Introduction

Human immunodeficiency virus (HIV), syphilis and hepatitis B are sexually transmitted infections (STIs) that, if left undiagnosed and untreated, can lead to serious complications and death. Despite improvements in the last decade, their prevalence remains high in Asia [1, 2]. In 2017, 5.2 million people were living with HIV in the Asia Pacific region [3] and 123,000 people died from HIV-related causes in 2021 [4]. The regional prevalence of HIV was 0.2% [4]. In 2012, an estimated 1.8 million women were infected with syphilis in the South-East Asia region [5] and 39 million people with hepatitis B with a prevalence of 2.0% [6].

These STIs can be transmitted from infected mothers to their children during pregnancy and childbirth, resulting in significant morbidity and mortality. The rate of mother-to-child transmission of HIV in Asia and the Pacific is relatively high, at 17%, among the estimated 61,000 women living with HIV who gave birth in the region in 2017 [3] and 1.3 million pregnant women are at risk of transmitting HBV to their newborns each year [7]. The global number of adverse pregnancy events attributable to maternal syphilis infection was estimated to be 52,307 in the South-East Asia Region and 13,472 in the Western Pacific Region [8].

Mother-to-child transmission (MTCT), also called vertical transmission, can be prevented with simple and effective interventions, including antenatal screening and treatment, prevention of male-to-female transmission during sexual intercourse, and improving community awareness. Antenatal screening is an essential tool to enable women to find out if they are infected and to take the necessary steps to access preventive treatment if they test positive in order to avoid MTCT [9]. Since 2010, an estimated 7,400 new HIV infections among children in the Asia Pacific region were averted because of interventions aimed at reducing the MTCT of HIV [3]. However, due to limited availability and access to these interventions [10], antenatal screening for STIs in Asia remains low [11]. Only three of the 17 reporting countries in the Asia-Pacific region met the global target of over 95% coverage for knowledge of HIV status among women receiving ANC in 2017 and six countries (Bangladesh, Timor-Leste, Papuz New Guinea, Lao People’s Democratic Republic, Indonesia, Singapore) reported coverage below 40% [11]. Only thirteen countries currently out of 17 countries have a policy of screening for hepatitis B during pregnancy, and very little data on hepatitis B screening coverage is currently available [10]. Most Asian countries also have no data on syphilis screening for pregnant women. Of the 28 countries in Asia and Pacific regions (according to WHO definitions of regions) reporting antenatal screening coverage for syphilis between 2010 and 2017, four countries reported coverage between 20% and 49% (India, Myanmar, Vanuatu, Papua New Guinea) and three reported coverage below 5% (Afghanistan, Indonesia, Solomon Islands) [11]. Yet unknowingly infected people can transmit infections to their sexual partners and infected women to their children through MTCT. This also prevents them from accessing timely treatment leading to long-term complications that generate significant costs for the health system. In addition, low uptake of STIs screening services can exacerbate existing health disparities, with vulnerable populations, such as marginalised communities or migrant populations, facing additional barriers to accessing screening services.

To guide a path towards triple elimination of MTCT of HIV, syphilis, and hepatitis B in Asia and the Pacific, the WHO developed a regional framework [10]. This framework aims to eliminate these three infections in newborns and infants by 2030 in Asia. The key recommendations emphasise an integrated approach to triple elimination, recognising the interconnectedness of the three diseases and the potential for resource optimisation and highlights the importance of strengthening health systems to effectively deliver comprehensive services and achieve universal health coverage. The framework focuses on building capacity, improving laboratory and diagnostic services, ensuring a reliable supply chain for medicines and commodities, and improving reporting systems. It recognises the need for collaboration between different sectors beyond the health sector and the importance of sustainable financing mechanisms to support the implementation of elimination programmes. Meanwhile, it encourages the participation of women living with HIV, women affected by syphilis, and mothers with hepatitis B, men and communities in the design, implementation, and evaluation of programmes and policies.

