2 Infectious Diseases in Obstetrics and Gynecology to reproductive choice for HIV-infected persons , and the most recent guidelines from the Southern African HIV

1 Division of Infectious Disease and Center for Global Health, Massachusetts General Hospital, Boston, MA 02114, USA 2 Harvard Medical School, Boston, MA 02115, USA 3 Division of Infectious Disease, Beth Israel Deaconess Medical Center, Boston, MA 02115, USA 4 McCord Hospital, PMTCT Programme, Durban 4001, South Africa 5 Faculty of Arts and Sciences, Simon Fraser University, Vancouver, BC, Canada V6B 5K3 6 Department of Psychiatry, Massachusetts General Hospital, Boston, MA 02114, USA 7 Department of Global Health and Social Medicine, Harvard Medical School, Boston, MA 02115, USA 8 Maternal, Adolescent, Child Health Division, University of the Witwatersrand, Durban 4110, South Africa

Cross-sectional studies indicate that people living with HIV are receptive to safer conception advice from providers [33][34][35][36], but that healthcare workers (HCWs) are not routinely engaging in conversations about fertility desires or plans, a crucial first piece of any reproductive health intervention [31,34,35,37]. In Cape Town, over 30% of HIVinfected women and 65% of HIV-infected men attending public sector clinics were interested in having additional children, yet only 19% and 6%, respectively, had discussed this with a HCW [38]. Among HIV-infected women in Johannesburg, with plans to conceive in the next year, 40% had ever had a conversation about fertility plans with a provider [34]. Conversations with HCWs about conception plans were also infrequent in Argentina [37], Brazil [39], and the United States [35]. Barriers to these conversations include a combination of patient (e.g., fear of judgment, lack of pregnancy planning), provider (e.g., limited experience, knowledge, or skills), and structural factors (e.g., competing healthcare demands, limited resources, poor integration of family planning and HIV services) [31, 35-37, 40, 41]. While some conversations may be initiated with HIV lay counselors, they may not have the skills to address clinical issues beyond their focused training [42,43].
Data demonstrating that ARVs minimize HIV transmission suggest that periconception risk-reduction interventions will require HCW involvement [16,[19][20][21][22]27]. In our conceptual framework for periconception risk behavior, HCWs have the potential to minimize risk behavior through providing information about HIV risk, offering prevention strategies, and promoting adherence to risk reduction strategies [44]. There are no data on practices in KwaZulu-Natal, the most HIV-affected province in South Africa, where 41% of pregnant women attending antenatal clinics are HIV positive [45]. A better understanding of current HCW knowledge, attitudes, and practices will enhance the provision of reproductive counseling for HIVinfected individuals by allowing for development of interventions that capitalize on HCW strengths and address weaknesses.
We present qualitative data resulting from interviews with 30 HIV-infected women and 20 HIV-infected men with serodiscordant sexual partners in Durban, South Africa. We previously reported on periconception risk behavior within this sample [33] and here focus on participant reports of their experiences with HCW provision of reproductive counseling. These data offer early insight into current HCW practices and may contribute to development of feasible safer conception interventions.

Study Setting, Patient Selection, Inclusion and Exclusion
Criteria. Participants were recruited from the antiretroviral (ARV) and preventing maternal-to-child-transmission (PMTCT) clinics within a state-aided (public/private partnership) general hospital serving a predominantly urban population from the greater Durban area where district antenatal clinic HIV prevalence is estimated at 41.5% [45]. In 2011, the ARV clinic was providing care and treatment to 4734 patients on ART. Sixty percent of these patients are women; the majority (>90%) are black South Africans. Patients pay approximately 25 USD per month for comprehensive HIV services, which includes the cost of ARVs. Pregnant patients pay approximately 35 USD per visit to access antenatal care, which includes PMTCT clinic services. In 2010, 200 HIV-infected pregnant women enrolled in this program.
Male participants were recruited from the ARV clinic and female participants were recruited from the ARV and PMTCT clinics. Inclusion criteria were (1) age 18-45 years; (2) HIV-positive; (3) pregnancy in the prior 12 months, including currently pregnant (for women); (4) partner of unknown or seronegative HIV status (prior to referent pregnancy) by participant report (father of the referent pregnancy for women, current sexual partner for men); (5) fluent in English or isiZulu; (6) able to give informed consent. Initial attempts to recruit men with partner pregnancy in the past year were unsuccessful, men were subsequently recruited independent of recent partner pregnancy. It is not clear if initial recruitment challenges were due to sensitivities of reporting partner pregnancy (in a setting where condoms are promoted strongly) or a paucity of men with recent partner pregnancy.

