Provider Attitudes Toward Oral Preexposure Prophylaxis for HIV Prevention Among High-Risk Men Who Have Sex with Men in Lima,Peru

Abstract

Oral preexposure prophylaxis (PrEP) was the first biomedical intervention to demonstrate efficacy in preventing HIV infection among men who have sex with men (MSM). Healthcare providers' attitudes toward PrEP will be critical in translating this finding into effective public health rollout programs. In a convenience sample of 186 healthcare providers in Peru, we assessed knowledge, barriers, and attitudes to prescribe and monitor HIV PrEP for high-risk MSM and transgender women, the populations with the highest HIV incidence in this setting. A total of 57.5% reported awareness of PrEP, and awareness was independently associated with caring for more than 50 MSM (OR: 3.67, p<0.002). Lack of local guidelines, concern about increased high-risk behavior, antiretroviral drug resistance, and limited availability of antiretrovirals for HIV-infected individuals were the most common barriers to prescribing PrEP. Of all physicians 44.6% indicated that they would be likely to prescribe oral PrEP now; likelihood to prescribe was higher if PrEP were supported by local guidelines (70.3%, p<0.001), if more trials supported its effectiveness (68.5%, p<0.001), and if intermittent use were shown to be effective (62.2%, p=0.019). Physicians were more likely to prescribe PrEP now if they care for more than 50 MSM (OR: 6.62, p=0.010). Infectious disease specialists were less likely to prescribe PrEP (OR: 0.10, p=0.003) than nonspecialists. Successful large-scale implementation of PrEP in Peru will require focused educational campaigns to increase awareness and address concerns among healthcare providers.

Introduction

HIV-1 infection continues to spread among vulnerable populations despite the availability of several behavioral interventions such as voluntary counseling and testing and the promotion of condom use. The effectiveness of these interventions for reducing risk behavior has been demonstrated in some settings¹ but not in others,² and HIV incidence remains high even in settings with fully implemented condom promotion policies. In Peru, while the prevalence and incidence of HIV in the general population are only 0.5%³ and 0.03%,⁴ respectively, men who have sex with men (MSM) and transgender women (TGW) experience rates that are comparable to those reported among heterosexual populations in sub-Saharan Africa.^5

–8 As in many other settings, MSM and TGW in Peru are in great need of effective and easy to implement prevention strategies.

In late 2010, the landmark proof-of-concept iPrEx trial was the first biomedical intervention shown to be efficacious in preventing HIV infection among MSM and TGW. The study demonstrated 44% efficacy in preventing HIV infection using daily oral co-formulated emtricitabine/tenofovir disoproxyl fumarate (FTC/TDF) as preexposure prophylaxis (PrEP).⁹ Self-reported compliance was high (≥89% at week 4), but plasma drug concentration collected in a subset of participants suggested that actual adherence was probably lower. Adherence was low in some sites outside the United States (U.S.), raising many questions about applicability to diverse populations, the critical importance of adherence counseling and monitoring, optimal dosing intervals, and method of delivery.¹⁰ Whereas different studies among MSM and TGW are either planned or in progress to assess these questions,^11

–16 other studies are trying to translate positive PrEP findings into programmatic priorities to address the need to identify and implement innovative evidence-based HIV prevention strategies.^{17

–26}

In addition to advocacy from populations at risk and governmental support of public health rollout programs, two critical aspects of a successful prevention program include a high-risk population willing to use such a method and providers willing to prescribe and monitor it. Given the magnitude of the HIV epidemic in Peru, MSM and TGW would benefit from access to PrEP. Although awareness of PrEP has been low among MSM and TGW, there is general enthusiasm about and interest in this HIV prevention method both in Peru and in other settings.^27

–30 Healthcare providers who are knowledgeable about PrEP and are comfortable prescribing it are also going to be a critical component of a successful PrEP implementation program since they would serve as a source of information for individuals at risk, provide counseling and testing, and be ready to ensure monitoring of potential side effects.³¹

Literature about provider attitudes toward PrEP and willingness to prescribe PrEP is limited and pertains primarily to U.S.-based physicians. Recent data demonstrated that the majority of Massachusetts providers would be willing to prescribe PrEP if further studies show high efficacy and no evidence of risk compensation, drug toxicity, or development of antiretroviral resistance among users.³² However, not much is known as to whether similar attitudes are prevalent among providers in developing settings, including Peru; reports are limited to qualitative studies with only a small number of providers.³³ In Peru, co-formulated FTC/TDF (marketed as Truvada) is not yet available for treatment of HIV, and its use for prevention is still far off. This presents a window of opportunity to examine provider attitudes and address potential barriers to prescribing Truvada for PrEP in anticipation of its availability and subsequent approval.

A one-time survey was administered to assess healthcare providers' attitudes toward oral PrEP for MSM and TGW at highest risk of HIV acquisition. In addition, we aimed to describe the concerns and barriers that would prevent healthcare practitioners from discussing or prescribing PrEP to these high-risk populations.

