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Reproductive Decision-Making and Periconception Practices Among HIV-Positive Men and Women Attending HIV Services in Durban, South Africa

Understanding reproductive decisions and periconception behavior among HIV-discordant couples is important for designing risk reduction interventions for couples who choose to conceive. In-depth interviews were conducted to explore reproductive decision-making and periconception practices among HIV-positive women with recent pregnancy (n = 30), and HIV-positive men (n = 20), all reporting partners of negative or unknown HIV-status, and attending HIV services in Durban, South Africa. Transcripts were coded for categories and emergent themes. Participants expressed strong reasons for having children, but rarely knew how to reduce periconception HIV transmission. Pregnancy planning occurred on a spectrum ranging from explicitly intended to explicitly unintended, with many falling in between the two extremes. Male fertility desire and misunderstanding serodiscordance contributed to HIV risk behavior. Participants expressed openness to healthcare worker advice for safer conception and modified risk behavior post-conception, suggesting the feasibility of safer conception interventions which may target both men and women and include serodiscordance counseling and promotion of contraception.


Introduction
In sub-Saharan Africa, the majority of new HIV infections occur in women of reproductive age [1]. HIV transmission in stable serodiscordant sexual partnerships exceeds 10% per year and may account for greater than 60% of new HIV infections in Africa [2,3]. The contribution of intended conception to incident HIV infection has not been measured; however, studies in the United States [4], Europe [5][6][7], and sub-Saharan Africa [8][9][10][11][12][13][14][15][16][17] report that 20-50% of HIVpositive individuals desire children. Individuals who engage in unprotected sex to conceive with a positive partner face a high risk of infection. If pregnancy does occur, ongoing unprotected sex during pregnancy is associated with increased risk of HIV transmission, with HIV incidence as high as 10% [18][19][20]. Nonetheless, fertility intentions and outcomes among serodiscordant couples remain high: among HIV-discordant couples in Uganda, 59% expressed a desire to have children [12], while in Nairobi annual pregnancy incidence among discordant couples was 9.7%, mostly occurring among women reporting fertility desire [21]. HIV-discordant couples are often advised not to have children, but complex cultural, economic, and social factors motivate many couples to reproduce [22][23][24][25][26][27][28][29][30][31][32][33]. Reproductive intentions may increase with improvement in access to antiretroviral therapy (ART) and the health and survival of people living with HIV [11,34,35].
HIV-discordant couples who desire children require strategies to protect HIV-negative partners and future children from HIV infection. Reproductive technologies including sperm washing are not widely accessible [36,37], whereas behavioral strategies (e.g., home manual insemination and unprotected sex limited to peak fertility) and medical strategies (e.g., male circumcision and treatment for sexually transmitted infections) are potential elements of periconception HIV risk reduction for serodiscordant couples in resource-limited settings [38][39][40][41][42][43][44][45]. Suppressive ART for the positive partner or topical or systemic pre-exposure prophylaxis (PrEP) for the negative partner may provide additional prevention options [46][47][48][49][50]. Prior to developing pharmaco-behavioral interventions, it is important to understand how serodiscordant couples approach reproductive decisions and consider periconception transmission risk.
Our objectives were to explore reproductive decisionmaking, understanding of horizontal transmission risk, and knowledge or deployment of periconception risk-modification practices among HIV-positive men and women with serodiscordant sexual partners in a high HIV-prevalence setting.

Study Setting, Patient Selection, Inclusion, and Exclusion Criteria
McCord Hospital is a state-aided (public/private partnership) general hospital serving a predominantly-urban population from the greater Durban area where provincial antenatal clinic HIV-prevalence is estimated at 39.5% [51]. The McCord HIV Clinic has provided care and treatment to approximately 7,000 patients on ART. Sixty percent of these patients are women; the majority ([90%) are Zulu. Patients pay approximately *25 USD per month for HIV services. Preventing Mother to Child Transmission (PMTCT) clinic services are free to those who access antenatal services (*35 USD per visit); in 2010, 200 pregnant women enrolled.
Male participants were recruited from the general HIV clinic and female participants were recruited from the HIV and PMTCT clinics. Inclusion criteria were (1) age 18-45 years; (2) HIV-positive; (3) pregnancy in the prior 12 months (for women); (4) partner of unknown or seronegative HIV-status (prior to referent pregnancy) by participant report; (5) fluent in English or isiZulu; and (6) able to give informed consent.

