Considerations for Implementing Oral Preexposure Prophylaxis: A Literature Review Timothy Joseph Sowicz, MSN, NP-C Anne M. Teitelman, PhD, FNP-BC, FAANP, FAAN Christopher Lance Coleman, PhD, MS, MPH, FAAN Bridgette M. Brawner, PhD, APRN Oral preexposure prophylaxis (PrEP) is in its infancy as an approved biomedical intervention; therefore, research is needed to understand the issues surrounding its implementation. The purpose of this literature review is to report the empirical research about PrEP to identify the salient issues surrounding its implementation. PubMed, Medline, and CINAHL databases were searched, yielding 45 articles meeting inclusion criteria for the review. Overall, we found patient awareness of PrEP varied and its use was low. Awareness was higher among providers. Patients were willing to use PrEP, but both patients’ and providers’ concerns may have impacted implementation of this intervention. PrEP requires a prescription, yet only five of the 45 articles addressed providerlevel factors. Research involving providers is needed to ensure that patient risk of becoming infected with HIV is accurately assessed, that PrEP is provided to those at high risk for HIV infection, and that frequent follow-up is conducted. (Journal of the Association of Nurses in AIDS Care, 25, 496-507) Copyright Ó 2014 Association of Nurses in AIDS Care Key words: HIV, oral preexposure prophylaxis, prevention

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pproximately 34 million people are infected with HIV globally (World Health Organization, 2013). In the United States alone, nearly 47,500 new HIV in-

fections occurred in 2010; the annual incidence rate has remained consistent since the 1990s despite behavioral and biomedical prevention interventions (Centers for Disease Control and Prevention [CDC], 2012a). Surveillance data have indicated that certain groups are disproportionately affected. For example, of all new HIV infections in the United States in 2010, 63% were among men who have sex with men (MSM; CDC, 2012a). Within the past decade, the HIV epidemic in young MSM (YMSM) has also become particularly disconcerting. More specifically, the number of new infections among YMSM increased by 22% from 2008 to 2010, and Black YMSM represented 55% of these cases (CDC, 2012a). These epidemiological trends highlight the

Timothy Joseph Sowicz, MSN, NP-C, is a doctoral student, University of Pennsylvania School of Nursing, Philadelphia, Pennsylvania. Anne M. Teitelman, PhD, FNP-BC, FAANP, FAAN, is the Patricia Bleznak Silverstein and Howard A. Silverstein Endowed Term Chair in Global Women’s Health Associate Professor of Nursing, University of Pennsylvania School of Nursing, Philadelphia, Pennsylvania. Christopher Lance Coleman, PhD, MS, MPH, FAAN, is a Fagin Term Associate Professor of Nursing and Multi-Cultural Diversity, Associate Professor of Nursing in Psychiatry, School of Medicine, University of Pennsylvania School of Nursing, Philadelphia, Pennsylvania. Bridgette M. Brawner, PhD, APRN, is an Assistant Professor of Nursing, University of Pennsylvania School of Nursing, Philadelphia, Pennsylvania, USA.

JOURNAL OF THE ASSOCIATION OF NURSES IN AIDS CARE, Vol. 25, No. 6, November/December 2014, 496-507 http://dx.doi.org/10.1016/j.jana.2014.07.005 Copyright Ó 2014 Association of Nurses in AIDS Care

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need for new HIV prevention strategies, with special emphasis on overly burdened groups. Biomedical interventions such as condoms (Weller & Davis, 2002), medical male circumcision (Siegfried, Muller, Deeks, & Volmink, 2009), and treatment as prevention (Cohen et al., 2011) are known to reduce the incidence of HIV infection, yet HIV remains a persistent public health threat. Recently, preexposure prophylaxis (PrEP)—the use of daily oral antiretroviral medications by uninfected persons—was approved for use in adults as a biomedical HIV prevention intervention. Whereas several factors will contribute to the long-term success (or lack thereof) of this new strategy, ultimately, PrEP efficacy hinges on two key components: (a) patients taking, and consistently adhering to, the medication; and (b) providers accurately assessing HIV risk, educating patients, and prescribing the medication. Successful implementation and maintenance of PrEP will require thoughtful consideration of patientand provider-level factors that will facilitate and/or obstruct PrEP uptake and adherence. Synthesis and critical evaluation of the existing literature is necessary to fill this gap in knowledge. Therefore, the purpose of this article is to examine empirical research about PrEP and identify salient issues surrounding its implementation as a new biomedical intervention that has the potential to decrease the incidence of HIV infection globally. Background information is provided on the initial rollout of PrEP, followed by findings from the literature review. The article concludes with a discussion of our current knowledge of PrEP implementation, as well as identification of areas for additional novel inquiry.