Materials and Methods

Participants and procedures

From March 2012 through July 2012, a convenience sample of 186 providers was recruited in Lima, Peru from a variety of sources: attendees of a national conference on HIV (69.9% of responders); healthcare institutions and organizations (30.1%), including IMPACTA and VIA LIBRE (HIV research non-governmental organizations—NGOs), EPICENTRO (a community-based organization for MSM), hospitals of the Ministry of Health and social security system, and urban sexually transmitted infection (STI) healthcare centers. Responders included healthcare providers and professionals with diverse experience working with individuals at risk for or living with HIV. A self-administered 40-question paper-based survey and an informed consent form (in Spanish) were distributed.

Eligibility criteria included age ≥18 years and working in a healthcare setting with patients with or at risk for HIV in Lima, Peru. Overall, approximately 700 surveys were distributed and 186 were completed for a response rate of 27%. No financial compensation was given for completing the survey.

The survey collected data on demographic characteristics (age, gender, occupation, level of training), type of practice, and number of MSM and HIV-positive patients cared for, as well as experience in prescribing antiretroviral treatment (ART), conducting HIV and STI testing, ART adherence counseling, and/or risk-reduction counseling as a part of their current job.

To assess awareness of oral PrEP, participants were asked: “Have you heard of PREEXPOSURE PROPHYLAXIS, which is the use of oral antiretrovirals taken BEFORE a high-risk exposure for the prevention of HIV acquisition?” In addition, physicians were asked whether they have ever prescribed PrEP to prevent HIV acquisition in MSM or TGW.

To evaluate potential barriers to prescribing PrEP, physicians were asked to rate on a scale from 0 (of little concern) to 10 (of extreme concern) how concerned they were about 10 issues such as access to medication, need for daily dosing, drug resistance, and risk behavior. Median score and interquartile range (IQR) were calculated for each barrier and then ranked.

Five questions were asked about the likelihood to prescribe PrEP now and under certain hypothetical situations: if the Ministry of Health of Peru approved guidelines for its use, if Truvada (FTC/TDF) or TDF alone had an indication for HIV prevention, if results of more clinical studies demonstrated efficacy for HIV prevention, and if it were shown that intermittent dosing before and after a high-risk sexual exposure is effective for the prevention of HIV. Likelihood to prescribe oral PrEP was assessed on a Likert scale from 0 (extremely unlikely) to 10 (extremely likely). Responses were dichotomized for analysis so that a response of 8 or higher was considered “likely to prescribe” and a response below 8 was considered “not likely to prescribe.” This cutoff was employed as it was used in similar studies on PrEP attitudes³⁴ and was considered a conservative estimate of a physician's likelihood to prescribe PrEP.

All participants provided written informed consent before participation. The study protocol and informed consent form were approved by both the Asociación Civil Impacta Salud y Educación and Columbia University Medical Center Institutional Review Boards in compliance with all applicable Peru and U.S. federal regulations governing the protection of human participants.

Statistical analysis

Responses were entered into an electronic database. Mann–Whitney U test and Chi-square or Fisher's exact tests were used to assess associations between variables. In the analysis evaluating factors associated with barriers to and likelihood of prescribing PrEP, only responses from physicians were used. To determine independent factors associated with provider awareness of or likelihood to prescribe PrEP in different scenarios, multivariable logistic regression analyses were conducted using backward stepwise elimination with the Wald test, including in the preliminary models only those variables that were significant at the p<0.20 level in the univariate analysis as well as responses on each of the potential barriers to prescribing PrEP. Multivariable analyses yielded odds ratio (OR) and 95% confidence intervals (CI). Friedman's test was used to determine if there were differences among various concerns rated by physicians. McNemar's test was used to assess differences between the likelihood of prescribing PrEP now versus prescribing PrEP under different hypothetical scenarios. All the above analyses were conducted using Statistical Package for the Social Sciences version 19.0 (SPSS Inc., Chicago, IL). All tests were two-sided and statistical significant associations were defined as p<0.05.

Results

The majority of participants were younger than 40 years old (51.1%), female (63.4%), mixed race (mestizo) (90.9%), and cared for fewer than 50 MSM (56.5%) and 50 HIV-positive (59.1%) patients (Table 1). Public hospitals were the most common place of practice (37.1%), followed by urban STI healthcare centers (17.7%) and NGOs (16.7%). Physicians constituted the greatest number of responders (40.3%), followed by nurses, midwives, and psychologists/counselors. Among physicians, slightly less than one-third were specialists in infectious diseases (ID), while the majority (68.0%) were general practitioners, internal medicine physicians, or physicians of another specialty. Those physicians who had at least 50 HIV patients in their practice were mostly ID specialists (69.6%).

Table 1.