Understanding barriers and facilitators influencing antenatal screening for STIs is essential to design effective screening interventions. The information will also be useful to help countries to achieve a key health target of the Sustainable Development Goals (SDGs), i.e., “end the epidemics of AIDS, tuberculosis, malaria and neglected tropical diseases and combat hepatitis, water-borne diseases, and other communicable diseases by 2030”. A systematic review conducted by Blackstone et al. [12] investigated the barriers and facilitators to routine antenatal HIV screening in sub-Saharan Africa, using literature published between 2000 and 2015. They identified the fear of the screening results, perceived stigma towards HIV-positive people, fear of the partner’s reaction in case of a positive test result, and perceived partner disapproval of the test as barriers to antenatal HIV screening. A high level of education, good knowledge of MTCT and HIV, and partner involvement in antenatal care were favourable factors for screening. Health system and provider issues affected the acceptance of antenatal screening. Good patient-provider communication, counselling to improve knowledge of pregnant women of the benefits of screening through counselling, and the perception that HIV screening is mandatory were facilitators to screening.

Barriers are likely to change over time, as societies evolve, beliefs change, or targeted interventions are put in place. There is no literature review summarising the evidence on barriers and facilitators to antenatal screening for HIV, syphilis, and hepatitis B in the Asian context. Factors affecting screening are likely to be different from those in the African context due to cultural and contextual differences. This hinders the development of targeted strategies and interventions to overcome barriers and improve the effectiveness of antenatal screening programmes. It also limits the application of the WHO framework towards triple elimination of MTCT of HIV, syphilis and hepatitis B. Health care providers in Asia may also lack guidance on how to effectively implement and improve antenatal screening programmes for STIs. Barriers preventing vulnerable communities from accessing screening are not known, which may contribute to disparities in health outcomes, with potentially negative impacts on maternal and child health.

In order to fill this evidence gap, this review aimed to investigate the barriers and facilitators to antenatal screening for HIV, syphilis, or hepatitis B for women in Asia. Its specific objectives were to identify available evidence and underline possible gaps in the research knowledge base surrounding this subject.

Methods and analysis

The review and its reporting comply with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist (S1 Table) and the protocol has been published on PROSPERO (registration number CRD42023435483).

Inclusion criteria

The eligibility criteria for study inclusion were developed using the acronym SPlDER: S sample; P phenomenon of interest; D design; E evaluation; R research type [13] (Table 1).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 1. Eligibility criteria for study inclusion.

https://doi.org/10.1371/journal.pone.0300581.t001

Results

After the selection process, 23 articles met the eligibility criteria and were included in the review. The PRISMA diagram provides an overview of the selection process (Fig 1).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Fig 1. PRISMA diagram of the research strategy.

https://doi.org/10.1371/journal.pone.0300581.g001

General study characteristics

Details about the articles included are presented in Table 2. Most included studies were on HIV screening, one was on syphilis screening [19], one on HIV and syphilis [20] and one on HIV, syphilis and hepatitis B [21]. Eight out of the 23 studies used data collected after 2015 [20, 22–28]. Six of the studies were conducted in Vietnam, five in India, three in Indonesia, two in Cambodia, and one each in Hong Kong, Mongolia, China, Afghanistan and Thailand. Nineteen of the studies (83%) used quantitative methods, three (15%) used qualitative methods, and one (2%) used mixed methods.

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 2. Characteristics of selected papers.

https://doi.org/10.1371/journal.pone.0300581.t002

In the four studies that used qualitative methods, pregnant women were interviewed as well as other individuals such as health providers, district managers, husbands, and mothers. Sample sizes in quantitative studies ranged from 114 to 122,351 pregnant women, most often recruited during ANC visits. The quantitative studies were all cross-sectional except one from Indonesia, which was longitudinal [25]. Most quantitative studies used logistic regression models to determine the association between potential barriers and the outcome of interest.

Overviews of the barriers and the facilitators identified

The barriers and facilitators identified in the included articles are presented based on the categories of the Andersen’s conceptual model (Table 3 and Fig 2).

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Fig 2. Flowchart of factors influencing antenatal screening for HIV, syphilis and hepatitis B based on the Andersen’s conceptual model.

https://doi.org/10.1371/journal.pone.0300581.g002

Download:

• PPT
  PowerPoint slide
• PNG
  larger image
• TIFF
  original image

Table 3. Barriers and facilitators to antenatal screening for HIV, syphilis and hepatitis B identified in the selected papers based on the Andersen’s conceptual model.

https://doi.org/10.1371/journal.pone.0300581.t003

Predisposing characteristics.

