV in the control group (SOC); p₂ is the proportion of mothers not screened for HBV, HCV, and HIV in the intervention group; d means the detectable difference. To estimate the sample size per arm = n₁ * VIF. Where VIF = 1 + {(cv²_sizes + 1) m^- -1}ρ. Where cv²_sizes is cluster variation, m^- is the average cluster size, ρ is inter-cluster correlation (ICC). VIF refers to variance inflation factor, also referred to as (deff) design effect.

To date, no study has been conducted to determine uptake of HBV, HCV, and HIV screening at one point of care (ANC) at the national level. Thus, the sample size estimation per arm that gives a power of 80%, with a 12% HBV, HCV, and HIV detectable difference between control and intervention, and considering 8.3% proportion of pregnant women screened for HBV in Lira, Northern Uganda, a high burden area, was used to estimate the sample size [25]. A 5% level of significance, at an Intraclass Correlation Coefficient (ICC) of 0.05, cluster size variation (0.2), and 5 clusters per arm. Thus, the total n = 1,410.

Sampling strategy: this study was health facility-based, where study participants were pregnant mothers coming to attend ANC in their first trimester. Both probability and non-probability sampling techniques were used. First, the five health facilities in the intervention group in Koboko District were purposively selected based on the evidence that they are “high volume facilities”. Second, the total number of pregnant women who attended first ANC prior to the study, in each of the (5) health facilities in the intervention group, was used to allocate study participants proportionately to size per facility. Third, a systematic sampling technique was used; a list of all the eligible mothers on every clinic day (Monday to Friday) was generated. A sampling interval (Kth=2, from 1,410/705) was then used to select study participants at ANC until the desired sample was achieved without randomization. A similar process was repeated in Maracha District at the selected “high volume” facilities until the required sample size was achieved.

Materials and data collection

Structured questionnaire: first, a standardized structured questionnaire was used to capture data about the study participants.

Laboratory register: a laboratory register was used to collect HBV, HCV, and HIV (screening) diagnosis results. The data collection questionnaire and consent forms were translated from English into local languages (Kakwa and Lugbara), respectively.

Laboratory diagnosis: HBV, HCV (3-5 mls) of whole blood was drawn from each study participant through a venous puncture. The serum was separated using a Vacutainer. The samples collected were then tested for HBV surface antigent HBsAg and anti-HCV antigen also referred to as antibodies at the point of testing, at one-care-point (ANC). Blood samples were first tested for HBsAg and anti-HCV antigen or antibodies, and samples tested positive for HBsAg were further tested for anti-HBC, anti-HBe, and HBeAg, respectively. While samples positive for anti-HCV were further tested for HCV ribonucleic acid (RNA). Study participants who tested HBs reactive were considered to have CHB infection. Participants found to have tested positive for anti-HCV were considered exposed to HCV, while study respondents found positive for HCV RNA were considered to have a chronic HCV infection [10]. HIV: the HIV antibody test was carried out using determine, StatPack, and UniGold as recommended in the prevention and treatment of HIV in Uganda [24]. Samples screened and found positive for HIV antibodies were considered HIV-positive and were then subjected to HIV viral-load and further management.

Study outcome and covariates: “effectiveness of integrating viral hepatitis B, C, and HIV using the integrated care model (ICM) to optimize screening among mothers at selected health facilities in the two study sites”. The covariates were: participant characteristics, knowledge, awareness, and HBV vaccination status among the study participants.

Statistical analysis: participants´ baseline characteristics were compared between the control and the intervention groups. Pearson Chi-square or Fishers´ exact tests were used to compare categorical variables, whereas the Wilcoxon-Mann-Whitney tests were used for continuous variables. HBV and HIV screening was the primary outcome for this study, and was generated by scoring 1 for a participant who had been screened for both HBV, HCV, and HIV and 0 if the participant had only 1 test done or none. The primary outcome was the difference in the proportion of HBV and HIV co-screening between the two comparison groups. We used inverse probability of treatment weighting (IPTW) and binomial generalized linear model (GLM) with identity link function to estimate the primary outcome. IPTW was used to balance the distribution of participants' characteristics across the treatment groups. The propensity score (PS) model to estimate the IPTW weights was fitted using a logistic regression model that included mother´s age, educational level, occupation, parity, awareness of risk of hepatitis B and C viruses, and HIV during pregnancy.

Ethical consideration: this study was approved by Clarke International University Research Ethics Committee (CIU-REC) (CLARKE-2022-388) and the Uganda National Council for Science and Technology (UNCST) (HS2706ES). All participants were asked to sign an informed consent form. Persons who could not write were asked to sign by thumb-printing. Only consenting mothers were enrolled, and all their data are treated with utmost confidentiality.

