DOI: 10.1111/hiv.12285 HIV Medicine (2016), 17, 133--142
© 2015 British HIV Association
ORIGINAL RESEARCH
Healthcare providers’ knowledge of, attitudes to and practice of pre-exposure prophylaxis for HIV infection M Desai,1,2 M Gafos,1 D Dolling,1 S McCormack1 and A Nardone2 and on behalf of the PROUD study 1 Clinical Trials Unit, Medical Research Council, London, UK and 2HIV/STI Department, Public Health England, London, UK Objectives
Pre-exposure prophylaxis (PrEP) has proven biological efficacy in reducing the risk of sexual acquisition of HIV. Healthcare providers’ (HCPs) knowledge of and attitudes to PrEP will be key to successful implementation. In England, PrEP is only available to men who have sex with men (MSM) through the open-label randomized PROUD pilot study of immediate or deferred use. Methods
In September 2013, a cross-sectional survey of UK HCPs distributed through sexual health clinics (219) and professional societies’ email lists (2599) and at a conference (80) asked about knowledge of, attitudes to and practice of PrEP. Results
Overall, 328 of 2898 (11%) completed the survey, of whom 160 of 328 (49%) were doctors, 51 (16%) sexual health advisers (SHAs), 44 (14%) nurses and 73 (22%) unspecified. Over a quarter (83 of 311; 27%) were involved in PROUD. Most respondents (260 of 326; 80%) rated their knowledge of PrEP as medium or high. Over half of respondents (166 of 307; 54%) thought PrEP should be available outside of a clinical trial. The main barriers to supporting PrEP availability outside a clinical trial were concerns about current evidence (odds ratio [OR] 0.13), lack of UK-specific guidance (OR 0.35), concerns about adherence (OR 0.38) and risk of sexual or physical coercion for patients to have condomless or higher risk sex (OR 0.42 in multivariate regression). Just over half (147 of 277; 53%) had been asked about PrEP by patients in the past year, including almost half of those working in a clinic not involved in the PROUD study (86 of 202; 43%). Conclusions
There is support for PrEP availability outside a clinical trial, but HCPs have residual concerns about its effectiveness and negative consequences, and the absence of UK-specific implementation guidance. Keywords: HIV, health services research, prevention Accepted 8 May 2015
sexual HIV acquisition [1] based on several placebocontrolled randomized trials [2–4]. Gay and other men having sex with men (GMSM) are most likely to acquire HIV infection in the UK. In 2013, the highest number of new HIV diagnoses (3250) ever reported among men who have sex with men (MSM) in England was recorded [5]. Three-fifths of MSM in the UK with a viral load compatible with onward transmission do not know that they have HIV infection [6]. Onward transmission risk could be
Introduction In 2012, the US Food and Drugs Administration approved the use of daily Truvada (tenofovir and emtricitabine) as pre-exposure prophylaxis (PrEP) to reduce the risk of
Correspondence: Dr Monica Desai, HIV & STI Department, CIDSC, Public Health England, 61 Colindale Ave, London NW9 5EQ, UK. Tel: 077 9516 0205; fax: 020 7670 4659; e-mail: [email protected]
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mitigated by adherence to annual or quarterly HIV testing, as recommended by national guidelines [7,8], combined with a universal offer of treatment. However, individuals at higher risk of HIV infection through frequent partner change or exposure to HIV within and outside of partnerships need additional tools to reduce the risk of acquiring and transmitting HIV. PrEP is a tool that reduces HIV infection risk and encourages regular testing and engagement with sexual health services, underscoring the potential for a large impact on the UK epidemic. Healthcare providers (HCPs) will be essential in the wider implementation of PrEP as a biomedical intervention [9]. While a few studies have assessed HCPs’ knowledge of, attitudes to and practice (KAP) of PrEP, none have been carried out in the UK. Sexual health is managed by a network of over 200 openaccess free clinics in the UK, with approximately 113 000 GMSM attendances in 2013 [10]. To roll out PrEP in this setting, evidence of effectiveness (as opposed to efficacy) and understanding of how to appropriately target PrEP, support adequate adherence [11], mitigate risk compensation [12], limit the emergence of drug resistance [13] and limit funding diversion from other prevention activities are required [14]. In the UK, ad hoc prescribing is discouraged in order to collect this evidence in a timely manner through clinical research [15]. The PROUD pilot study in England explores some of these issues through an open-label design randomizing eligible GMSM to receive daily oral tenofovir/emtricitabine immediately or after 12 months (www.proud.mrc.ac.uk). We conducted a cross-sectional KAP survey of PrEP among UK HCPs in order to inform the possible wider implementation of PrEP as an HIV prevention intervention.
Methods Design We conducted an anonymous cross-sectional survey of UK HCPs’ KAP of PrEP. Attitudes towards the evidence base, prescribing and clinical management, patient safety, prioritization and commissioning and provision of PrEP were examined (see web supplement for survey tool). HCP attitudes to post-exposure prophylaxis (PEP) were also examined given that PrEP availability may impact on PEP use and experiences with PEP may influence attitudes to PrEP. The study used similar domains to those used by Puro et al. in a survey of Italian HCPs [16]. The survey was developed in-house and reviewed for ambiguities by six HCPs prior to roll-out. The survey was available in paper or online using Select Survey® (ClassApps, Kansas City, Missouri, USA) format depending on participant preference.
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Participant recruitment Between September and November 2013, sexual HCPs working in the UK who see HIV-negative patients were recruited via email through three professional societies: the British HIV Association (BHIVA), the British Society for HIV and Sexual Health (BASHH) and the Society of Sexual Health Advisers (SSHA). SSHA members were also recruited at their conference on 21 September 2013 and via social media using the SSHA twitter feed. Sexual health nurses were also recruited via the Genitourinary Medicine Network (GUMNet), a sentinel network of 29 sexual health clinics, coordinated by Public Health England (PHE).
Data analysis All data analyses were performed in STATA version 10.1 (www.stata.com). Univariate analysis used a χ2 test of proportions or a two-tailed Fisher’s exact test where numbers were less than five in any one group. Missing values were excluded from statistical analyses and the denominator for that group is presented in the results tables. Descriptive analysis explored missing data for systematic omission from a particular group. A large proportion (17%) did not report profession; a sensitivity analysis assessed the impact of this group on the survey results. Multi-item scales asked questions about attitudes to the evidence base, prescribing and clinical management, patient safety, prioritization and commissioning and provision of PrEP. Attitudes were ranked from the most negative to the most positive attitudes to PrEP for all respondents, and according to whether or not they supported use of PrEP outside a clinical trial. Univariate and multivariate logistic regression analysis was used to assess which attitudes were barriers to PrEP availability. Polychoric correlation examined explanatory variables for correlation. Free text responses were quantified and coded. Clinic name responses were matched to Local Authority diagnosed HIV prevalence using data from the Health Protection Agency 2011 and HIV Scotland (http://www.hpa.org.uk/ webc/HPAwebFile/HPAweb_C/1228207184991,http://www .hivscotland.com/data-and-research/regional-statistics/).
Sample size We assumed that 70% of participants would believe that PrEP should be available in the UK outside of a clinical trial, similar to support of PrEP in the Puro study [16]. Because a lower bound of < 50% support would be important, we set a confidence width of 20% and estimated that a sample size of 265 participants was required, assuming a
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response rate of 30%. Previous online surveys of medical providers have achieved response rates of 20–50% [17].
Table 1 Respondent demographics
n (%)
Consent and ethics The survey was reviewed by PHE’s Research and Development Office and was determined to be a service evaluation involving healthcare workers, and thus not requiring ethical approval.
Results Respondent demographics Eleven per cent (328 of 2898; 11.3%) of those sampled returned the survey. Of the 328 respondents, 234 responded from the professional societies, 51 from GUMNet clinics, 34 from the SSHA conference and nine from other sources (e.g. sent a link by a colleague). The response rate was 23% (51 of 219) from GUMNet clinics, 9% (234 of 2599) from the professional societies and 43% (34 of 80) from the conference sample. Over half of respondents (160 of 272; 59%) were doctors, 51 of 272 (19%) were SHAs, 44 of 272 (16%) were nurses and 17 of 272 (6%) were of other professions (Table 1). Approximately a quarter of respondents (83 of 211; 27%) were involved in the PROUD pilot study. Over half of respondents were female (175 of 272; 64%) and the majority (178 of 272; 65%) were over 40 years of age. Almost all respondents worked in a sexual health clinic (250 of 270; 93%) and over half (94 of 177; 53%) worked in clinics located in a high (> 2 per 1000 population aged 15–59 years) diagnosed HIV prevalence area. Respondents were from 97 different sexual health clinics across England, Wales and Scotland. Fifty-six participants (17%) did not complete any of the demographic questions. Of these, a similar proportion (4%) accessed the survey from each of the three sources or did not state where they accessed the survey. This group had been asked about both PrEP and PEP by patients less often than those who stated their profession. However, their responses to all other questions did not affect the sensitivity analysis for profession.
