A conceptual framework for understanding HIV risk behavior in the context of supporting fertility goals among HIV-serodiscordant couples

Many people living with HIV choose to have children^1–8 and require safer conception services to support their goals while minimizing the risk of HIV transmission to partner and child. Although the right to reproductive choice for people with HIV is protected under South African law, most South African (and global) HIV prevention and treatment programs focus on abstinence, condoms and pregnancy prevention as strategies to minimize HIV transmission.⁹ These approaches present HIV-serodiscordant couples who wish to conceive with the dilemma of putting the HIV-uninfected partner at risk of acquiring HIV or else setting aside desires for a child.^{3,4,6,10–13} For serodiscordant couples who desire and achieve pregnancy, the risk of HIV acquisition and transmission may increase during pregnancy.^14–16 In addition, an acutely infected woman is more likely to transmit HIV to the child.¹⁷ Failure to communicate about and facilitate access to available risk reduction strategies for people living with HIV and their partners may contribute to new HIV infections among HIV-discordant couples and their children.^18–20

Increasingly, calls have been made for the integration of reproductive health services for people living with HIV.^21,22 Recent guidelines presented by the Southern African HIV Clinicians Society recommend that services should support people with HIV who choose to conceive.²³ An expanding range of behavioral and pharmacological strategies may reduce HIV transmission risk for serodiscordant couples who wish to have a child.^23–25 Behavioral strategies (home artificial insemination for couples where the woman is HIV-infected, unprotected sex limited to peak fertility),^23,26 male circumcision for couples where the male partner is HIV-uninfected,^27–29 antiretroviral therapy³⁰ and pre-exposure antiretroviral prophylaxis^26,31–35 present options for HIV-discordant couples to minimize periconception HIV transmission risk and realize fertility goals.³⁶ Periconception refers to the time period around attempted or actual conception. However, many clinicians do not, in the course of routine HIV-related clini cal consultations, ask their clients about childbearing desires.^8,9,18 Additionally, most HIV-affected couples neither share their plans for pregnancy with health care providers nor seek advice on how to have a safer pregnancy.^5,18,37–41 HIV specialists, including program managers and health care professionals, need to acknowledge and sup port the fertility desires of serodiscordant couples. As men and women with HIV live longer, healthier lives, the significance of safer conception coun seling for HIV-serodiscordant couples as a reproductive right is becoming more widely appreciated.^42–44 For both rights-based and public health-based reasons, safer conception counseling should be included as a public health strategy to reduce HIV incidence among men, women and their children in settings with gener alized HIV epidemics.^45–47

Developing a conceptual framework for understanding periconception HIV risk among serodiscordant couples

Prior to rolling out safer conception intervention strategies, it is important to understand the context of reproductive decision-making, perceptions of HIV risk associated with conception (periconception risk), and periconception risk behavior among HIV-discordant couples. Informed by a recent qualitative study we conducted (summa rized below and presented in full elsewhere),⁴⁶ together with related literature as supporting evidence, we propose a conceptual framework highlighting key issues to consider in the provision of safer conception services to HIV-discordant couples. Our framework draws attention to some of the socially embedded and relationship-related complexities that may underpin safer conception intervention strategies and that, we argue, may fundamentally mediate the anticipated intervention trajectory in terms of safer conception outcomes.

Our recent qualitative study among men and women with HIV in Durban, South Africa explored the dynamics of reproductive decision-making, knowledge of horizontal transmission risk, and knowledge and use of safer conception strategies, as well as exposure to HIV risk while trying to become pregnant. The findings were based on semi-structured interviews with 30 women with HIV and 20 men with HIV. All study participants had HIV-negative sexual partners or partners of unknown status.⁴⁶ All female study participants had experienced a pregnancy in the previous 12 months. Study participants voiced clear reasons for desiring children. They were rarely aware of safer conception strategies to reduce the risk of HIV transmission while trying to conceive, and engaged in unprotected sex in order to become pregnant. In addition, pregnancy planning occurred along a spectrum ranging from planned and wanted to unplanned and unwanted, with pregnancies very rarely being explicitly planned but often desired. Many female participants who reported an unintended pregnancy revealed strong male partner desire for that same pregnancy. Misconceptions about serodiscordance and fatalism regarding eventual seroconcordance (believing that both partners would eventually become HIV-positive) appeared to contribute to riskier behavior. While most study participants had not sought out clinical advice for safer conception, they expressed openness to receiving this. In summary, the study findings suggest that safer conception interventions are feasible; that such interventions should target both men and women; and that they should include serodiscordance counseling and promotion of contraception.⁴⁶

Based on this study and a synthesis of the HIV-related literature on fertility desires, contraception and pregnancy, we developed a conceptual framework to describe the dynamics involved in conception-related HIV risk behaviors in a South African setting. While the conceptual framework was informed by research carried out in South Africa, the theoretical concepts and constructs supporting the framework apply to many settings where sexual transmission of HIV must be considered for safer conception. The framework identifies factors that influence periconception HIV risk behavior among serodiscordant couples in order to guide future design and implementation of integrated HIV, reproductive health and family planning services.