Limitations of the study: out of the total sample of 1,388 participants, none tested positive for HCV in the intervention group, and only 3 tested HCV positive in the control group. This is probably because the health workers decided to screen every participant who was eligible since the same blood sample was used as opposed to assessing for signs and symptoms such as nausea, fever, abdominal pain, and jaundice as per guidelines (WHO, 2025). Moreover, the anti-HCV kits were provided for 30% of the total study population. Therefore, the proportion of the participants tested positive was so negligible thus not considered in the analysis. Nevertheless, other secondary outcomes such as awareness and knowledge levels were tracked.

Results     

Participants´ characteristics: the study enrolled 1396 participants, 705 (50.5%) in the intervention arm and 691 (49.5%) in the control arm, giving a 99% response rate as shown in Table 1. The overall median age of the pregnant mothers was 23 years with an interquartile range (IQR) of 20.0 to 28.0 years. The median age in the intervention was lower than that in the control group (median age 23.0, IQR 20.0 to 28.0 years vs 24 years, IQR 20.0 to 29.0 years, respectively). The majority of the participants were married, 1340 (98.0%) overall, 682 (98.1) in the intervention group, and 658 (97.8) in the control group. Most of the participants had primary education: 944 (70.1%) overall, 463 (69.8%) in the intervention group vs 658 (97.8%) in the control group. Most participants were unemployed, 1120 (80.7%), and 609 (87.1%) in the intervention group vs 511 (74.3%) in the control group. The median parity was the same for both groups: 2.0, interquartile range 1.0 to 4.0.

This study established a pooled HBsAg positivity prevalence rate of 2.1%, with the intervention group at 0.7% and the control group at 1.7%. The 2.1% positivity rate lies in the intermediate range, based on the WHO classification of <2% mild (low), intermediate 2-8%, or high endemicity ≥8% of HBV infection (WHO, 2015). The prevalence of HCV was 0.224% and HIV 0.15%, respectively.

Impact of the intervention on HBV, HCV and HIV screening, awareness and HBV vaccination in pregnant mothers: there was a significant impact of the intervention on HBV, HCV and HIV screening, awareness and vaccination among pregnant mothers (p<0.05) as shown in Table 2. Screening for both HBV and HIV was 652 (92.5%) in the intervention group and 623 (90.2%) in the control group. The weighted difference from inverse probability treatment weighting was 3.4 percentage points 95% CI: 0.2% to 6.6% (p=0.013) in the intervention compared to the control group. Awareness of HBV, HCV, and HIV risks during pregnancy was also significantly higher in the intervention group, 640 (92.4%), compared to the control group, 487 (70.7%). There was a 21.6 percentage point difference (95% CI: 17.7 to 25.6, p<0.001). Most participants reported having received awareness messages during the antenatal visits, 376 (32.3%), followed by outpatient department visits, 694 (59.6%) (Figure 1). Similarly, overall HBV vaccination rates among mothers in the intervention group compared to the control group were higher by a 9.7 percentage point difference 95% CI: 5.0 to 14.5 (453 (80.2%) vs. 472 (70.4%), p<0.0001).

The impact of the intervention on all outcomes was not significantly different across the age strata (<25 years versus ≥25 years) as shown in Table 3. All interactions between intervention covariates and age strata had p-values>0.05 (Table 3, subgroup analysis).

Awareness of HBV, HCV, and HIV risks during pregnancy was also significantly higher in the intervention group, 640 (92.4%), compared to the control group, 487 (70.7%). There was a 21.6 percentage point difference (95% CI: 17.7 to 25.6, p<0.001). Most participants reported having received awareness messages during the antenatal visits, 376 (32.3%), followed by outpatient department visits, 694 (59.6%) (Figure 1).

Discussion     

The primary outcome in this study was optimizing HBV and HIV screening among mothers at selected health facilities in the two study sites using the integrated care model. The covariates were: participant characteristics, knowledge, awareness, and HBV vaccination status among the study participants. The study established a significant impact of the intervention on HBV and HIV screening among the study participants. Screening for both HBV and HIV was over ninety percent in the intervention group, and exactly ninety percent in the control group. The weighted difference from inverse probability treatment weighting was a 3.4 percentage point difference in the intervention compared to the control group.