Knowledge of PrEP Over three-quarters of respondents (260 of 326; 80%) rated their knowledge of PrEP as medium or high. More doctors rated their knowledge as medium or high (144/160; 90%) than either nurses (27 of 44; 61%) or SHAs (36 of 51; 71%; P < 0.001) (Table 2). Among those rating their knowledge as high or medium, 71% (175 of 247) felt that they knew enough about PrEP to have an informed discussion with
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Gender Male Female Missing Age < 29 years 30–39 years 40–49 years 50–59 years > 60 years Missing Profession Doctor Health adviser Nurse Other Missing Time working in sexual health/HIV < 1 year 1–5 years 6–15 years > 15 years Missing Place of work Sexual health Other Missing Diagnosed HIV prevalence of sexual health clinic local authority (per 1000 aged 15–59 years) < 1 per 1000 1–2 per 1000 > 2 per 1000 Missing Involved in PROUD pilot study Yes Doctors Health advisers Nurses Other No Missing
Total number
97 (36) 175 (64) 56
272
13 (5) 81 (30) 94 (35) 71 (26) 13 (5) 56
272
272 160 (59) 51 (19) 44 (16) 17 (6) 56 5 (2) 56 (21) 123 (45) 88 (32) 56
272
250 (93) 20 (7) 58
270
44 (25) 39 (22) 94 (53) 151
177
83 (27) 45 (17) 15 (6) 12 (5) 11 (5) 228 (73) 17
311 255
311
patients, and this percentage was significantly higher among doctors (116 of 131; 89%) compared with nurses (17 of 33; 52%) and SHAs (18 of 33; 55%; P < 0.001). A higher proportion of male respondents rated their knowledge of PrEP as high or medium (88 of 97; 91%) compared with female respondents (131 of 175; 75%; P = 0.002). The difference in high/medium self-rated knowledge between genders was seen among doctors (97% of male versus 86% of female doctors; P = 0.029), but was nonsignificant among SHAs (90% of male versus 53% of female SHAs; P = 0.062) and nurses (70% of male versus 71% of female nurses; P = 1.000). However, there was no difference in self-rated high/medium knowledge of PrEP when comparing age groups, with 153 of 188 respondents
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Table 2 Reported knowledge of pre-exposure prophylaxis (PrEP) Professional group [n (%)]
Question
Response
Overall [n (%)]
Doctors
Health advisers
Nurses
P-values
How would you rate your knowledge of PrEP?
High Medium Low Never heard of it Missing No Yes Missing No Yes Missing
90 (28) 170 (52) 60 (18) 6 (2) 2 71 (23) 240 (77) 17 132 (42) 179 (58) 17
63 (39) 81 (51) 15 (9) 1 (1) 0 39 (24) 121 (76) 0 43 (27) 117 (73) 0
6 (12) 30 (59) 15 (29) 0 (0) 0 4 (8) 47 (92) 0 33 (65) 18 (35) 0
5 (11) 22 (50) 13 (30) 4 (9) 0 11 (25) 33 (75) 0 26 (59) 18 (41) 0
< 0.001
Aware of PROUD study
Know enough about PrEP to have informed discussion with patients
0.022
< 0.001
Table 3 Healthcare providers’ attitudes to pre-exposure prophylaxis (PrEP) by support for PrEP availability outside a clinical trial*
Attitude statement PrEP should be widely available based on current evidence Comfortable prescribing PrEP without UK-specific guidance Patients will adhere to daily PrEP No risk of physical or sexual coercion on PrEP PrEP will not impact on funding of other prevention methods Time to engage in prevention counselling for PrEP PrEP effective prevention tool in ‘real world’ PrEP more effective than PEP for frequent PEP users PrEP will have greater impact than behavioural interventions on preventing HIV infection Lack of stigma for patients on PrEP Support from gay community and gay press for PrEP Patients won’t be perceived to be HIV positive by their partners PrEP will have a greater impact than testing and care on the HIV epidemic Truvada safe drug for PrEP PrEP will not lead to an increase in STIs Little impact of PrEP on ARV resistance
HCPs who support PrEP availability outside clinical trial (%)
HCPs who do not support PrEP availability outside clinical trial (%)
Positive attitude
Undecided
Negative attitude
Positive attitude
Undecided
Negative attitude
61 15 33 61 20 76 32 66 39
32 10 42 33 39 13 29 22 28
31 75 24 6 42 11 38 11 33
31 5 10 36 7 62 8 48 17
26 26 33 46 8 31 20 33 44
43 69 57 18 85 7 72 19 39
64 86 66 13
23 12 24 21
13 2 10 66
44 81 49 5
31 17 33 6
25 2 19 89
73 36 30
23 26 50
4 38 20
55 17 7
18 29 23
27 54 70
ARV, antiretroviral; HCP, healthcare provider; PEP, post-exposure prophylaxis; STI, sexually transmitted infection. *Attitudes have been ordered by greatest to the least barrier to PrEP availability in multivariate regression analysis.
(81%) < 50 years old and 66 of 84 (78%) ≥ 50 years old rating their knowledge as high/medium (P = 0.621). Most doctors (129 of 160; 81%) had read the BASHH/ BHIVA position statement on PrEP, but significantly fewer SHAs (22 of 51; 43%) and nurses (16 of 44; 36%) had done so (P < 0.001). Of the randomized controlled trials (RCTs) conducted to test PrEP efficacy, participants were most familiar with the results of iPrEx (high or medium knowledge, 153 of 312; 49%) and least familiar with the VOICE (81 of 312; 26%) and CDC-TDF2 (272 of 312; 23%) studies. The majority of participants were aware of the PROUD study (240 of 311; 77%), even if they were not directly
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involved (157 of 228; 69%), and this was broadly similar among groups accessing the survey from each of the different sources.
Attitudes to PrEP Half of respondents (166 of 307; 54%; 95% CI 48–60%) thought that PrEP should be available in the UK outside of a clinical trial (Table 3), and this proportion was higher among nurses (29 of 44; 66%; 95% CI 50–80%) and SHAs (37 of 51; 73%; 95% CI 58–84%) than doctors (66 of 160; 41%; 95% CI 34–49%; P < 0.001). There was no difference
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Healthcare workers' atudes to PrEP
137
Posive atude towards PrEP Undecided Negave atude towards PrEP
PrEP will have a greater impact than tesng and care on the HIV epidemic Comfortable prescribing PrEP without UK specific guidance PrEP will not impact on funding of other prevenon methods PrEP effecve prevenon tool in ‘real world’ Lile impact of PrEP on ARV resistance Paents will adhere to daily PrEP PrEP will have greater impact than behavioural intervenons on prevenng HIV… PrEP will not lead to an increase in STIs PrEP should be widely available based on current evidence No risk of physical or sexual coercion on PrEP PrEP more effecve than PEP for frequent PEP users Paents not perceived to be HIV posive if taking PrEP Lack of sgma for paents on PrEP Time to engage in prevenon counseling for PrEP Truvada safe drug for PrEP Support from gay community and gay press for PrEP
0%
10%
20%
30%
40%
50%
60%
70%
80%
90% 100%
Fig. 1 Healthcare providers’ attitudes to pre-exposure prophylaxis (PrEP) overall. ARV, antiretroviral; PEP, post-exposure prophylaxis; STI, sexually transmitted infection.