Several predisposing characteristics were reported as either barriers or facilitators to antenatal screening for HIV and syphilis. In three studies conducted in Vietnam and India, age was associated with antenatal screening of HIV [22, 32, 33]. Pharris et al. [32] found that younger Vietnamese women were more likely to be screened while Bharucha et al. [33] found the opposite result in India. Khuu et al. [22] identified being younger than 30 years old as a barrier to antenatal screening.

Low education status of pregnant women was a barrier to antenatal screening in three studies conducted in Vietnam [22, 23, 29] and one in India [28]. Similarly, one study conducted in Hong Kong [39] and one in India [36] identified higher education as a facilitator to antenatal screening. However, the level of education associated with a positive likelihood of being screened varied between studies. For example, Khuu et al. [22] showed that nine or more years of education was associated with more acceptance of screening in Vietnam, whereas Sarin et al. [36] showed that this was true at more than six years of education in rural India.

Pregnant women’s knowledge about HIV and PMTCT was associated with antenatal screening decisions. Lack of knowledge about HIV amongst pregnant women [28, 34, 36, 38], about the MTCT services [34], and about the availability of HIV testing facilities [35] were identified as barriers to screening in four studies in India, one in Cambodia and one in Thailand. Similarly, three studies conducted in Cambodia, Hong Kong and China found that a better knowledge of HIV amongst pregnant women was associated with a higher screening uptake [37, 39, 41]. Moreover, Munkhuu et al. [19] found similar results for syphilis in their study conducted in Mongolia. Lack of knowledge about syphilis amongst pregnant women was associated with lower screening uptake. A study conducted in India [28] found that low exposure to mass media was associated with lower HIV screening uptake. Similarly in Hong Kong, Lee et al. [39] identified access to HIV information by means of posters, pamphlets, videos, and group talks as a facilitator to screening.

Enabling factors.

The role of enabling factors such as wealth, place of residence, husbands and health workers’ roles, social and cultural norms or screening cost has been discussed in several articles.

Low household wealth or socio-economic status was a barrier even in countries where antenatal screening was free of charge. Three studies conducted in Mongolia, Vietnam, and India found low socio-economic status as being a barrier to antenatal screening for HIV [19, 23, 28]. Pharris et al. [32] identified higher economic status as a facilitator to antenatal screening for HIV in Vietnam.

Various studies have shown that the place of residence was associated with antenatal screening for HIV [22, 23, 25, 28, 30, 32, 33] and syphilis [19]. A study conducted in Vietnam [23] and another conducted in India [28] identified living in a rural area as a barrier to antenatal screening for HIV. Similarly, Wulandari et al. [25] and Pharris et al. [32] found that living in an urban area and a semi-urban area were facilitators to antenatal screening of HIV in Vietnam and Indonesia respectively. Proximity to the hospital is also a factor influencing antenatal screening uptake. Khuu et al. [22] and Nguyen, Christoffersen, and Rasch [30] found that living further away from the hospital (over 20km in the case of Khuu et al.) was a barrier to antenatal screening for HIV. Similar results were found by Munkhuu et al. [19] in Mongolia for the antenatal screening of syphilis. Meanwhile, Bharucha et al. [33] identified living closer to the hospital as a facilitator for antenatal screening of HIV in India.

Two studies conducted in Vietnam found a significant effect of occupation on the decision to be tested. For example, housewives, or labourers/farmers were less likely to be tested for HIV [22, 29]. Kakimoto et al. [37] identified high partner education level as a facilitator to antenatal screening in Cambodia. Meanwhile, Chu, Vo [23] found a negative association between belonging to ethnic minorities and being tested during pregnancy.

