Over the last several years it has become clear that reproductive health messages in HIV care must address more than pregnancy prevention. Globally, studies have documented high fertility desires and intentions among people living with HIV (PLWH).1 In South Africa, where there are over 6 million PLWH,2 between 20 and upwards of 60% desire or intend to have a child at some point in the future.3–6 Indeed, many women living with HIV (WLWH) have biological children after their HIV diagnosis, necessitating appropriate clinical intervention to prevent perinatal transmission. Studies show that pregnancy incidence among WLWH in sub-Saharan Africa is high, particularly among those on antiretroviral therapy (ART).7,8 In addition, given that upwards of one-third of stable heterosexual couples in South Africa are serodiscordant,9,10 preventing HIV transmission while couples are trying to conceive is critical.
Clinical and behavioral strategies for reducing HIV transmission risk to infants and partners offer PLWH with options to more safely achieve reproductive goals to have biological children. Use of ART during pregnancy and throughout the breastfeeding period has dramatically reduced the risk of perinatal transmission to <3% in South Africa and other sub-Saharan African countries.11,12 ART for HIV-positive partners, the use of antiretroviral drugs by uninfected partners as pre-exposure prophylaxis (PrEP), and medical male circumcision have been shown to effectively reduce sexual HIV transmission13,14 and are recommended strategies for safer conception.15–17 Additional methods for minimizing infection or re-infection of seroconcordant partners that are specific to conception attempts include condomless intercourse only during the fertile period (ie, timed condomless intercourse) and self-insemination with the HIV-negative partner's sperm.17,18 Assisted reproductive technology offers methods such as sperm washing and in vitro fertilization, although these options are generally not affordable in South Africa and often unavailable in more resource limited settings.19,20 Outside of pregnancy attempts, condom use during pregnancy remains the primary method for preventing transmission to partners.
These strategies for safer conception and pregnancy have been well articulated in national and international guidelines for both serodiscordant and seroconcordant couples21–23 but not yet routinely implemented as part of clinical care for PLWH in low resource settings.24–26 Documenting the demand, receipt, and uptake of safer conception messages in HIV care can help inform implementation of relevant services for PLWH desiring biological children. To date, the need for safer conception services has been based primarily on evidence that many PLWH desire and intend to have children. Although such findings highlight the potential risk of HIV transmission during the periconception period, empirical relationships between fertility intentions and condomless sex remain largely untested. Similarly, low levels of provider–patient communication about fertility intentions,4,27,28 a key first step in the provision of safer conception services, point to inadequate implementation of available strategies. However, the extent to which PLWH receive messages about safer conception and pregnancy in HIV care and employ strategies to minimize HIV transmission is largely unknown.
Using data from a prospective cohort of WLWH engaged in public sector ART care in South Africa, we examine potential differences in the number of condomless sex acts by fertility intentions, while controlling for known and hypothesized confounders. We then compare receipt of safer conception messages between those with positive fertility intentions (regardless of pregnancy outcome) and those with negative fertility intentions who became pregnant (ie, an unplanned pregnancy). Finally, among WLWH with positive fertility intentions, we assess indicators of the use of safer conception methods and examine differences based on partner HIV serostatus.
Data for this analysis were collected as part of a prospective study on fertility intentions, contraceptive use, ART regimens, and pregnancy incidence among a cohort of WLWH on ART. Convenience sampling was used to recruit participants from 4 public ART clinics in Johannesburg, South Africa. To meet the eligibility criteria, women had to be aged 18–35 years, not pregnant at enrollment, on or initiating ART at enrollment, and sexually active within the prior 12 months. Women were excluded if they had given birth in the prior 3 months or had been sterilized, had a hysterectomy, or were otherwise diagnosed as infertile based on self-report and review of clinical records. Of the approximately 3000 women ages 18–35 attending the study sites, about 28% were enrolled in the study.
Study procedures have been described previously.4,8 Briefly, study staff conducted individual baseline interviews between August 2009 and January 2010. Fertility intentions, contraceptive use, and pregnancy testing were assessed during each routine clinical visit for 1 year after study enrollment. Routine visits occurred every 1–3 months based on clinic protocol and provincial ART supply, with an average time of 2 months between visits. Clinical and laboratory measures at each visit were confirmed through medical records. Women who became pregnant during their 1 year follow-up period were followed throughout pregnancy. Participants completed an endline interview with study staff 1 year post-enrollment. Written informed consent was provided by all participants. The University of the Witwatersrand Human Research Ethics Committee approved the study protocol (M090719).