Findings from this study are consistent with available literature; for instance, a study conducted in China observed that similar efforts to integrate the three infectious diseases targeting triple elimination had already been recognized and implemented by some countries in the Western Pacific Region [25]. For example, China has an elimination of mother-to-child transmission (EMTCT) strategy that integrates provision of the essential package of services for universal HIV, hepatitis B, and syphilis screening where all three tests are offered concurrently without any charge. Relatedly, a quasi-experimental nonrandomized preintervention-post intervention comparison on integrating ANC and prevention of mother-to-child transmisson (PMTCT) established that countries such as Zambia that rolled out option a policy, a “one stop shop” were able to increase screening for HIV among pregnant women, streamline combination antiretroviral therapy (cART) initiation by consolidating service provision along a continuum of care and potentially decreasing time spent and wasted in referral models, as well as ‘lost opportunity´ by the pregnant mothers in accessing screening services [26]. Thus, regardless of policy option, an integrated model with one location and one provider may reduce stigma or fear of public disclosure as the clinic offers maternal/child health services in addition to HIV care; this is important to consider for family-centric HIV care models.

More recently, a health facility-based study on HIV, viral hepatitis B, C, and syphilis screening targeting pregnant women at ANC conducted in Angola observed that integrating HBV, HCV, and HIV screening at ANC, including HBV vaccination, minimizes and reduces ‘lost opportunity´ by the pregnant mother [1]. This therefore reinstates the fact that integrating services for infectious diseases must be widely adopted in all health facilities as a low-cost, but high-impact prevention strategy.

Contrary to the findings from this study, an ecological study conducted in Indonesia using four years data, from 2017 to 2020 noted that the programme did not succeed in achieving its set goal, for example, it was established that the number of pregnant mothers getting tested for HIV, and HBV infections was not even [27]. The screening goal for the triple elimination program was 60% of all pregnant mothers served by integrated antenatal care (ANC) in 2018, 70% in 2019, 80% in 2020, 90% in 2021, and 100% in 2022 [28]. Another study conducted in Indonesia established that pregnant women remain major stakeholders in achieving the WHO goal of eliminating hepatitis by the year 2030, as mother-to-child transmission of HBV is a major route of transmission, particularly in hepatitis B infection endemic countries [27].

Therefore, best practice requires that screening for vertically transmitted infections is mandatory and should be done at the first ANC visit. This is consistent with the WHO framework for implementing triple elimination of mother-to-child transmission of HIV, syphilis and hepatitis B virus. This framework strengthens WHO´s global commitment to address the vertical transmission of viral hepatitis B, HIV and other infectious diseases including syphilis [14]. Awareness of HBV, HCV, and HIV risks during pregnancy was also assessed in this study, and comparisons were made between the intervention and control groups, respectively. This study observed significant differences in the level of awareness among the study participants. Awareness of the risks of HBV, HCV, and HIV was higher in the intervention group compared to the control group, with a 21.6 percentage point difference. This was mainly because of the effect of the intervention; more awareness and health education sessions were held in the intervention group by the health care workers at ANC during and after screening. Similar sessions were held during clinical assessment for participants who tested positive for HBV and required referrals, as shown in Figure 1.

This observation was also well documented in a non-randomized experimental study conducted in Egypt with a focus on assessing pregnant women's knowledge regarding HBV infection. It was noted that more than two-thirds of the study participants had poor knowledge regarding HBV infection at the pre-intervention phase [29]. Nevertheless, the same study noted a statistically significant difference between the results of the post-intervention phase compared to the pre-intervention phase regarding knowledge about hepatitis B virus infection. This is very likely because of the targeted intervention at ANC, such as health education on HBV and other infectious diseases during the project implementation phase. Findings from other studies that corroborate with those from this study include the one by Adeyemi et al. that noted low levels of awareness and knowledge on viral hepatitis B among pregnant mothers seeking HBV screening and vaccination services at ANC in Nigeria [30]. Similarly, low levels of knowledge among pregnant mothers at ANC were recorded in South Sudan [31].

Contrary to findings from this study on the level of knowledge among study participants in the control group, a similar study conducted in Nepal found that study participants were aware of HBV and HIV [32]. For instance, when asked about their knowledge of HBV and other STDs, the majority of the study participants said they had heard and had some knowledge of the mode of transmission and/or symptoms. Available literature has documented that what normally affects patients, such as pregnant mothers seeking knowledge and awareness on viral infections such as HIV, is stigma. As a result, patients further delay screening and care due to shame and fear of judgement, as well as limiting themselves from obtaining information about their own health [31]. Thus, targeted adherence counselling for HIV among pregnant mothers has been shown to be an effective strategy for reducing stigma and increasing community knowledge, which in turn boosts uptake of screening services.