in support for provision outside a clinical trial between those involved in the PROUD study (49 of 81; 60%) and those who were not involved (117 of 226; 52%; P = 0.176). Two-thirds of respondents supported targeted PrEP availability on the NHS (217 of 279; 78%) rather than making it freely available to all, which only 9% supported (24 of 281). The majority of those supporting PrEP availability in the UK outside of a clinical trial felt that it should be targeted to GMSM with acute rectal sexually transmitted infections (STIs) (121 of 166; 73%), to couples for conception (128 of 166; 77%) and to GMSM in monogamous serodiscordant relationships (103 of 166; 62%), with fewer respondents preferring to target PrEP to other groups such as injecting drug users (49 of 166; 29%). Figure 1 illustrates attitudes to PrEP overall and Table 3 details attitudes to PrEP by support for availability outside a clinical trial. Attitudes are presented as positive statements in Table 3 for ease of comparison, but in their original form in Supplementary Table S1. Overall, participants had positive attitudes about support from the gay community for the availability of PrEP (84%), drug safety (67%), and having time to counsel patients (66%) and were not concerned about patients being stigmatized for being on PrEP (58%) or being wrongly perceived as being HIV positive (56%). The main concerns
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highlighted were prescribing without UK-specific guidance (80%), concern about funding diversion (55%), lack of confidence in real-world effectiveness (53%), and lack of confidence in patient adherence (23%). Of note, 118 of 282 (42%) felt that PrEP would result in risk compensation, compared with 91 of 282 (32%) who did not. The multivariate logistic model shows that the odds ratio for HCPs supporting PrEP availability outside a clinical trial was lowest when disagreeing with the statement ‘PrEP should be made widely available based on current evidence’ (Table 4), suggesting that this attitude was the greatest barrier to support for PrEP availability. HCPs who felt strongly about this also typically held concerns about whether ‘PrEP is an effective prevention tool in “real world” ’; these terms were correlated (correlation coefficient −0.66). The second greatest barrier was whether a HCP was ‘comfortable prescribing PrEP without UK-specific guidance’ although this was not statistically significant, followed by concerns that ‘patients will (not) adhere to daily PrEP’ and ‘risk of sexual or physical coercion for patients’ by sexual partners. Several other attitudes in Table 4 were important predictors in the univariate model, but not in the multivariate model. They were not highly correlated with other variables. Concern that patients will be wrongly perceived as
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Table 4 Odds of supporting pre-exposure prophylaxis (PrEP) availability outside a clinical trial if the respondent strongly disagreed with/disagreed with/was undecided about the attitude statement The odds ratio of supporting PrEP availability outside a clinical trial when strongly disagreeing or disagreeing with/undecided about the attitude statement*
Attitude statement PrEP should be widely available based on current evidence Comfortable prescribing PrEP without UK-specific guidance Patients will adhere to daily PrEP No risk of physical or sexual coercion on PrEP PrEP will not impact on funding of other prevention methods Time to engage in prevention counselling for PrEP PrEP effective prevention tool in ‘real world’ PrEP more effective than PEP for frequent PEP users PrEP will have greater impact than behavioural interventions on preventing HIV infection Lack of stigma for patients on PrEP Support from gay community and gay press for PrEP Patients won’t be perceived to be HIV positive by their partners PrEP will have a greater impact than testing and care on the HIV epidemic Truvada safe drug for PrEP PrEP will not lead to an increase in STIs Little impact of PrEP on ARV resistance
Univariate OR (95% CI)
Univariate P value
Multivariate OR (95% CI)
Multivariate P value
0.10 (0.06, 0.17) 0.44 (0.20, 1.00) 0.24 (0.14, 0.39) 0.43 (0.27, 0.67) 0.21 (0.08, 0.52) 0.53 (0.33, 0.85) 0.16 (0.08, 0.35) 0.35 (0.18, 0.67) 0.40 (0.25, 0.64)
< 0.001 0.051 < 0.001 < 0.001 < 0.001 0.008 < 0.001 0.001 < 0.001
0.13 (0.07, 0.26) 0.35 (0.12, 1.00) 0.38 (0.20, 0.74) 0.42 (0.21, 0.86) 0.43 (0.13, 0.39) 0.54 (0.29, 1.00) 0.61 (0.24, 1.51) 0.71 (0.29, 1.73) 0.73 (0.38, 1.39)
< 0.001 0.051 0.005 0.017 0.160 0.051 0.291 0.450 0.341
1.36 (0.86, 2.13) 0.78 (0.13, 4.76) 1.69 (1.07, 2.65) 0.32 (0.14, 0.83)
0.185 0.789 0.024 0.019
0.98 (0.48, 1.99) 0.75 (0.06, 9.09) 0.93 (0.47, 1.86) 1.02 (0.31, 3.33)
0.960 0.818 0.842 0.971
0.49 (0.17, 1.39) 0.73 (0.45, 1.20) 0.38 (0.22, 0.64)
0.180 0.230 < 0.001
1.23 (0.30, 4.99) 1.45 (0.73, 2.86) 1.45 (0.65, 3.21)
0.772 0.293 0.360
Significant values are shown in bold. ARV, antiretroviral; CI, confidence interval; OR, odds ratio; PEP, post-exposure prophylaxis. *In the logistic regression analysis, the odds ratio (OR) is the odds of supporting PrEP availability outside a clinical trial compared with the odds of not supporting PrEP availability outside a clinical trial where respondents strongly disagreed or disagreed with the attitude. For example, participants were 83% less likely to support PrEP availability outside a clinical trial if they disagreed with/strongly disagreed with/were undecided about the attitude that PrEP should be widely available based on current evidence, compared with those who agreed or strongly agreed with that attitude in the multivariate analysis.
Table 5 Practice of pre-exposure prophylaxis (PrEP) Professional group [n (%)]
PROUD clinic [n (%)]
Question
Response
Overall [n (%)]
Doctors
Health advisers
Nurses
P value
Yes
No
P value
Asked about PrEP by patients in past year
No Yes Missing 0 1–5 6–10 > 10 Missing
130 (47) 147 (53) 51 27 (19) 87 (60) 9 (6) 22 (15) 2
73 (46) 87 (54) 0 19 (22) 48 (55) 6 (7) 14 (16) 0
22 (43) 29 (57) 0 7 (24) 16 (55) 1 (3) 5 (17) 0
25 (60) 17 (40) 2 1 (6) 12 (71) 2 (12) 2 (12) 0
0.218
14 (19) 61 (81) 0 3 (5) 32 (52) 7 (11) 19 (31) 0
116 (57) 86 (43) 0 24 (29) 55 (65) 2 (2) 3 (4) 2
< 0.001
Number of times asked about PrEP in past year
being HIV positive was significant in the univariate, but not multivariate model and was correlated with concerns about stigma (correlation coefficient 0.63).
0.667
< 0.001
The majority of respondents had been asked about PrEP by GMSM (120 of 147; 82%), compared with 36% who had been asked about it by heterosexual serodiscordant couples and 35% for conception.
Practice of PrEP Over half (147 of 277; 53%) of respondents had been asked about PrEP by their patients in the past year (Table 5). This proportion was highest in PROUD clinics (61 of 75; 81%), but of note almost half of respondents from non-PROUD clinics had also been asked about PrEP (86 of 202; 43%).
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Pre-exposure prophylaxis (PrEP) and post-exposure prophylaxis (PEP) More respondents had discussed taking or had prescribed PEP in the past year (255 of 275; 93%) compared with PrEP. Just over half (152 of 273; 56%) believed that PrEP
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would be a more effective prevention option than PEP for frequent PEP users compared with only 49 of 273 (18%) who did not agree.
Discussion Key results This is the first study of HCPs’ KAP of PrEP in the UK. It reports a high level of perceived knowledge of PrEP, but equipoise for PrEP availability outside of a clinical trial. Despite the highest perceived knowledge of PrEP, support was lowest among doctors, who would be taking responsibility for prescribing and monitoring safety. This may reflect doctors’ familiarity with the studies on PrEP, where adherence was variable and the impact of risk compensation may not reflect behaviours in the real world. It may also reflect doctors’ concerns about transferability of efficacy study findings to the ‘real world’ where adherence may differ. The awareness of the BASHH/BHIVA recommendation that PrEP be used within the context of clinical studies was also greater among doctors. Our findings are generally consistent with those of other studies of HCPs who reported willingness to prescribe PrEP, but had residual concerns regarding safety, resistance, efficacy and cost [16,18–21]. Among Italian HCPs, 69% reported adequate knowledge of PrEP [16], and this percentage was highest among those who were actively involved in HIV education and care. Awareness of PrEP trial results was higher among USA survey respondents than seen in our study [19,20]. This may be attributable to the published guidance on prescribing PrEP in the USA and highlights the need for greater awareness of evidence around PrEP among HCPs in the UK. The main barriers to supporting PrEP availability outside a clinical trial in our study were concerns about current evidence, real-world effectiveness of PrEP, lack of UK-specific guidance, adherence and the risk of sexual or physical coercion for patients to have higher risk sex (e.g. condomless or with an HIV-positive partner) by partners. These concerns will hinder roll-out if not addressed. Realworld effectiveness data from open-label and demonstration studies, longer term monitoring of PrEP uptake and risk compensation and a clear UK-specific implementation guideline will go some way to alleviating these concerns. A major barrier to roll-out of PrEP was the concern about implementing PrEP without UK-specific guidance. This is unsurprising given the strong ethos of guidelinedriven sexual health clinical practice in the UK. However, doctors were less concerned about the need for UK-specific guidance, and this may reflect their experience in prescribing PEP off-licence. Clear UK-specific implementation
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guidance within a clinical and funding framework may also address the high level of concern expressed about funding diversion from other prevention strategies to PrEP if guidelines are able to demonstrate cost-effectiveness of a PrEP strategy. It is interesting that respondents remain concerned about the real-world effectiveness of PrEP despite strong evidence to support its biological efficacy and early guidance and later endorsement by the Centers for Disease Control and Prevention and the World Health Organization (WHO). This concern may reflect the lack of European population data, the wide diversity in adherence to PrEP across the different RCTs, and the lack of long-term PrEP data to demonstrate significant ‘real-world’ impact. Concerns about adherence are unsurprising given the importance of adherence for efficacy highlighted by PrEP trials. More recent data from iPrEx Open-Label Extension, published after this survey, suggest high levels of adherence to PrEP in an open-label, but not real-world, setting [22]. Qualitative interviews with USA providers have identified similar doubts to those of participants in this study, about patients’ ability to adhere to a drug for prevention and the required frequent clinic visits [23–25]. Our survey also highlights ongoing concerns about risk compensation and selection pressure on antiretroviral drug resistance, in line with but to a lesser degree than other studies [16,20]. Data from the open-label extension of the Partners PrEP study demonstrate no risk compensation [26] based on self-reported behaviour and STIs; however, these participants were introduced to PrEP under intensive placebo-controlled trial conditions. To date, there are no open-label randomized controlled data available among GMSM populations taking PrEP addressing the impact of risk compensation on effectiveness. There are good data from randomized placebo-controlled trials of PrEP to suggest that PrEP will have little impact on antiretroviral drug resistance and any PrEP education programme should address this concern among HCPs. Drug resistance has in general only been observed in those who were seroconverting at baseline while taking PrEP. This included low-level M184 resistance, which disappeared 24 months after stopping the drug [27]. Data from the FEMPrEP study showed PrEP selected resistance, but this was infrequent [28]. Although modelling studies suggest that there may be a small increase in antiretroviral drug resistance associated with PrEP roll-out, it is unlikely to be a major contributor to antiretroviral resistance [29]. The urgency of UK-specific guidance on PrEP is underscored by the high proportion of respondents in our survey who have already been asked about PrEP by patients outside of the PROUD pilot study. Although reported use of PrEP is low in community surveys [30], the level of interest
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has been high [31,32]. These surveys were conducted before the PROUD study started, and the results of our survey suggest that community awareness of PrEP has increased. Given the pressures on the UK sexual health budget, respondents’ concerns about the diversion of funding from other HIV prevention and treatment initiatives is unsurprising, and is shared by their USA counterparts [19]. Finally, although HCPs who had concerns about PrEP cited the possibility of coercion of patients by sexual partners, only a small proportion of respondents were concerned about their patients being stigmatized for taking PrEP, in contrast to reports from demonstration study participants in the USA [33]. PrEP-related stigma in the US studies included peer stigma concerning PrEP leading to increased risk-taking behaviour, PrEP diverting resources away from HIV-positive people, and clinicians’ judgemental attitudes towards the decision to use PrEP. It will be important to explore this issue among GMSM who have actual experience of PrEP in England.
