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Prevention Research

Current US Guidelines for Prescribing HIV Pre-exposure Prophylaxis (PrEP) Disqualify Many Women Who Are at Risk and Motivated to Use PrEP

Calabrese, Sarah K. PhDa,b; Willie, Tiara C. PhDb,c,d; Galvao, Rachel W. BAa,e; Tekeste, Mehrit BAa; Dovidio, John F. PhDb,f,g; Safon, Cara B. MPHg,h; Blackstock, Oni MD, MPHb,i; Taggart, Tamara PhD, MPHb,j; Kaplan, Clair MSN, APRN, MHSk; Caldwell, Abigail MSN, APRNk; Kershaw, Trace S. PhDb,g

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: August 1, 2019 - Volume 81 - Issue 4 - p 395-405
doi: 10.1097/QAI.0000000000002042

Abstract

INTRODUCTION

HIV pre-exposure prophylaxis (PrEP) is a highly effective method of HIV prevention.1,2 In the United States, PrEP uptake has risen dramatically among men since its 2012 federal approval, but remains low among women: Women account for less than 5 percent of PrEP users3 despite representing 19% of new HIV diagnoses.4 Further efforts are needed to promote PrEP uptake among women, including implementation of clinical practice standards that improve women's PrEP access.

The year 2018 marked the release of an updated (“2017”) version of the US Clinical Practice Guideline for PrEP by the US Centers for Disease Control and Prevention (CDC).5 This comprehensive informational resource, commonly referred to as “the CDC guidelines,” updates an earlier (2014) version of the guidelines,6 which consolidated and elaborated early interim CDC guidance published between 2011 and 2013 for different key populations.7–9 The CDC guidelines are intended to support clinicians and policymakers in making PrEP available to people at substantial risk of HIV. Indeed, clinicians have reported such guidelines to be a key influence on PrEP comfort and decision-making in practice,10,11 and the CDC guidelines form the foundation of clinical recommendations adopted at state and organization levels.12,13

The guidelines contain PrEP eligibility criteria to help identify patients at substantial HIV risk, defined separately for men who have sex with men, heterosexual women and men, and people who inject drugs, but state 2 different versions—guidance summary criteria and recommended indications criteria. Although overlapping, there are several inconsistencies between guidance summary criteria and recommended indications criteria within each risk group; for women at risk due to heterosexual activity, the 2 versions of criteria diverge in a potentially critical way: Although both require women's knowledge of their own risk behavior, only the recommended indications criteria also require women to either know their partners' HIV risk or recognize a potentially asymptomatic sexually transmitted infection (STI).14,15 Specifically, the first and less restrictive version of criteria, the guidance summary criteria,5(p.13) stipulates that women should be HIV-uninfected and lists the following indicators of substantial HIV risk: HIV-positive sexual partner, recent bacterial STI (syphilis or gonorrhea), high number of sex partners, history of inconsistent or no condom use, commercial sex work, and high-prevalence area or network. Thus, to meet the guidance summary criteria, women need only know about their own risk behavior. The second version of criteria, the recommended indications criteria,5(p. 36) specifies that women should be HIV-uninfected, heterosexually active adults who are not in a monogamous relationship with a recently tested, HIV-negative partner and should be characterized by 1 or more of the following: (1) in an ongoing serodiscordant sexual relationship, (2) infrequently uses condoms during sex with 1 or more male partners of unknown HIV status who are known to be at substantial risk (eg, because of injection practices or sex with other men), and (3) had syphilis or gonorrhea within the past 6 months. Thus, for women at sexual risk to meet criteria according to the recommended indications criteria, women need to know that (1) a partner's HIV status is positive, (2) a partner is engaging in risk behavior, or (3) they themselves have a potentially asymptomatic STI.

Although a key objective of the CDC guidelines is to identify women at substantial risk of HIV as potential PrEP candidates, the effectiveness of both the guidance summary criteria and the recommended indications criteria in achieving that objective has not been explicitly investigated. Understanding whether these 2 versions of eligibility criteria distinguish women who are at risk and motivated to use PrEP is critical because many providers use them as screening criteria when deciding whether to discuss and prescribe PrEP during patient encounters.