Several articles identified that their husband play a key role in women’s decision to be screened. Fear of negative reactions from their husbands [34], husband’s disapproval [29] and lack of support [40], and beliefs that their husbands have a bad attitude towards HIV testing [27] were identified as barriers to screening in India, Thailand, Indonesia and Vietnam respectively. Two studies conducted in Cambodia [37, 38] found that the perceived need to obtain partner’s authorisation is a barrier to screening for HIV. Similar findings were found in Afghanistan by Todd et al. [21] for antenatal screening of syphilis and hepatitis B. Similarly, Sarin et al. [36] reported that having discussions with spouses about HIV in India encouraged women’s screening for HIV.

Various studies have shown that social and cultural factors were key barriers to antenatal screening for HIV, syphilis or hepatitis B. Todd et al. [21] identified stigma toward infected people as a barrier to antenatal screening for HIV, syphilis, and hepatitis B in Afghanistan. Similar results were found by Baker et al. [20] in Indonesia for the screening of HIV and syphilis, and Lubis et al. [24] and Rogers et al. [34] for the screening of HIV. This last article also identified the fear of negative reactions from parents and community as a barrier. Similarly, Li et al. [41] found that lower perception of social stigma was associated with higher screening uptake.

Time was also associated with antenatal screening decisions for HIV and syphilis. It was a barrier both from the supply and the demand side. Working pregnant women reported that limited opening hours of screening centres were a major health-facility related barrier to antenatal screening for HIV in Indonesia [24]. Limited time to inform women properly about HIV during pregnancy and antenatal screening [40] as well as limited time to perform screening for syphilis [19] were barriers to antenatal screening in Thailand and Mongolia. From the demand side, long travel time to access antenatal screening services was associated with lower HIV screening uptake in Thailand [40]. Similarly, lack of time was identified as a barrier to screening for HIV and syphilis in Indonesia by Baker et al. [20]. Meanwhile, Bharucha et al. [33] found that being offered testing too late in pregnancy as associated with lower screening uptake for HIV.

The type of screening provider was a factor associated with screening in various studies. Hạnh, Gammeltoft, and Rasch [31] showed that, in Vietnam, having the first antenatal check-up at a commune health station was a factor associated with an increased probability of being tested, compared with district and provincial health facilities. Similarly and in the same country, having received ANC only at a private clinic/hospital was found to be a barrier [22]. However, in India, Sarin et al. [36] found that seeking ANC at government district hospitals and private clinics, as opposed to community health centres not equipped with either HIV counselling or testing facilities, had a positive effect on the probability of receiving HIV screening. Similar results were found by Bharuch et al. [33] in India. Some facilities lack screening materials and this was associated with lower screening of syphilis in Mongolia [19] and lower screening of HIV and syphilis in Indonesia [20]. In addition, a study carried out in Indonesia [24] revealed that the lack of antenatal care and screening services in the same building was a barrier to HIV screening. In Cambodia, the lack of access to ANC services outside the capital city was a barrier to screening for HIV [38].

Healthcare workers play a key role in screening decisions. In Vietnam, Dinh, Detels and Nguyen [29] found that a poor perception of healthcare availability was negatively associated with screening for HIV. Fear that healthcare workers would become impatient with them or that their questions would not be considered important was a barrier in Thailand [40], and concern that healthcare workers were opposed to antenatal screening for syphilis impeded testing in Mongolia [19]. Similarly, Lee et al. [39] identified health worker recommending HIV testing as a facilitator of screening. A study conducted in Vietnam [32] identified never having received antenatal HIV counselling as a barrier to screening and another identified a language barrier between health workers and women as barriers [40]. High acceptance of screening for HIV, syphilis and hepatitis B was also a factor increasing screening uptake in Afghanistan [21]. Pakki et al. [26] and Lubis et al. [24] found that, in Indonesia, health worker training as well as reward and punishment system to motivate them was associated with higher antenatal HIV screening. This is consistent with findings reported in Indonesia for HIV and syphilis screening [20]. Todd et al. [21] found that provider perceptions of low infection rates and assumptions on a person’s likelihood of infection based on a healthy appearance were associated with lower screening uptake of HIV, syphilis and hepatitis B in Afghanistan. Baker et al. [20] also identified shortage of laboratory personnel as a barrier to screening.

