Secondary Logo

Journal Logo

Condomless Sex Among Virally Suppressed Women With HIV With Regular HIV-Serodiscordant Sexual Partners in the Era of Treatment as Prevention

Patterson, Sophie MBChB, PhD*,†; Carter, Allison MPH*,†; Nicholson, Valerie*; Webster, Kath*; Ding, Erin MSc; Kestler, Mary MD‡,§; Ogilvie, Gina MD, PhD‡,§; de Pokomandy, Alexandra MSc, MD‖,¶; Loutfy, Mona MD, MPH#,**; Kaida, Angela MSc, PhD*

JAIDS Journal of Acquired Immune Deficiency Syndromes: December 1, 2017 - Volume 76 - Issue 4 - p 372–381
doi: 10.1097/QAI.0000000000001528
Epidemiology
Free

Background: Sexual HIV transmission does not occur with sustained undetectable viral load (VL) on antiretroviral therapy (ART). Awareness of ART prevention benefits and its influence on condom use among women with HIV (WWH) remain unexplored. We estimated prevalence and correlates of condomless sex with regular HIV-serodiscordant partners among WWH with undetectable VL on ART.

Methods: We used baseline questionnaire data from the community-based longitudinal Canadian HIV Women's Sexual and Reproductive Health Cohort Study (CHIWOS). We included WWH self-reporting vaginal/anal sex with ≥1 HIV-negative/unknown status regular partner within 6 months, and undetectable VL (<50 copies/mL) on ART. We excluded participants exclusively reporting female partners or missing condom-use data. Condomless sex was defined as <100% condom use within 6 months. The primary explanatory variable was awareness of ART prevention benefits. Logistic regression identified factors independently associated with condomless sex.

Results: Of 271 participants (19% of the CHIWOS cohort), median age was 41 (interquartile range: 34–47), 51% were in a relationship, 55% reported condomless sex, and 75% were aware of ART prevention benefits. Among women aware, 63% reported condomless sex compared with 32% of women not aware (P < 0.001). Factors independently associated with condomless sex included being aware of ART prevention benefits (adjusted odds ratio: 4.08; 95% confidence interval: 2.04 to 8.16), white ethnicity, ≥high-school education, residing in British Columbia, and being in a relationship.

Conclusions: Virally suppressed women aware of ART prevention benefits had 4-fold greater odds of condomless sex. Advancing safer sex discussions beyond condoms is critical to support women in regular serodiscordant partnerships to realize options for safe and satisfying sexuality in the Treatment-as-Prevention era.

*Faculty of Health Sciences, Simon Fraser University, Burnaby, British Columbia, Canada;

Department of Epidemiology and Population Health, British Columbia Centre for Excellence in HIV/AIDS, St. Paul's Hospital, Vancouver, British Columbia, Canada;

Oak Tree Clinic, British Columbia Women's Hospital and Healthcare Centre, Vancouver, British Columbia, Canada;

§Department of Medicine, Division of Infectious Diseases, University of British Columbia, Vancouver, British Columbia, Canada;

Chronic Viral Illness Service, McGill University Health Centre, Montreal, Québec, Canada;

Department of Family Medicine, McGill University, Montreal, Québec, Canada;

#Women's College Research Institute, Women's College Hospital, Toronto, Ontario, Canada; and

**Department of Medicine, University of Toronto, Toronto, Ontario, Canada.

Correspondence to: Angela Kaida, MSc, PhD, Faculty of Health Sciences, Simon Fraser University, Blusson Hall Rm 10522, 8888 University Drive, Burnaby, BC V5A 1S6, Canada (e-mail: kangela@sfu.ca).

CHIWOS is funded by the Canadian Institutes of Health Research (CIHR), the CIHR Canadian HIV Trials Network (CTN 262), the Ontario HIV Treatment Network (OHTN), and the Academic Health Science Centres (AHSC) Alternative Funding Plans (AFP) Innovation Fund. S.P. received support in the form of a Study Abroad Studentship from the Leverhulme Trust, A.C. received support from a CIHR Doctoral Award, A.d.P. received salary support through the Fonds de Recherche du Quebéc—Santé (FRQS) (Chercheur-boursier clinicien), and A.K. received salary support through a Tier 2 Canada Research Chair in Global HIV and Sexual and Reproductive Health.

Presented at 25th Annual Canadian Conference on HIV/AIDS Research; May 13, 2016; Winnipeg, Manitoba, Canada as an oral presentation.

The authors have no conflicts of interest to disclose.

S.P., A.C., and A.K. conceived the idea for this analysis. A.K., A.d.P., and M.L. contributed to design and acquisition of data. Data preparation and statistical analysis were conducted by E.D. Data interpretation was performed by S.P., E.D., and A.K. S.P. drafted the initial manuscript under the supervision of A.K., and all authors contributed to the final version. All authors have critically reviewed and approved the final manuscript, gave approval for publication and act as guarantors of the work.

The CHIWOS Research Team members are listed in Appendix 1.