The present research was undertaken to evaluate both versions of CDC guideline criteria (guidance summary criteria and recommended indications criteria) among a large sample of HIV-negative women recently engaged in care at Connecticut Planned Parenthood centers. We pursued 3 main objectives: First, we sought to describe the eligibility of sociodemographic groups differentially affected by HIV (eg, non-Hispanic black vs. white women4,16) according to guidance summary and recommended indications criteria and to assess whether the relative eligibility of these groups aligned with the epidemiological risk profile of HIV. Second, we sought to determine whether women with existing HIV risk factors and motivation to use PrEP would be deemed eligible according to guidance summary and recommended indications criteria, and how the 2017 update to the 2014 guidelines affected such eligibility. A third, exploratory objective was to investigate the pervasiveness of CDC guideline criteria within state-level PrEP eligibility recommendations and whether different states used different versions of the CDC criteria (guidance summary vs. recommended indications criteria).

METHODS

Methods described below have also been reported elsewhere.17,18

Procedures

In February of 2017, an email inviting Connecticut Planned Parenthood patients to participate in an anonymous online survey was distributed to 11,238 patients. The survey was restricted to patients who had agreed to receiving email communication from Planned Parenthood (77%), were 18 years and older, and recently engaged in care at Planned Parenthood centers in 3 small cities with the highest annual number of HIV infections in Connecticut: Bridgeport, Hartford, and New Haven.19 Recent care engagement, determined through patients' medical records, was defined as attending 1 or more visits in the past 10 months. Interested patients followed a survey link embedded in the recruitment email, completed an online consent form, responded to survey questions (median time = 36 minutes), and received compensation ($10 gift card). The survey closed to new participants once 973 had enrolled and initiated the survey—which occurred within 100 hours of deploying the recruitment email—to avoid exceeding the recruitment maximum of 1000. All procedures were approved by the Yale University Human Investigation Committee.

Measures

All measures were self-administered through the online survey. Additional details about measures of PrEP eligibility, HIV risk, and PrEP motivation beyond the descriptions below are available as supplemental digital content (see Text Summary, Supplemental Digital Content 1, http://links.lww.com/QAI/B319).

PrEP Eligibility

Eligibility was conceptualized as a dichotomous variable, coded as (1) eligible vs. (0) ineligible, and determined separately for each version of CDC guideline criteria (guidance summary criteria and recommended indications criteria). Operationalization of each individual criterion (wording of associated survey item[s]) and the number/combination of criteria needed to qualify as eligible by each version are detailed in Table 1.

TABLE 1.
TABLE 1.:
Operationalization of CDC Guideline Eligibility Criteria for Women*†‡§
TABLE 1-A.
TABLE 1-A.:
Operationalization of CDC Guideline Eligibility Criteria for Women*†‡§

Sociodemographic Characteristics

Sociodemographic characteristics included gender, race/ethnicity, sexual orientation, education, employment, household income, age, and geographic location.

HIV Risk Indicators

HIV risk indicators spanned 3 categories:

  • Sexual health risk indicators included STIs (diagnosed in lifetime and perceived in past 6 months), PrEP use (lifetime and current), post-exposure prophylaxis (PEP) use (lifetime), emergency contraception use (lifetime), and pregnancy (lifetime unwanted and current).
  • Behavioral risk indicators included vaginal or anal sex with multiple (2 or more) male partners (past 6 months); condomless vaginal or anal sex with a male partner (past 6 months); condomless vaginal or anal sex with an HIV-positive or status-unknown male partner (past 6 months); anticipated increase in number of sexual partners (future 6 months); anticipated decrease in condom use (future 6 months); sex in exchange for money, drugs, or other goods (lifetime); and injection drug use (past 6 months).
  • Relationship risk indicators included experiencing intimate partner violence (current relationship of 1 or more years); experiencing reproductive coercion (lifetime); involvement in an ongoing sexual relationship with a potentially viremic HIV-positive male partner; and involvement in an ongoing relationship with a male partner of unknown HIV status (current relationship of 1 or more months).

PrEP Motivation Indicators

PrEP motivation indicators included self-perceived HIV risk (self-rated “very” or “extremely” likely to get HIV in lifetime), PrEP interest (“very” or “extremely” interested in learning more about PrEP), and PrEP intention20 (“probably” or “definitely” would take PrEP if available for free).