Fertility Intentions and Pregnancy Status
Fertility intentions were assessed at baseline using 3 items that asked about current and future intentions. Those participants not currently trying to conceive (yes/no) were asked about intentions in the next 12 months (yes/no/don't know). Those answering “no” or “don't know” were asked if they would try to conceive someday in the future (yes/no/don't know). Participants indicated at each follow-up visit if they were currently trying to conceive. Pregnancy was assessed amongst all participants at each visit using a urine-based assay administered by study staff and confirmed through repeat testing. Pregnancies were classified as planned or unplanned based on reported fertility intentions before pregnancy diagnosis.
Messages About and Use of Safer Conception Strategies
Communication with providers about fertility intentions was assessed among all participants at baseline, and was reassessed during the final study visit (endline) among participants trying to conceive (regardless of pregnancy outcome) and those with an unplanned pregnancy. Participants were asked what medical advice they had received about conceiving from their ART provider; responses were open-ended and categorized by the interviewers using a list of options. Additionally, those participants trying to conceive at endline were asked about their use of safer conception strategies, including timed condomless intercourse and self-insemination at home.
Clinical and Behavioral Indicators of Safer Conception
CD4 cell count and viral load throughout follow-up were confirmed through medical records and used to examine viral suppression and CD4 count ≥350 cells per microliter as indicators of safer conception method use. Dichotomous variables for knowledge of current viral load and for 95% ART adherence in the prior 2 weeks were based on participants' self-report. Participants reported their total number of sex acts and acts during which a condom was used with any partner in the prior 30 days. Partner information was based on participant self-report, including whether they told their main sexual partner about their HIV status, whether their partner was HIV-positive (dichotomized as yes and no/unknown), and if so, whether their partner was currently on ART and the length of treatment.
To describe the sample, χ2 and Wilcoxon rank sum tests were used to compare distributions or medians of demographic characteristics and variables related to HIV, relationships, and fertility intentions between participants trying to conceive at time of pregnancy or end of study follow-up and those not trying to conceive at time of pregnancy or end of study follow-up. Among women with partners at endline, bivariate and multivariate negative binomial regression models were used to examine differences in the number (count) of condomless sex acts in the past 30 days by fertility intentions. Negative binomial modeling was used over Poisson regression due to overdispersion in the data (the variance was greater than the conditional mean).29 The adjusted model for condomless sex acts included age, baseline condom use, partner HIV serostatus, and disclosure of HIV status, in addition to fertility intentions—the primary exposure of interest. Variables were included in the final model if they were associated with the outcome at the P < 0.20 level in bivariate analyses. Age was also included in the final model, as was partner HIV status which is important to understand the impact of HIV disclosure to a partner. To compare receipt of safer conception messages between those with positive fertility intentions (regardless of pregnancy outcome) and those with negative fertility intentions who became pregnant (ie, an unplanned pregnancy), we used χ2 statistics. Similarly, among WLWH trying to conceive at time of pregnancy or end of study follow-up, we describe indicators of safer conception method uptake overall and use χ2 statistics to compare women with an HIV-negative partner or partner of unknown status and women with an HIV-positive partner. Figure 1 summarizes the analytic samples for each analysis, which differ according to the relevance of scientific questions based on women's fertility intentions and pregnancy status.
Of the 850 women enrolled in the study, 831 completed the baseline survey and at least 1 or more follow-up visits. Overall, 39.7% were in seroconcordant partnerships, 25.3% were in serodiscordant partnerships, and 35.0% indicated that their partner's HIV status was unknown. Table 1 presents baseline characteristics of participants according to fertility intentions at the end of their study follow-up. Partner serostatus at baseline did not differ between those trying to conceive and those not trying to conceive (P = 0.267). Nearly one-quarter (23.1%) were trying to conceive at endline or had a planned pregnancy during study follow-up but had not become pregnant, indicating some potential subfertility. Of those, the majority (63.6%) were not trying to conceive at baseline.
Overall, about one-quarter of women in relationships at endline (n = 667) reported any condomless sex acts in the prior 30 days. In both unadjusted and adjusted analyses (Table 2), those trying to conceive were over 3 times more likely to have had condomless sex compared with those not trying to conceive (adjusted incidence rate ratio: 3.17, 95% confidence interval: 1.95 to 5.16). Baseline condom use was the only other significant predictor of condomless sex. Partner serostatus was not associated with condomless sex—those with HIV-negative/unknown status partners were equally likely to have condomless sex compared with those with HIV-positive partners. In a sensitivity analysis using the same model from Table 2, but further disaggregating HIV unknown status partners from HIV negative or HIV positive partners, there was no statistical difference between these 3 groups in condomless sex acts (results not shown).