Received April 13, 2017

Accepted July 21, 2017

Back to Top | Article Outline

INTRODUCTION

With increased efficacy of antiretroviral therapy (ART), people with HIV are living longer and healthier lives,1 and interest and opportunities are increasingly focused on optimizing sexual health among this population.2–4 Condoms have traditionally been promoted as the primary safer sex option in serodiscordant partnerships, reducing the risk of sexual HIV transmission by 80%.5 However, condoms do not meet the safer sex needs for all people with HIV, particularly for women who experience inequities negotiating condom use,6,7 or for those in mutually disclosed sexual partnerships who engage in condomless sex to conceive8,9 or for enhanced sexual pleasure and intimacy.4,10

In 2008, the Swiss Federal AIDS Commission released a statement declaring that people with HIV with no concurrent sexually transmitted infections (STIs), who adhered to ART for 6 months and achieved an undetectable HIV viral load (VL) (<40 copies/mL) posed no risk of transmitting HIV to a serodiscordant sexual partner.11 This statement was met with substantial debate, with concerns raised regarding its potential impact on sexual behaviors of people with HIV and risks of increased HIV incidence.12,13 However, with the release of landmark findings from the HPTN 052 randomized controlled trial,14 and findings from the PARTNER15,16 and Opposites Attract studies,17 evidence in support of the Swiss Statement is undeniable,14,15,17–19 furthering a global movement toward adopting Treatment-as-Prevention (TasP) initiatives.20,21

With growing consensus that the risk of sexual HIV transmission to sexual partners is zero in the presence of an undetectable VL through ART use,14,16 an undetectable VL constitutes a highly effective form of safer sex within HIV-serodiscordant partnerships.22–24 Fundamentally, TasP offers a promise in redefining sexual relationships for people with HIV, shifting the focus toward supporting ART uptake and adherence rather than risk-based sexual behavior discourses, both within scientific4 and advocacy communities.25 Consequently, awareness of the HIV prevention benefits of ART may influence sexual decision making among people with HIV.26–32 Although previous work has identified no association between condomless sex and ART use26,33–35 or ART-related viral suppression,26,36–38 some studies have suggested that people with HIV who are aware of HIV prevention benefits of ART are embracing and translating this science to inform decisions related to condomless sex with an undetectable VL.26,29,32

In Canada and elsewhere, awareness of the HIV prevention benefits of ART is advancing among people with HIV, with community groups and activists leading the promotion of this science through “Undetectable = Untransmittable” campaigns.39,40 Few quantitative studies have focused specifically on awareness of the HIV prevention benefits of ART to prevent sexual HIV transmission and its influence on condom-use practices among women with HIV (WWH).31,32 This question remains unexplored in Canada, a setting where TasP has been heavily promoted in some provinces.41

Within a community-based cohort study by, with, and for WWH across Canada, we measured the prevalence and correlates of condomless sex with serodiscordant regular sexual partners among women with an undetectable VL on ART. Specifically, we assessed the association between condomless sex and awareness of HIV prevention benefits of ART, to infer whether WWH in Canada are using ART as a safer sex option to minimize HIV transmission to HIV-serodiscordant regular partners. This work adopts a feminist lens in alignment with a critical field of scholarship that explores the potential for TasP to promote sex-positive approaches and support the sexual rights of WWH.2,4

Back to Top | Article Outline

METHODS

Data Source

We used cross-sectional baseline questionnaire data from the Canadian HIV Women's Sexual and Reproductive Health Cohort Study (CHIWOS, www.chiwos.ca), a community-based study enrolling WWH, described in detail elsewhere.42,43 CHIWOS was established to assess barriers to and facilitators of accessing women-centered HIV care for women across Canada, and to explore the mental, sexual, and reproductive health benefits of this health care approach. CHIWOS has enrolled 1424 women from British Columbia (BC), Ontario, and Quebec, the provinces comprising most (81%) WWH nationally.44

CHIWOS is grounded in the principles of Critical Feminist theory45 and Community-Based Research (CBR). CHIWOS involves WWH and allied clinicians, researchers, and community partners as core partners throughout the research. Peer Research Associates (PRAs, WWH trained in research skills) contributed to questionnaire development, led participant outreach and recruitment, and administered questionnaires.

Recruitment was conducted between August 27, 2013, and May 1, 2015. Women were eligible for inclusion if they were aged 16 years and older, self-identified as a woman with HIV and resided in 1 of the 3 study provinces. Recruitment was conducted in regional community and clinic settings, through peer outreach and word of mouth.46 Particular efforts were made to recruit populations disproportionately affected by HIV or underserved by research or health services, including transwomen, lesbian/bisexual/queer women, Indigenous women, and black women.

At baseline, participants completed a PRA-administered survey of approximately 90 minutes, with questions assessing reproductive, sexual, mental, and women's health outcomes, and use of HIV/AIDS services. The survey was administered by PRAs online in English or French using FluidSurveys software.

Ethical approval was granted by the Research Ethics Boards of Simon Fraser University, University of British Columbia/Providence Health, Women's College Hospital, and McGill University Health Centre. Participants provided voluntary informed consent and were provided with $50 honoraria.

Back to Top | Article Outline

Inclusion Criteria

We included women self-reporting vaginal/anal sex in the past 6 months with at least 1 HIV-negative/unknown HIV status regular sexual partner (defined in the survey as an intimate noncommercial sexual partner with whom women had multiple sexual encounters, for a “long period of time”, and who they did not exchange drugs, money, etc., as defined by the participant). We also restricted inclusion to women self-reporting an undetectable HIV plasma VL (<50 copies/mL) on ART at interview. A validity study showed self-reported VL to be strongly predictive of laboratory-confirmed (true) VL in CHIWOS.47 We excluded participants exclusively reporting female sexual partners in the preceding 6 months or missing condom-use data. These criteria were applied to obtain a sample of women who would be positioned to benefit from the use of ART as an HIV prevention strategy during sex with regular serodiscordant male partners.

Back to Top | Article Outline

Measures

Primary Outcome

The primary outcome variable was condomless sex, defined as self-reporting <100% male or female condom use during vaginal/anal penetrative intercourse with at least 1 regular male partner within 6 months before the baseline interview.