Demographic Characteristics of Survey Responders

Characteristic	N=186
Age, years
20–29	27 (14.5)
30–39	68 (36.6)
40–49	64 (34.4)
50–59	27 (14.5)
Gender
Female	118 (63.4)
Male	67 (36.0)
Ethnicity
Mixed race (mestizo)	169 (90.9)
Other	16 (8.6)
Level of training/position
Physician^a	75 (40.3)
Nurse	49 (26.3)
Psychologist/counselor	21 (11.3)
Midwife	27 (14.5)
Other^b	13 (7.0)
Type of provider^c
General physician, internal medicine, or other specialty	51 (27.4)
Infectious disease physician	24 (12.9)
Principal role/responsibility at work^d
Prescription of antiretroviral treatment	32 (17.2)
Provision of adherence to antiretroviral treatment	46 (24.7)
Diagnosis and treatment of sexually transmitted infections	58 (31.2)
Provision of risk-reduction counseling	83 (44.6)
Type of practice^d
Ministry of Health (public) hospital	69 (37.1)
Social security system care center	7 (3.8)
Urban sexually transmitted infection healthcare center	33 (17.7)
Non-governmental organization	31 (16.7)
Private practice	12 (6.5)
Number of men who have sex with men patients
0	24 (12.9)
1–24	55 (29.6)
25–49	26 (14.0)
50–99	21 (11.3)
>99	32 (17.2)
Number of HIV-positive patients
0	15 (8.1)
1–24	68 (36.6)
25–49	27 (14.5)
50–99	14 (7.5)
>99	36 (19.4)

Includes generalists, residents in training, and specialists.

Includes biologists, pharmacists, dentists, medical students, technicians, and other clinic research staff.

Among all physicians.

Question had more than one option.

Data are no. (%) of subjects with characteristic. Total denominators varied slightly because of missing data.

Awareness of PrEP among all healthcare providers

A substantial proportion (57.5%) of healthcare providers had heard of oral PrEP (Table 2). Providers whose principal role was to prescribe ART, compared to others, were more likely to be aware of oral PrEP (81.3% vs. 53.7%, p=0.005). Providers caring for at least 50 MSM were more likely to be aware of PrEP than providers with fewer MSM in their practice (80.4% vs. 49.0%, p<0.001); similarly, providers caring for at least 50 HIV-positive patients were more likely to be aware of oral PrEP than their counterparts caring for fewer HIV infected patients (77.1% vs. 50.9%, p=0.003). Furthermore, ID physicians were more likely to have heard of oral PrEP than others physicians (83.3% vs. 54.9%, p=0.021).

Table 2.

Awareness of Preexposure Prophylaxis Among All Healthcare Providers

Characteristic	Heard of oral PrEP N (%)	p
Overall (N=186)	107 (57.5)
Age		0.903
20–29	15 (55.6)
30–39	39 (58.2)
40–49	36 (58.1)
50–59	17 (65.4)
Gender		0.161
Female	62 (54.4)
Male	44 (65.7)
Ethnicity		0.438
Mestizo	95 (57.6)
Other	11 (68.8)
Occupation		0.285
Physician	48 (64.0)
Non-physicians	59 (55.7)
Type of physician		0.021
ID specialist	20 (83.3)
Non-ID specialist	28 (54.9)
Principal role/responsibility at work
Prescription of antiretroviral treatment	26 (81.3)	0.005
Other role	79 (53.7)
Type of practice		0.872^a
Ministry of Health (public) hospital	40 (58.8)
Social security system care center	2 (28.6)
Urban sexually transmitted infection healthcare center	20 (62.5)
Non-governmental organization	26 (83.9)
Private practice	6 (54.5)
Number of MSM patients		<0.001
<50	51 (49.0)
50+	41 (80.4)
Number of HIV-positive patients		0.003
<50	56 (50.9)
50+	37 (77.1)

p-value calculated by comparing those practicing in public hospitals to those practicing in other institutions.

p-values are calculated for the difference between levels of each variable: e.g., between female and male providers.

PrEP, preexposure prophylaxis; MSM, men who have sex with men; ID, infectious disease.

In multivariable analysis, only caring for more than 50 MSM patients remained independently associated with awareness of oral PrEP (OR: 3.67, 95% CI: 1.63–8.27, p<0.002).

Barriers to prescribing PrEP among physicians

There were statistically significant differences in how physicians ranked their concerns about PrEP (p<0.001). The most common concerns about prescribing PrEP included the lack of formal Peru Ministry of Health guidelines regarding its use (median=9.0, IQR: 7.0–10.0), concern about increased high-risk behavior (median=8.0, IQR: 6.0–10.0), limited availability of antiretrovirals for people infected with HIV (median=8.0, IQR: 6.0–10.0), and risk of inducing antiretroviral drug resistance (median=8.0, IQR: 5.0–9.0) (Fig. 1). ID and non-ID physicians expressed similar concerns regarding prescribing PrEP, with the exception of the concern about inexperience managing antiretrovirals, which was higher among non-ID physicians (median=7.0, IQR: 5.5–9.0) than ID physicians (median=5.0, IQR: .75–8.0; p=0.017).