Limitations There were several limitations to our survey. Firstly, our response rate was low but similar to that reported in similar surveys [16,20] and the respondents were a representative sample of sexual health practitioners, both geographically and in terms of HIV burden. Technical problems meant that the survey was initially unavailable online for a short period of time, which may have deterred potential respondents from taking part. Therefore, the results of this survey are not fully representative of HCP attitudes to and practice of PrEP in England. At the SSHA conference, some participants may have completed the questionnaire after a presentation on PrEP, so their responses may not be indicative of knowledge before the conference. Nonetheless, as this survey was carried out during the first year of the first UK PrEP study, it provides important baseline data on HCPs’ KAP of PrEP. Time and financial constraints precluded qualitative interviews to inform our survey. The survey was guided by the Puro et al. study, which used focus groups to develop the questionnaire and was conducted in Italy where PrEP is also not widely available. We were unable to test the validity of the multiscale items using a test–retest method, however inter-reliability testing using Cronbach’s alpha demonstrated internal consistency. Although the response rate was low, we exceeded our target sample of 265. In our sample size calculation, we assumed that support would be similar to that in the Italian survey and that 70% of respondents would agree with PrEP being available in the UK outside a clinical trial. Support was lower than this at 54%, and only 41% among doctors.
© 2015 British HIV Association
Participants were asked to self-rate their knowledge of PrEP on a scale of high, medium and low. These categories are subjective, and may be subject to response bias and influenced by gender, profession and professional experience. Therefore, the gender difference in self-rated knowledge could be reflective of gender differences in rating knowledge rather than true differences in knowledge [34]. Finally, despite testing the questionnaire for ambiguities prior to roll-out, some questions may have been interpreted differently by respondents to the survey objectives. For example, when asking about physical or sexual coercion, the survey intended to ask about risk to patients of coercion from sexual partners to have higher risk sex. However, this could have been misinterpreted as coercion to use PrEP. This lack of clarity was not, however, noted by respondents in the survey comments.
Conclusions There is modest support among HCPs for PrEP availability outside a clinical trial, in particular targeted to GMSM, suggesting that they see the need and are willing to add this new technology to existing risk reduction packages. However, there are residual concerns that need to be explored before PrEP roll-out will have universal support, especially around availability based on current evidence, adherence, physical or sexual coercion and the need for UK-specific guidance. Despite some differences by profession, barriers to PrEP were expressed across the board and will need to be addressed through collection of UK-specific data so that PrEP can be targeted to maximize public health benefit. Results from the PROUD study will be published in 2015 and will explore effectiveness and many of these issues in a ‘real-world’ setting. Informed by these data, detailed UK-specific modelling of the transmission dynamics of HIV in the UK is required to assess the impact of any risk compensation and ‘real-life’ variations in adherence on the cost-effectiveness of a PrEP programme in England. Such data are vital to informing a national PrEP policy and guidance. The urgency to collect this information increases as community awareness and engagement gather momentum.
Acknowledgements Thanks to the participants who completed the survey, the British HIV Association (BHIVA), the British Association for Sexual Health and HIV (BASHH), the Society of Sexual Health Advisers (SSHA) and GUMNet for distributing the survey.
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Conflicts of interest: The authors have no conflicts of interest to declare. Funding: No funding was received for this study.
Author contribitions MD conceived the study, designed the survey tool, wrote the protocol, performed data analysis and wrote the first draft of the paper. MG conceived the study and contributed to writing the protocol, designing the survey tool and writing the paper. DD contributed to designing the survey and writing the paper and performed data analyses. SM contributed to designing the survey, writing the survey and writing the paper. AN contributed to designing the survey, writing the protocol and writing the paper.
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7 Aghaizu ABA, Nardone A, Gill ON, Delpech VC, contributors. HIV in the United Kingdom 2013 Report: Data to End 2012. London, Public Health England, 2013. 8 National Institute for Health and Clinical Excellence. Increasing the Uptake of HIV Testing Among Men Who Have Sex with Men. London, NICE, 2011. 9 Krakower D, Mayer KH. Engaging healthcare providers to implement HIV pre-exposure prophylaxis. Curr Opin HIV Aids 2012; 7: 593–599. 10 Public Health England. STI Data Tables for England 2013. Table 5: All STI Diagnoses and Services by Gender and Sexual Risk, 2009 to 2013. London, Public Health England, 2014. 11 van der Straten A, Van Damme L, Haberer JE, Bangsberg DR. Unraveling the divergent results of pre-exposure prophylaxis trials for HIV prevention. AIDS 2012; 26:
Data sharing statement Extra data are available by e-mailing the corresponding author, MD.
Ethics
F13–F19. doi: 10.1097/QAD.0b013e3283522272. 12 Golub SA, Kowalczyk W, Weinberger CL, Parsons JT. Preexposure prophylaxis and predicted condom use among high-risk men who have sex with men. J Acquir Immune Defic Syndr 2010; 54: 548–555. doi: 10.1097/QAI.0b013e3181e19a54. 13 Hurt CB, Eron JJ Jr, Cohen MS. Pre-exposure prophylaxis
The survey was reviewed by Public Health England’s Research and Development Office and was determined to be a service evaluation involving healthcare workers, and thus not requiring ethical approval.
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and antiretroviral resistance: HIV prevention at a cost? Clin Infect Dis 2011; 53: 1265–1270. doi: 10.1093/cid/cir684. 14 Horberg M, Raymond B. Financial policy issues for HIV preexposure prophylaxis: cost and access to insurance. Am J Prev Med 2013; 44 (1 Suppl 2): S125–S128. doi: 10.1016/j.amepre.2012.09.039, S0749-3797(12)00696-4 [pii]. 15 McCormack S, Fidler S, Fisher M. The British HIV Association/British Association for Sexual Health and HIV Position Statement on pre-exposure prophylaxis in the UK. Int J STD AIDS 2012; 23: 1–4. doi: 10.1258/ijsa.2011.051211. 16 Puro V, Palummieri A, De Carli G, Piselli P, Ippolito G. Attitude towards antiretroviral pre-exposure prophylaxis (PrEP) prescription among HIV specialists. BMC Infect Dis 2013; 13: 217. 17 Health Policy & Economic Research Unit. National Survey of GP Opinion 2011. London, British Medical Association, 2011. 18 Tripathi A, Ogbuanu C, Monger M, Gibson JJ, Duffus WA. Preexposure prophylaxis for HIV infection: healthcare providers’ knowledge, perception, and willingness to adopt future implementation in the southern US. South Med J 2012; 105: 199–206. doi: 10.1097/SMJ.0b013e31824f1a1b, 00007611–201204000-00005 [pii]. 19 Mimiaga MJ, White JM, Krakower DS, Biello KB, Mayer KH. Suboptimal awareness and comprehension of published preexposure prophylaxis efficacy results among physicians
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study. Secondary Drug resistance among HIV-1 seroconverters in the FEM-PrEP study. 2012. Available at http://www.informedhorizons.com/resistance2012/pdf/ Presentations/Liegler.pdf. 29 Abbas UL, Hood G, Wetzel AW, Mellors JW. Factors influencing the emergence and spread of HIV drug resistance arising from rollout of antiretroviral pre-exposure prophylaxis (PrEP). PLoS ONE 2011; 6: e18165. doi: 10.1371/journal.pone.0018165. 30 Aghaizu A, Mercey D, Copas A, Johnson AM, Hart G, Nardone A. Who would use PrEP? Factors associated with intention to use among MSM in London: a community survey. Sex Transm Infect 2013; 89: 207–211. doi: 10.1136/sextrans-2012-050648. 31 Young I, Li J, McDaid L. Awareness and willingness to use HIV pre-exposure prophylaxis amongst gay and bisexual men in Scotland: implications for biomedical HIV prevention. PLoS ONE 2013; 8: e64038. doi: 10.1371/journal.pone.0064038. 32 SIGMA Research. The Sigma Panel Insight Blast 6: Prospective Attitudes to HIV Pre-Exposure Prophylaxis (PrEP). London, SIGMA Research, 2011. 33 Liu A, Cohen S, Follansbee S et al. Early experiences implementing pre-exposure prophylaxis (PrEP) for HIV prevention in San Francisco. PLoS Med 2014; 11: e1001613. 34 Hayes BC, Tariq VN. Gender differences in scientific knowledge and attitudes toward science: a comparative study of four Anglo-American nations. Public Underst Sci 2000; 9: 433–447. doi: 10.1088/0963-6625/9/4/306.