Procedures.
We conducted in-depth, qualitative, individual interviews to explore reproductive decision-making, sexual transmission risk understanding and practices, and periconception risk understanding and practices [33]. Here, we focus on data from the questions "What have health care workers advised you about having children (after knowing your status)?" and "What advice have you received around getting pregnant/having children safely (since knowing your status)?" Participants were recruited from March through July 2010 via purposive sampling from patients awaiting clinical consultation. After obtaining informed consent, a genderconcordant research assistant trained in qualitative interviewing techniques interviewed participants in a private setting in isiZulu or English. Interviews lasted approximately 30-90 minutes and were recorded, translated, and transcribed. Participants did not receive compensation for participation.
Transcripts were independently reviewed and coded, and resultant conceptual categories and emergent themes were discussed by the research team using content analysis [46,47]. Several 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). Gynecology   3

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. 73% of women were diagnosed with HIV prior to the referent pregnancy. Women had an average of 2 (SD 1) pregnancies (including current), 1.1 (SD 0.7) prior live births, 0.9 (SD 0.6) living children, and 18 (60%) were pregnant at the time of interview. We have previously detailed the complexities of pregnancy intention in this sample, but about a third (11) of women described the referent pregnancy as explicitly planned [33]. Men had an average of 0.9 (SD 1) living children; three (16%) reported partner pregnancy in the past year.

Overview.
We have presented a conceptual framework for considering factors that impact periconception risk behavior [44]. Structural, individual, and dyadic domains affect access to risk reduction information (e.g., knowledge that ARVs can reduce sexual transmission risk), motivation (e.g., to adhere to prevention strategies), and ability to implement behavioral change (e.g., partnership dynamics and discussions of safer sex practices). Within this framework, HCWs have the potential to minimize risk behavior through providing HIV-affected couples with information about HIV transmission and conception, supporting disclosure, providing ARVs as prevention, and promoting adherence to HIV risk reduction strategies [44]. Here, we present data exploring participant experiences with reproductive counseling from HCWs. We present themes suggesting that, in this sample, HIV-infected men and women in serodiscordant partnerships (1) are aware of and receptive to the idea that one should speak to an HCW prior to becoming pregnant, (2) seldom seek or receive conception advice from healthcare workers, and (3) when advice is shared, patients receive a range of information around safer conception. In addition, (4) men are eager for safer conception advice.

Aware of and Open to Safer Conception and Pregnancy
Information from HCWs. Most participants indicated that they had been informed by a HCW that they should seek advice when they were ready to conceive. In some cases, participants communicated that this advice might help minimize transmission to a child, and in some cases to a partner. This awareness was related to general information shared by counselors during routine ARV adherence training sessions (group adherence training sessions prior to ART initiation are routine in South Africa), regardless of the participant's fertility goals at the time.

Seldom Seek Safer Conception Information Prior to
Conception. While most participants were aware that they should approach a healthcare worker prior to conception, few sought, or received safer conception advice. Participants described several barriers to accessing reproductive counseling prior to conception including fear of judgment from nurses and financial challenges.  Additional barriers may be related to dyadic factors. For example, participants described that they were told to seek reproductive counseling at the ARV clinic with their partners. However, about a third of participants had not disclosed his/her HIV status to their partner, making this scenario unlikely. Further, about a third of the women in this sample described the referent pregnancy as unplanned.