Overview

Our model (Figure 1) explores conception-related HIV risk behavior by building on recently proposed frameworks that integrate theory across individual, couples-based and structural levels.^48,49 We draw on the Information-Motivation-Behavioral Skill (IMB) Model of HIV Preventative Behavior as one component of the framework.⁵⁰ After considering how the complexities of our primary study data could be represented by different theories and models of behavioral change (e.g. social cognitive theory, stages of change), the research team chose the IMB model as a base on which to develop a more comprehensive framework. The IMB model is useful, from an individual-level perspective, in guiding our understanding of HIV prevention behavior change. It incorporates terms that are familiar and easily interpretable, and has been widely utilized as a theoretical model for HIV prevention and reproductive health promotion.^51,52 The IMB model, however, does not take into account all types of individual-level factors, nor does it acknowledge the role of structural and relationship factors. Our framework seeks to highlight multiple types of structural, individual and couples-based determinants of conception-related decision-making and risk behavior.^40,41,45,46

The conceptual framework consists of: (1) the overarching structural context, (2) individual-level male and female determinants, and (3) couple-level determinants out of which the relationship context arises, all of which impact (4) HIV and pregnancy risk reduction behaviors and ultimately (5) desired outcomes of safer conception interventions.

• The structural domain

The structural domain, which frames and influences all aspects of the conceptual framework, consists of the overarching sociopolitical, economic and cultural context within which individuals are located. Economic and social constraints (e.g. poverty), and cultural and behavioral norms (e.g. hegemonic masculinities) form part of this context and influence HIV risk behavior (e.g. heightened risk through intimate partner violence).^53–58 Gender ideologies including the enactment and perpetuation of norms surrounding manhood and womanhood are also located within the structural domain. Unequal employment opportunity in the context of pervasive poverty, as in South Africa, may enhance unequal power relations between men and women. Men may be afforded greater decision-making power, leaving women with little autonomy within relationships. Similarly, patriarchal-based societies, also part of the South African context, reinforce and regulate cultural expectations regarding how a “proper” woman should behave;⁵⁹ this encompasses the regulation of family planning and childrearing.^60,61 Structural factors are important in that they provide a strong incentive or disincentive for people to act in a given way.⁶²

Health systems, laws and policies are also key components of the structural context. For example, health systems may impact conception-related HIV transmission risk to couples through information or support given; provider attitudes towards clients expressing the desire to have a child; and availability of risk reduction services (e.g. instruction about limiting sex without condoms to peak fertility). Similarly, laws and policies may prevent individuals from accessing particular clinical services (e.g. early antiretroviral treatment for the infected partner). By incorporating the structural domain, our framework highlights that any safer conception intervention for serodiscordant couples must account for key structural factors in the setting in which it is to be implemented.

• Individual determinants

The next domain of the proposed framework includes individual-level determinants, taking into account both partners. Individual factors such as overall health, HIV status and desire or intention to have a child affect reproductive and HIV risk behavior. For example, a person with HIV whose health improves as a result of taking antiretro virals may want to have a child. Our proposed model identifies “fertility desire” and “pregnancy intention” as two distinct determinants: as defined here, fertility desire is the wish for a child in the undefined future, and pregnancy intention is the conscious intention to become pregnant, or impregnate a partner, in the near future. Information and motivation about HIV and conception also comprise an important subset of individual factors.⁶³ For example, a man must know his HIV status (information), be sufficiently compelled to disclose to a partner (motivation) and be able to effectively communicate with his partner (behavioral skill) in order to engage in safer conception strategies with that partner. Similarly, for those who do not desire pregnancy, information about appropriate contraceptive strategies, motivation and the skills to consistently use them are all required to prevent unwanted pregnancies.

Individual-level information about HIV risk and conception is important. Many HIV-discordant couples do not understand the concept of sero discordance.^46,64 Many individuals in our study assumed that their sexual partner(s) would necessarily share the same HIV status. Alternately, some HIV-positive individuals reported that when their partners tested HIV-negative, this was evidence of partners being innately protected against the virus.⁴⁶ Both misconceptions may lead to riskier behaviors. Information that effectively explains serodiscordance may improve understanding of HIV transmission risk and motivate couples to protect themselves and/or others from potential risk.