FIG. 1.

Concerns about prescribing oral preexposure prophylaxis (PrEP) by physicians in Lima, Peru. Seventy-five physicians were asked to rate on a scale (from 0 to 10) how concerned they were about the following potential barriers when considering prescribing PrEP. A median score was calculated for each category of concern. Shown are the median score (with IQR) for all physicians and infectious disease (ID) and non-ID physicians. *ID and non-ID physicians expressed similar concerns regarding prescribing PrEP, with the exception that ID physicians were less concerned about inexperience with prescribing antiretrovirals (ART) (p=0.017).

Likelihood of prescribing PrEP among physicians

Among the physicians who completed the survey, likelihood to prescribe oral PrEP at the time this survey was conducted was 44.6%. There was no difference in the likelihood to prescribe PrEP now than if Truvada (FTC/TDF) or TDF alone had an indication for the prevention of HIV acquisition (47.3%, p=0.832); however, likelihood to prescribe increased if PrEP for HIV prevention were supported by Peru Ministry of Health guidelines (70.3%, p<0.001), if more clinical trials supported its effectiveness (68.5%, p<0.001), and if intermittent use were shown to be effective (62.2%, p=0.019).

Likelihood to prescribe oral PrEP either now or under hypothetical scenarios differed with physician specialty and patient population. For example, likelihood to prescribe it now was lower among ID compared to non-ID specialists (29.2% vs. 52.0%, p=0.083). If Truvada (FTC/TDF) or TDF alone had an indication for HIV prevention and if more clinical trials supported its effectiveness, physicians caring for more than 50 HIV-positive patients would be more likely to prescribe PrEP compared to providers with fewer patients (69.6% vs. 37.0%, p=0.020 and 86.4% vs. 60.9%, p=0.049, respectively).

In multivariable analysis, ID compared to non-ID specialists were less likely to prescribe PrEP now (OR: 0.098, 95% CI: 0.02–0.45, p=0.003), while physicians with at least 50 MSM patients under their care had a higher likelihood of prescribing PrEP (OR: 6.62, 95% CI: 1.58–27.80, p=0.010). These differences disappeared under hypothetical situations that demonstrated support for the efficacy of PrEP or if external sources (such as the Ministry of Health) provided support for its use.

Interestingly, prescribers who indicated a high level of concern about the need for daily dosing were more likely to prescribe PrEP now (OR: 1.31, 95% CI: 1.02–1.67, p=0.036) if Truvada (FTC/TDF) or TDF alone had an indication for HIV prevention (OR: 1.38, 95% CI: 1.01–1.89, p=0.045), and if it were supported by guidelines from the Ministry of Health (OR: 1.31, 95% CI: 1.01–1.70, p=0.041). In multivariable analysis, increasing concerns for other barriers were also associated with the likelihood of prescribing PrEP under certain hypothetical scenarios (Table 3).

Table 3.

Factors Associated with Likelihood to Prescribe Preexposure Prophylaxis Now and Under Certain Hypothetical Scenarios Among Physicians

	Hypothetical scenarios
	Likely to prescribe PrEP now		Indication for HIV prevention		Use supported by MoH ^a guidelines		More clinical trials supporting effectiveness		Intermittent use shown to be effective
Variables	OR (95% CI)	p	OR (95% CI)	p	OR (95% CI)	p	OR (95% CI)	p	OR (95% CI)	p
Type of practice/specialty
ID specialist	0.10 (0.02–0.45)	0.003	—	—	—	—	—	—	—	—
>50 MSM^b under care	6.62 (1.58–27.80)	0.010	—	—	—	—	3.63 (0.96–13.77)	0.058	—	—
Concern about^a
Limited availability of ART^c for HIV treatment	1.25 (0.97–1.61)	0.081	—	—	—	—	—	—	1.22 (0.99–1.51)	0.062
Need for daily dosing	1.31 (1.02–1.67)	0.036	1.38 (1.01–1.89)	0.045	1.31 (1.01–1.70)	0.041	—	—	—	—
Access	—	—	1.76 (1.01–3.07)	0.048	1.78 (1.08–2.93)	0.023	—	—	—	—
Affordability	—	—	0.63 (0.39–1.03)	0.067	0.59 (0.35–0.99)	0.046	—	—	—	—
Lack of MoH^d guidelines	—	—	2.31 (1.23–4.35)	0.009	—	—	—	—	—	—
Inexperience with ART^c	—	—	—	—	1.19 (0.99–1.44)	0.069	—	—	1.20 (1.00–1.44)	0.049
Side effects	—	—	—	—	—	—	1.39 (1.06–1.81)	0.017	—	—

Expressed concerns for prescribing PrEP measured by asking physicians to rate on a scale from 0 to 10.