Supporting Information Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1 Attitudes to PrEP questionnaire responses with univariate and multivariate association with support for PrEP outside a clinical trial.
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ORIGINAL RESEARCH
Healthcare providers’ knowledge of, attitudes to and practice of pre-exposure prophylaxis for HIV infection M Desai,1,2 M Gafos,1 D Dolling,1 S McCormack1 and A Nardone2 and on behalf of the PROUD study 1 Clinical Trials Unit, Medical Research Council, London, UK and 2HIV/STI Department, Public Health England, London, UK Objectives
Pre-exposure prophylaxis (PrEP) has proven biological efficacy in reducing the risk of sexual acquisition of HIV. Healthcare providers’ (HCPs) knowledge of and attitudes to PrEP will be key to successful implementation. In England, PrEP is only available to men who have sex with men (MSM) through the open-label randomized PROUD pilot study of immediate or deferred use. Methods
In September 2013, a cross-sectional survey of UK HCPs distributed through sexual health clinics (219) and professional societies’ email lists (2599) and at a conference (80) asked about knowledge of, attitudes to and practice of PrEP. Results
Overall, 328 of 2898 (11%) completed the survey, of whom 160 of 328 (49%) were doctors, 51 (16%) sexual health advisers (SHAs), 44 (14%) nurses and 73 (22%) unspecified. Over a quarter (83 of 311; 27%) were involved in PROUD. Most respondents (260 of 326; 80%) rated their knowledge of PrEP as medium or high. Over half of respondents (166 of 307; 54%) thought PrEP should be available outside of a clinical trial. The main barriers to supporting PrEP availability outside a clinical trial were concerns about current evidence (odds ratio [OR] 0.13), lack of UK-specific guidance (OR 0.35), concerns about adherence (OR 0.38) and risk of sexual or physical coercion for patients to have condomless or higher risk sex (OR 0.42 in multivariate regression). Just over half (147 of 277; 53%) had been asked about PrEP by patients in the past year, including almost half of those working in a clinic not involved in the PROUD study (86 of 202; 43%). Conclusions
There is support for PrEP availability outside a clinical trial, but HCPs have residual concerns about its effectiveness and negative consequences, and the absence of UK-specific implementation guidance. Keywords: HIV, health services research, prevention Accepted 8 May 2015
sexual HIV acquisition [1] based on several placebocontrolled randomized trials [2–4]. Gay and other men having sex with men (GMSM) are most likely to acquire HIV infection in the UK. In 2013, the highest number of new HIV diagnoses (3250) ever reported among men who have sex with men (MSM) in England was recorded [5]. Three-fifths of MSM in the UK with a viral load compatible with onward transmission do not know that they have HIV infection [6]. Onward transmission risk could be
Introduction In 2012, the US Food and Drugs Administration approved the use of daily Truvada (tenofovir and emtricitabine) as pre-exposure prophylaxis (PrEP) to reduce the risk of
Correspondence: Dr Monica Desai, HIV & STI Department, CIDSC, Public Health England, 61 Colindale Ave, London NW9 5EQ, UK. Tel: 077 9516 0205; fax: 020 7670 4659; e-mail: [email protected]
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mitigated by adherence to annual or quarterly HIV testing, as recommended by national guidelines [7,8], combined with a universal offer of treatment. However, individuals at higher risk of HIV infection through frequent partner change or exposure to HIV within and outside of partnerships need additional tools to reduce the risk of acquiring and transmitting HIV. PrEP is a tool that reduces HIV infection risk and encourages regular testing and engagement with sexual health services, underscoring the potential for a large impact on the UK epidemic. Healthcare providers (HCPs) will be essential in the wider implementation of PrEP as a biomedical intervention [9]. While a few studies have assessed HCPs’ knowledge of, attitudes to and practice (KAP) of PrEP, none have been carried out in the UK. Sexual health is managed by a network of over 200 openaccess free clinics in the UK, with approximately 113 000 GMSM attendances in 2013 [10]. To roll out PrEP in this setting, evidence of effectiveness (as opposed to efficacy) and understanding of how to appropriately target PrEP, support adequate adherence [11], mitigate risk compensation [12], limit the emergence of drug resistance [13] and limit funding diversion from other prevention activities are required [14]. In the UK, ad hoc prescribing is discouraged in order to collect this evidence in a timely manner through clinical research [15]. The PROUD pilot study in England explores some of these issues through an open-label design randomizing eligible GMSM to receive daily oral tenofovir/emtricitabine immediately or after 12 months (www.proud.mrc.ac.uk). We conducted a cross-sectional KAP survey of PrEP among UK HCPs in order to inform the possible wider implementation of PrEP as an HIV prevention intervention.
Methods Design We conducted an anonymous cross-sectional survey of UK HCPs’ KAP of PrEP. Attitudes towards the evidence base, prescribing and clinical management, patient safety, prioritization and commissioning and provision of PrEP were examined (see web supplement for survey tool). HCP attitudes to post-exposure prophylaxis (PEP) were also examined given that PrEP availability may impact on PEP use and experiences with PEP may influence attitudes to PrEP. The study used similar domains to those used by Puro et al. in a survey of Italian HCPs [16]. The survey was developed in-house and reviewed for ambiguities by six HCPs prior to roll-out. The survey was available in paper or online using Select Survey® (ClassApps, Kansas City, Missouri, USA) format depending on participant preference.
© 2015 British HIV Association
Participant recruitment Between September and November 2013, sexual HCPs working in the UK who see HIV-negative patients were recruited via email through three professional societies: the British HIV Association (BHIVA), the British Society for HIV and Sexual Health (BASHH) and the Society of Sexual Health Advisers (SSHA). SSHA members were also recruited at their conference on 21 September 2013 and via social media using the SSHA twitter feed. Sexual health nurses were also recruited via the Genitourinary Medicine Network (GUMNet), a sentinel network of 29 sexual health clinics, coordinated by Public Health England (PHE).
Data analysis All data analyses were performed in STATA version 10.1 (www.stata.com). Univariate analysis used a χ2 test of proportions or a two-tailed Fisher’s exact test where numbers were less than five in any one group. Missing values were excluded from statistical analyses and the denominator for that group is presented in the results tables. Descriptive analysis explored missing data for systematic omission from a particular group. A large proportion (17%) did not report profession; a sensitivity analysis assessed the impact of this group on the survey results. Multi-item scales asked questions about attitudes to the evidence base, prescribing and clinical management, patient safety, prioritization and commissioning and provision of PrEP. Attitudes were ranked from the most negative to the most positive attitudes to PrEP for all respondents, and according to whether or not they supported use of PrEP outside a clinical trial. Univariate and multivariate logistic regression analysis was used to assess which attitudes were barriers to PrEP availability. Polychoric correlation examined explanatory variables for correlation. Free text responses were quantified and coded. Clinic name responses were matched to Local Authority diagnosed HIV prevalence using data from the Health Protection Agency 2011 and HIV Scotland (http://www.hpa.org.uk/ webc/HPAwebFile/HPAweb_C/1228207184991,http://www .hivscotland.com/data-and-research/regional-statistics/).
Sample size We assumed that 70% of participants would believe that PrEP should be available in the UK outside of a clinical trial, similar to support of PrEP in the Puro study [16]. Because a lower bound of < 50% support would be important, we set a confidence width of 20% and estimated that a sample size of 265 participants was required, assuming a
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response rate of 30%. Previous online surveys of medical providers have achieved response rates of 20–50% [17].
