Introduction

HIV was the sixth leading cause of death among women of reproductive age, 15 - 49 years, in El Salvador in 2010 [1], and has persisted among the 10 leading causes of death for all ages among persons in El Salvador between 1999 and 2009 [2–8]. The number of people living with HIV/AIDS in El Salvador has been rising since the late 1990s and currently ranges between 28,000 and 34,000 [9,10]. Underreporting of HIV cases has been repeatedly cited as a major problem [11,12]. With an HIV prevalence of 4.5 - 5.5 cases per thousand residents [9,10], El Salvador has the third highest prevalence in Latin America. About 2,000 children aged 0 – 14 years are known to be currently living with HIV in El Salvador [10]. In addition, mother-to-child transmission (MTCT) accounts for 6% of new cases of the various HIV transmission modes, the second highest MTCT attributable risk percentage among Latin American countries [10]. However, national authorities report a considerably lower fraction, not exceeding 0.2%, of new HIV cases attributable to MTCT, whereas 7% of newborns from HIV-infected mothers are also HIV-infected. Health is a big focus of the Salvadorian government [13], and health authorities have adopted a nationwide program for prevention of MTCT (PMTCT), with a goal of having an HIV-free newborn generation by 2015 [12] or reducing MTCT from the current 7% to only 2% [9]. The program focuses on diagnosing and treating HIV-positive pregnant women and is making great progress to date [9,12].

The World Health Organization considers HIV screening to be the first and most crucial step in PTMCT, and the U.S. Centers for Disease Control and Prevention (CDC) recommends widespread HIV screening in health care settings and early universal screening for HIV for pregnant women [14–17]. The current national guidelines around PMTCT in El Salvador, published in 2012, recommend HIV screening for every pregnant woman within the first 3 months of pregnancy. An initial voluntary, confidential, and free-of-charge rapid HIV test is offered during the first antenatal care visit. Positive tests are sent for confirmation by ELISA 3^rd or 4^th generation. Women are informed of their HIV status four weeks later or earlier, during the next antenatal care visit. Women who are confirmed as HIV-infected are offered universal free-of-charge antiretroviral treatment (ART) as soon as possible and are given condoms and counseled on avoiding unsafe sex. They are also offered substitute milk for their infant for up to 18 months of life. ART is also recommended for up to a month and a half for these infants. Pregnant women are also offered HIV screening at labor if no previous screening was performed. In the case where women are found HIV-infected at or close to labor, specific ART guidelines are also applied to prevent MTCT [18].

It has been reported that more than 97% of pregnant women were tested for HIV in El Salvador in 2007 [12,19], an even higher rate than the 96% reported in Ontario, Canada, for 2010 [20]. If this quasi-universal HIV screening for pregnant women is valid, it could be one of the biggest achievements in antenatal care service delivery. Given that this antenatal HIV screening is not mandatory, while recognizing its relevance to women and children’s health, there could be an overestimation of the true percent of screened pregnant women, especially with an absence of details on the data source for the reported estimate [19]. We also expect that variations in the screening uptake exist by sociodemographic and health care characteristics. To help local authorities make informed decisions for targeted interventions around PMTCT, we analyzed data on HIV screening at last pregnancy from a representative sample of childbearing-age women in El Salvador as part of the Salud Mesoamerica (SM2015) Initiative. Specifically, our objectives were 1) to estimate the percent of pregnant women screened for HIV through antenatal care, and 2) to identify screening predictors and barriers at the sociodemographic and health care level.

Methods

Results

Between March and June 2011, we interviewed a total of 4,730 women aged 15 - 49 years. Of these, 3,757 women (79.4%) had ever given birth and 2,929 (77.9%) of them had had at least one pregnancy over the last five years. Sociodemographic characteristics of these women are detailed in Table 1. Use of antenatal care was high, as 2,792 women (95.3%) reported receipt of at least one antenatal care visit during their last pregnancy; of the 137 remaining women, 76 did not answer the question about receipt of antenatal care, and 61 reported not having received antenatal care during pregnancy. Data related to HIV screening were analyzed for the 2,792 women who reported receipt of at least one antenatal care visit during their last pregnancy. Figure 1 details the sample of women included in our analysis.

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Figure 1. Distribution of women from those eligible to be interviewed to those included in the analysis sample.

https://doi.org/10.1371/journal.pone.0082760.g001

Among the 2,792 women included in the analysis, 83% reported being screened for HIV during their last pregnancy as part of antenatal care — only two participants had a missing answer when asked about receiving HIV screening. This 83% rate increased by less than 2% when analysis was restricted to pregnancies over the last two years; among the 1,324 women who had their last pregnancy within two years and received antenatal care, 1,117 (84.7% weighted percent) were screened for HIV.

HIV screening uptake varied from a low of 69.1% among women who were not seen by a medical doctor during antenatal care, to a high of 93.7% among women who attended college (Figure 2). Variation of HIV screening was statistically significant through all sociodemographic and health care-related characteristics, except when the health care provider type was a nurse aide. Being seen by a nurse aide during antenatal care was not associated with receiving an HIV test (Table 2).

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Figure 2. Distribution of HIV screening during pregnancy by socio-demographic and health care-related characteristics.

https://doi.org/10.1371/journal.pone.0082760.g002

When all characteristics were adjusted in the multivariate logistic regression, marital status was not sustained in the model, but all other characteristics were maintained (Table 3).

Women were divided into four age-group categories. Compared to women 20 - 29 years old, women of all other age groups had a lower chance to be screened. Chances for screening increased by women’s educational level and for women living in a household of the highest monthly expenditure tertile, compared to women with no education or those who only took a literacy course, and women living in a household of the lowest monthly expenditure tertile. Women who did not benefit from medical insurance coverage had lower chances for being screened compared to those who did.