Motivation and behavioral skills (the skill-set and perceived ability to effect a particular strategy) are critical components of managing HIV risk.^65,66 One example of motivation that influences a person’s actions is perceived HIV risk to self, partner or fetus; another example of motivation is desire for a child. The relationship between pregnancy intention (motivation) and actual contraceptive use (behavior skill) is complex.⁶¹ For example, women who report not intending to become pregnant may do little or nothing to prevent pregnancy.^67,68 Our study found that while very few pregnancies in the study population were planned, some unintended pregnancies were still desired.⁴⁶ While this may relate to limited awareness of or ability to access contraception, it may also be due to the complex nature of pregnancy intention where pregnancies are desired, but not explicitly planned.⁶⁹ Recognizing the different permutations of desire for a child and pregnancy intention (e.g. allowing for the reality that a woman may not plan to become pregnant in the immediate future but may also have a strong underlying desire to have a child with her partner) is essential for preventing HIV transmission and unintended pregnancy, as well as supporting healthy pregnancies.

An individual also requires specific skills, includ ing self-efficacy, to carry out safer conception strategies.^70,71 HIV disclosure to a partner is generally considered a key step for HIV prevention, but it requires effective communication skills.^72–74 In addition, while antiretrovirals can reduce the risk of transmission to an HIV-uninfected partner, it is critical that the partner living with HIV adheres to the medications.^30,75,76 For both those who desire children and those who do not, fertility desires, perceptions of fertility and prior experience with contraception will influence motivations and therefore behavior.

• Couples-based context and key mediating factors

The framework draws particular attention to couple-level determinants. Couples-based dynamics occur at the intersection between the male and female spheres of the conceptual framework, out of which the relationship context arises. Conception and associated HIV transmission behaviors necessarily occur in a male-female pair. Some individ uals do not wish to have a child or additional children. However, this individual-level decision may be challenged by a partner who desires a child and who influences reproductive decision-making. The key role of men in periconception decisions was highlighted in our study by the finding that an unintended pregnancy by the woman was often desired by the man.⁴⁶ Other studies confirm the importance of men in reproductive desires and periconception behavior.^{3,4,9,13,67,77,78} Including men in discussions regarding contraception and safer sex practices at the health care facility and community level is vital for successful implementation of safer conception strategies specifically, as well as reproductive and sexual health more broadly

‘Know Your Status’ Ministry of Health van, Lesotho, 2009

Key mediating factors arising from the couples-based interaction occur within the realm of the relationship context, as indicated by the triangle in the conceptual framework. While the relationship context can include many elements, we highlight gender power dynamics and communication skills, which will likely have a powerful impact on conception and HIV transmission risk behaviors, regardless of individual-level capacities. For example, Mittal and colleagues found that relationship factors such as intimate partner violence directly affected sexual risk behavior independently of individual motivation and behavioral skills.⁶⁶ In the case of HIV and gender-based violence, female-controlled contraception to prevent unwanted pregnancy and pre-and post-exposure antiretroviral prophylaxis to reduce the woman’s risk of HIV infection are priorities for HIV prevention and for reproductive, maternal and child health.

Communication skills may also determine how individual-level factors are mediated in the context of the relationship. Effective communication between couples is critical for interventions that affect sexual behavior to work (e.g. condom use, limiting unprotected sex to peak fertility in order to conceive).^49,79 Crepaz and Marks found that among serodiscordant couples, those who disclosed and discussed the need for safer sex were more likely to practice safer sex than those who only disclosed.⁷² In our study population, there was very little reported communication between couples about sex.⁴⁶ Couples counseling to improve communication and to educate men and women on detrimental gendered norms and behaviors is central to the success of any periconception risk reduction intervention.

Other social factors, external to feelings regarding the partnership, may affect the interplay between the individual and couple levels. For example, a woman may choose to maintain a current relationship despite the risk it poses to her if she perceives herself as entirely dependent on her partner. In her efforts to preserve this relationship, the woman may behave in ways that do not reflect her individual-level desires or intentions: she may consciously accede to her partner’s desire for a child in the interest of continuing the relationship even if she has no particular desire for a child herself.

• Risk reduction behavior

Safer conception interventions include HIV prevention and pregnancy prevention as represented within the second series of circles in the conceptual framework.

HIV prevention, independent of pregnancy plans, includes condom use, medical male circumcision, antiretroviral therapy for the HIV-infected partner and pre-exposure prophylaxis for the HIV-uninfected partner. While some individuals and couples may rely on condoms for prevention of both HIV and pregnancy, it is essential that they use an additional effective contraceptive method if they wish to further reduce the risk of unintended pregnancy.^80–85 There are several safe, reversible contraception options for women living with HIV, including intrauterine devices and barrier methods.²³ Tubal ligation and vasectomy offer permanent contraception should this be desired. Combined oral contraceptives and injectable progestins are effective as pregnancy prevention although recent data suggest there may be an increased risk of HIV transmission with progesterone-only injectable hormonal contraceptives.⁸⁶ Given these findings and the fact that no contraceptive method is completely effective, couples should receive counseling on the need for concurrent use of condoms as an important HIV prevention and contraceptive strategy. In the event of an unintended and unwanted pregnancy, appropriate and context-specific support and inter ventions (including safe and legal pregnancy termination) should be available and accessible.