Table 1 Respondent demographics
n (%)
Consent and ethics The survey was reviewed by PHE’s Research and Development Office and was determined to be a service evaluation involving healthcare workers, and thus not requiring ethical approval.
Results Respondent demographics Eleven per cent (328 of 2898; 11.3%) of those sampled returned the survey. Of the 328 respondents, 234 responded from the professional societies, 51 from GUMNet clinics, 34 from the SSHA conference and nine from other sources (e.g. sent a link by a colleague). The response rate was 23% (51 of 219) from GUMNet clinics, 9% (234 of 2599) from the professional societies and 43% (34 of 80) from the conference sample. Over half of respondents (160 of 272; 59%) were doctors, 51 of 272 (19%) were SHAs, 44 of 272 (16%) were nurses and 17 of 272 (6%) were of other professions (Table 1). Approximately a quarter of respondents (83 of 211; 27%) were involved in the PROUD pilot study. Over half of respondents were female (175 of 272; 64%) and the majority (178 of 272; 65%) were over 40 years of age. Almost all respondents worked in a sexual health clinic (250 of 270; 93%) and over half (94 of 177; 53%) worked in clinics located in a high (> 2 per 1000 population aged 15–59 years) diagnosed HIV prevalence area. Respondents were from 97 different sexual health clinics across England, Wales and Scotland. Fifty-six participants (17%) did not complete any of the demographic questions. Of these, a similar proportion (4%) accessed the survey from each of the three sources or did not state where they accessed the survey. This group had been asked about both PrEP and PEP by patients less often than those who stated their profession. However, their responses to all other questions did not affect the sensitivity analysis for profession.
Knowledge of PrEP Over three-quarters of respondents (260 of 326; 80%) rated their knowledge of PrEP as medium or high. More doctors rated their knowledge as medium or high (144/160; 90%) than either nurses (27 of 44; 61%) or SHAs (36 of 51; 71%; P < 0.001) (Table 2). Among those rating their knowledge as high or medium, 71% (175 of 247) felt that they knew enough about PrEP to have an informed discussion with
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Gender Male Female Missing Age < 29 years 30–39 years 40–49 years 50–59 years > 60 years Missing Profession Doctor Health adviser Nurse Other Missing Time working in sexual health/HIV < 1 year 1–5 years 6–15 years > 15 years Missing Place of work Sexual health Other Missing Diagnosed HIV prevalence of sexual health clinic local authority (per 1000 aged 15–59 years) < 1 per 1000 1–2 per 1000 > 2 per 1000 Missing Involved in PROUD pilot study Yes Doctors Health advisers Nurses Other No Missing
Total number
97 (36) 175 (64) 56
272
13 (5) 81 (30) 94 (35) 71 (26) 13 (5) 56
272
272 160 (59) 51 (19) 44 (16) 17 (6) 56 5 (2) 56 (21) 123 (45) 88 (32) 56
272
250 (93) 20 (7) 58
270
44 (25) 39 (22) 94 (53) 151
177
83 (27) 45 (17) 15 (6) 12 (5) 11 (5) 228 (73) 17
311 255
311
patients, and this percentage was significantly higher among doctors (116 of 131; 89%) compared with nurses (17 of 33; 52%) and SHAs (18 of 33; 55%; P < 0.001). A higher proportion of male respondents rated their knowledge of PrEP as high or medium (88 of 97; 91%) compared with female respondents (131 of 175; 75%; P = 0.002). The difference in high/medium self-rated knowledge between genders was seen among doctors (97% of male versus 86% of female doctors; P = 0.029), but was nonsignificant among SHAs (90% of male versus 53% of female SHAs; P = 0.062) and nurses (70% of male versus 71% of female nurses; P = 1.000). However, there was no difference in self-rated high/medium knowledge of PrEP when comparing age groups, with 153 of 188 respondents
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Table 2 Reported knowledge of pre-exposure prophylaxis (PrEP) Professional group [n (%)]
Question
Response
Overall [n (%)]
Doctors
Health advisers
Nurses
P-values
How would you rate your knowledge of PrEP?
High Medium Low Never heard of it Missing No Yes Missing No Yes Missing
90 (28) 170 (52) 60 (18) 6 (2) 2 71 (23) 240 (77) 17 132 (42) 179 (58) 17
63 (39) 81 (51) 15 (9) 1 (1) 0 39 (24) 121 (76) 0 43 (27) 117 (73) 0
6 (12) 30 (59) 15 (29) 0 (0) 0 4 (8) 47 (92) 0 33 (65) 18 (35) 0
5 (11) 22 (50) 13 (30) 4 (9) 0 11 (25) 33 (75) 0 26 (59) 18 (41) 0
< 0.001
Aware of PROUD study
Know enough about PrEP to have informed discussion with patients
0.022
< 0.001
Table 3 Healthcare providers’ attitudes to pre-exposure prophylaxis (PrEP) by support for PrEP availability outside a clinical trial*
Attitude statement PrEP should be widely available based on current evidence Comfortable prescribing PrEP without UK-specific guidance Patients will adhere to daily PrEP No risk of physical or sexual coercion on PrEP PrEP will not impact on funding of other prevention methods Time to engage in prevention counselling for PrEP PrEP effective prevention tool in ‘real world’ PrEP more effective than PEP for frequent PEP users PrEP will have greater impact than behavioural interventions on preventing HIV infection Lack of stigma for patients on PrEP Support from gay community and gay press for PrEP Patients won’t be perceived to be HIV positive by their partners PrEP will have a greater impact than testing and care on the HIV epidemic Truvada safe drug for PrEP PrEP will not lead to an increase in STIs Little impact of PrEP on ARV resistance
HCPs who support PrEP availability outside clinical trial (%)
HCPs who do not support PrEP availability outside clinical trial (%)
Positive attitude
Undecided
Negative attitude
Positive attitude
Undecided
Negative attitude
61 15 33 61 20 76 32 66 39
32 10 42 33 39 13 29 22 28
31 75 24 6 42 11 38 11 33
31 5 10 36 7 62 8 48 17
26 26 33 46 8 31 20 33 44
43 69 57 18 85 7 72 19 39
64 86 66 13
23 12 24 21
13 2 10 66
44 81 49 5
31 17 33 6
25 2 19 89
73 36 30
23 26 50
4 38 20
55 17 7
18 29 23
27 54 70
ARV, antiretroviral; HCP, healthcare provider; PEP, post-exposure prophylaxis; STI, sexually transmitted infection. *Attitudes have been ordered by greatest to the least barrier to PrEP availability in multivariate regression analysis.
(81%) < 50 years old and 66 of 84 (78%) ≥ 50 years old rating their knowledge as high/medium (P = 0.621). Most doctors (129 of 160; 81%) had read the BASHH/ BHIVA position statement on PrEP, but significantly fewer SHAs (22 of 51; 43%) and nurses (16 of 44; 36%) had done so (P < 0.001). Of the randomized controlled trials (RCTs) conducted to test PrEP efficacy, participants were most familiar with the results of iPrEx (high or medium knowledge, 153 of 312; 49%) and least familiar with the VOICE (81 of 312; 26%) and CDC-TDF2 (272 of 312; 23%) studies. The majority of participants were aware of the PROUD study (240 of 311; 77%), even if they were not directly
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involved (157 of 228; 69%), and this was broadly similar among groups accessing the survey from each of the different sources.
Attitudes to PrEP Half of respondents (166 of 307; 54%; 95% CI 48–60%) thought that PrEP should be available in the UK outside of a clinical trial (Table 3), and this proportion was higher among nurses (29 of 44; 66%; 95% CI 50–80%) and SHAs (37 of 51; 73%; 95% CI 58–84%) than doctors (66 of 160; 41%; 95% CI 34–49%; P < 0.001). There was no difference
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Healthcare workers' atudes to PrEP
137
Posive atude towards PrEP Undecided Negave atude towards PrEP
PrEP will have a greater impact than tesng and care on the HIV epidemic Comfortable prescribing PrEP without UK specific guidance PrEP will not impact on funding of other prevenon methods PrEP effecve prevenon tool in ‘real world’ Lile impact of PrEP on ARV resistance Paents will adhere to daily PrEP PrEP will have greater impact than behavioural intervenons on prevenng HIV… PrEP will not lead to an increase in STIs PrEP should be widely available based on current evidence No risk of physical or sexual coercion on PrEP PrEP more effecve than PEP for frequent PEP users Paents not perceived to be HIV posive if taking PrEP Lack of sgma for paents on PrEP Time to engage in prevenon counseling for PrEP Truvada safe drug for PrEP Support from gay community and gay press for PrEP
0%
10%
20%
30%
40%
50%
60%
70%
80%
90% 100%
Fig. 1 Healthcare providers’ attitudes to pre-exposure prophylaxis (PrEP) overall. ARV, antiretroviral; PEP, post-exposure prophylaxis; STI, sexually transmitted infection.