Back to Top | Article Outline

Explanatory Variables

Explanatory variables were selected after a priori literature review.26–38 The primary explanatory variable was awareness of HIV prevention benefits of ART. Participants were asked, “How do you think taking ARVs changes your risk of transmitting HIV?” A 5-point Likert scale was used for response options with participant responses dichotomized as follows “Makes the risk of transmission a lot lower” vs. “Makes the risk of transmission a little lower/makes no difference/makes the risk of transmission a little/a lot higher/don't know”. Participants responding “Makes the risk of transmission a lot lower” were classified as being aware of HIV prevention benefits of ART, to accurately reflect current scientific evidence that the risk of sexual HIV transmission with an undetectable VL on ART approaches zero.14,16,48 We also conducted a sensitivity analysis investigating a less conservative definition of awareness of HIV prevention benefits of ART, collapsing “a lot lower” and “a little lower” vs. all other responses to observe whether this affected the associations observed.

We assessed additional covariates of condomless sex, including sociodemographic variables [age at interview (per year increase), race/ethnicity (white vs. Indigenous vs. African/Caribbean/black vs. other and multiple ethnicities), born in Canada (yes vs. no), personal annual income (<$20,000 vs. ≥$20,000), formal education (<high school vs. ≥high school), history of incarceration (yes vs. no), history of injection drug use (yes vs. no), and sex work in past 6 months (exchanged sex for money, drugs, clothing, and possessions) (yes vs. no)]; clinical variables [years living with HIV, whether a health care provider had discussed the impact of VL on HIV transmission risk (yes vs. no)]; sexuality and relationship variables {satisfaction with current sex life [completely/very/reasonably satisfactory vs. not very/not at all satisfactory], number of sex partners within past 6 months, type of sexual partners in past 6 months [regular exclusively vs. regular and casual partners], length of relationship with regular sexual partners [years], in a relationship at interview [yes (married/common law/living-apart relationship) vs. no (single/separated/widowed/divorced)]}; reproductive health variables [previous pregnancy (yes vs. no), future pregnancy intentions (yes vs. no)]; HIV-related stigma variables (fear of HIV status disclosure in the month before interview) (yes vs. no), HIV-related stigma (measured using the 10-item HIV Stigma Scale, with scores ≥median recorded as “high” HIV-related stigma vs. “low”49,50); and current sexual (yes vs. no) and physical (yes vs. no) violence.

Imputation methods were used to recode data for 5 participants who preferred not to report their partner's HIV status to preserve statistical power and avoid biases associated with excluding these participants from the model. These participants were recorded as reporting HIV status unknown/serodiscordant partners. Where data related to other covariates were missing during the model selection process, participants affected were excluded from the final model.

Back to Top | Article Outline

Statistical Analysis

We calculated the proportion of participants who self-reported condomless sex in the 6 months before interview. Sociodemographic, behavioral, clinical, and sexual and reproductive characteristics were compared between participants reporting condomless sex versus those who did not, using Pearson χ2 test for categorical variables (Fisher exact test for small cell counts) and the Wilcoxon rank-sum test for continuous variables.

Multivariable logistic regression identified covariates independently associated with condomless sex. Candidates for model inclusion were variables having P <0.2 in the bivariable analysis or variables considered a priori to influence likelihood of condomless sex after literature review. Model selection was determined by minimizing the Akaike information criterion and maintaining type III P values. P values were 2-sided and considered significant at P <0.05. All analyses were conducted using SAS 9.4 software (SAS Institute Inc., Cary, NC).

Back to Top | Article Outline

RESULTS

Of the 1424 women enrolled in CHIWOS, we excluded 773 women self-reporting no consensual sex (including oral sex) in the 6 months before interview, 70 women self-reporting no anal/vaginal sex, 182 women self-reporting all HIV concordant regular partners, and 15 women self-reporting female partners exclusively. Finally, we excluded 13 women for whom condom-use data were missing, and 100 women who did not have an undetectable HIV VL (>50 copies/mL) on ART, yielding an analytic sample of 271 participants.

The median age of women was 41 [interquartile range (IQR): 34–47] and the median years living with HIV was 11 (IQR: 6–18) (Table 1). Overall, 34% of participants were resident in BC, 35% in Ontario, and 31% in Quebec. In terms of ethnicity, 16% women reported Indigenous ancestry, 32% were African, Caribbean, or black, and 48% were white. Overall, 80% of participants reported regular sexual partnerships exclusively within 6 months before the interview, with no casual sexual partners. The median duration of regular sexual partnerships was 3 years (IQR: 1–8). At the time of interview, 51% of women reported being in a relationship and 84% of women were satisfied with their sex lives. The median HIV-related stigma score in the sample was 57.5 (IQR: 41.3–67.5), with 47% of women reporting high HIV-related stigma.

TABLE 1-a

TABLE 1-a

TABLE 1-b

TABLE 1-b

Back to Top | Article Outline

Condomless Sex and Awareness of HIV Prevention Benefits of ART

Condomless sex was reported by 149 (55%) participants in the 6 months before the interview (Table 1). Although all participants were on ART and self-reported an undetectable VL, 203 (75%) women were aware of the HIV prevention benefits of ART and 224 (83%) had discussed the impact of VL on HIV transmission risk with their provider. Of women aware of ART prevention benefits, 63% reported condomless sex, compared with 32% of women not aware (P < 0.001).

In logistic regression, factors positively associated with condomless sex included awareness of the HIV prevention benefits of ART [adjusted odds ratio (AOR): 4.08; 95% confidence interval (CI): 2.04 to 8.16], ≥high-school education (AOR: 2.36; 95% CI: 1.01 to 5.53), and being in a relationship (AOR: 1.78; 95% CI: 1.02 to 3.11) (Table 2). African, Caribbean, or black compared with white race/ethnicity (AOR: 0.36; 95% CI: 0.18 to 0.74), and residence in Ontario (AOR: 0.40; 95% CI: 0.19 to 0.83) or Quebec (AOR: 0.26; 95% CI: 0.12 to 0.59) compared with BC were negatively associated with condomless sex.