Analysis

The analytic sample was restricted to participants who identified as women (“woman” or “transgender woman”), reported no previous HIV diagnosis, and responded to all PrEP eligibility questions for both sets of criteria (guidance summary criteria and recommended indications criteria). For a given set of criteria, women who met the subset of criteria pertaining to heterosexual activity, injection drug-related activity, or both were deemed eligible by those criteria (see eTables 1 and 2, Supplemental Digital Content 2, http://links.lww.com/QAI/B319 for supplementary analyses of eligibility by criteria pertaining to heterosexual activity only and injection drug-related activity only). Frequency distributions were calculated to describe sample characteristics. Logistic regressions were conducted to compare the probability of being eligible within sociodemographic categories. State-level eligibility criteria were compiled by searching state health department websites for PrEP-specific content. Specifically, 2 coauthors (R.W.G. and M.T.) independently searched for PrEP criteria and other PrEP-related information on health department websites for all states and Washington, DC, reconvening to compare their lists of online sources (uniform resource locators [URLs] recorded for each state) and create a master list of sources. An initial coding scheme developed by the principal investigator (S.K.C.) was iteratively refined through multiple rounds of coding and discussion. Based on the final coding scheme, R.W.G. and M.T. systematically recorded PrEP eligibility criteria specified on state health department websites and coded PrEP-related links provided on these websites. S.K.C. reviewed and finalized all recorded criteria and assigned codes.

RESULTS

Sociodemographic and Behavioral Characteristics

Of the 973 Connecticut Planned Parenthood patients enrolled in the survey, 679 met criteria for inclusion in the analytic sample (Fig. 1). No participants identified as transgender women. Most participants identified as non-Hispanic white (33.9%) or black (35.8%). The mean age was 28.2 (SD = 7.5). As compared to HIV-negative female participants who were excluded from analyses because they did not answer all required items (n = 153), a larger percentage of participants included in analyses were white (33.9% of included vs. 24.2% of excluded; χ2[1] = 5.38, P = 0.020). There was no significant difference in age distribution (57.0% of included vs. 51.6% of excluded were older than 25 years; χ2[1] = 1.46, P = 0.227). As compared to the larger population of HIV-negative female patients 18 years and older who were recently engaged in care at the 3 Planned Parenthood centers from which the sample was drawn (n = 12,426), a larger percentage of our sample was white (33.9% of study sample vs. 28.9% of patient population; χ2[1] = 7.71, P = 0.005) and older than 25 years (57.0% of study sample vs. 52.0% of patient population; χ2[1] = 6.47, P = 0.011). Additional sociodemographic characteristics are displayed in Table 2.

FIGURE 1.
FIGURE 1.:
Summary of participant enrollment and inclusion within analytic sample. aOur enrollment maximum was established as 1000 participants. To avoid exceeding this maximum, we closed the survey to new participants when 973 had enrolled because additional patients had clicked on the survey link but not yet consented and we were uncertain whether they would continue on to enroll. bParticipant self-reported being 18 years or older on screening item and subsequently reported being 17 years old in a demographic survey question. cEligibility assessable by all 4 sets of CDC guideline criteria: (1) 2017 guidance summary recommended indications criteria, (2) 2017 guidance summary criteria, (3) 2014 recommended indications criteria, and (4) 2014 guidance summary criteria.
TABLE 2.
TABLE 2.:
Sociodemographic Differences in PrEP Eligibility Among Women

Over the preceding 6 months, the majority of participants (89.1%) reported vaginal or anal sex with 1 or more men, of which 90.2% reported inconsistent or no condom use. When heterosexually active participants were asked whether they had condomless vaginal or anal sex with an HIV-positive or status-unknown male partner in particular, 91.9% reported they had not, 4.5% reported they had, and 3.6% reported they did not know. Few participants (0.7%) reported injecting drugs.

PrEP Eligibility

There were substantial differences in the prevalence of women eligible for PrEP based on guidance summary vs. recommended indications criteria: 559 (82.3%) of the 679 women were eligible based on guidance summary criteria, and 10 women (1.5%) were eligible based on recommended indications criteria. A similar pattern of difference in percent eligibility according to guidance summary criteria vs. recommended indications criteria was evident within all sociodemographic categories (Table 2). Logistic regression analyses predicting eligibility according to guidance summary criteria found 2 significant sociodemographic predictors: sexual orientation and employment. Gay/lesbian women were less likely to qualify for PrEP than heterosexual women, and unemployed women were less likely to qualify than employed women. Logistic regression analyses predicting eligibility according to recommended indications criteria were not performed because of the low number of participants deemed eligible (less than 10 observations in all subgroups).