Men who have sex with men.

Antiretroviral treatment.

Peru Ministry of Health.

All variables remaining in the final multivariate regression models are reported. No adjustment was conducted to build these models.

Of note, only three physicians stated that they had previously prescribed PrEP to MSM or TGW, but no information on the antiretroviral PrEP regimen was obtained.

Discussion

To our knowledge, this is the first study to provide quantitative data about providers' awareness, attitudes, and experience regarding oral PrEP in a developing country. Among 186 Peruvian healthcare professionals, close to half of whom were physicians, awareness of oral PrEP was high at over 50%, but only a minority of physicians indicated a willingness to prescribe it at the time the survey was administered.

Awareness of PrEP was nearly 4-fold higher among healthcare providers with a larger MSM practice. This is not surprising, considering that MSM in Peru are a high-risk population for HIV infection, and healthcare providers caring for them are more likely to be aware of new HIV prevention methods that are targeted for this community. In particular, they may be more familiar with the iPrEx study and its scientific community education efforts conducted in the city (36% of the entire sample size of the iPrEx study was enrolled in Lima⁹).

Interestingly, although awareness of PrEP was higher among ID compared to non-ID specialists, likelihood to prescribe at the time the study was conducted was lower among specialists. This may be because ID physicians, who often see sicker HIV-positive patients and have more experience prescribing ART, are more concerned about adherence and long-term side effects of PrEP. These issues may make them less willing to use antiretrovirals freely in HIV-negative patients, compared to generalists who may desire to take advantage of this additional opportunity to prevent HIV infection in their patients. Moreover, those who cared for a significant number of MSM patients were almost 7-fold more likely to prescribe PrEP, and potentially saw it as an important new tool to prevent the spread of HIV in this heavily affected community.

For those who were likely to prescribe PrEP now or under hypothetical scenarios (if there were an indication for Truvada as PrEP, or if there were formal guidelines from the Ministry of Health), there was high concern about the need for daily use. Although mathematical modeling suggests that it may be sufficient to take oral PrEP two or three times a week with the same efficacy,³⁵ evidence from clinical studies to date suggests that oral PrEP will work only with daily adherence. Physicians who are willing to prescribe PrEP understand the importance of daily dosing, which will be critical to emphasize when counseling patients about adherence to this intervention.

Previous qualitative studies conducted among a small number of providers in Peru reported that the most important and commonly mentioned barriers were access to PrEP among high-risk groups, cost-effectiveness, adherence, and side effects.³³ Our data, in contrast, demonstrate that the greatest concerns to prescribing oral PrEP were lack of formal guidelines from the Peruvian Ministry of Health, limited availability of antiretrovirals for those already infected with HIV, increase in risky sexual behavior, and development of drug resistance. Potential side effects were of least concern to our responders. Surveys conducted among U.S. and Canadian providers reported a similar level of concern about the development of ART resistance, but much less concern about risk compensation than noted in our study.^32,36,37 In fact, one survey among New York City providers showed that risk compensation and limited availability of antiretrovirals for HIV-positive patients were of least concern among a list of 11 potential barriers to prescribing PrEP.³⁷

As a developing country with an increasing prevalence of HIV, Peru has only a limited amount of antiretrovirals for HIV-positive individuals, let alone HIV-negative individuals; thus, Peruvian providers may be less likely to prescribe relatively scarce drugs to at-risk patients. However, certain hypothetical scenarios, such as the introduction of normative guidelines or more data supporting the efficacy of PrEP, appeared to increase the likelihood of prescribing oral PrEP among all physicians. For example, if the Ministry of Health provided guidelines for use of PrEP, 70.3% of physicians would be likely to prescribe it. Support from the Ministry of Health could help alleviate concerns about the lack of availability of antiretrovirals for HIV-infected patients since physicians may feel they are getting approval from the government that PrEP is a cost-effective use of limited resources. In addition, formal guidelines about regular HIV testing, risk reduction counseling, and monitoring around PrEP could help address ways to reduce the development of drug resistance and minimize risk compensation, as has been done in the U.S.³⁸ Differences between ID and non-ID specialists' willingness to prescribe PrEP disappeared under our hypothetical scenarios, suggesting that ID specialists may be waiting for more guidelines and clinical data about optimal dosing around high-risk exposure before prescribing it.