Table 3 presents endline data on provider–patient communication about fertility intentions and receipt of safer conception messages from a clinical provider by fertility intentions. Women with positive fertility intentions were more likely to have received any fertility-related advice compared with those with unplanned pregnancies (76.3% vs. 49.1%, P < 0.001). On average women trying to conceive reported receiving information about 1.1 safer conception methods, as compared with 0.8 among women with unplanned pregnancies (t test comparison, P = 0.018). Across both groups, the most commonly received advice (∼30%) was for participants to wait for their CD4 cell count to increase and receipt of this advice was similar across groups (P = 0.360). The median target CD4 count recommended was 350 cells per microliter, although advice ranged from 200 to 600 cells per microliter. Only about one-fifth of those trying to conceive at endline received information about waiting until their viral load was undetectable, and receipt of this advice did not vary based on fertility intentions (P = 0.838). Advice regarding timed condomless intercourse around ovulation was least common, with just 13.5% of those trying and 3.6% of those with unplanned pregnancies receiving information about this strategy (P = 0.044).
Indicators of safer conception method utilization among women trying to conceive at endline (n = 169) are reported in Table 4, which includes comparisons by partner HIV serostatus. Overall, less than one-fifth (17.1%) reported using timed condomless intercourse, and use of this strategy was even lower among those in a serodiscordant vs. concordant partnership (8.5% vs. 26.9%, P = 0.010). In addition, the majority of participants (56.5%) with a planned pregnancy with HIV-negative/unknown partners did not use condoms every time during pregnancy. The majority of women had an undetectable viral load at their most recent bloodwork before conception (84.0%), which was comparable between women in serodiscordant and seroconcordant relationships. Actual awareness of HIV viral load results before conception was 61% overall and did not differ between groups (P = 0.988).
The findings from this study demonstrate high need for and low receipt and uptake of safer conception messages among a prospective cohort of WLWH on antiretroviral therapy in South Africa. Positive fertility intentions were associated with increased likelihood of condomless sex when controlling for other relevant factors and in fact, were the only significant predictor aside from baseline condom use. We are aware of only one previous study to empirically show an association between positive fertility intentions and increased likelihood of condomless sex among PLWH.30 Our adjusted analysis builds on their bivariate findings and what is known about fertility intentions, pregnancy incidence, and serodiscordant partnerships4,7,31 to further demonstrate the necessity of specific safer conception services for PLWH as part of HIV prevention programs.
Beyond further documenting the need for services, our analysis provides important baseline information about the state of safer conception service implementation in HIV care in South Africa before release of the national guidelines for safer conception. By the end of study participation, nearly two-thirds of women trying to conceive or with a planned pregnancy reported discussing fertility intentions with a provider, which is higher than what was documented at baseline (∼41%) or in other reports.4,30,32 This improvement may reflect progress in efforts to improve provider–patient communication about this topic or it may be a direct effect of study participation. Nevertheless, more women intending to conceive reported speaking to a provider about fertility intentions compared with those with unplanned pregnancies, suggesting that these conversations may continue to be largely patient-initiated, as has been previously documented.26,28,33
The increase in conversations about fertility intentions is reflected in the majority of women having received some piece of safer conception advice from a health care provider, though the focus of the counseling was largely on improving the health of the woman before pregnancy and rarely about methods to reduce HIV transmission during conception attempts. Even receipt of messages about improving CD4 cell count, the most common advice, was low. Of note, few participants had received advice about viral suppression, which is a central safer conception strategy. This finding may be due to generally high viral suppression in this cohort on treatment. Nevertheless, re-enforcing messages around viral suppression before attempted conception is important; in this study, only about 60% of women trying to conceive were aware of their viral load, suggesting that many women are not explicitly using viral suppression as a method for safer conception. Furthermore, we did not observe many differences in receipt of medical advice between those trying to conceive or with a planned pregnancy and those with unplanned pregnancies. These findings suggest that even if providers are aware of patients' positive fertility intentions they are not providing sufficient information about safer conception methods, an issue that has been raised in prior qualitative research.32,34
As further evidence of inadequate implementation, indicators of safer conception method utilization among women trying to conceive suggest that uptake of risk reduction strategies is suboptimal. Disclosure to a partner was relatively high compared with other recent findings,31 which may be due to increased time since HIV diagnosis and increased relationship duration in this cohort. However, fewer women in serodiscordant partnerships reported disclosing to their partner compared with those with seroconcordant partners. Utilization of timed condomless intercourse was also lower among those with HIV-negative/unknown partners compared with seroconcordant partners, a surprising and concerning finding that may reflect the lower disclosure among this subgroup or repeated messaging by health care providers about the importance of condom use. Of note, more women reported using timed condomless intercourse than receiving messages about this strategy from a provider, suggesting that they may be familiar with this method from other sources. Condom use during pregnancy was also lower among those with HIV-negative/unknown partners compared with seroconcordant partners, pointing to the importance of counseling about safer sex behaviors not only during the periconception period but throughout pregnancy.