TABLE 2

TABLE 2

Back to Top | Article Outline

Sensitivity Analysis

When we expanded the definition of awareness of HIV prevention benefits of ART to also include participants reporting the belief that ART “makes the risk of transmission a little lower”, 236 (87%) participants were aware of HIV prevention benefits of ART. When this alternative definition was applied in the logistic regression analysis, awareness of HIV prevention benefits of ART remained positively associated with condomless sex (AOR: 7.46; 95% CI: 2.88 to 19.37) (Table 3), with a stronger effect estimate.

TABLE 3

TABLE 3

Back to Top | Article Outline

DISCUSSION

In a Canadian community-based cohort of WWH, we observed that awareness of the HIV prevention benefits of ART was associated with a 4-fold increased odds of condomless sex among women with an undetectable VL on ART and regular HIV-serodiscordant sexual partners. We also found independent associations between condomless sex and ethnicity, education, province of interview, and relationship status. These findings suggest that some WWH are embracing and translating the evidence behind TasP to inform their own sexual decision making.

Among this cohort of virally suppressed women, condomless sex was reported by 55% of women overall and by 63% of women who were aware of the HIV prevention benefits of ART. The relationship between awareness of HIV prevention benefits of ART and condomless sex persisted in the adjusted logistic regression analysis. Our findings support the hypothesis that awareness of HIV prevention benefits of ART influences condom-use practices and suggest that some women with an undetectable VL on ART are embracing the HIV prevention benefits of ART as a safer sex option to avert HIV transmission to HIV-serodiscordant regular partners, consistent with qualitative reports from women and couples themselves.4,25

Our findings align with previous work in this field. Analyses using data collected in earlier treatment eras (before 2004) within the Women's Interagency HIV Study revealed a positive association between awareness of HIV prevention benefits of ART and condomless sex.31,32 This association has similarly been reported by empirical analyses in the modern TasP era.29,30 Notably, the Swiss Cohort Study evaluated sexual behaviors before and after the release of the Swiss Consensus Statement in 200811 and found that participants interviewed after the release of the statement were more likely to report condomless sex; an association that was stronger among those with VL suppression.27 Furthermore, an accelerated increase in the prevalence of condomless sex was observed among Swiss Cohort Study participants in stable partnerships in the years after the release of the Swiss Consensus Statement (between 2008 and 2013).28 Although our study is cross-sectional, it adds to the evidence base that viral suppression with ART is increasingly being accurately viewed as an HIV prevention and safer sex strategy for WWH, particularly as evidence in support of TasP become more widely acknowledged.

In our analysis, partnered relationship status at interview was independently associated with condomless sex, consistent with previous work in local and international settings,27,28,36,51,52 likely reflecting a mutual decision between partners in a disclosed relationship to engage in condomless sex. Women educated beyond high school and reporting white ethnicity had greater odds of reporting condomless sex. This finding may be attributed to greater treatment optimism among women with higher socioeconomic backgrounds. Previous work supports this hypothesis, observing that people with HIV who are from marginalized socioeconomic groups or who are isolated from HIV services are less likely to be aware of HIV prevention benefits of ART.30,53,54 Residence in BC compared with Ontario or Quebec was also an independent correlate of condomless sex among women in this cohort, likely reflecting the localized, province-wide expansion of TasP in BC.55

Although all women in our analytic sample reported an undetectable VL on ART, one-quarter of participants were not fully aware of the accompanying HIV prevention benefits. Moreover, 17% of women had never discussed TasP with their health care provider. These echo findings from an analysis in the Italian Donne con Infezione Da HIV (DIDI) study, observing no association between condomless sex and undetectable VL on ART among WWH in serodiscordant partnerships, suggesting either low awareness or application of the HIV prevention benefits of ART.36 These findings stress the need to convey the HIV prevention benefits of ART to all women, to promote access to the full array of safer sex options to make informed sexual decisions in the TasP era.

Although our analysis supports the hypothesis that awareness of the HIV prevention benefits of ART influences condom-use practices, condomless sex was not consistently reported among women who were aware of HIV prevention benefits of ART. Besides concerns related to HIV transmission, complex relationship priorities, gender dynamics, fears of disclosure, and stigma also shape sexual behavior, in addition to considerations around pregnancy and STI prevention.9,56,57 In a climate of growing HIV criminalization, WWH may also use condoms to protect themselves against potential charges for HIV nondisclosure to sexual partners. In Canada, people with HIV are legally obligated to disclose their HIV status to sexual partners before sex that represents a realistic possibility of HIV transmission.58,59 The legal obligation to disclose is avoided only during condom-protected vaginal sex in the context of a low VL (<1500 copies/mL).59

Previous work suggests that people with HIV remain apprehensive about the HIV prevention benefits of ART.56 Women may be aware of the HIV prevention benefits of ART but be reluctant and fearful of foregoing condoms, given the decades-long discourse of risk, contamination, fear, and stigma, in addition to the virtually exclusive promotion of male condom use for HIV prevention. Although HIV prevention benefits of ART are clear on a population health level, it can be challenging to translate this messaging into individual-level clinical counseling. For instance, earlier research reported that genital HIV RNA viral shedding may occur among individuals who have an undetectable plasma HIV VL,60–62 raising the possibility of onward HIV transmission. Furthermore, previous work has suggested that coinfection with an STI may compromise the prevention benefits conveyed by an undetectable HIV VL on ART.61,63 However, more recent studies in the modern ART era have shown that HIV viral suppression is maintained despite coinfection with STIs.13,15,64 Incorporation of this new evidence into sexual health messaging is slow and both providers and, understandably, some WWH remain apprehensive. Additional efforts are required to support WWH navigating sexual decision making within an environment still largely framed by an antiquated risk discourse, rather than reflecting established scientific evidence of sexual HIV transmission in the context of viral suppression on ART.