Safer conception and safer contraception should include as many HIV prevention strategies as possible. Safer conception strategies include manual insem ination if the male partner is HIV-negative,²³ sperm washing if the male partner is HIV-positive^87–89 and limiting unprotected sex to peak fertility to reduce HIV exposure (timed conception).²³ In addition, viral load suppression through antiretroviral therapy reduces horizontal and vertical HIV transmission risk,^30,90–92 while local or systemic pre-exposure prophylaxis for the HIV-negative partner can confer additional protection.^31–35 Prerequisites to accessing these strategies are HIV testing, linkage to care and, in most cases, HIV disclosure.

• Desired outcomes

The final domain of the conceptual framework highlights the desired outcomes of the safer conception intervention, that is, reduced risk of HIV transmission, conception for those who desire it and successful contraception for those who do not desire a pregnancy. All preceding domains influence and impact behaviors that will ultimately determine these outcomes.

Using the conceptual framework to identify points of intervention

Integrated sexual and reproductive health programs for HIV-affected couples can address periconception risk through combination prevention approaches, including pharmacologic and behav ioral strategies. The conceptual framework introduced here identifies structural-, individual-and couple-level factors to consider in the development of periconception risk reduction interventions. Since structural-level factors can fundamentally impact the feasibility of risk-reduction strategies, they must be carefully considered when designing safer conception interventions. Although change in the structural domain may be difficult for health practitioners to effect, some of the other factors identified here may be addressed directly in periconception risk reduction interventions. We draw particular attention to the couple level, where effective communication skills and awareness of gendered norms within relationships may influence many individual-level determinants, for example, sexual coercion. Periconception risk reduction interventions need to account for mediating factors occurring within the relationship context since these factors may ultimately influence vulnerability to HIV despite individual-level capacity.

There is some indication that men and women may be more willing to engage in HIV risk reduction in the context of protecting a future child.^46,93 The wellbeing of future or actual children offers a potential strategy to open risk-reduction communication between couples.⁹³ While the willingness to communicate about safer sex in these instances may, in reality, only be temporary, it is a key entry point for HIV risk reduction strategies, particularly in the context of unequal power relationships.

Interventions that include antiretrovirals will necessarily involve health care workers. By better understanding the complex processes underlying periconception risk behavior, as proposed by the conceptual framework, health care workers may optimize their supportive role by helping to limit their clients’ exposure to HIV risk through the provision of information and through couples-based counseling that addresses disclosure, serodiscordance and risk reduction strategies. They may also affect individuals’ actions by encouraging adherence to risk reduction strategies.

Health care workers may experience ethical conflicts in providing safer conception services, especially in settings with high rates of poverty and intimate partner violence.^53,84 For instance, a male partner may seek safer conception services for himself and his partner, but on individual consultation the female partner may indicate that she does not desire a child, and insists that this cannot be communicated to her partner. Health care providers may also face situations where a person living with HIV wishes to access safer conception services but has not yet disclosed his/her HIV status to the partner. Drawing attention to ethical sensitivities that may arise in providing safer conception interventions should be a part of reproductive counseling training for health care providers.

Conclusion

While there is increasing consensus regarding the need for safer conception services for HIV-affected couples, service provision is conceptually, ethically and technically complex. The reality is that HIV-affected couples are likely to fulfill their fertility desires even when aware of the risks involved and in the absence of periconception support services. Providing these services offers opportunities not only to reduce HIV transmission to partners and children, and to support pregnancy intentions, but also to begin to address long-term relationship dynamics which contribute to gendered vulnerabilities and high-risk HIV transmission behaviors.

The conceptual framework presented in this article is intended for testing, refinement and further development. In its current form, it offers insight into some complexities that researchers, policy makers and health care workers should consider when developing and delivering interventions for serodiscordant couples who wish to conceive. While the conceptual framework was informed by research carried out in South Africa, as noted earlier, the theoretical concepts and constructs supporting the framework may apply to many settings. Given the success of couples-based interventions,^94–96 it is suggested that at a minimum couples-based counseling be incorporated rou tinely into safer conception services.

Acknowledgements

Dr. Matthews received funding support from the American Society of Tropical Medicine and Hygiene/Burroughs Wellcome Fund Postdoctoral Fellowship in Tropical Infectious Diseases, the Mark and Lisa Schwartz Family Foundation and a K23 award (NIMH MH095655).

Dr. Bangsberg was supported by the Mark and Lisa Schwartz Family Foundation and by a K24 award (NIMH MH087227).