HIV Risk Indicators and PrEP Eligibility

Figure 2 shows PrEP eligibility by risk indicator. Within all risk indicator groups, more women were eligible for PrEP based on guidance summary vs. recommended indications criteria, with the latter disqualifying most women. Similar patterns were evident when heterosexual risk criteria and injection drug-related risk criteria were examined separately (see eTables 1 and 2, Supplemental Digital Content 2, http://links.lww.com/QAI/B319). Comparison of eligibility based on 2014 vs. 2017 criteria revealed that the guideline update had little impact on women's eligibility (see eTable 3, Supplemental Digital Content 2, http://links.lww.com/QAI/B319).

FIGURE 2.
FIGURE 2.:
PrEP eligibility according to 2017 CDC criteria among subgroups of women reporting various risk indicators. aEligibility assessment assumed all participants were not in a high-prevalence area or network. If all participants were assumed to be in a high-prevalence area or network, 100% would be eligible based on guidance summary criteria for all risk indicators. bA total of 349 participants responded to survey items corresponding to the “experienced intimate partner violence” risk indicators because only participants who reported having sex with men or both men and women and having a current sexual/romantic relationship for 1+ year (n = 357) were gated to those items (and 8 responses were missing). For all risk indicators besides the “experienced intimate partner violence” risk indicator, the total number of participants who responded to corresponding survey items ranged from 651 to 679 because of survey gating/display logic, missing responses, and exclusion of “prefer not to say” responses (see Supplemental Digital Content 1, http://links.lww.com/QAI/B319 for description of gating/display logic and eTable 1, Supplemental Digital Content 2, http://links.lww.com/QAI/B319 for total respondents per risk indicator). cMan who is known to have a detectable level of HIV or whose viral suppression status is unknown to participant.

PrEP Motivation Indicators and PrEP Eligibility

Five women perceived themselves to be at high risk of HIV, of which 4 were eligible based on guidance summary criteria and zero were eligible based on recommended indications criteria. Of the 108 women who were “very” or “extremely” interested in learning more about PrEP, more were eligible based on guidance summary criteria (79.6%) vs. recommended indications criteria (4.6%). Likewise, of the 211 women who reported they “probably” or “definitely” would take PrEP, more were eligible based on guidance summary (82.5%) vs. recommended indications criteria (2.8%) (see eTable 4, Supplemental Digital Content 2, http://links.lww.com/QAI/B319).

Risk and Motivation Indicators Combined and PrEP Eligibility

Figure 3 displays PrEP eligibility according to both sets of criteria for the full sample, women with 1 or more risk indicators, women with 1 or more motivation indicators, and women with both risk and motivation indicators. Among the 234 women reporting both, 86.8% were eligible by guidance summary criteria and 2.6% by recommended indications criteria.

FIGURE 3.
FIGURE 3.:
Schematic representation of PrEP eligibility according to 2017 CDC criteria among women at risk of HIV, motivated to use PrEP, or both. RI eligible, % eligible according to CDC recommended indications criteria. GS eligible, % eligible according to CDC guidance summary criteria.

Pervasiveness of CDC Guideline Criteria

Many state websites specified eligibility criteria that were the same or similar to CDC guideline criteria and/or linked directly or indirectly to CDC guideline criteria online (42 of 50 states and DC; see eTable 5, Supplemental Digital Content 3, http://links.lww.com/QAI/B319). There was variability in the version of CDC guideline criteria adopted; some states specified criteria more similar to guidance summary criteria and others specified criteria more similar to recommended indications criteria. Three states neither specified PrEP criteria for women on their website nor linked to CDC or other web pages related to PrEP.

DISCUSSION

This study demonstrated that many women who report known HIV risk factors, motivation to take PrEP, or both would not be considered eligible for PrEP according to the criteria set forth in the CDC guidelines. This was found for both versions of criteria in the guidelines—guidance summary criteria and recommended indications criteria—but was especially true for the latter, according to which the majority (98.5%) of women were disqualified. The insensitivity of the criteria to women who could benefit from PrEP is disconcerting in the context of 7,300 new HIV infections occurring among US women annually4 and disproportionately low levels of reported PrEP awareness21,22 and uptake.3 It is further concerning given the potential reach of these criteria: Our review of state guidelines found that most states either specify eligibility criteria similar to CDC criteria, link to CDC criteria, or both.