This study also established that the points of service delivery were where the study participants accessed messages and information about HBV, HCV, and HIV at the study sites that increased their knowledge and awareness. These include: the ANC, while the other proportion of participants received awareness at the outpatient department, during health facility visits. Similar findings were well documented in a study conducted in Nigeria where the majority of the respondents received HBV screening, and hemoglobin information from ANC clinics, while another proportion received it from mass media, with the smallest number receiving it from health workers [32]. In the same vein, findings from a study conducted in Pakistan found that pregnant women had limited knowledge of hepatitis B, hepatitis C, and HIV [33]. Whereas they heard about the three infectious diseases, there was no evidence that they knew how these viral diseases are spread. The low level of knowledge about viral infections among pregnant mothers led to low risk assessment and ‘lost opportunity´ in terms of timely screening and better management in the event that the mother tests positive. Low level of knowledge and awareness about HBV has been documented in other studies; for instance, studies conducted in Nigeria and Ghana, respectively among pregnant mothers at ANC observed that the majority of respondents had never known, or tested for HBV [31,34]. Out of those who were aware, they mentioned radio as their main source of accessing information, and worship centers as the least.

Other studies that found low levels of HBV, HCV, and HIV knowledge and awareness among pregnant mothers include a study conducted in Southern Nigeria and in Cameroon. The two studies observed that the majority of the respondents did not know some important ways by which hepatitis B infection could be contracted, and only a few had sought HBV screening services. It was clear that knowledge on prevention and transmission of HIV, Hepatitis B and C was generally poor [27,35,36].

This study observed that HBV vaccination rates among mothers were higher by a 9.7 percentage point difference between the intervention compared to the control group. The findings observed in this study are not consistent with a lot of existing literature on the level of HBV vaccine uptake among pregnant mothers at ANC, especially using the integrated approach. An experimental study conducted in Egypt established that at baseline more than two-thirds of the study participants had no vaccination against HBV, and about two-fifths of them were not aware of the HBV vaccine [28]. Similarly, less than one third of the study participants started vaccination because of family history of HBV. Another related hospital-based study conducted in Ethiopia on HBV and HCV screening among 1121 pregnant women showed that only 20 (1.8%) of the study participants were vaccinated against HBV before the study period [37]. This denotes very low HBV vaccination uptake among pregnant women.

The first-ever national pilot cross-sectional study was carried out among pregnant women targeting hepatitis B vaccination coverage. Out of the total sample of the study participants, only 13.2% were vaccinated against HBV for one to three doses. The vaccination schedules completed were: three doses (8/159, 5.0%), two doses (5/159, 3.1%), and one dose (8/159, 5.0%). The findings show poor coverage of the full-dose (3 doses) per schedule and per study participant. All the study participants reported having received hepatitis B vaccine prior to pregnancy, and over 50% of them had not heard of hepatitis B vaccination [38]. The WHO recommends that three HBV vaccines must be completed at 0, one month, and (within) or up to six months [39]. Some of the reasons documented for non-uptake of vaccination included: lack of awareness of the vaccine, inadequate access to the vaccine, and positivity to hepatitis B virus, which does not necessitate the participant to vaccinate as per the guidelines [38]. Such structural and systems issues must be addressed so as to enhance uptake of the HBV vaccine by pregnant mothers at the ANC.

Other low HBV vaccination uptake levels were reported in another study conducted in Nigeria, in which they found that 19.5% had been screened, while only 9.7% were vaccinated [40]. This shows that overall HBV vaccination uptake among the study participants was low. Nevertheless, there was an increased likelihood of adequate knowledge, previous screening, and vaccination among the study participants who were health workers. Other positive predictors of knowledge and vaccination were tertiary education and tertiary care. There was inadequate knowledge about hepatitis B infection among pregnant women in the study area, with significant differences at the various levels of care; for instance, in lower health facilities, screening and vaccination were also sub-optimal. This suggests that dissemination of information, universal screening and vaccination services for pregnant women in Nigeria require scaling up.

Lastly, a study conducted in Lubaga Hospital, a non-profit facility in Kampala, Central Uganda that focused on HBV virus infection and vaccination-related data in which 385 pregnant women were recruited as the study participants established that 3 out of every 4 expectant mothers (74%) were hesitant to uptake the hepatitis B virus infection vaccine [41]. The majority of the study participants were between the ages of 18 and 28 years and had attained at least secondary education. Predictors of vaccine hesitancy included secondary education attainment or below, being inadequately informed about hepatitis B virus infection and vaccination, having a correct perception of risk towards HBV infection, and displaying bad behavioural skills towards HBV prevention. The extremely high HBV infection vaccine hesitancy among the study participants invariably represents a low uptake of hepatitis B vaccination among the study participants.