A few other countries' governments have already provided interim guidelines for the use of oral PrEP. In mid-July 2012, the U.S. Food and Drug Administration (U.S. FDA) approved Truvada (FTC/TDF) for oral PrEP,³⁹ and the World Health Organization (WHO),⁴⁰ the U.S. Centers for Disease Control and Prevention (U.S. CDC),³⁸ the British Association for Sexual Health and HIV (BASHH),⁴¹ as well as the South African HIV Clinicians Society (SA-HIV Society)⁴² have all published interim guidelines recommending FTC/TDF-based PrEP as a useful strategy to enhance the effectiveness of a comprehensive HIV prevention strategy among populations at risk. Truvada is not yet available commercially in Peru, but will be available in early 2014. So far, the Peruvian government has not issued guidelines regarding the use of PrEP among high-risk populations, although limited data suggest that Peruvian national policymakers may support the introduction of PrEP among individuals at risk for HIV infection.³³ Furthermore, other data show that a strategic PrEP intervention that is rapidly scaled and targets groups at highest risk (MSM and TGW) could be a cost-effective intervention in Peru.²⁶ When Truvada becomes available, the Ministry of Health will likely recommend its use in treatment, but not prevention. However, our study suggests that official Peru Ministry of Health support of PrEP would lead to an increase in PrEP prescribing practices.

One important note is that the U.S. FDA approved Truvada toward the end of our study. Only six participants (including two physicians) took our survey shortly after the FDA's approval. However, the information about new guidelines and indications from the U.S. FDA are likely to take longer to reach providers in Peru and are thus less likely to affect their opinions right away. These respondents were more likely influenced by data from iPrEx, which recruited heavily from Peru and demonstrated that daily adherence of FTC/TDF was effective in MSM. Even so, our data suggest that FTC/TDF having an indication for HIV prevention would not increase the likelihood that physicians would prescribe PrEP.

One major limitation of our study is that we used a convenience sample, where most of those surveyed came to attend a national HIV conference and were more likely to be motivated to learn about new discoveries in the literature, and thus be better informed about HIV prevention methods. In addition, our response rate of 27% was low and included only 75 physicians. Those who were most interested in PrEP may have been more likely to respond, creating a selection bias. Furthermore, some healthcare providers in our study may have been involved in the iPrEx study since it heavily recruited from Lima. While we did not specifically ask respondents if they worked at an iPrEx site, only three physicians had stated that they had previously prescribed PrEP to MSM or TGW; thus, up to three physicians may have been directly involved in iPrEx. While this number is small (4.0% of all physicians surveyed), these factors together limit the generalizability of results to other healthcare professionals in Peru, and our sample may have overestimated the proportion of people who were aware of and prescribed PrEP. Another major limitation is that participants responded only to what they would likely do now and in certain hypothetical situations, not what they actually did. Answers to our survey questions may serve as only a weak proxy for what providers would do in real-life situations when faced with patients at high risk for HIV infection.

Our results highlight the importance of effective educational campaigns that will be needed to increase awareness and address concerns of PrEP among providers and healthcare professionals. Prior to a successful large-scale implementation of PrEP to prevent the transmission of HIV in Peru, healthcare providers must be knowledgeable about PrEP, be willing to counsel their at-risk patients about it, and prescribe and monitor its use over time. Our study suggests that more clinical trials and approval by the Peruvian government may increase physicians' willingness to prescribe PrEP. Only then will PrEP contribute to an effective comprehensive HIV preventive strategy that will be necessary to achieve incremental reductions in the incidence of HIV among high-risk MSM and TGW living in Peru.

Footnotes

Acknowledgments

The authors would like to acknowledge all of the participants as well as the Asociación Civil Impacta Salud y Educación (IMPACTA) staff without whom this study would not have been possible. This work was supported by a grant from the Doris Duke Charitable Foundation to Columbia University College of Physicians and Surgeons to fund International Clinical Research Fellow, Eric C. Tang and by unrestricted discretionary core funds from IMPACTA. The funding sources played no role in the study design, data collection, data analysis, data interpretation, writing of the manuscript, or the decision to submit the article for publication.

Author Disclosure Statement

No conflicts of interest are reported.

References

Coates

, Grinstead

, Gregorich

, et al.: Efficacy of voluntary HIV-1 counselling and testing in individuals and couples in Kenya, Tanzania, and Trinidad: A randomised trial. Lancet, 2000; 356:103–112.

Fonner

, Denison

, Kennedy

, O'Reilly

, and Sweat

: Voluntary counseling and testing (VCT) for changing HIV-related risk behavior in developing countries. Cochrane Database Syst Rev, 2012; 9:CD001224.

Carcamo

, Campos

, Garcia

, et al.: Prevalences of sexually transmitted infections in young adults and female sex workers in Peru: A national population-based survey. Lancet Infect Dis, 2012; 12:765–773.

Alarcón

, Pun

, Gutiérrez

, et al.: Estimación y Análisis de la Incidencia de VIH en Población Adulta del Perú: Resultados de la Aplicación del Modelo Matemático MoT. Rev Peru Med Exp Salud Pública, 2012; 29:452–460.

Sanchez

, Lama

, Peinado

, et al.: High HIV and ulcerative sexually transmitted infection incidence estimates among men who have sex with men in Peru: Awaiting an effective preventive intervention. JAIDS, 2009; 51:S47–S51.