in support for provision outside a clinical trial between those involved in the PROUD study (49 of 81; 60%) and those who were not involved (117 of 226; 52%; P = 0.176). Two-thirds of respondents supported targeted PrEP availability on the NHS (217 of 279; 78%) rather than making it freely available to all, which only 9% supported (24 of 281). The majority of those supporting PrEP availability in the UK outside of a clinical trial felt that it should be targeted to GMSM with acute rectal sexually transmitted infections (STIs) (121 of 166; 73%), to couples for conception (128 of 166; 77%) and to GMSM in monogamous serodiscordant relationships (103 of 166; 62%), with fewer respondents preferring to target PrEP to other groups such as injecting drug users (49 of 166; 29%). Figure 1 illustrates attitudes to PrEP overall and Table 3 details attitudes to PrEP by support for availability outside a clinical trial. Attitudes are presented as positive statements in Table 3 for ease of comparison, but in their original form in Supplementary Table S1. Overall, participants had positive attitudes about support from the gay community for the availability of PrEP (84%), drug safety (67%), and having time to counsel patients (66%) and were not concerned about patients being stigmatized for being on PrEP (58%) or being wrongly perceived as being HIV positive (56%). The main concerns
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highlighted were prescribing without UK-specific guidance (80%), concern about funding diversion (55%), lack of confidence in real-world effectiveness (53%), and lack of confidence in patient adherence (23%). Of note, 118 of 282 (42%) felt that PrEP would result in risk compensation, compared with 91 of 282 (32%) who did not. The multivariate logistic model shows that the odds ratio for HCPs supporting PrEP availability outside a clinical trial was lowest when disagreeing with the statement ‘PrEP should be made widely available based on current evidence’ (Table 4), suggesting that this attitude was the greatest barrier to support for PrEP availability. HCPs who felt strongly about this also typically held concerns about whether ‘PrEP is an effective prevention tool in “real world” ’; these terms were correlated (correlation coefficient −0.66). The second greatest barrier was whether a HCP was ‘comfortable prescribing PrEP without UK-specific guidance’ although this was not statistically significant, followed by concerns that ‘patients will (not) adhere to daily PrEP’ and ‘risk of sexual or physical coercion for patients’ by sexual partners. Several other attitudes in Table 4 were important predictors in the univariate model, but not in the multivariate model. They were not highly correlated with other variables. Concern that patients will be wrongly perceived as
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Table 4 Odds of supporting pre-exposure prophylaxis (PrEP) availability outside a clinical trial if the respondent strongly disagreed with/disagreed with/was undecided about the attitude statement The odds ratio of supporting PrEP availability outside a clinical trial when strongly disagreeing or disagreeing with/undecided about the attitude statement*
Attitude statement PrEP should be widely available based on current evidence Comfortable prescribing PrEP without UK-specific guidance Patients will adhere to daily PrEP No risk of physical or sexual coercion on PrEP PrEP will not impact on funding of other prevention methods Time to engage in prevention counselling for PrEP PrEP effective prevention tool in ‘real world’ PrEP more effective than PEP for frequent PEP users PrEP will have greater impact than behavioural interventions on preventing HIV infection Lack of stigma for patients on PrEP Support from gay community and gay press for PrEP Patients won’t be perceived to be HIV positive by their partners PrEP will have a greater impact than testing and care on the HIV epidemic Truvada safe drug for PrEP PrEP will not lead to an increase in STIs Little impact of PrEP on ARV resistance
Univariate OR (95% CI)
Univariate P value
Multivariate OR (95% CI)
Multivariate P value
0.10 (0.06, 0.17) 0.44 (0.20, 1.00) 0.24 (0.14, 0.39) 0.43 (0.27, 0.67) 0.21 (0.08, 0.52) 0.53 (0.33, 0.85) 0.16 (0.08, 0.35) 0.35 (0.18, 0.67) 0.40 (0.25, 0.64)
< 0.001 0.051 < 0.001 < 0.001 < 0.001 0.008 < 0.001 0.001 < 0.001
0.13 (0.07, 0.26) 0.35 (0.12, 1.00) 0.38 (0.20, 0.74) 0.42 (0.21, 0.86) 0.43 (0.13, 0.39) 0.54 (0.29, 1.00) 0.61 (0.24, 1.51) 0.71 (0.29, 1.73) 0.73 (0.38, 1.39)
< 0.001 0.051 0.005 0.017 0.160 0.051 0.291 0.450 0.341
1.36 (0.86, 2.13) 0.78 (0.13, 4.76) 1.69 (1.07, 2.65) 0.32 (0.14, 0.83)
0.185 0.789 0.024 0.019
0.98 (0.48, 1.99) 0.75 (0.06, 9.09) 0.93 (0.47, 1.86) 1.02 (0.31, 3.33)
0.960 0.818 0.842 0.971
0.49 (0.17, 1.39) 0.73 (0.45, 1.20) 0.38 (0.22, 0.64)
0.180 0.230 < 0.001
1.23 (0.30, 4.99) 1.45 (0.73, 2.86) 1.45 (0.65, 3.21)
0.772 0.293 0.360
Significant values are shown in bold. ARV, antiretroviral; CI, confidence interval; OR, odds ratio; PEP, post-exposure prophylaxis. *In the logistic regression analysis, the odds ratio (OR) is the odds of supporting PrEP availability outside a clinical trial compared with the odds of not supporting PrEP availability outside a clinical trial where respondents strongly disagreed or disagreed with the attitude. For example, participants were 83% less likely to support PrEP availability outside a clinical trial if they disagreed with/strongly disagreed with/were undecided about the attitude that PrEP should be widely available based on current evidence, compared with those who agreed or strongly agreed with that attitude in the multivariate analysis.
Table 5 Practice of pre-exposure prophylaxis (PrEP) Professional group [n (%)]
PROUD clinic [n (%)]
Question
Response
Overall [n (%)]
Doctors
Health advisers
Nurses
P value
Yes
No
P value
Asked about PrEP by patients in past year
No Yes Missing 0 1–5 6–10 > 10 Missing
130 (47) 147 (53) 51 27 (19) 87 (60) 9 (6) 22 (15) 2
73 (46) 87 (54) 0 19 (22) 48 (55) 6 (7) 14 (16) 0
22 (43) 29 (57) 0 7 (24) 16 (55) 1 (3) 5 (17) 0
25 (60) 17 (40) 2 1 (6) 12 (71) 2 (12) 2 (12) 0
0.218
14 (19) 61 (81) 0 3 (5) 32 (52) 7 (11) 19 (31) 0
116 (57) 86 (43) 0 24 (29) 55 (65) 2 (2) 3 (4) 2
< 0.001
Number of times asked about PrEP in past year
being HIV positive was significant in the univariate, but not multivariate model and was correlated with concerns about stigma (correlation coefficient 0.63).
0.667
< 0.001
The majority of respondents had been asked about PrEP by GMSM (120 of 147; 82%), compared with 36% who had been asked about it by heterosexual serodiscordant couples and 35% for conception.
Practice of PrEP Over half (147 of 277; 53%) of respondents had been asked about PrEP by their patients in the past year (Table 5). This proportion was highest in PROUD clinics (61 of 75; 81%), but of note almost half of respondents from non-PROUD clinics had also been asked about PrEP (86 of 202; 43%).
© 2015 British HIV Association
Pre-exposure prophylaxis (PrEP) and post-exposure prophylaxis (PEP) More respondents had discussed taking or had prescribed PEP in the past year (255 of 275; 93%) compared with PrEP. Just over half (152 of 273; 56%) believed that PrEP
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would be a more effective prevention option than PEP for frequent PEP users compared with only 49 of 273 (18%) who did not agree.