Although our findings suggest that some WWH are aware of condomless sex with an undetectable VL on ART as an effective strategy to prevent HIV transmission to serodiscordant sexual partners, supporting comprehensive protection should also offer regular STI/HIV testing for partners and couples, and expanded female-controlled contraception options to minimize the risk of unintended pregnancy.65 This is particularly relevant given that previous work has suggested that WWH in Canada primarily rely on the male condom for contraception.42

Back to Top | Article Outline

Limitations

We did not capture STI acquisition within the CHIWOS baseline questionnaire, as such the impact of STIs on condom-use practices or awareness of HIV prevention benefits of ART could not be assessed. The condom-use variable used in this analysis is self-reported, and may be subject to social desirability bias, which may underestimate the prevalence of condomless sex.

Although CHIWOS represents the largest cohort of WWH in Canada, findings generated from this analysis may not be generalizable to women in other Canadian provinces or international settings. Five participants preferred not to disclose their partner's HIV status and were recorded as reporting HIV status unknown/serodiscordant partners, which may have introduced information bias into our analysis. However, when we repeated the logistic regression after excluding these participants, the results remained unchanged (results not shown).

We restricted inclusion to women with regular HIV-serodiscordant sexual partners, as we did not ask about the HIV status of casual partners nor condom-use practices within casual relationships in the CHIWOS questionnaire. Considerations and recommendations for practicing condomless sex in the context of an undetectable VL on ART may be different for women engaging in casual sexual encounters with nonregular partners. Although women in casual relationships may also translate their awareness of ART prevention benefits to inform condom-use practices, these data were not collected within CHIWOS. Finally, as we limited this analysis to women with an undetectable VL, we were unable to evaluate the impact of TasP messaging on condom-use practices of WWH with a detectable VL on ART.

It is important to acknowledge the high prevalence of sexual inactivity in this cohort. We excluded 773 women self-reporting no recent consensual sex from this analysis. Although the perspectives of sexually inactive WWH were not captured within this analysis, previous work has shown that many complex reasons drive sexual inactivity among WWH.66 Among CHIWOS participants, fear of transmitting HIV to sexual partners has been identified as a key factor driving intentional sexual abstinence.66 Although previous work has shown that awareness of HIV prevention benefits of ART is not a significant correlate of sexual inactivity in the CHIWOS cohort, women who have engaged in discussions around the prevention benefits of ART with their health care provider have been shown to demonstrate lower odds of sexual inactivity.42 Our analysis adds to this body of work revealing how the awareness of the HIV prevention benefits of ART expands HIV prevention options and may influence sexual decision making of sexually active WWH with serodiscordant male partners in the TasP era.

Back to Top | Article Outline

CONCLUSIONS

Within a sample of Canadian WWH with an undetectable VL on ART and reporting regular HIV-serodiscordant sexual partners, most were aware of the HIV prevention benefits of ART. We also observed an association between awareness of HIV prevention benefits of ART and condomless sex. Our findings support that an undetectable VL on ART may be accurately viewed as a safer sex option to minimize HIV transmission risk to HIV-serodiscordant regular male partners among WWH. However, awareness of the HIV prevention benefits of ART is not universal, and decisions related to safer sex strategies remain complex. This work highlights the critical need to advance safer sex discussions beyond condom use to better support WWH to make informed sexual decisions, and fully realize options for healthy, safe, pleasurable, and satisfying sexuality in the TasP era.23

Back to Top | Article Outline

ACKNOWLEDGMENTS

The CHIWOS Research Team thanks women living with HIV for their contributions to this study. We also thank the national team of coinvestigators, collaborators, and Peer Research Associates and acknowledge the national Steering Committee, our 3 provincial Community Advisory Boards, the national CHIWOS Aboriginal Advisory Board, the BC Centre for Excellence in HIV/AIDS for data support and analysis, and all our partnering organizations for supporting the study.

