Provider views of pre-exposure prophylaxis (PrEP) for cisgender women – where do women fit in HIV elimination in Australia?

Introduction

HIV continues to cause significant global impact, with an estimated 38 million people living with HIV worldwide.¹ Pre-exposure prophylaxis (PrEP) is an effective method of preventing HIV, involving the use of antiretroviral medications in HIV-negative people.² There are approximately 29 500 people living with HIV (PLWH) in Australia, the majority of whom are gay, bisexual or other men who have sex with men (GBMSM).³ Widespread PrEP uptake has contributed to significant reductions in HIV notifications among Australian born GBMSM over the past 10 years.^3,4

Women and girls are disproportionately affected by HIV globally, accounting for more than 50% of all PLWH, but are not a priority population in most high-income countries.¹ Approximately 12% of PLWH in Australia are women.³ Unlike the success of PrEP in GBMSM in Australia, declines in HIV incidence among other populations, including cisgender women, have not been observed.³ Health Equity Matters (formerly known as the Australian Federation of AIDS Organisations) has set out Agenda 25, with the goal of ending HIV transmission in Australia by 2025.^3,5 Agenda 25 highlights the importance of reaching all populations at risk of HIV, with specific mention of women.^5,6

Although the incidence is low, certain subgroups of Australian women may be at higher risk of HIV. Around half of new diagnoses in heterosexual women occur in those born overseas^3,7 and Aboriginal and Torres Strait Islander woman are disproportionately affected.³ Of new HIV diagnoses among GBMSM, the percentage of men also reporting sex with women has increased over the past 10 years and late diagnosis is more common among men who have both male and female sexual partners, suggesting these women with GBMSM sexual partners may be at risk of HIV.³ A 2018 survey of women connected with the queer community in Sydney demonstrated an increase in the proportion of women who reported often having unprotected sex with a gay or bisexual man.⁸ Female sex workers and women who inject drugs may also be at risk, though the HIV incidence in these populations in Australia is low.³

Oral co-formulated tenofovir and emtricitabine for the prevention of HIV has been subsidised by the Australian Pharmaceutical Benefits Scheme (PBS) since April 2018.² Long-acting injectable PrEP is licenced but not government subsidised and use is very limited.⁹ Early Australian PrEP guidelines classified an individual’s HIV risk as high or low, and eligibility was restricted to patients identified as high risk.² In an effort to expand PrEP access to all at risk people however, current guidelines outline criteria for suitability rather than eligibility.² Although there are no specific criteria for women, the criteria for heterosexual people include: condomless anal or vaginal intercourse (CLAVI) with a serodiscordant partner who has a detectable viral load, for conception or if there is undue anxiety; CLAVI with a male bisexual partner of unknown status; plans to travel to high HIV prevalence countries where they anticipate CLAVI; and concerns of deteriorating mental health or substance use with a history of increased HIV acquisition risk in this setting.²

Despite guidelines that affirm PrEP suitability for women, there has been limited uptake in Australia. A review of individuals dispensed PBS-subsidised PrEP between April 2018 and June 2022 found only 2% were female, although this does not differentiate between cisgender women and gender diverse people.¹⁰ Estimations of PrEP coverage for women in other non-endemic countries are similarly low; only 10% of US women identified as eligible by prevailing guidelines were prescribed PrEP in 2019.¹¹ Evidence also suggests substantial discontinuation of PrEP for women after initiation, including in the Australian context.^12,13

A major barrier to uptake is low PrEP awareness in PrEP-eligible cisgender women.^14,15 Other reported barriers for women include a low self-perceived risk of HIV, having other priorities, concerns about potential side effects, adherence difficulties, cost, poor access, negative experiences or a lack of trust with healthcare providers and experiences of stigma.^12,16,17 Provider based barriers include clinician difficulties identifying at-risk women,¹⁰ lack of knowledge about PrEP, time constraints, concern about efficacy and cost to patients.^18,19 Potential PrEP enablers for women include increasing education and expanding public health messaging to services where women access health care.¹⁶ Provider perspectives on enablers are limited in available literature¹⁹ although some qualitative studies have recommended an increase in training for providers and resources for women.^18,20

The aim of this descriptive qualitative study^14,15 was to explore PrEP prescribing for Australian cisgender women^A from the provider’s perspective. Through interviews with prescribers, we aimed to determine the barriers to uptake and enablers to facilitate PrEP prescribing, in light of the new opportunities to focus on HIV prevention in sub-populations that have received less attention than GBMSM.