Preexposure Prophylaxis PrEP is a safe, effective biomedical intervention for the prevention of HIV infections. Peterson et al. (2007) conducted the first study demonstrating PrEP safety in HIV-uninfected women (N 5 936) in three African countries who were randomized to receive either tenofovir disoproxil fumarate (TDF) or placebo. The experimental arm did not have more adverse effects compared to the control arm. However, two of the sites were closed prematurely, and the study was not powered sufficiently to deter-

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mine efficacy. In 2010 the results of the Preexposure Prophylaxis Initiative (iPrEx) study were published (Grant et al., 2010). Study participants (MSM and transgender [TG] females in six countries; N 5 2,499) were randomized to receive either oral emtricitabine (FTC)-TDF or placebo. There was a 44% reduction in incident HIV infections in the experimental group. Participants in the experimental group who had a detectable level of the study drug in the blood compared to those who did not were found to have a ‘‘relative reduction in HIV risk of 92%’’ (Grant et al., 2010, p. 2597). The results of three additional clinical trials of PrEP were published in 2012; two demonstrated efficacy while one did not. The Partners Preexposure Prophylaxis study included more than 4,700 heterosexual, serodiscordant couples (SDC) in two African countries who were randomized to receive daily oral TDF, daily oral FTC-TDF, or placebo (Baeten et al., 2012). Those receiving TDF and FTC-TDF had a relative reduction of incident HIV infections, by 62% and 75%, respectively (Baeten et al., 2012). The TDF2 study group found that FTC-TDF was 62.2% effective in preventing HIV infections among heterosexual women and men (N 5 1,219) in Botswana (Thigpen et al., 2012). The Preexposure Prophylaxis Trial for HIV Prevention among African Women study enrolled more than 2,100 women in two African countries and randomized them to either FTC-TDF or placebo. Thirty-three women in the experimental group and 35 in the placebo group became infected with HIV and the study was stopped early for lack of efficacy (Van Damme et al., 2012). The authors attributed the lack of efficacy of FTCTDF to poor medication adherence, as ‘‘less than 40% of the HIV-uninfected women had evidence of recent pill use at visits that were matched to the HIV-infection window for women with seroconversion’’ (Van Damme et al., 2012, p. 419). Pill use was measured by drug-level analyses. Given poor adherence, the study may have been inadequately powered to detect an effect of FTC-TDF (Van Damme et al., 2012). The results of the Vaginal and Oral Interventions to Control the Epidemic (VOICE) study were announced in March 2013. Tenofovir vaginal gel, oral tenofovir, and TruvadaÒ (FTCTDF; Gilead, Foster City, CA) were found to be ineffective in preventing HIV among women (N 5 5,029)

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in three African counties (National Institute of Allergy and Infectious Diseases [NIAID], 2013). The investigators attributed these findings to suboptimal adherence to study drugs among the participants (NIAID, 2013). In June 2013, the results of the Bangkok Tenofovir study were published. More than 2,400 HIV-uninfected persons who injected drugs in the previous year were enrolled and randomized to receive either oral TDF or placebo. This study showed a reduction in HIV incidence by 48.9% (Choopanya et al., 2013). Following the results of the iPrEx study in 2010, the CDC (2011) released guidelines for the use of PrEP in MSM. On July 16, 2012, the U.S. Food and Drug Administration (2012) approved FTC-TDF for use as PrEP in individuals at high risk for becoming infected with HIV. The following month, the CDC (2012b) released guidelines for PrEP use in heterosexual adults. Recently, the International Association of Providers of AIDS Care (IAPAC) released a consensus statement endorsing the use of PrEP among high-risk individuals as part of ‘‘a comprehensive risk reduction package’’ (Mayer et al., 2013, p. 214). While other biomedical interventions such as condoms and male circumcision have proven to be effective in decreasing the incidence of HIV infections, the number of new infections in the United States has remained consistent in recent years. Now that safety and efficacy of PrEP have been demonstrated in several randomized controlled trials, patient- and provider-level factors surrounding its use and provision outside of experimental conditions must be explored to identify facilitators and barriers to implementation among those at risk of becoming infected with HIV.