Sanchez

, Lama

, Kusunoki

, et al.: HIV-1, sexually transmitted infections, and sexual behavior trends among men who have sex with men in Lima, Peru. JAIDS, 2007; 44:578–585.

Lama

, Lucchetti

, Suarez

, et al.: Association of herpes simplex virus type 2 infection and syphilis with human immunodeficiency virus infection among men who have sex with men in Peru. J Infect Dis, 2006; 194:1459–1466.

Lama

, Sanchez

, Suarez

, et al.: Linking HIV and antiretroviral drug resistance surveillance in Peru: A model for a third-generation HIV sentinel surveillance. JAIDS, 2006; 42:501–505.

Grant

, Lama

, Anderson

, et al.: Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med, 2010; 363:2587–2599.

10.

Poynten

, Zablostska

, and Grulich

: Considerations regarding antiretroviral chemoprophylaxis in MSM. Curr Opin HIV AIDS, 2012; 7:549–556.

11.

AIDS Vaccine Advocacy Coalition: Ongoing and Planned Pre-Exposure Prophylaxis (PrEP) Trials. Accessed at www.avac.org/ht/a/GetDocumentAction/i/3113 on March 21, 2013. AVAC, 2012.

12.

Division of AIDS (DAIDS), U.S. National Institute of Allergy and Infectious Diseases (NIAID), U.S. National Institute of Mental Health (NIMH), et al.: HPTN 067 The ADAPT study: A phase II, randomized, open-label, pharmacokinetic and behavioral study of the use of intermittent oral emtricitabine/tenofovir disoproxil fumarate pre-exposure prophylaxis (PrEP). South Africa, Thailand. Accessed at www.hptn.org/web%20documents/HPTN067/Protocol/067ProtocolV3_01Dec2011.pdf on June 6, 2013.

13.

French National Institute for Health and Medical Research-French National Agency for Research on AIDS and Viral Hepatitis (Inserm-ANRS) and Molina

: On demand antiretroviral pre-exposure prophylaxis for HIV in men who have sex with men (IPERGAY). France. Accessed at http://clinicaltrials.gov/show/NCT01473472 on June 6, 2013.

14.

National Institute of Allergy and Infectious Diseases (NIAID), HIV Prevention Trials Network, and Gulick RM: HPTN 069 NEXT-PReP: Phase II randomized, double-blind, study of safety and tolerability of maraviroc, maraviroc+entricitabine, maraviroc+tenofovir or tenofovir+emtricitabine for preexposure prophylaxis to prevent HIV transmission in at-risk men who have sex with men and in at-risk women. United States and Puerto Rico. Accessed at www.hptn.org/research_studies/HPTN069.asp#StudySummary on June 6, 2013.

15.

Mutua

, Sanders

, Mugo

, et al.: Safety and adherence to intermittent pre-exposure prophylaxis (PrEP) for HIV-1 in African men who have sex with men and female sex workers. PLoS One, 2012; 7:e33103.

16.

MRC Clinical Trials Unit, McCormack S, and Dunn D: PROUD Pre-exposure option for reducing HIV in the UK: and open-label randomisation to immediate or deferred daily Truvada for HIV negative gay men. United Kingdom. Accessed at www.ctu.mrc.ac.uk/plugins/StudyDisplay/protocols/PROUD%20protocol%20v1.1%2010September2012.pdf on June 6, 2013.

17.

iPrExOLE: iPrEx Open Label Extension. Brazil, Ecuador, Peru, South Africa, Thailand, and United States. Accessed at www.iprexole.com/1pages/aboutus/aboutus-whatisiprexole.php on March 21, 2013.

18.

National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), and San Francisco Department of Public Health (SFDPH): The DEMO project. United States. Accessed at www.sfdph.org/dph/files/newsMediadocs/2012PR/DemoProjectFINAL.pdf on June 6, 2013.

19.

California Collaborative Treatment Group, Morris

, and Moore

: CCTG 595: Text messaging to improve adherence to PrEP in high-risk MSM. United States. Accessed at http://clinicaltrials.gov/show/NCT01761643 on June 6, 2013.

20.

HIV Prevention Trials Network, Shoptaw

, Magnus

, et al.: HPTN 073 Black men who have sex with men (MSM) pre-exposure prophylaxis (PrEP). United States. Accessed at www.clinicaltrials.gov/show/NCT01808352 on June 6, 2013.

21.

Oswaldo Cruz Foundation and Grinsztejn B: Implementation of the pre-exposure prophylaxis (PrEP) to HIV: a demonstrative project (DemoPrEP). Brazil. Accessed at http://clinicaltrials.gov/show/NCT01989611 on December 28, 2013.

22.

National Institute of Mental Health and Underhill K: PrEP for HIV prevention in MSM: Mixed-methods study of behavior & message framing. United States. Accessed at http://cira.yale.edu/projects/prep-hiv-prevention-msm-mixed-methods-study-behavior-message-framing on June 6, 2013.