This study also established that the impact of the intervention on all outcomes was not significantly different across the age strata (<25 years versus ≥25 years). All interactions between intervention covariates and age strata had p-values >0.05. This means that Integration as the intervention in this study had an impact on the younger study population (less than 25 years of age), who were the majority. Over 95% of the younger study participants, especially <25 years, were impacted by the intervention outcome, such as increased uptake of HBV, HCV, and HIV screening, HBV vaccination, and a high level of knowledge and awareness of the three infectious diseases, both in the intervention and control groups, respectively.

Findings from this study are consistent with those observed in a study conducted in Indonesia where the majority of respondents were within the age range of early adulthood, which aligns with a higher susceptibility to hepatitis B infection, as supported by other similar studies [31]. For instance, another separate study conducted in Indonesia reported that the majority of the pregnant women who participated in the study were in their early stage of childbearing age [42]. Nevertheless, there was no statistically significant relationship between age and the covariates. Two studies conducted in neighbouring South Sudan and Uganda observed that younger age groups of the study participants took up screening services, and showed higher rates of infection [34,30-42]. For instance, about 43.3% of those aged 15-25 years tested positive, compared to 27.7% of those over 30 years. However, there was no statistically significant association between age and hepatitis B status. This young stage of life normally involves several biological, social, and economic changes that can influence health-seeking behavior and risk exposure [43]. Factors such as increased social interaction and reproductive health activities could contribute to this age group's enhanced risk perception. It could also mean that countries such as Uganda and South Sudan may have a similar population pyramid where the majority of the population is young. Overall, the findings of this study highlighted the critical significance of improving maternal knowledge regarding hepatitis B to foster positive attitudes toward its prevention, particularly in the context of vertical transmission.

On the contrary, in a study conducted in Nigeria, it was observed that the mean age of the pregnant women was 28.84 ± 4.74 years, and the majority were in the 25-34 years age range, a much older age group compared to the findings from other studies [31]. Similar findings were also observed in a non-randomized experimental study conducted in Egypt. The study reported that nearly half of the population were in the age group (25-<35) [28]. However, there was statistical significance between age and pregnant women's knowledge and attitude regarding hepatitis B virus infection.

Conclusion     

The need for early detection of HBV, HCV, and HIV in the first trimester, reduction of ‘lost opportunity´ by pregnant mothers in accessing HBV, HCV, and HIV risk awareness, screening, HBV vaccination, treatment care, and support at one point of care underscores the necessity of integrated care using the ICM. This study established a pooled HBsAg positivity rate of 2.1%. The ICM intervention had the following positive outcomes: optimization of HBV and HIV screening uptake, high level of HBV, HCV, and HIV awareness in the intervention group. The majority of study participants accessed messages and information about HBV, HCV, and HIV from ANC, followed by the Outpatient Department. More study participants were vaccinated against HBV in the intervention group. Using the ICM for HBV, HCV, and HIV at one point of care (ANC) can enhance early detection and improve the mother and newborn´s health outcomes, thereby reducing disease progression. This approach can also strengthen public health responses for triple elimination.

Competing interests     

The authors declare no competing interests.

Authors' contributions     

John Bosco Alege conceptualized the study, collected data, and wrote the first draft research report, including the draft manuscript; Alloys Orago provided technical inputs in the design of the study methodology; John Paul Oyore provided overall guidance from conceptualizing the study, reviewing the research protocol, results and the report; Philippa Musoke provided technical input in the field during data collection, ensuring quality of sampling and the laboratory tests, validation and technical review of the results. All the authors read and approved the final version of this manuscript.

Acknowledgments     

This manuscript was developed out of a Ph. D (Doctoral) research project. Therefore, we would like to acknowledge the study participants and the health workers at the study sites in Koboko and Maracha districts, respectively. We thank all the research supervisors for their technical guidance throughout this research project. Finally, the data collection for this study was supported by the Fogarty International Center of the National Institutes of Health, U.S. Department of State´s Office of the U.S. Global AIDS Coordinator and Health Diplomacy (S/GAC), and President´s Emergency Plan for AIDS Relief (PEPFAR) under Award Number 1R25TW011213. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Tables and figure     

Table 1: demographic characteristics of study participants in the intervention and control groups

Table 2: study outcomes disaggregated by primary outcome, sensitivity analysis, and other (secondary) outcomes

Table 3: study outcome subgroups of participants disaggregated by age, sensitization received, and vaccination status

Figure 1: place where participants reported having received sensitization and awareness about the risk of HBV, HCV, and HIV

References