Materials and methods

Participant inclusion criteria were:

Participant recruitment occurred from February 2022 to October 2022. Participants were recruited through direct email contact with Australian wide prescribers and services, including individual prescribers on publicly available online lists, sexual health clinics, general practices, refugee health services, university health services, infectious disease clinics and family planning clinics. Snowball sampling was utilised in addition to direct contact. We aimed to capture a broad range of experiences, with prescribers from a variety of locations, services and professions. Recruitment continued until data saturation occurred.¹⁶

A draft interview guide was developed based on a review of the literature and research team discussion. A pilot interview was conducted with an experienced sexual health clinician in February 2022 to refine the guide. Semi-structured interviews were conducted via video or teleconference. The interviews covered participant experience prescribing PrEP for cisgender women, and enablers and barriers for prescribing. Participants completed a short demographic questionnaire and provided written informed consent. Participants were reimbursed for their time with an AUD50 voucher.

All interviews were performed by Principal Investigator (PI) Lade, an Anglo-Australian female Sexual Health Advanced Trainee. Four participants were known to PI Lade on a professional basis. Interviews were recorded and transcribed by an external company and identifying information was removed. A framework analysis was conducted¹⁷ with an initial code frame derived from the literature and the topic guide. Initial thematic analysis was performed deductively by PI Lade using NVivo, a qualitative data analysis software.²¹ In keeping with a descriptive qualitative methodology, the analysis remained grounded in the data, such that data might also be coded inductively²² and codes were regularly discussed with the wider research team. Data was reduced in coding matrices and grouping used to identify the main themes in the data.

This study was approved by the Joint University of Wollongong and Illawarra Shoalhaven Local Health District Health and Medical Human Research Ethics Committee (2021/ETH11873).

Results

Seventeen participants were interviewed for between 15 and 38 min. Nine participants identified as female and eight as male. The majority were sexual health physicians (SHP) (n = 11, 64.7%), with other professional backgrounds also represented (Table 1). Fifteen participants worked primarily in publicly funded sexual health clinics, though four of these participants also worked in another setting – one in a family planning clinic and three in general practice. The majority of participants worked in New South Wales (n = 10, 58.8%). Most participants were experienced PrEP prescribers, with only two self-identifying as new prescribers. Prescribers reported predominantly prescribing PrEP to GBMSM patient cohorts, with some participants also prescribing to trans and gender diverse people. All reported limited experience prescribing PrEP for cisgender women, with less than five cases in the preceding 12 months. Three participants reported only prescribing PrEP to a woman once in their career.

Identified barriers and enablers to PrEP prescribing for women in Australia are in Table 2. The provider pathway for PrEP prescribing to women is outlined in Fig. 1.

Fig. 1.

Provider pathway for PrEP prescribing for cisgender women.

The three main themes that emerged were:

Discussion

The focus of Australia’s HIV response has been on GBMSM. The significant impact of PrEP on preventing HIV transmission has encouraging potential for eliminating all transmission in Australia,⁴ warranting a focus on other populations, including women. To date, PrEP prescribing for women in Australia has been very limited,¹⁰ as reflected by participant responses. Participants reported most experience prescribing PrEP for women in serodiscordant relationships, as reflected in the literature²⁵ and likely due to serodiscordant status being easily identifiable.¹³ Other potential PrEP indications may rely on knowledge of partner risk factors (e.g. GBMSM status) and are therefore difficult for clinicians to ascertain.²⁶ Women may underestimate or be unaware of their risk.^25,27 Women are also less likely to be asked about PrEP indications than other groups,²⁵ suggesting that women at risk of HIV may not be offered PrEP.¹³ Experienced PrEP providers were likely trained in the era of ‘eligibility’ for PrEP and may easily have missed the nuances in the updated PrEP guidelines which have pivoted towards making PrEP available to anyone who is suitable or requests it.² Participants also described the need for women to meet multiple risk factors in order to receive PrEP, which is not in keeping with PrEP suitability criteria in current Australian guidelines.⁵ These responses highlight that clinician assumptions of HIV risk for women may be inaccurate and hinder PrEP provision.