Methods PubMed and Medline databases were searched in July and August 2013 using the medical subject heading (MeSH) term, primary prevention and the key words: pre-exposure prophylaxis and preexposure prophylaxis, which yielded 327 articles. The CINAHL database was searched using the key words pre-exposure prophylaxis, yielding 22 results. The key words, preexposure prophylaxis, were also searched separately in the CINAHL database and

yielded 13 results. The term primary prevention was not used in either of the CINAHL database searches because, when combined with each of the other key words, zero results were yielded. Each of these searches was limited to the English language and humans and, combined, yielded 362 articles. Exact duplicates were identified and deleted by hand, yielding 167 articles. Each of these titles were reviewed and excluded if unrelated to oral PrEP for the prevention of HIV infection. This yielded 116 results. The abstracts of these articles were evaluated and the full article was read if the article was based on empirical research (i.e., qualitative or quantitative research methods). Articles were excluded if they were review pieces, opinions, letters, case vignettes, dissertations, or commentaries. PrEP safety and efficacy studies were also excluded, as this endeavor was restricted to PrEP implementation. Articles that used mathematical models to predict the effectiveness of PrEP in reducing HIV infections prior to the publication of the iPrEx study results (December 30, 2010) were also excluded because data from subsequent studies demonstrating PrEP efficacy in humans were available by that time. The reference lists of the articles meeting inclusion criteria were hand searched and included if they met the inclusion criteria. A total of 45 articles were included in our review.

Results The majority of the studies (N 5 40) focused on patient-level factors, and very few addressed provider-level factors (N 5 5). Thirty-two of the 40 studies involving patients included data on PrEP awareness, use, and/or willingness to use. Participant characteristics in the studies varied widely and included MSM, seroconcordant couples, SDCs, female sex workers, TG persons, and heterosexuals from around the globe. MSM were included as participants in 37 of the 40 studies involving patients, thereby giving particular attention to this group. Patient-Level Factors PrEP awareness. Overall, awareness of PrEP among participants ranged from none (Brooks et al.,

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2012) to 81% (Saberi et al., 2012). The majority of the studies that provided data on awareness were conducted prior to the release of the iPrEx study results (i.e., prior to empirical efficacy data on PrEP in humans) and ranged from none (Nodin, CarballoDieguez, Ventuneac, Balan, & Remien, 2008) to 25% (Kellerman et al., 2006). Postpublication, overall awareness ranged from 19% (Krakower et al., 2012) to 81% (Saberi et al., 2012). Only one study explicitly compared awareness pre- and postpublication of the iPrEx study results (Krakower et al., 2012). In this study, 12.5% (N 5 398) were aware prepublication and 19% (N 5 4,558) postpublication (Krakower et al., 2012). While it is not surprising that awareness would be higher postpublication of the iPrEx findings, it is important to consider patient understanding of what PrEP is and how it is used when interpreting these results. For example, Saberi et al. (2012) found that 27% of a sample (N 5 32) of male couples mistook postexposure prophylaxis (PEP) for PrEP. Accurately defining PEP and PrEP is important because potentially inflated rates of awareness may misinform the design of interventions using PrEP. In the studies reporting awareness of PrEP that included exclusively MSM, some commonalities among participants were noted. Those aware of PrEP were more likely to have used PEP previously (Krakower et al., 2012; Mimiaga, Case, Johnson, Safren, & Mayer, 2009), had unprotected anal intercourse (UAI), were under the influence of drugs during sex (Liu et al., 2008; Mimiaga et al., 2009), had an HIV test in the past (Rucinski et al., 2013; Voetsch, Heffelfinger, Begley, Jafa-Bhushan, & Sullivan, 2007), and had multiple sex partners (Rucinski et al., 2013; Voetsch et al., 2007). These findings suggest that those with greater risk of HIV acquisition have more awareness of PrEP. Overall, PrEP awareness was higher following the release of the iPrEx results and among patients with greater risk for becoming infected with HIV. However, there was wide variability in awareness between studies and there was evidence that participants mistook PEP for PrEP (Saberi et al., 2012). What is reassuring is that there was evidence that MSM who engaged in high-risk sexual behaviors were aware of PrEP and had used other biomedical interventions for prevention (e.g., HIV screening, PEP).