Costs of screening was also identified as factor influencing HIV and syphilis screening uptake. Tests being seen as expensive by pregnant women was identified as a barrier to HIV and syphilis screening in Indonesia [20]. Similarly, Crozier et al. [40] found that costs of screening and transportation represent barriers to screening of HIV and syphilis in Thailand.

At the national-level, enabling factors were identified by two studies in Mongolia and Indonesia [19, 20]. Munkhuu et al. [19] identified the complexity of the syphilis testing service system as a barrier to antenatal screening. Similarly, Baker et al. [20] found that poor dissemination of national policy on screening, not seeing screening as a priority intervention, and funding consisting of multiple small-scale sources were barriers to HIV and syphilis screening in Indonesia.

Finally, Crozier, Chotiga et Pfeil [40] showed that having only one ANC check-up was associated with low screening uptake.

Need factors.

Few need factors were identified as barriers or facilitators in antenatal screening for HIV and syphilis. Four studies conducted in Hong Kong, Vietnam and Thailand found that low perceived risk of HIV was associated with low screening [29, 32, 39, 40]. Similarly, Lee, Yang, and Kong [41] found that, in China, high perceived risk of HIV was associated with high screening. In a study investigating barriers and facilitators in the delivery of antenatal testing for anaemia, HIV, and syphilis, Baker et al. [20] identified perceived low prevalence of HIV and syphilis as barriers to antenatal screening in Indonesia. Two studies found that believing that HIV testing was not important during pregnancy was associated with a lower screening uptake in Indonesia and Vietnam [22, 27]. Similar Lee et al. [39] identified the perception of the benefits of HIV screening as a factor facilitating it. Finally, Munkhuu et al. [19] found that women who previously reported STIs were less likely to be screened in Mongolia.

Discussion

This study is the first to provide a narrative synthesis of the current literature on barriers and facilitators to antenatal screening for HIV, syphilis and hepatitis B in Asia. This systematic review of qualitative, quantitative and mixed-method studies shows that there are research gaps into the factors influencing screening for syphilis and hepatitis B, with most of the studies reviewed focusing on HIV. This review therefore effectively allows conclusions to be drawn about HIV alone.

Antenatal screening for HIV in Asia is influenced by a range of factors including predisposing characteristics (age, education level, wealth, place of residence, knowledge about HIV), enabling factors (husband support, health facilities characteristics, health workers’ support and training) and need factors (risk perception, perceived benefits of screening). These factors are similar to those identified in a review conducted by Blackstone et al. [12] in sub-Saharan Africa. In our literature review, as in the sub-Saharan African context, being better-off and highly educated were identified as facilitators. In both contexts, pregnant women’s lack of knowledge about HIV appears to be a significant barrier to antenatal HIV screening. Our results suggest that antenatal screening could be improved by facilitating access to information for women, their husbands and health workers. Most studies have emphasised the importance of improving dissemination of information about HIV and HIV testing in order to improve uptake of antenatal screening. Unlike Blackstone et al.’s review of the literature in the sub-Saharan African context [12], our review did not identify fear of results as such as a barrier to testing, but more broadly fear of partner reactions and potential violence in the event of a positive result. We did not find that cultural gender norms to be barrier, such as "testing is a woman’s business", as found by Blackstone et al. [12]. However, women in this review mentioned the need to obtain a husband’s approval to undergo screening. In both African and Asian contexts, societal stigma towards HIV-positive people proved to be a major barrier to HIV testing. Our findings, and those of Blackstone et al. [12], suggest that antenatal screening could be improved by strengthening the health care system. Both reviews highlighted the role of healthcare and communication professionals in increasing antenatal screening rates. In the sub-Saharan African context the perception of screening being mandatory was a barrier to screening, but this did not emerge in our literature review.

Although the studies we reviewed were all conducted in Asia, they spanned very different contexts. It is reasonable to assume that the barriers to antenatal screening will differ between Hong Kong and India for instance. Guidelines about screening and adherence to guidelines differ between countries. A review of maternal health care policies in eight countries in the Western Pacific region [42] found that WHO recommendations on antenatal HIV screening were not included in antenatal care guidelines in two countries. In 2018, 37 countries in the Asia Pacific region promoted antiretroviral therapy for all pregnant and breastfeeding women living with HIV, but in six of these countries, the policy is being implemented in less than 50% of all maternal and child health sites [43]. Reported barriers in the Hong Kong study were mainly focused on the demand side [39], whereas the Mongolia study identified many supply-side barriers [19]. This highlights the need for qualitative studies in Asian contexts to investigate context-dependent factors that may be missed in quantitative studies.