The research has identified many more barriers than enablers to PrEP prescribing to Australian women (Table 2). A common barrier reported was low awareness of PrEP for women among clinicians and patients, which is consistent with international data.^8,25,28–32 There was concern about lack of awareness among GPs, including from participants working within this profession. Primary care providers have previously identified limited knowledge about PrEP and lack of confidence as prescribing barriers.^33,34 One US survey found that although 90% of primary care physicians reported some type of PrEP education, only 55% self-assessed as competent to prescribe.³⁴ Australian HIV experts have also expressed concerns that PrEP delivery in primary care relies on an empowered and knowledgeable patient managing an ‘unprepared GP’.³⁵ Our participants consistently recommended public and clinician education, and this has been echoed in the US,^25,32 with a call from women for awareness through public health messaging including traditional advertising, social media and communication from health services.^30,31

Participants reported that compared to GBMSM patients, PrEP prescribing for women occurred in the context of competing priorities and longer consultations, which was a barrier to prescribing. Australian primary care data demonstrate that GPs manage significantly more problems per consult with female patients.³⁶ Women have also reported that time limitations in consultations prevent rapport building and open discussion of sexual health including PrEP.^25,37 This highlights inadequacies in the current model of sexual healthcare provision for Australian women.

Expansion of existing services was a common recommendation, although participants disagreed about where and how. PrEP access in general practice was predominantly suggested by sexual health physicians. This indicates a continuation of the ‘purview paradox’ seen in the early stages of PrEP implementation both in Australia and internationally, whereby neither HIV specialists nor GPs believe they should be responsible for PrEP.^38,39 HIV specialists have considered PrEP to be in the realm of general practice, although many were also critical of GP-led PrEP provision.^35,38,40,41 GPs however, have described feeling unable to provide PrEP due to time constraints, lack of training and difficulty building expertise due to lack of patient demand.^38,40,41 Responses from our participants suggest women are similarly impacted by this gap in PrEP ownership.

The question remains – where is the best place is for at-risk women to access PrEP in Australia? Women have reported a preference for PrEP-initiation where they usually access medical care or through reproductive healthcare services.^30,31,37 Data from the US indicate that almost three-quarters of women access PrEP via general practice or women’s health services.⁴² Our participants also proposed access via refugee and reproductive health services; however, when investigators contacted these services during recruitment, none reported experience prescribing PrEP. Australian research has demonstrated PrEP discontinuation is higher for patients receiving PrEP from low caseload prescribers.¹² Consequently, women may be at risk of early cessation when receiving PrEP from inexperienced prescribers, including low caseload GPs and other services suggested by participants.

There are several limitations to this study. Four participants were known to the interviewer on a professional basis, which may have impacted upon responses, although efforts were made to ensure participant comfort with the interview. The data may not represent Australia nationally as more than half of participants were based in NSW, where there are higher rates of PrEP dispensing.⁴³ The majority of participants were sexual health physicians. As high-caseload prescribers are responsible for prescribing to the majority of patients, this may reflect the very limited experience of PrEP provision to women in Australia.⁴³ Travel medicine clinicians were not specifically recruited in this study and may be of interest for future research, in order to capture experience prescribing PrEP to women travelling to high HIV prevalence countries.⁴⁴

Conclusion and recommendations

This study has demonstrated limited PrEP prescribing for Australian cisgender women, even among PrEP-experienced prescribers. It highlights the substantial barriers to PrEP access for women in high-income countries: limited awareness amongst patients and clinicians, difficulties with risk assessment and a lack of women-focused sexual health services. Despite Agenda 25’s goal to reach all those affected, it is evident we are leaving women behind in the race to achieve HIV elimination in Australia. Women have specific needs for PrEP delivery that are not being met by the current model in Australia. Echoing the calls of our participants, we recommend targeted education on broader PrEP prescribing to both experienced and inexperienced providers. National PrEP guidelines should be updated to specifically discuss PrEP for women rather than subsuming women under ‘heterosexual populations’. Participants disagreed on the most appropriate service to provide PrEP for women and the literature is similarly conflicted. Further research among women regarding preferences and opportunities for PrEP access would help guide our model of delivery. Clear clinical ownership over Australian women’s sexual health issues, including PrEP implementation, is required.