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PrEP use. The use of PrEP was reported in 15 of the articles included in this review. Overall use ranged from 0% (Leonardi, Lee, & Tan, 2011; Poynten et al., 2010) to 7.8% (Saberi et al., 2012). The largest percentage of use was reported in male seroconcordant couples and SDCs (Saberi et al., 2012). This was the same study where PEP was mistaken for PrEP; therefore, the upward parameter of 7.8% may not have accurately reflected actual PrEP use. Similarly, Koblin et al. (2008) found that of 14 people who reported having ever used PrEP, most were likely to have actually used PEP based on their reported duration of use (i.e., many reported not having PrEP awareness and that they were prescribed a 30-day supply of medication). Some common factors associated with PrEP use across studies were self-identifying as gay, being African American/Black, and having UAI with a male partner (Holt et al., 2012; Kellerman et al., 2006; Krakower et al., 2012; Rucinski et al., 2013). Age associated with PrEP use was reported as 18 to 30 years (Rucinski et al., 2013) in one study and 19 to 42 in another (Holt et al., 2012). A study of YMSM (ages 16–20 years) did not report PrEP awareness or use (Mustanski, Johnson, Garofalo, Ryan, & Birkett, 2013). As with PrEP awareness, PrEP use was associated with sexual behaviors that increased the risk of becoming infected with HIV. Use has also been associated with discussions about HIV prevention strategies with providers (Krakower et al., 2012). Given that PrEP requires a prescription, providers must be knowledgeable about this new intervention, comfortable in discussing sexual health, and willing to prescribe PrEP. Willingness to use PrEP. Overall, willingness to use PrEP ranged from 17% (Fuchs et al., 2013) to 93.8% (Heffron et al., 2012). Data collection for most of these studies occurred prior to the release of the iPrEx study results, indicating that even without empirical evidence of the efficacy of this new biomedical intervention, patients were willing to try new approaches to protect themselves from HIV acquisition. Variables associated with a patient’s willingness to use PrEP were numerous, with some varying widely between samples: income ranged from low (Barash

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& Golden, 2010) to moderate (Mimiaga et al., 2009); age ranged from younger (Holt et al., 2012) to older (Barash & Golden, 2010; Krakower et al., 2012); and education attainment from lower (Jackson et al., 2012; Mimiaga et al., 2009; Zhang et al., 2013) to higher (Mustanski et al., 2013). Commonalities among variables between samples were: being nonWhite (Fuchs et al., 2013; Golub, Kowalczyk, Weinberger, & Parsons, 2010; Liu et al., 2008; Wingood et al., 2013; Zhang et al., 2013); having higher risk perception of HIV acquisition (Holt et al., 2012; Krakower et al., 2012); and engaging in UAI (Heffron et al., 2012; Krakower et al., 2012; Leonardi et al., 2011; Liu et al., 2008; Mimiaga et al., 2009). These variables indicated that those at higher risk for becoming HIV infected may have been more willing to use PrEP, which was a similar finding for both PrEP awareness and use. Facilitators and barriers of PrEP use. Because much of the literature discussed willingness to use PrEP, it is important to address the facilitators and barriers to the adoption of PrEP that were identified in this review, many of which could be a facilitator or a barrier. For example, if the cost of PrEP were prohibitive, it would be a barrier to use. But if PrEP were low to no cost, this might facilitate greater use. Commonly identified facilitators were low cost, efficacy, accessibility, ease of use, medication safety, and a reduction in fear and anxiety about becoming infected with HIV. Barriers were potential adverse effects of the antiretroviral medications and stigma related to taking PrEP (Brooks et al., 2011; Galea et al., 2011; Golub, Gamarel, Rendina, Surace, & Lelutiu-Weinberger, 2013; Mutua et al., 2012; Saberi et al., 2012; Smith, Toledo, Smith, Adams, & Rothenberg, 2012; Tangmunkongvorakul et al., 2013). Risk perception. Those at highest risk of acquiring HIV have been identified as a group to whom PrEP should be targeted; therefore, patients and providers will need to appropriately assess HIV infection risk in clinical settings. The evidence related to the association between perceived risk for becoming infected with HIV and willingness to use PrEP is conflicting. Increased risk perception was associated with increased willingness in MSM and