Back to Top | Article Outline

The CHIWOS Research Team

Rahma Abdul-Noor (Women's College Research Institute), Aranka Anema (University of British Columbia), Jonathan Angel (Ottawa Hospital Research Institute), QC—Jean-Guy Baril (Université de Montréal), Fatimatou Barry (Women's College Research Institute), Greta Bauer (University of Western Ontario), Kerrigan Beaver (Women's College Research Institute), Denise Becker (Positive Living Society of British Columbia), Anita Benoit (Women's College Research Institute), Jason Brophy (Children's Hospital of Eastern Ontario), Lori Brotto (University of British Columbia), Ann Burchell (Ontario HIV Treatment Network), Claudette Cardinal (Simon Fraser University), Allison Carter (British Columbia Centre for Excellence in HIV/AIDS and Simon Fraser University), Angela Cescon (British Columbia Centre for Excellence in HIV/AIDS), Lynne Cioppa (Women's College Research Institute), Jeffrey Cohen (Windsor Regional Hospital), Guillaume Colley (British Columbia Centre for Excellence in HIV/AIDS), Tracey Conway (Women's College Research Institute), Curtis Cooper (Ottawa Hospital Research Institute), Jasmine Cotnam (Women's College Research Institute), Janette Cousineau (Women's College Research Institute), Janice Dayle (McGill University Health Centre), Marisol Desbiens (Women's College Research Institute), Hania Dubinsky (McGill University Health Centre), Danièle Dubuc (McGill University Health Centre), Janice Duddy (Pacific AIDS Network), Brenda Gagnier (Women's College Research Institute), Jacqueline Gahagan (Dalhousie University), Claudine Gasingirwa (Women's College Research Institute), Nada Gataric (British Columbia Centre for Excellence in HIV/AIDS), Saara Greene (McMaster University), Trevor Hart (Ryerson University), Catherine Hankins (UNAIDS), Bob Hogg (British Columbia Centre for Excellence in HIV/AIDS and Simon Fraser University), Terry Howard (Positive Living Society of British Columbia), Shazia Islam (Women's College Research Institute), Evin Jones (Pacific AIDS Network), Charu Kaushic (McMaster University), Alexandria Keating (ViVA and Southern Gulf Islands AIDS Society), Logan Kennedy (Women's College Research Institute), Mary Kestler (Oak Tree Clinic, BC Women's Hospital and Health Centre), Maxime Kiboyogo (McGill University Health Centre), Marina Klein (McGill University Health Centre), Gladys Kwaramba (Women's College Research Institute), Andrea Langlois (Pacific AIDS Network), Rebecca Lee (CIHR Canadian HIV Trials Network), Lynne Leonard (University of Ottawa), Johanna Lewis (Women's College Research Institute), Viviane Lima (British Columbia Centre for Excellence in HIV/AIDS), Elisa Lloyd-Smith (Providence Health Care), Carmen Logie (University of Toronto), Shari Margolese (Women's College Research Institute), Carrie Martin (Native Women's Shelter of Montreal), Renee Masching (Canadian Aboriginal AIDS Network), Lyne Massie (Université de Québec à Montréal), Melissa Medjuck (Positive Women's Network), Brigitte Ménard (McGill University Health Centre), Cari Miller (Simon Fraser University), Deborah Money (Women's Health Research Institute), Marvelous Muchenje (Women's Health in Women's Hands), Mary Mwalwanda (Women's College Research Institute), Mary (Muthoni) Ndung'u (Women's College Research Institute), Valerie Nicholson (Simon Fraser University), Illuminée Nzikwikiza (McGill University Health Centre), Kelly O'Brien (University of Toronto), Nadia O'Brien (McGill University Health Centre and Université de Montréal), Gina Ogilvie (British Columbia Centre for Disease Control), Susanna Ogunnaike-Cooke (Public Health Agency of Canada), Joanne Otis (Université du Québec à Montréal), Ali Palmer (Simon Fraser University), Sophie Patterson (Simon Fraser University), Doris Peltier (Canadian Aboriginal AIDS Network), Yasmeen (Ashria) Persad (Women's College Research Institute), Neora Pick (Oak Tree Clinic, BC Women's Hospital and Health Centre), Alie Pierre (McGill University Health Centre), Jeff Powis (Toronto East General Hospital), Karène Proulx-Boucher (McGill University Health Centre), Corinna Quan (Windsor Regional Hospital), Janet Raboud (Ontario HIV Treatment Network), Anita Rachlis (Sunnybrook Health Science Centre), Edward Ralph (St. Joseph's Health Care), Stephanie Rawson (Simon Fraser University, BC), Eric Roth (University of Victoria), Danielle Rouleau (Centre Hospitalier de l'Université de Montréal), Sean Rourke (Ontario HIV Treatment Network), Sergio Rueda (Ontario HIV Treatment Network), Mercy Saavedra (Women's College Research Institute), Kate Salters (Simon Fraser University), Margarite Sanchez (ViVA and Southern Gulf Islands AIDS Society), Roger Sandre (Haven Clinic), Jacquie Sas (CIHR Canadian HIV Trials Network), Paul Sereda (British Columbia Centre for Excellence in HIV/AIDS), Fiona Smaill (McMaster University), Stephanie Smith (Women's College Research Institute), Marcie Summers (Positive Women's Network), Tsitsi Tigere (Women's College Research Institute), Wangari Tharao (Women's Health in Women's Hands), Jamie Thomas-Pavanel (Women's College Research Institute), Christina Tom (Simon Fraser University, BC), Cécile Tremblay (Centre Hospitalier de l'Université de Montréal), Benoit Trottier (Clinique l'Actuel), Sylvie Trottier (Centre Hospitalier Universitaire de Québec), Christos Tsoukas (McGill University Health Centre), Sharon Walmsley (Toronto General Research Institute), Kath Webster (Simon Fraser University), Wendy Wobeser (Kingston University), Jessica Yee (Native Youth Sexual Health Network), Mark Yudin (St-Michael's Hospital), and Wendy Zhang (British Columbia Centre for Excellence in HIV/AIDS). All other CHIWOS Research Team Members wish to remain anonymous.