Procedures
The research focus was to explore periconception risk understanding and practices. We aimed to describe as many new and different understandings and practices as possible.
This requires an open-ended methodology based on an inductive approach to data collection and analysis [52]. We therefore conducted qualitative research with in-depth interviews to explore reproductive decision-making, horizontal transmission risk understanding and practices, and periconception risk understanding and practices. Participants were recruited through purposive sampling from patients awaiting clinical consultation. After obtaining informed consent, a gender-concordant research assistant interviewed participants in a private setting in isiZulu or English. Interviews were recorded, translated, and transcribed.
Transcripts were independently reviewed and coded, and resultant conceptual categories and emergent themes were discussed by the research team [52,53]. The authors reviewed coding categories and emergent themes with the research assistants in order to explore additional themes and confirm accuracy of interpretation.
Ethics approvals were obtained from the McCord Hospital Research Ethics Committee (Durban, South Africa) and from the Partners Healthcare Institutional Review Board (Boston, USA).

Demographics
Baseline demographic data, HIV history, reported partner HIV-status, and reproductive history for 30 female and 20 male participants are shown in Table 1. Women and men averaged 30 (SD 4) and 34 (SD 6) years of age, respectively, and had been diagnosed with HIV for a mean of 3 years (SD 2 women, SD 5 men). Seventy-three percent of women and 60% of men had completed secondary school while 63% of women and 75% of men reported current employment. All women had a pregnancy in the past year and 73% were diagnosed with HIV prior to the referent pregnancy. Women had an average of 2.1 (SD 1.1) pregnancies (including current), 1.1 (SD 0.7) prior live births, 0.9 (SD 0.6) living children, and 18 (60%) were pregnant. Men had an average of 0.9 (SD 1.0) living children; three (16%) reported partner pregnancy in the past year.

Overview
The data are presented as periconception attitudes and practices of serodiscordant couples with the goal of informing interventions to reduce periconception HIV transmission. We first describe (1) reproductive decisionmaking. A priori, or pre-defined, categories included reasons for and deterrents to having children. Emergent themes included the role of men in pregnancy decisions and the spectrum of pregnancy planning. We then describe (2) horizontal transmission risk understanding and practices, and (3) periconception risk understanding and practices. A priori categories included knowledge and practice of safer sex strategies to prevent horizontal transmission in general and in the context of conception. An emergent theme was post-conception HIV risk reduction to protect the unborn child.

A. Reasons for Having Children
Most male participants in this sample expressed a desire for children in the future; those who did not desire children in the future reported at least one living child. They described a variety of motivations for having children including personal preference, family pressure, to continue the family name, to express manhood, to express commitment to a partner, or to increase social capital. Women described the importance of having children in order to meet marital or other responsibilities to a partner or his family, to avoid abandonment by a spouse, to fulfill responsibilities to her own family, for emotional gratification, and as an important manifestation of womanhood. For some, HIV infection and perceived imminent mortality conferred increased urgency on reproductive goals. I think [it is important for a man to have children] because children are a gift from God. They leave a legacy of the family and they extend and expand your surname so that it won't die when you die, your legacy won't perish. [Man #13, 28 years old, partner HIV-negative] It is important [to have children] nowadays because if you are an only child to your parents and their hope is in you, if you get sick-because most of the time we young people die-then my child will grow up and help my mother when she is sick. So I see it as important. When you do not have children and you are married you find that your husband says that you must give him children because he paid a lot of money so you need to also produce in order to pay. If you tell him that you do not want any children he will go look for someone else who will have kids for him. [Woman #27, 34 years old, partner HIV-status unknown]

B. Deterrents to Having Children
Men and women who did not want children cited financial reasons or already having enough children, often despite social and cultural pressures to have more children. Participants voiced concerns over orphaning a child, vertical transmission, or infecting a negative partner.

D. Pregnancy Planning
We asked participants whether their recent pregnancy had been planned, whether it was desired by themselves and/or the partner, and how they and their partner felt about the referent pregnancy. Responses revealed that pregnancy intention occurs on a spectrum with a minority of pregnancies explicitly intended. The following quote is an example of a woman who explicitly planned and wanted her pregnancy: Two participants had heard of traditional healers offering safer conception strategies but neither participant had firsthand knowledge. A number of participants sought information from healthcare providers and the internet in order to learn about and, in some cases, carry-out safer conception strategies. This included delaying conception until the positive partner's viral load was suppressed and home manual insemination (for male-uninfected couples: the man ejaculates into a condom or other receptacle, then semen is inserted into the vaginal canal via a syringe or reversed condom). Some participants mentioned microbicides and oral prophylaxis as potential strategies.