TG females (Golub et al., 2013; Holt et al., 2012). Conversely, Khawcharoenporn, Kendrick, and Smith (2012) found, in a sample of high-risk heterosexuals, that those with lower perceived risk were less willing to use PrEP; and in a sample of female sex workers in China, willingness to use PrEP was not associated with perceived risk of HIV acquisition (Jackson et al., 2013). Conducting accurate risk assessments is essential for targeting PrEP to highrisk patients because patient perception of risk may not be congruent with actual risk. For example, in a sample of high-risk individuals (as determined using preset characteristics), 84% felt they were low risk (Khawcharoenporn et al., 2012). Adherence. The efficacy of PrEP has been related to medication adherence (Grant et al., 2010). Reasons for missing medication doses found in this review were forgetting, being away from home, being busy, having a change in routine, being without medications, and using alcohol or drugs (Hosek et al., 2012; Mutua et al., 2012). Potential medication sharing was also identified as a practice that would affect adherence, as well as selling medication (Eisingerich et al., 2012; Mansergh et al., 2010; Smith, Toledo et al., 2012; Voetsch et al., 2007). Participants noted that, over time, it became easier to take a daily pill (Guest et al., 2010). When deciding to initiate PrEP, providers should consider these factors to maximize adherence, therefore decreasing the risk of HIV acquisition. Risk compensation and behavioral disinhibition. Increases in risky sexual behaviors with the use of PrEP are a concern of potential users and providers. Golub et al. (2010) distinguished between behavioral disinhibition and risk compensation. Behavioral disinhibition occurs when a person decreases her or his self-control over risky sexual behaviors because they are taking PrEP. Risk compensation happens when a person has a decreased self-perception of risk because of the use of PrEP (Golub et al., 2010). Of 10 studies that addressed risk compensation, four reported that it would occur (Galea et al., 2011; Golub et al., 2013; Khawcharoenporn et al., 2012; Liu et al., 2008) and 6 reported that it would not occur (Brooks et al., 2012; Elst et al., 2013; Guest et al., 2008; Holt et al., 2012; Mustanski

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et al., 2013; Smith, Toledo et al., 2012). In a study exploring condom use by MSM (N 5 630), 72.5% of the men indicated that PrEP would need to be effective always or almost always for them not to use a condom during anal sex. In the same sample, 12.3% indicated that they would not use a condom during anal sex if PrEP were effective less than half the time (Koblin et al., 2011). While most would require high PrEP efficacy to forego condom use, others said that even with PrEP efficacy less than 50%, they would not use condoms. This was an important finding for providers to consider so that they include appropriate counseling on the utility of condoms in preventing the transmission of other sexually transmitted infections (STIs). Provider-Level Factors Patients are not PrEP’s only stakeholders. Health care providers, public health personnel, AIDS service organizations, nongovernmental organizations, and policymakers all play a role in the planning, implementing, and monitoring of PrEP as a biomedical prevention intervention, yet few empirical research studies have been conducted with participants from these groups. Five studies, conducted on five continents, of the aforementioned groups were included in this review. The studies reported on knowledge, use, and perceptions of PrEP, how these may vary depending on specialization of health care providers (HCPs), and the implementation of PrEP. In a sample of Canadian health care and service providers (N 5 160), 64.4% and 15.6%, respectively, were somewhat and not at all familiar with PrEP. However, only 12.5% of this sample was HCPs. The majority of the sample was service providers (e.g., outreach workers and administrators) who are not licensed to prescribe PrEP (Senn, Wilton, Sharma, Fowler, & Tan, 2013). Of 360 HCPs in family and STI practices in two states (South Carolina and Mississippi) in the United States, the mean PrEP knowledge score was 5.6 out of a maximum of 8 (a higher score being indicative of greater knowledge; Tripathi, Ogbuanu, Monger, Gibson, & Duffus, 2012). In a multinational study of 91 nongovernmental organization representatives, health care workers, and policymakers from seven countries, 55% were aware of PrEP. However, among the 35