Back to Top | Article Outline

REFERENCES

1. Patterson S, Cescon A, Samji H, et al. Life expectancy of HIV-positive individuals on combination antiretroviral therapy in Canada. BMC Infect Dis. 2015;15:274.
2. Kumar S, Gruskin S, Khosla R, et al. Human rights and the sexual and reproductive health of women living with HIV—a literature review. J Int AIDS Soc. 2015;18(suppl 5):20290.
3. Amin A. Addressing gender inequalities to improve the sexual and reproductive health and wellbeing of women living with HIV. J Int AIDS Soc. 2015;18(suppl 5):20302.
4. Persson A. “The world has changed”: pharmaceutical citizenship and the reimagining of serodiscordant sexuality among couples with mixed HIV status in Australia. Sociol Health Illn. 2016;38:380–395.
5. Weller S, Davis K. Condom effectiveness in reducing heterosexual HIV transmission. Cochrane database Syst Rev. 2002:Cd003255.
6. Stevens P, Galvao L. “He won't use condoms”: HIV-infected women's struggles in primary relationships with serodiscordant partners. Am J Public Health. 2007;97:1015–1022.
7. Pulerwitz J, Amaro H, De Jong W, et al. Relationship power, condom use and HIV risk among women in the USA. AIDS care. 2002;14:789–800.
8. Ngure K, Mugo N, Celumcde C, et al. A qualitative study of barriers to consistent condom use among HIV-1 serodiscordant couples in Kenya. AIDS care. 2012;24:509–516.
9. McDonald K. “The old-fashioned way”: conception and sex in serodiscordant relationships after ART. Cult Health Sex. 2011;13:1119–1133.
10. Spongberg M, Kippax S, Crawford J, et al. “If it's not on…”: heterosexuality for HIV positive women. Venereology. 1996;9:15–23.
11. Vernazza P, Hirschel B, Bernasconi E, et al. Les personnes séropositives ne souffrant d'aucune autre MST et suivant un traitement antirétroviral efficace ne transmettent pas le VIH par voie sexuelle. Bull des Médecins Suisses. 2008;89:165–169.
12. Vernazza P. The debate continues: does “undetectable” mean “uninfectious”? HIV Ther. 2009;3:113–116.
13. Vernazza P, Bernard E. HIV is not transmitted under fully suppressive therapy: the Swiss Statement—eight years later. Swiss Med Wkly. 2016;146:w14246.
14. Cohen M, Chen Y, McCauley M, et al. Final results of the HPTN 052 randomized controlled trial: antiretroviral therapy prevents HIV transmission [Oral presentation, 8th IAS Conference on HIV Pathogenesis, Treatment and Prevention]. J Int AIDS Soc. 2015;18(suppl 4):15.
15. Rodger A, Cambiano V, Bruun T, et al. HIV Transmission Risk through Condomless Sex if HIV+ Partner on Suppressive ART: PARTNER Study. Boston, MA: CROI; 2014.
16. Rodger AJ, Cambiano V, Bruun T, et al. Sexual activity without condoms and risk of HIV transmission in serodifferent couples when the HIV-positive partner is using suppressive antiretroviral therapy. JAMA. 2016;316:171–181.
17. Grulich A, Bavinton B, Jin F, et al. HIV Transmission in Male Serodiscordant Couples in Australia, Thailand and Brazil [Oral Presentation: 1019LB]. Seattle, WA: CROI; 2015.
18. Attia S, Egger M, Muller M, et al. Sexual transmission of HIV according to viral load and antiretroviral therapy: systematic review and meta-analysis. AIDS. 2009;23:1397–1404.
19. Loutfy MR, Wu W, Letchumanan M, et al. Systematic review of HIV transmission between heterosexual serodiscordant couples where the HIV-positive partner is fully suppressed on antiretroviral therapy. PLoS One. 2013;8:e55747.
20. WHO. Antiretroviral Treatment as Prevention of HIV and TB. 2012. Available at: http://http://www.who.int/hiv/pub/mtct/programmatic_update_tasp/en/.
21. Montaner JS. Treatment as prevention–a double hat-trick. Lancet. 2011;378:208–209.
22. Haire B, Kaldor J. HIV transmission law in the age of treatment-as-prevention. J Med Ethics. 2015;41:982–986.
23. Lasry A, Sansom S, Wolitski R, et al. HIV sexual transmission risk among serodiscordant couples: assessing the effects of combining prevention strategies. AIDS. 2014;28:1521–1529.
24. Kaida A, Patterson S, Carter A, et al. Contraceptive choice and use of dual protection among women living with HIV in Canada: priorities for integrated care. Perspect Sex Reprod Health. 2017 [In Press].
25. Welbourn A. Desires denied. In: Jolly S, Cornwall A, Hawkins K, eds. Women, Sexuality and the Political Power of Pleasure. London, NY: Zed Books; 2013.
26. Crepaz N, Hart T, Marks G. Highly active antiretroviral therapy and sexual risk behavior: a meta-analytic review. JAMA. 2004;292:224–236.
27. Hasse B, Ledergerber B, Hirschel B, et al. Frequency and determinants of unprotected sex among HIV-infected persons: the Swiss HIV cohort study. Clin Infect Dis. 2010;51:1314–1322.
28. Kouyos RD, Hasse B, Calmy A, et al. Increases in condomless sex in the Swiss HIV cohort study. Open Forum Infect Dis. 2015;2:ofv077.
29. Chen Y. Treatment-related optimistic beliefs and risk of HIV transmission: a review of recent findings (2009–2012) in an era of treatment as prevention. Curr HIV/AIDS Rep. 2013;10:79–88.
30. Hanif H, Bastos F, Malta M, et al. Where does treatment optimism fit in? Examining factors associated with consistent condom use among people receiving antiretroviral treatment in Rio de Janeiro, Brazil. AIDS Behav. 2014;18:1945–1954.
31. Wilson T, Minkoff H. Brief report: condom use consistency associated with beliefs regarding HIV disease transmission among women receiving HIV antiretroviral therapy. JAIDS. 2001;27:289–291.
32. Wilson T, Feldman J, Vega M, et al. Acquisition of new sexual partners among women with HIV infection: patterns of disclosure and sexual behavior within new partnerships. AIDS Educ Prev. 2007;19:151–159.
33. Bunnell R, Ekwaru J, Solberg P, et al. Changes in sexual behavior and risk of HIV transmission after antiretroviral therapy and prevention interventions in rural Uganda. AIDS. 2006;20:85–92.
34. Kennedy C, O'Reilly K, Medley A, et al. The impact of HIV treatment on risk behaviour in developing countries: a systematic review. AIDS Care. 2007;19:707–720.
35. Venkatesh K, Flanigan T, Mayer K. Is expanded HIV treatment preventing new infections? Impact of antiretroviral therapy on sexual risk behaviors in the developing world. AIDS. 2011;25:1939–1949.