Discussion
Our findings expand on prior work demonstrating that people living with HIV in sub-Saharan Africa have deeplyingrained personal and culturally-embedded reasons for having children [16,27,29,54,55]. These beliefs remain intact when HIV-positive individuals have partners of negative or unknown HIV-status [12]. Practical deterrents to having children include financial constraints and having met procreation goals. HIV-specific fears of vertical transmission, orphaning a child, horizontal transmission, and peripartum health are also factors; each of these may be mitigated with improved access to ART and PMTCT programs [34,56]. These findings add to a robust global literature arguing for improved counseling and care services for HIV-positive individuals who choose to have children [17,21,34,[57][58][59][60]. Independent of fertility goals, many study participants were confused by the nature of serodiscordance, leading to riskier behavior, as described by Bunnell and colleagues in Uganda [61]. These findings suggest that routine couples-based counseling about serodiscordance may be a critical first-step to safer sex and/or safer periconception behavior [62]. In addition, while the majority of participants had disclosed their HIV-status to the primary partner, many had not. Strategies for navigating the complexities of disclosure will be a necessary component of any safer conception intervention [62][63][64].
Among participants who planned pregnancies with a serodiscordant partner, some individuals or partners had sought advice from healthcare providers or the internet, but the majority of participants did not know how to minimize sexual transmission risk while allowing for conception. Some described knowingly risking horizontal HIV transmission in order to conceive. These data support a harmreduction approach to reproductive counseling: in the absence of counseling that acknowledges reproductive goals, HIV-discordant couples who choose to have children take unnecessary risks to conceive [45].
While prior work has suggested patient reluctance to engage with healthcare workers in reproductive counseling [15,16,60,[65][66][67][68], many study participants had received advice about childbearing from healthcare workers or suggested that clinicians might serve as helpful resources. This may have been specific to our study site, or may indicate evolving attitudes among healthcare workers towards the reproductive goals of people living with HIV. If these findings are replicated on a larger scale, a periconception counseling intervention may be successfully delivered in healthcare settings. Because a combined prevention program will likely include suppressive ART for the positive partner [48] or periconception oral or topical PrEP [46,47,49,50,69], it may be important to base such interventions in a healthcare setting. In addition, because HIV-positive men and women may suffer from infertility [70][71][72][73][74], clinical consultation to assess fertility prior to recommending conception strategies will be necessary.
The finding that couples modify behavior to protect the baby after conception may reflect PMTCT counseling messages at this study site. Regardless, uptake of behavioral change was high, suggesting that promoting safer conception interventions as a strategy to protect the child may be successful. Viral load suppression with ART is an important strategy to reduce sexual transmission for serodiscordant couples [48,75,76]. A minority (9/22 or 40%) of women who became pregnant after HIV diagnosis were on ART at the time of conception and only one participant mentioned ART as a strategy to minimize periconception transmission. Encouraging couples to delay conception until the positive partner meets criteria for ART and achieves a suppressed viral load could reduce transmission by 96% [48].
The data support a broad approach to family planning messages. A minority of pregnancies were explicitly planned, some were explicitly unintended and unwanted, and the remainder occurred on a spectrum between these two extremes. Women who do not plan pregnancy but want to become pregnant may be difficult to identify with standard questions that ask if they plan to become pregnant. More nuanced questions that address fertility desire should be incorporated [77]. Men play a dominant role in pregnancy decisions, as supported by prior work in South Africa, Kenya, Malawi, Uganda, and Nigeria [12, 14-16, 27, 54, 78]. These data suggest that a reproductive counseling intervention must target men as well as women, and must include promotion of contraception other than male condoms (e.g., IUD, hormonal contraception) to avoid unwanted pregnancy. Interventions to engage men in contraception and family planning have been effective in several sub-Saharan African settings [78][79][80].

Limitations
These qualitative data from a small, purposive sample are not generalizable. In addition, many participants had relatively high education and were employed and may not be representative of patients who attend free government clinics. By design, we interviewed the HIV-positive member of serodiscordant couples, yet uninfected partners would be the target population for a prevention intervention and should be the focus of future research. Socially desirable responses may have affected some of the findings (e.g., reporting of safer sex practices by women enrolled in a PMTCT program).

Conclusions
These data emphasize the importance of childbearing to HIV-discordant couples and describe a paucity of known strategies for reducing periconception transmission, but reveal openness to safer conception advice and uptake of behavior change to protect the unborn child. The findings support expanding existing interventions to promote safer sex and to prevent unwanted or unintended pregnancy, including couples-based counseling about serodiscordance and promotion of contraception other than male condoms. The crucial male role in pregnancy decisions suggests the importance of targeting men in safer conception interventions. Individuals in our sample were amenable to healthcare worker advice, suggesting that future combination prevention strategies could be successfully implemented in a healthcare setting. from the Mark and Lisa Schwartz Family Foundation. Dr. Bangsberg was supported by the Mark and Lisa Schwartz Family Foundation and by a K24 award (NIMH MH087227).
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