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health care workers included in the sample, 46% were not aware of PrEP (Wheelock et al., 2012). One study involving physicians in Massachusetts compared PrEP knowledge pre- and postpublication of the iPrEx trial results (White, Mimiaga, Krakower, & Mayer, 2012). Prepublication, 79% (N 5 178) were aware of PrEP and 92% (N 5 115) were aware postpublication. In this same sample, 7% prescribed PrEP prepublication and 4% postpublication (White et al., 2012). The authors did not discuss why prescriptions for PrEP declined following the publication of the iPrEx results. In four of the five studies involving providers, the perceived challenges with PrEP were reported with some similarities across studies, such as adverse effects and toxicities, adherence, the development of drug resistance, cost, and risk compensation (Arnold et al., 2012; Tripathi et al., 2012; Wheelock et al., 2012; White et al., 2012). Other concerns were supply, education, and training for patients and providers, and the effects on HIV stigma and criminalization (Wheelock et al., 2012). Providerperceived benefits were also reported and, in addition to decreasing HIV incidence, included being a method of prevention for those who were unable to negotiate condom use and PrEP provision as a means for increasing resources for HIV prevention (Tripathi et al., 2012; Wheelock et al., 2012). Providers felt that PrEP would be of additional benefit to the public’s health, particularly in SDCs where antiretroviral treatment could be used as treatment in the infected partner and prevention in the uninfected partner (Arnold et al., 2012). Providers noted that guidelines from the CDC and the U.S. Preventive Services Task Force, as well as professional specialty organizations would influence their decisions to prescribe PrEP. An additional consideration included more efficacy data specific to certain at-risk groups (White et al., 2012). In two studies, providers were questioned about the level of PrEP efficacy that would be needed for them to prescribe it. PrEP would need to have a mean efficacy of 71% for physicians in Massachusetts to feel comfortable prescribing it (White et al., 2012) and a median efficacy of 60% by those supporting its approval by Health Canada (Senn et al., 2013). In the sample of Canadian providers, 53.8% felt that PrEP was not yet ready to be made widely available (Senn et al., 2013).

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Discussion The body of literature on PrEP included in this review is broadly categorized into patient- and provider-level factors associated with PrEP. Almost 90% of the reviewed articles involved patient-level factors and, of these, 80% included data on PrEP awareness, use, and willingness to use. It should be noted that many of the studies on patients were conducted prior to the release of PrEP efficacy data in humans; therefore, much of this work was grounded in hypothetical data. Now that the safety and efficacy of PrEP is well documented in humans, and guidance from the CDC on the use of PrEP in adults is available, research into its implementation must be undertaken. Patient preferences for the type of prescriber, dosing regimen, cost, adverse effects, and effectiveness of PrEP will likely influence initiation of and adherence to PrEP (Galea et al., 2011), and further research including providers is needed to understand the practice-related issues surrounding PrEP. Overall, a wide range of awareness of PrEP was found among patient participants; awareness was associated with behaviors more likely to lead to HIV infection (Liu et al., 2008; Mimiaga et al., 2009; Saberi et al., 2012). Similar to PrEP awareness, the overall range for willingness to use PrEP was wide; however, it was encouraging that many participants would be interested in using PrEP to prevent HIV infection. The variables associated with willingness to use PrEP were not always concordant between studies. However, participants with higher perceived risks for HIV acquisition (Holt et al., 2012; Krakower et al., 2012) and who engaged in UAI (Heffron et al., 2012; Krakower et al., 2012; Leonardi et al., 2011; Liu et al., 2008; Mimiaga et al., 2009) were willing to use PrEP. Increased awareness and willingness to use PrEP indicates that PrEP might be an effective intervention for high-risk patients. PrEP use was lower than either awareness of or willingness to use PrEP. This is not surprising given that most of the research reviewed here took place before the release of PrEP efficacy data in humans and because Truvada was not approved for HIV prevention until July 2012. Because PrEP efficacy is affected by medication adherence (Grant et al., 2010), additional research