At the health care level, women had less chance to be screened for HIV if they were not seen by a physician during antenatal care compared to those who were, or if they received antenatal care in health care settings different from a public hospital. Chances of HIV screening increased for women who received a higher number of antenatal care visits and those whose antenatal care visit was not led by a nurse compared to their counterparts.

Discussion

We found disparities in reported uptake of HIV screening through antenatal care among pregnant women in El Salvador despite high rates of screening in general and an increase in prenatal care use since 2005 [22]. Among our representative sample of Salvadorian women of the lowest wealth quintile, less than 83% reported being screened for HIV during their last pregnancy. This rate is lower than the previously reported 97% for the year 2007 [12,19] and rates reported in other more or less developed countries, such as Canada and Uganda [20,23]. However, it is higher than the 76% of pregnant women served by the Indian Health Services who were screened for HIV in the United States in 2009 [24]. Moreover, this rate is not equal across different categories of women and different health care delivery settings.

Disparities were significant at the environmental, demographic, social, and structural levels. Rates of HIV screening varied dramatically by geographic areas. While areas with higher HIV incidence should be prioritized for HIV prevention in general, and specifically for PMTCT, women residing in these areas were less likely to be tested. This finding is noteworthy as it points out not only the inequity in health care provision across regions of the same country, but an unmet need in the most affected areas [21]. Advocates of targeted HIV screening usually recommend restricting screening to those who are the most at risk [25,26]. In countries like the United States, where MTCT contributes to less than 0.1% of new cases, the American College of Obstetricians and Gynecologists, the CDC, and the U.S. Preventive Services Task Force recommend a universal, opt-out HIV screening process for pregnant women that is not linked to a risk assessment [15,27,28]. In addition, WHO has recommended universal prenatal screening as part of its multi-pronged, global approach to achieve an AIDS-free generation [14]. Hence, targeting pregnant women for routine, opt-out HIV screening is consistent with current guidance for PMTCT globally.

Women’s age was also a determinant for screening. The oldest mothers had the lowest chance of being tested. It is possible that health care providers estimate that women of a certain age might not be at risk for HIV. Prevention of different infectious diseases possibly transmitted through and during pregnancy is not subject to the mother’s age [29], and this should not be any different in the case of HIV simply due to stigma or assumptions about HIV risk based on age.

At the social level, education and economy determined screening rates. There is approximately a 20% difference in screening rates between the least and the most educated mothers. The latter group seems more knowledgeable about the importance of this screening and its relevance both to their and their child’s health. Less educated women, however, might still be living with the fear of HIV-related stigma or just misperceiving their risk and the severity of the disease. This finding goes along with other reports on HIV knowledge and perception in Central America. In El Salvador, only 72% of women of reproductive age know about the test for HIV detection, with more than a 17% urban/rural disparity; less than 50% of women know more than one way to prevent HIV, and less than 66% of rural women know that HIV can be asymptomatic [22].

In our sample, employed women tended to be less screened compared to other women. This finding warrants more investigation as we expected that employment would have a positive impact on women’s health-seeking behavior because it empowers them financially and socially.

Similarly to educational level, screening increased by household monthly expenditure level. This is reflective of the health care barriers encountered by the poor, who should be a primary target for prevention interventions based on the local epidemiology of HIV in El Salvador. More so, this finding goes along with access to medical insurance. If El Salvador aims for an HIV-free generation, screening should be available at no cost for those who choose it.

At the structural level, the type of health care provider, the health care setting, and the frequency of antenatal care visits were additional determinants in HIV screening disparities. The failure of health care systems to detect HIV infection during pregnancy has been documented in other Latin American countries [31]. Our findings suggest that HIV screening and prevention education should be strengthened for the nurses, physicians, and other caregivers who provide prenatal care so that antenatal prevention opportunities can be optimized [30]. Ideally, all health care providers should be able to perform a screening test, as they are simple and easy to administer and can save many lives. On the other hand, availability and promotion of basic antenatal care services, including HIV screening at the first prenatal visit, should be unified across all types of health care settings in El Salvador [15].

Our findings are subject to recall bias as women were asked to provide information on their last pregnancy, which could have been five years prior to the survey. However, when data were restricted to the last two years, the rate of screening increased by less than two percent. Also, it is possible that participants might be unaware of the tests they received due to their lack of knowledge around laboratory assessments, and providers might have followed an opt-out strategy for screening which was missed by our participants.

A second limitation to our study is that our sample was selected from the areas that had the highest concentration of the poorest populations in El Salvador. However, we made no distinction between participants during the survey recruitment based on economic level.

By screening pregnant women and monitoring and treating those who are infected, MTCT can be reduced and prevented.

Today, through the provision of appropriate health care to HIV-infected pregnant women during pregnancy and delivery, and for newborns soon after birth, the rate of HIV transmission can be reduced to less than 2%; in the absence of intervention, it can be as high as 25% among the non-breastfeeding population [32,33]. Pregnant women in El Salvador have differential rates of HIV screening. The disparities we found in HIV screening for pregnant women should be alarming to policymakers and health officials who are working hard to fight the HIV epidemic in El Salvador [12]. The goal of an HIV-free generation can be met only if HIV surveillance among pregnant women is strengthened. Ensuring availability, provision, and financial access to HIV screening among all pregnant women equally is the first and the most crucial step toward this goal. This would require eliminating the currently persisting disparities in HIV screening that are hindering the success that has been achieved so far in PTMCT in El Salvador.