Because there has not been a national training of providers in safer conception methods or other large-scale implementation efforts after release of the national guidelines in South Africa, these data likely contribute to our understanding of the extent to which safer conception methods are currently implemented as part of routine HIV care, a relatively new area of inquiry. A number of recent qualitative studies suggest inadequate implementation26,32,34–37 yet we are aware of only 2 previous quantitative examinations of safer conception-related knowledge and practices among PLWH.31,38 These cross-sectional studies from Uganda and South Africa, which respectively focused on individuals with positive fertility intentions and serodiscordant partners, concluded that knowledge and use of safer conception methods was low.31,38 Our study confirms and extends their findings, presenting prospective data that includes fertility intentions and pregnancy outcomes as well as information on both serodiscordant and seroconcordant partnerships. We compare indicators of uptake by partner serostatus to understand if periconception risk reduction strategies are being used by those who need them most while at the same time recognizing that safer conception methods are also relevant for preventing re-infection among seroconcordant partners.
There are several limitations to this analysis. Given that this study was conducted before PrEP efficacy was established, we do not have counseling and partner utilization data on PrEP, which is now an important safer conception strategy.16 We also did not assess male partner medical circumcision status. Our comparison group for receipt of safer conception messages by fertility intentions is limited to women with unplanned pregnancies, given that participants who did not conceive during study follow-up and were not trying to conceive at endline were not asked about safer conception medical advice from a provider. Additionally, for some indicators of safer conception method uptake (eg, ART adherence, viral load suppression) women may not intentionally be using these as strategies for safer conception. Nevertheless, these data indicate the extent to which HIV transmission risk was minimized among those who had conceived or were currently trying to conceive. It is important to note that this study is based on data from a sample of WLHW recruited from ART clinics and is not generalizable to WLWH not in care or on ART, who may be even less aware of safer conception methods. Our sample also did not include men, whose knowledge and use of safer conception methods is important, particularly within the context of serodiscordant partnerships, nor did we document horizontal transmission between partners attempting to conceive.
Despite these limitations, our findings underscore the importance of concerted efforts to improve implementation of safer conception services and incorporate such services as a standard of care for PLWH. Beyond provider training and identification of appropriate task sharing between higher- and lower-level providers, systems-level innovation is needed to help deliver messages about and monitor use of safer conception strategies. Future research should move toward assessment of implementation models, such as integration of counseling services into existing HIV care or linkage and referral systems that first and foremost educate patients about viral suppression, timed condomless intercourse, and self-insemination as safer conception options.24 Simply presuming that patients on treatment will be virally suppressed is likely insufficient; rather providers need to take an active role in helping patients select and adhere to the most appropriate set of strategies given their treatment history and partnership context. One implementation project in South Africa has demonstrated the feasibility of offering safer conception services within the context of primary care for PLWH,33 and this model can perhaps be brought to scale once outcomes have been reported. However, this model has also highlighted that even amongst those on treatment, lack of viral suppression is a barrier to safer conception.33 In addition to clinic-based approaches, community-level education about safer conception will likely help create appropriate demand for and uptake of services.
More broadly, infrastructure and protocols used for counseling and services to prevent perinatal transmission, a primary focus of safer conception counseling in the South African context,26,33 should also be leveraged to include messages about reducing sexual HIV transmission risk. Likewise, current HIV treatment and prevention strategies, particularly the WHO prevention of mother-to-child transmission Option B+ and PrEP, offer opportunities for safer pregnancy among those who have already conceived and/or safer conception among serodiscordant couples.16,39 HIV care and prevention of mother–child-transmission cascades40,41 may also offer frameworks for assessing and monitoring safer conception implementation, which will involve successively identifying PLWH who desire children, providing appropriate counseling and services, and ensuring adherence to recommended practices to ultimately optimize conception and pregnancy outcomes. Regardless of the combination of strategies used, it is incumbent on public health professionals to ensure that women and men receive and use safer conception strategies that will minimize HIV transmission risk and help them more safely fulfill their fertility intentions.
The authors thank Taha E. Taha with the Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health and Francois Venter with Wits Reproductive Health and HIV Institute (WRHI), University of the Witswatersrand for their contributions to this study. The authors are grateful to all of the participants for sharing their time and experiences and the study staff for their efforts and dedication to the participants.
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