Discussion Key results This is the first study of HCPs’ KAP of PrEP in the UK. It reports a high level of perceived knowledge of PrEP, but equipoise for PrEP availability outside of a clinical trial. Despite the highest perceived knowledge of PrEP, support was lowest among doctors, who would be taking responsibility for prescribing and monitoring safety. This may reflect doctors’ familiarity with the studies on PrEP, where adherence was variable and the impact of risk compensation may not reflect behaviours in the real world. It may also reflect doctors’ concerns about transferability of efficacy study findings to the ‘real world’ where adherence may differ. The awareness of the BASHH/BHIVA recommendation that PrEP be used within the context of clinical studies was also greater among doctors. Our findings are generally consistent with those of other studies of HCPs who reported willingness to prescribe PrEP, but had residual concerns regarding safety, resistance, efficacy and cost [16,18–21]. Among Italian HCPs, 69% reported adequate knowledge of PrEP [16], and this percentage was highest among those who were actively involved in HIV education and care. Awareness of PrEP trial results was higher among USA survey respondents than seen in our study [19,20]. This may be attributable to the published guidance on prescribing PrEP in the USA and highlights the need for greater awareness of evidence around PrEP among HCPs in the UK. The main barriers to supporting PrEP availability outside a clinical trial in our study were concerns about current evidence, real-world effectiveness of PrEP, lack of UK-specific guidance, adherence and the risk of sexual or physical coercion for patients to have higher risk sex (e.g. condomless or with an HIV-positive partner) by partners. These concerns will hinder roll-out if not addressed. Realworld effectiveness data from open-label and demonstration studies, longer term monitoring of PrEP uptake and risk compensation and a clear UK-specific implementation guideline will go some way to alleviating these concerns. A major barrier to roll-out of PrEP was the concern about implementing PrEP without UK-specific guidance. This is unsurprising given the strong ethos of guidelinedriven sexual health clinical practice in the UK. However, doctors were less concerned about the need for UK-specific guidance, and this may reflect their experience in prescribing PEP off-licence. Clear UK-specific implementation
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guidance within a clinical and funding framework may also address the high level of concern expressed about funding diversion from other prevention strategies to PrEP if guidelines are able to demonstrate cost-effectiveness of a PrEP strategy. It is interesting that respondents remain concerned about the real-world effectiveness of PrEP despite strong evidence to support its biological efficacy and early guidance and later endorsement by the Centers for Disease Control and Prevention and the World Health Organization (WHO). This concern may reflect the lack of European population data, the wide diversity in adherence to PrEP across the different RCTs, and the lack of long-term PrEP data to demonstrate significant ‘real-world’ impact. Concerns about adherence are unsurprising given the importance of adherence for efficacy highlighted by PrEP trials. More recent data from iPrEx Open-Label Extension, published after this survey, suggest high levels of adherence to PrEP in an open-label, but not real-world, setting [22]. Qualitative interviews with USA providers have identified similar doubts to those of participants in this study, about patients’ ability to adhere to a drug for prevention and the required frequent clinic visits [23–25]. Our survey also highlights ongoing concerns about risk compensation and selection pressure on antiretroviral drug resistance, in line with but to a lesser degree than other studies [16,20]. Data from the open-label extension of the Partners PrEP study demonstrate no risk compensation [26] based on self-reported behaviour and STIs; however, these participants were introduced to PrEP under intensive placebo-controlled trial conditions. To date, there are no open-label randomized controlled data available among GMSM populations taking PrEP addressing the impact of risk compensation on effectiveness. There are good data from randomized placebo-controlled trials of PrEP to suggest that PrEP will have little impact on antiretroviral drug resistance and any PrEP education programme should address this concern among HCPs. Drug resistance has in general only been observed in those who were seroconverting at baseline while taking PrEP. This included low-level M184 resistance, which disappeared 24 months after stopping the drug [27]. Data from the FEMPrEP study showed PrEP selected resistance, but this was infrequent [28]. Although modelling studies suggest that there may be a small increase in antiretroviral drug resistance associated with PrEP roll-out, it is unlikely to be a major contributor to antiretroviral resistance [29]. The urgency of UK-specific guidance on PrEP is underscored by the high proportion of respondents in our survey who have already been asked about PrEP by patients outside of the PROUD pilot study. Although reported use of PrEP is low in community surveys [30], the level of interest
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has been high [31,32]. These surveys were conducted before the PROUD study started, and the results of our survey suggest that community awareness of PrEP has increased. Given the pressures on the UK sexual health budget, respondents’ concerns about the diversion of funding from other HIV prevention and treatment initiatives is unsurprising, and is shared by their USA counterparts [19]. Finally, although HCPs who had concerns about PrEP cited the possibility of coercion of patients by sexual partners, only a small proportion of respondents were concerned about their patients being stigmatized for taking PrEP, in contrast to reports from demonstration study participants in the USA [33]. PrEP-related stigma in the US studies included peer stigma concerning PrEP leading to increased risk-taking behaviour, PrEP diverting resources away from HIV-positive people, and clinicians’ judgemental attitudes towards the decision to use PrEP. It will be important to explore this issue among GMSM who have actual experience of PrEP in England.
Limitations There were several limitations to our survey. Firstly, our response rate was low but similar to that reported in similar surveys [16,20] and the respondents were a representative sample of sexual health practitioners, both geographically and in terms of HIV burden. Technical problems meant that the survey was initially unavailable online for a short period of time, which may have deterred potential respondents from taking part. Therefore, the results of this survey are not fully representative of HCP attitudes to and practice of PrEP in England. At the SSHA conference, some participants may have completed the questionnaire after a presentation on PrEP, so their responses may not be indicative of knowledge before the conference. Nonetheless, as this survey was carried out during the first year of the first UK PrEP study, it provides important baseline data on HCPs’ KAP of PrEP. Time and financial constraints precluded qualitative interviews to inform our survey. The survey was guided by the Puro et al. study, which used focus groups to develop the questionnaire and was conducted in Italy where PrEP is also not widely available. We were unable to test the validity of the multiscale items using a test–retest method, however inter-reliability testing using Cronbach’s alpha demonstrated internal consistency. Although the response rate was low, we exceeded our target sample of 265. In our sample size calculation, we assumed that support would be similar to that in the Italian survey and that 70% of respondents would agree with PrEP being available in the UK outside a clinical trial. Support was lower than this at 54%, and only 41% among doctors.
© 2015 British HIV Association
Participants were asked to self-rate their knowledge of PrEP on a scale of high, medium and low. These categories are subjective, and may be subject to response bias and influenced by gender, profession and professional experience. Therefore, the gender difference in self-rated knowledge could be reflective of gender differences in rating knowledge rather than true differences in knowledge [34]. Finally, despite testing the questionnaire for ambiguities prior to roll-out, some questions may have been interpreted differently by respondents to the survey objectives. For example, when asking about physical or sexual coercion, the survey intended to ask about risk to patients of coercion from sexual partners to have higher risk sex. However, this could have been misinterpreted as coercion to use PrEP. This lack of clarity was not, however, noted by respondents in the survey comments.
Conclusions There is modest support among HCPs for PrEP availability outside a clinical trial, in particular targeted to GMSM, suggesting that they see the need and are willing to add this new technology to existing risk reduction packages. However, there are residual concerns that need to be explored before PrEP roll-out will have universal support, especially around availability based on current evidence, adherence, physical or sexual coercion and the need for UK-specific guidance. Despite some differences by profession, barriers to PrEP were expressed across the board and will need to be addressed through collection of UK-specific data so that PrEP can be targeted to maximize public health benefit. Results from the PROUD study will be published in 2015 and will explore effectiveness and many of these issues in a ‘real-world’ setting. Informed by these data, detailed UK-specific modelling of the transmission dynamics of HIV in the UK is required to assess the impact of any risk compensation and ‘real-life’ variations in adherence on the cost-effectiveness of a PrEP programme in England. Such data are vital to informing a national PrEP policy and guidance. The urgency to collect this information increases as community awareness and engagement gather momentum.
Acknowledgements Thanks to the participants who completed the survey, the British HIV Association (BHIVA), the British Association for Sexual Health and HIV (BASHH), the Society of Sexual Health Advisers (SSHA) and GUMNet for distributing the survey.
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Conflicts of interest: The authors have no conflicts of interest to declare. Funding: No funding was received for this study.
Author contribitions MD conceived the study, designed the survey tool, wrote the protocol, performed data analysis and wrote the first draft of the paper. MG conceived the study and contributed to writing the protocol, designing the survey tool and writing the paper. DD contributed to designing the survey and writing the paper and performed data analyses. SM contributed to designing the survey, writing the survey and writing the paper. AN contributed to designing the survey, writing the protocol and writing the paper.
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7 Aghaizu ABA, Nardone A, Gill ON, Delpech VC, contributors. HIV in the United Kingdom 2013 Report: Data to End 2012. London, Public Health England, 2013. 8 National Institute for Health and Clinical Excellence. Increasing the Uptake of HIV Testing Among Men Who Have Sex with Men. London, NICE, 2011. 9 Krakower D, Mayer KH. Engaging healthcare providers to implement HIV pre-exposure prophylaxis. Curr Opin HIV Aids 2012; 7: 593–599. 10 Public Health England. STI Data Tables for England 2013. Table 5: All STI Diagnoses and Services by Gender and Sexual Risk, 2009 to 2013. London, Public Health England, 2014. 11 van der Straten A, Van Damme L, Haberer JE, Bangsberg DR. Unraveling the divergent results of pre-exposure prophylaxis trials for HIV prevention. AIDS 2012; 26:
Data sharing statement Extra data are available by e-mailing the corresponding author, MD.
Ethics
F13–F19. doi: 10.1097/QAD.0b013e3283522272. 12 Golub SA, Kowalczyk W, Weinberger CL, Parsons JT. Preexposure prophylaxis and predicted condom use among high-risk men who have sex with men. J Acquir Immune Defic Syndr 2010; 54: 548–555. doi: 10.1097/QAI.0b013e3181e19a54. 13 Hurt CB, Eron JJ Jr, Cohen MS. Pre-exposure prophylaxis
The survey was reviewed by Public Health England’s Research and Development Office and was determined to be a service evaluation involving healthcare workers, and thus not requiring ethical approval.
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Supporting Information Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1 Attitudes to PrEP questionnaire responses with univariate and multivariate association with support for PrEP outside a clinical trial.
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