23.

Fenway Community Health and Mayer K: Pre-exposure prophylaxis adherence intervention for MSM (PrEPare). United States. Accessed at www.clinicaltrials.gov/show/NCT01632397 on June 6, 2013.

24.

Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) and Hosek

: An open label demonstration project and phase II safety study of pre-exposure prophylaxis use among 15 to 17 year old young men who have sex with men (YMSM). United States. Accessed at www.clinicaltrials.gov/show/NCT01769456 on June 6, 2013.

25.

Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) and Hosek

: An open label demonstration project and phase II safety study of pre-exposure prophylaxis. United States. Accessed at www.clinicaltrials.gov/show/NCT01772823 on June 6, 2013.

26.

Gomez

, Borquez

, Caceres

, et al.: The potential impact of pre-exposure prophylaxis for HIV prevention among men who have sex with men and transwomen in Lima, Perú: A mathematical modeling study. PLoS Med, 2012; 9:e1001323.

27.

Krakower

, Mimiaga

, Rosenberger

, et al.: Limited awareness and low immediate uptake of pre-exposure prophylaxis among men who have sex with men using an internet social networking site. PLoS One, 2012; 7:e33119.

28.

Eisingerich

, Wheelock

, Gomez

, Garnett

, Dybul

, and Plot

: Attitudes and acceptance of oral and parenteral HIV preexposure prophylaxis among potential user groups: A multinational study. PLoS One, 2012; 7:e28238.

29.

Galea

, Kinsler

, Salazar

, et al.: Acceptability of pre-exposure prophylaxis as an HIV prevention strategy: Barriers and facilitators to pre-exposure prophylaxis uptake among at-risk Peruvian populations. Int J STD AIDS, 2011; 22:256–262.

30.

Peinado

, Lama

, Galea

, et al.: Acceptability of oral versus rectal HIV preexposure prophylaxis among men who have sex with men and transgender women in Perú. J Int Assoc Provid AIDS Care, 2013; 12(4):278–283.

31.

Krakower

and Mayer

: Engaging healthcare providers to implement HIV pre-exposure prophylaxis. Curr Opin HIV AIDS, 2012; 7:593–599.

32.

White

, Mimiaga

, Krakower

, and Mayer

: Evolution of Massachusetts physician attitudes, knowledge, and experience regarding the use of antiretrovirals for HIV prevention. AIDS Pat Care STDs, 2012; 26:395–405.

33.

Wheelock

, Eisingerich

, Gomez

, Gray

, Dybul

, and Plot

: Views of policymakers, healthcare workers and NGOs on HIV pre-exposure prophylaxis (PrEP): A multinational qualitative study. BMJ Open, 2012; 2:e001234.

34.

Mimiaga

, Case

, Johnson

, Safren

, and Mayer

: Preexposure antiretroviral prophylaxis attitudes in high-risk Boston area men who report having sex with men: Limited knowledge and experience but potential for increased utilization after education. JAIDS, 2009; 50:77–83.

35.

Anderson

, Glidden

, Liu

, et al.: Emtricitabine-tenofovir concentrations and pre-exposure prophylaxis efficacy in men who have sex with men. Sci Transl Med, 2012; 4:151.

36.

Senn

, Wilton

, Sharma

, Fowler

, and Tan

: Knowledge of and opinions on HIV pre-exposure prophylaxis among front-line service providers at Canadian AIDS Service Organizations. AIDS Res Hum Retroviruses, 2013; 29(9):1183–1189.

37.

Kapur

, Tang

, Tieu

, Koblin

, Ellman

, and Sobieszczyk

: Knowledge, attitudes and willingness of New York City providers to prescribe oral pre-exposure prophylaxis (PrEP) for HIV prevention. XIX International AIDS Conference, Washington, DC, 2012. Abstract WEPE273.

38.

Centers for Disease Control and Prevention (CDC): Interim guidance: preexposure prophylaxis of the prevention of HIV Infection in men who have sex with men. MMWR Morb Mortal Wkly Rep, 2011; 60:65–68.

39.

U.S. Food and Drug Administration (USFDA): FDA approves first drug for reducing the risk of sexually acquired HIV infection. United States. Accessed at www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm312210.htm on March 21, 2013.

40.

World Health Organization (WHO): Guidance of oral pre-exposure prophylaxis (PrEP) for serodiscordant couples, men and transgender women who have sex with men at high risk of HIV: Recommendations for use in the context of demonstration projects. Switzerland. Accessed at http://apps.who.int/iris/bitstream/10665/75188/1/9789241503884_eng.pdf on March 21, 2013.

41.

McCormack

, Fidler

, and Fisher

: 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.

42.

Southern African HIV Clinicians Society Consensus Committee: Guidelines for the safe use of pre-exposure prophylaxis in men who have sex with men who are at risk for HIV infection. S Afri J HIV Med, 2012; 13:40–55.