is needed in this area of patient care. Chronic care and implementation science models have been proposed to enhance the effectiveness of, and adherence to, prevention interventions using PrEP (Elzarrad, Eckstein, & Glasgow, 2013). Adherence can also be enhanced through interventions and prescribing practices that incorporate as many patient preferences for PrEP as possible. However, at this time, many of the ideal characteristics of PrEP that patients have identified are not available. Awareness of PrEP was generally higher among providers than patients. Some of the concerns expressed by providers have been addressed now that efficacy has been demonstrated in several studies, among different groups of people, and the CDC has released guidance for health care providers for prescribing PrEP. Research is needed to determine whether provider awareness of and prescribing practices with PrEP have changed based on this additional information. While the literature on other biomedical interventions was not reviewed here, studies conducted with providers to assess the awareness and use of such things as PEP and STI treatment as prevention may uncover other missed opportunities for HIV prevention. Risk assessment will be important for the provision of PrEP. In a modeling study to predict the costeffectiveness of PrEP in MSM, PrEP would prevent more infections in the general MSM population, but would cost more than if it were targeted to only MSM at high risk for HIV infection (Juusola, Brandeau, Owens, & Bendavid, 2012). Only one study in this review stratified participants into risk groups using stipulated characteristics of HIV risk (Khawcharoenporn et al., 2012). In the three studies included in this review that assessed perceived risk of acquiring HIV, risk perception was low overall. Published HIV risk prediction indices (Gerbert, Bronstone, McPhee, Pantilat, & Allerton, 1998; Menza, Hughes, Celum, & Golden, 2009; Smith, Pals, Herbst, Shinde, & Carey, 2012) should be incorporated into sexual health histories, thereby decreasing barriers to adequately assessing HIV risk, such as avoiding discussions of sexual orientation, sexual practices, and substance use between patients and providers due to discomfort, as well as provider inability to elicit thorough sexual health histories and insufficient knowledge of the health care needs of

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sexual minorities (Krakower & Mayer, 2012). Future research should explore self-perceived risk versus actual risk as determined by one of the risk indices. Research now needs to focus on how HCPs and health care systems assess risk, identify potential PrEP users, adhere to guidelines when prescribing PrEP, develop and maintain relationships with patients to promote honest conversations around sex, and maximize adherence. The limitations of this review include that most of the articles involving patients were composed of adult MSM, the results of which may not be generalizable to other groups such as heterosexuals or adolescents. Only one study reviewed included YMSM. YMSM are disproportionately infected with HIV (CDC, 2012a), and the patient-level factors of adults may not be the same for adolescents. Further research on use of PrEP in this group is needed, as well as guidelines for PrEP use in adolescents.

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biomedical intervention might not impact HIV incidence to its fullest potential. Nurses have the ability to bridge the gap between patients and prescribers and will be invaluable in educating individuals and communities about PrEP. Nurses, particularly those practicing in primary care settings, can use HIV risk-screening tools to identify patients who may benefit from PrEP. These tools may generate further discussion between nurses and patients about other methods for reducing HIV risk such as HIV screening, consistent use of condoms, decreasing the number of sex partners, and avoiding sex while under the influence of alcohol or drugs. PrEP requires routine follow-up, including screening for STIs and monitoring kidney function. Nurses can manage these visits and collaborate with prescribers to develop standing orders for laboratory testing and medication refills. This continuity of care may enhance adherence to medications and follow-up appointments as well as build trust with individual patients.

Conclusions Key Considerations The findings from our literature review indicate that awareness of PrEP among patients is variable. Awareness is higher among providers compared to patients; PrEP use, however, remains low. Reassuringly, willingness to use PrEP is moderate to high among patients. With the release of additional PrEP efficacy data and guidelines from the CDC (2012b) on the use of PrEP in adults, as well as an endorsement from IAPAC for the use of PrEP, some of the concerns with PrEP among providers have been addressed. Data on provider-level factors with PrEP and the use of PrEP in adolescents are sparse. Research is needed on self-perceived risk of HIV acquisition among potential users compared to actual risk as determined using validated HIV risk prediction models. Additional inquiry is needed to understand how HCPs assess risk for HIV acquisition, conduct sexual health histories, and create environments conducive to the exchange of sensitive, sometimes stigmatizing and/or criminalizing information, especially among sexual minorities. While factors such as access, adherence, and cost are important to the successful implementation of PrEP, without first engaging patients and providers, this promising

 Patient awareness of preexposure prophylaxis (PrEP) varies and its use has been low.  Awareness of PrEP is higher among providers than among patients.  There is scant research on provider-level factors related to the implementation of PrEP.  Research on how providers identify patients who may benefit from PrEP is needed.

Disclosures The authors report no real or perceived vested interests that relate to this article that could be construed as a conflict of interest.

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