Range in Quality of Information Shared by Providers about Safer Conception in the Context of HIV Infection.
Participants reported a range of information received from providers. At one end of the spectrum, some participants had not received advice about options for having children since their HIV diagnosis, including in the setting of expressing plans for having children. Others had received helpful safer conception information from doctors or nurses at PMTCT, ARV, and gynecology clinics. Risk reduction strategies that participants had learned included artificial insemination, intercourse timed to peak fertility, manual insemination (for male-uninfected couples-the uninfected male ejaculates into a condom or other container and the semen is inserted into the woman's vaginal canal via a syringe or reversed condom), sperm washing, and intercourse with lubrication (to avoid abrasions). Several male participants became quite interested in safer conception options during the interview and planned to seek out additional advice from a HCW. One participant (B12, 35-year-old man) responded to a question about fertility desire by saying, "so in the situation that I am in now I do not think I want to have children again," but by the end of the interview he asks:

Is it possible to have children if I am positive and my partner is negative?
Another participant initially stated, "I have two kids at the moment. Even before I was diagnosed [with HIV], we were not planning to have more . . . Two is enough." However, by the end of the interview, he asks: Women were not particularly eager for advice. However, this may simply reflect the study sample given that fewer women were planning a future pregnancy and many were still close to or in the midst of a current pregnancy.