As stigmatisation of people with STDs is one of the main factors preventing pregnant women from being screened, interventions should provide information and counselling to pregnant women and their husbands, tailored to low-literacy populations to help reduce stigma and increase uptake [36, 38, 39]. Raising awareness within communities of the importance of male partner involvement, the benefits of screening and adherence to treatment could increase demand for antenatal screening services. However, studies on awareness campaigns about HIV in Vietnam [44] and Thailand [45] showed that the stigma attached to social judgement is difficult to reduce. Various studies recommended the integration of HIV screening into community level ANC services [23, 25, 30, 31, 39] and the development of opt-out approaches for those who prefer not to test [29, 35], as recommended in sub-Saharan Africa by Blackstone et al. [12]. We found that husbands play a key role in encouraging pregnant women to undergo screening. Interventions to improve husbands’ knowledge and involvement in maternal and newborn health had a positive impact on maternal health behaviour in Bangladesh [46] and Nepal [47]. To reduce social and financial barriers to antenatal screening, screening should be offered to pregnant women universally free of cost [32, 39]. Currently, national budgets do not cover all the costs associated with antenatal screening in all Asian countries. In the 17 Asian countries for which data on the cost of screening pregnant women for HIV, syphilis and hepatitis B were available in 2017, HIV screening of pregnant women was free in all of these countries, syphilis screening in 14 countries and hepatitis B screening was free in eight countries [11]. Finally, the quality of services depends on the availability and capacity of healthcare workers. To reduce the persistence of inappropriate healthcare practices in pregnancy, interventions need to develop health worker training programmes on STIs and pregnancy screening. A successful initiative in Cambodia in decreasing risky sexual intercourse and improving the access to sexual and reproductive health care services has focused on training community health workers in sexual and reproductive, maternal, neonatal, child and adolescent health [48].

Adolescent pregnancy is still common in the region with 3.7 million births to adolescent girls aged 15–19 every year in Asia and the Pacific [49]. Pregnant adolescents are very vulnerable and are known to have poor outcomes for both mother and child [50]. This systematic review of the literature highlighted a lack of age-specific data, particularly in relation to adolescent pregnancy, and confirmed the need to fill this research gap. Similarly, a systematic literature review of interventions addressing health outcomes for pregnant adolescents in low- and middle-income countries highlighted the need to develop studies to design high-quality care and services for pregnant adolescents [51].

Several limitations to this study should be noted. Firstly, most studies sampled pregnant women through ANC services. However, women who have not sought ANC may face the greatest barriers to testing. Due to resource constraints, only articles in English were reviewed, which may limit access to the grey literature and studies published in other languages (especially Chinese). Finally, different studies were undertaken in different contexts and using different methods. This heterogeneity limits our ability to compare between studies. However, this systematic review follows a rigorous method of article selection and analysis. It complements existing literature reviews on barriers to antenatal screening, particularly in sub-Saharan Africa [12, 52].

Conclusion

The main barriers to antenatal screening in this systematic review were stigmatisation of infected individuals, lack of involvement of husbands and healthcare system factors. To improve uptake of antenatal screening interventions to improve community and husband involvement, awareness campaigns with communities and health workers, and training of health workers on STI issues are needed. While countries vary in their contexts and implementation of international recommendations on integrated antenatal screening for STIs, in all settings the planning, implementation, reporting and monitoring of interventions to eliminate mother-to-child transmission require coordination between different health system stakeholders at national, regional and local levels to avoid gaps or duplication. Global, regional and national guidelines need to be harmonised to avoid gaps and duplication between disease-specific and maternal and child health programs and guidelines. Integration of services for different diseases should be prioritised where possible. However, studies to examine the barriers and facilitators to antenatal screening for syphilis and hepatitis B and to examine the behavioural determinants of antenatal screening in Asia are still needed.

Supporting information