36. Cicconi P, Monforte A, Castagna A, et al. Inconsistent condom use among HIV-positive women in the “Treatment as Prevention Era”: data from the Italian DIDI study. J Int AIDS Soc. 2013;16:18591.
37. Suzan-Monti M, Lorente N, Demoulin B, et al. Sexual risk behaviour among people living with HIV according to the biomedical risk of transmission: results from the ANRS-VESPA2 survey. J Int AIDS Soc. 2016;19:20095.
38. Zakher B, Blazina I, Chou R. Association between knowledge of HIV-positive status or use of antiretroviral therapy and high-risk transmission behaviors: systematic review. AIDS care. 2014;26:514–521.
39. POZ Magazine. 5 Reasons “HIV Undetectable” must Mean “Untransmittable” 2016. Available at: https://http://www.poz.com/blog/5-reasons-hiv-undetectable-must-mean-untransmittable.
40. CATIE. Three Reasons Why CATIE Supports U=U for Sexual Transmission 2017. Available at: http://http://www.catie.ca/en/pif/spring-2017/three-reasons-why-catie-supports-uu-sexual-transmission.
41. Lourenco L, Lima VD, Heath K, et al. Process monitoring of an HIV treatment as prevention program in British Columbia, Canada. JAIDS. 2014;67:e94–e109.
42. Kaida A, Carter A, De Pokomandy A, et al. Sexual inactivity and sexual satisfaction among women living with HIV in Canada in the context of growing social, legal, and public health surveillance. J Int AIDS Soc. 2015;18(suppl 5):20284.
43. Loutfy M, Greene S, Kennedy VL, et al. Establishing the Canadian HIV Women's sexual and reproductive health cohort study (CHIWOS): operationalizing community-based research in a large national quantitative study. BMC Med Res Methodol. 2016;16:101.
44. Public Health Agency of Canada. Population Specific HIV/AIDS Status Report: Women 2012. Available at: http://librarypdf.catie.ca/pdf/ATI-20000s/26407.pdf.
45. Rhode D. Feminist critical theories. Stanford L Rev. 1990;42:617–638.
46. Webster K, Carter A, Proulx-Boucher K, et al. Strategies for recruiting women living with HIV in community-based research: lessons from Canada. Prog Community Health Partnersh. [In press].
47. Carter A, de Pokomandy A, Loutfy M, et al. Validating a self-report measure of HIV viral suppression: an analysis of linked questionnaire and clinical data from the Canadian HIV Women's Sexual and Reproductive Health Cohort Study. BMC Res Notes. 2017;10:138.
48. Loutfy M, Tyndall M, Baril JG, et al. Canadian consensus statement on HIV and its transmission in the context of criminal law. Can J Infect Dis Med Microbiol. 2014;25:135–140.
49. Berger B, Ferrans C, Lashley F. Measuring stigma in people with HIV: psychometric assessment of the HIV stigma scale. Res Nurs Health. 2001;24:518–529.
50. Wright K, Naar-King S, Lam P, et al. Stigma scale revised: reliability and validity of a brief measure of stigma for HIV+ youth. J Adolesc Health. 2007;40:96–98.
51. Marshall BD, Milloy MJ, Kerr T, et al. No evidence of increased sexual risk behaviour after initiating antiretroviral therapy among people who inject drugs. AIDS. 2010;24:2271–2278.
52. Ayiga N. Rates and predictors of consistent condom-use by people living with HIV/AIDS on antiretroviral treatment in Uganda. J Health Popul Nutr. 2012;30:270–280.
53. Rojas Castro D, Fugon L, Bourgeois-Fisson E, et al. The “Swiss Statement”: who knows about it? How do they know? What are its effects on people living with HIV/AIDS? AIDS care. 2012;24:1013–1019.
54. Brennan D, Welles S, Miner M, et al. HIV treatment optimism and unsafe anal intercourse among HIV-positive men who have sex with men: findings from the positive connections study. AIDS Educ Prev. 2010;22:126–137.
55. Montaner JS, Lima VD, Barrios R, et al. Association of highly active antiretroviral therapy coverage, population viral load, and yearly new HIV diagnoses in British Columbia, Canada: a population-based study. Lancet. 2010;376:532–539.
56. Persson A. Reflections on the Swiss Consensus Statement in the context of qualitative interviews with heterosexuals living with HIV. AIDS Care. 2010;22:1487–1492.
57. Ezeanochie M, Olagbuji B, Ande A, et al. Fertility preferences, condom use, and concerns among HIV-positive women in serodiscordant relationships in the era of antiretroviral therapy. Int J Gynaecol Obstet. 2009;107:97–98.
58. Supreme Court of Canada. R. v. D.C. 2 S.C.R. 626. 2012. Available at: http://scc-csc.lexum.com/scc-csc/scc-csc/en/item/10010/index.do.
59. Supreme Court of Canada. R. v. Mabior. 2 S.C.R. 584. 2012. Available at: https://scc-csc.lexum.com/scc-csc/scc-csc/en/item/10008/index.do.
60. Baeten JM, Kahle E, Lingappa JR, et al. Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med. 2011;3:77ra29.
61. Kovacs A, Wasserman SS, Burns D, et al. Determinants of HIV-1 shedding in the genital tract of women. Lancet. 2001;358:1593–1601.
62. Cu-Uvin S, DeLong AK, Venkatesh KK, et al. Genital tract HIV-1 RNA shedding among women with below detectable plasma viral load. AIDS. 2010;24:2489–2497.
63. Kalichman S, Pellowski J, Turner C. Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: systematic review with implications for using HIV treatments for prevention. Sex Transm Infect. 2011;87:183–190.
64. Kelley CF, Haaland RE, Patel P, et al. HIV-1 RNA rectal shedding is reduced in men with low plasma HIV-1 RNA viral loads and is not enhanced by sexually transmitted bacterial infections of the rectum. J Infect Dis. 2011;204:761–767.
65. Loutfy M, Margolese S, Money D, et al. Canadian HIV pregnancy planning guidelines. J Obstetrics Gynecol Can. 2012;34:575–590.
66. Kaida A, Patterson S, Nicholson V, et al. The influence of the criminalization of HIV non-disclosure on intentional sexual inactivity among women living with HIV in Canada (Abstract SS3.04, Oral). Paper presented at: 26th Canadian Association of HIV Research (CAHR) Conference; April 6–9, 2017; Montreal, Quebec.
Keywords:

HIV; women; condomless sex; antiretroviral therapy; Canada; CHIWOS

Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.