Discussion
These qualitative data suggest that HIV-infected patients are increasingly aware of reproductive counseling opportunities. Many participants understood that HCWs may have valuable advice to offer to facilitate safer conception and were open to seeking this advice. While few participants had sought advice, some participants had received safer conception advice from healthcare encounters.
Prior studies suggest that the majority of HIV-infected patients are not receiving reproductive counseling and are reluctant to engage with healthcare workers to discuss reproductive plans [12,35,36,39,[49][50][51]. Schwartz et al. [34, page 73] presented data collected during 2009 and reported that only 41% of HIV-infected women reported that an "ART healthcare provider had spoken with them about their options should they want to conceive in the future". In work by Cooper et al., collected in 2006, 19% of women and 6% of men had "consulted a doctor, nurse, or counselor in HIV care about fertility intentions" [38, page S44]. The fact that many participants, including men, in this small sample knew that HCWs may have advice to offer captures data not mentioned in prior studies. These data suggest that clinical settings may be adapting to accommodate the fertility goals of people living with HIV.
Many participants reported the expectation that they could access detailed counseling if they returned to the clinic when they were ready to have a child. From work by our group and others, several facts of periconception practice make this clinical approach precarious. Waiting to talk to a provider until one is ready to have a child eliminates the opportunity to discuss the risks of having children in order to inform the decision to have biologic children [24,52,53]. Many men and women living with HIV do not know their partner's status and/or have not disclosed to their partners. Prior to testing and disclosure, it is impossible for an individual or a couple to assess sexual transmission risk in the context of conception. Continued efforts to promote couple-based testing and supported disclosure are critical [54]. For those who decide to have children, a preconception conversation with a healthcare worker should include an assessment of the HIV-infected partner's health; the HIV status of the partner; if the woman is positive, a discussion of the risks of pregnancy when HIV infected; risks of transmission to a partner with various periconception risk reduction strategies; fertility assessment; the increased risk of transmission and acquisition during unprotected sex during pregnancy; the risks of perinatal transmission [44]. Furthermore, asking individuals or couples to return when they are ready to have children presupposes conception planning. However, many pregnancies are not explicitly planned [55,56]. Providing up-front information about the options for safer conception may communicate the importance of preconception planning-to protect the future child and the partner. Recent data from Johannesburg (South Africa) suggest high fertility intentions at ART initiation [34], reflecting the importance of providing safer conception information at treatment initiation and in followup. In addition, decisions about conception are often dyadic. A partner 6 Infectious Diseases in Obstetrics and Gynecology (who is not attending clinic) may make decisions about having children-if his or her partner has not been educated it is impossible for them to have an informed conversation about the risks and options for safer conception. In addition, life transitions may be quick and there may be plans for pregnancy long before a next visit with a provider [57].
Expecting a patient to raise the issue of fertility plans on his or her own may be problematic. While not a theme in our data, published data suggest that women and men living with HIV hesitate to reveal fertility plans to HCWs for fear of judgment [36,58]. It is not part of routine clinical practice to expect patients to tell providers when they are ready to discuss health behavior change (e.g., smoking, substance abuse, exercise, sexual behavior)-the onus is on the provider to actively inquire about behaviors that compromise health. Routine assessment of fertility goals and plans should be incorporated into clinical care for people living with HIV, with subsequent recommendations for safer conception or effective contraception options, depending on fertility goals. How to execute this in overburdened healthcare systems is a challenge but may require increased training in fertility intention assessment and comprehensive reproductive counseling for counselors.
Participants had learned of safer conception strategies from HCWs including artificial insemination, intercourse timed to peak fertility, sperm washing, home manual insemination, and intercourse with lubrication to avoid abrasions. The frequency with which sperm washing and artificial insemination was raised is interesting since these are some of the least accessible (geographically, economically) strategies for reducing transmission risk. Simpler risk reduction strategies such as delaying conception until the infected partner is on treatment with suppressed HIV RNA viral load, timing sex without condoms to peak fertility, circumcision for the male partner if he is uninfected, and manual insemination are likely to be more feasible. Our semistructured interview guide was not designed to probe specifically about particular techniques and it is possible that participants were more likely to recall discussions about and have faith in hightech concepts such as sperm washing compared to behavioral modifications such as timing unprotected sex to peak fertility. In addition, patients may have received limited information, perhaps due to insufficient clinician training on this topic. The WHO guidelines for serodiscordant couples offer some safer conception recommendations, in addition, a more comprehensive guideline was recently published by the Southern African HIV Clinicians Society and will be helpful for clinicians [32,54]. HCW training on the interpretation and application of these guidelines should be a priority for promoting comprehensive reproductive health counseling.
We found that, in this sample, male participants were eager to engage with HCWs in order to seek reproductive counseling. Prior data suggests that providers may have less insight into male reproductive intentions [31] and that men are less likely to seek advice from providers [38]. We previously published on the important role of men in conception decisions from an earlier analysis of these data [33], an observation which has been reported by others [9,11,12,36,[59][60][61]. As reproductive counseling is integrated into HIV care, it will be crucial to increase male involvement. Interventions to engage men in contraception and family planning have been effective in several sub-Saharan African settings [61][62][63]. In addition, the dyadic nature of conception decisions and periconception risk behavior emphasizes the importance of a couple-oriented counseling approach when feasible [44].
The main limitations of the data are inherent to qualitative research-findings from this small qualitative sample are meant to generate hypotheses to pursue in future larger scale research. In addition, our participants were attending clinical services at a semiprivate hospital and may not represent the broader population who access public sector care or those who do not access any healthcare. While this clinic does not have a formal program for safer conception counseling, several of the authors previously worked at this clinic which may have heightened some of the clinic providers' awareness around reproductive counseling for people living with HIV. Finally, patient perspectives of past experiences with provider counseling may not accurately reflect what occurred; provider perspectives are also needed to understand current practices.

Conclusion
These are the first data to explore patient experiences with provider provision of reproductive counseling in KwaZulu Natal, where 41% of women attending antenatal clinics are HIV infected [45]. This work suggests that men and women living with HIV are aware that safer conception options may be available and are interested in accessing this information. Further, there is a clear need to expand the quality and reach of periconception risk reduction information to both providers and patients. These data serve as important hypothesis generation to guide future research as reproductive counseling interventions are developed.