Our first study objective was to describe the eligibility of sociodemographic groups differentially affected by HIV and to assess whether the relative eligibility of these groups aligned with the epidemiological risk profile of HIV. Analyses based on guidance summary criteria revealed few significant sociodemographic differences in eligibility. Within sociodemographic categories, women seemed similarly likely to qualify for PrEP, except for women who were unemployed (vs. employed) and gay or lesbian (vs. heterosexual) being less so. Therefore, overall, the relative eligibility of sociodemographic groups did not align with the epidemiological risk profile of HIV. Fortunately, it also did not oppose that profile; recent studies with men who have sex with men have reported that black men, who are disproportionately affected by HIV, were less likely to meet CDC eligibility criteria than white men.23,24 Rather, to the extent that eligibility determines access, our data suggest that CDC criteria would be unlikely to reduce HIV disparities among women but also unlikely to substantively exacerbate them.

Our second objective was to determine whether women with existing HIV risk factors and motivation to use PrEP would be deemed eligible according to both versions of criteria, and how the 2017 update to the 2014 guidelines affected such eligibility. As noted above, the 2 versions of criteria both disqualified some women reporting risk and motivation indicators, but the recommended indications criteria in particular disqualified nearly all. The 2017 update had minimal impact. These findings underscore the need for guideline reform. Modifying 1 version of criteria (guidance summary or recommended indications criteria) to match the other or eliminating 1 version of criteria altogether would strengthen the clarity of the guidelines and reduce discrepancies in assessments of eligibility.14 However, even the guidance summary criteria disqualified some women who could benefit from PrEP, and eliminating or modifying recommended indications criteria would not resolve this issue. Therefore, we recommend that the guidelines also explicitly state the limitations of using eligibility criteria for screening purposes and recommend discussing PrEP with all patients as part of routine sexual health care to guard against missed opportunities.14,25

Among the limitations of current CDC criteria are their emphasis on past behavior.26 The risk indicators we considered reflected not only past risk behavior but also future behavior. Many women in our sample reported they anticipated decreasing their condom use, increasing their number of sexual partners, or both in the next 6 months, and some of these women were disqualified by both sets of criteria. These anticipated behavioral changes highlight the potential fluidity of sexual behavior and the inherent shortcoming of criteria that rely on past behavior to predict future risk. Likewise, our findings with respect to past risk behavior should be interpreted within this context, recognizing that not all women reporting past risk factors will be at future risk.

Risk prediction is indeed a complicated and imperfect process—for providers and for patients. Less than 1 percent of participants reported perceiving themselves to be at significant risk of HIV, although many more reported objective indicators of risk (eg, over 10 times as many reported a recent STI). Previous research has documented a mismatch between perceived risk and risk behavior, with women routinely underestimating their risk.27 Notably, despite the low risk perception reported, 31% of participants reported they “probably” or “definitely” would take PrEP if it was freely available, suggesting underestimation of risk is not an insurmountable barrier to PrEP uptake. For some women with high intention to take PrEP despite low perceived risk, this could reflect a different motivation for taking PrEP (eg, anxiety reduction). Accordingly, the CDC guidelines could encourage patient–provider discussions of the holistic impact that PrEP has on well-being, including psychosocial benefits.

Our final objective was to examine the pervasiveness of CDC guideline criteria within state-level eligibility criteria presented online. Nearly all states (84%) and DC seem to have duplicated, adapted, or linked to the CDC guideline criteria, underscoring the relevance and reach of the CDC guidelines as a clinical standard and potential determinant of access. Some state criteria more closely aligned with the guidance summary criteria and others with the recommended indications criteria. Variability in state-level eligibility criteria could contribute to state-level disparities in providers' perceptions of the “appropriate” PrEP candidate and associated rates of PrEP prescription. Thus, guideline reform is needed at both national and state levels, and active efforts will be necessary to translate CDC guideline revisions into state-level guideline updates.

This study has limitations that are important to acknowledge and invite follow-up study. Participants were recruited from Connecticut Planned Parenthood centers and may not represent women in other geographic areas or with different levels of health care engagement. Risk factors were self-reported, and the study was cross-sectional; use of biological risk markers28 or a longitudinal design monitoring actual seroconversion29 would strengthen inferences regarding the sensitivity of eligibility criteria to women's HIV risk. In addition, social desirability bias may have led to underreporting of risk indicators and overreporting of motivation indicators, particularly because the survey was distributed by participants' source of health care.

CONCLUDING REMARKS

Release of the CDC guidelines coincided with a marked increase in PrEP uptake in the United States30 and has supported adoption of PrEP in clinical practices across the country. However, the current findings suggest that the eligibility criteria they present fail to identify many women who could benefit from PrEP; this failure may contribute to low and inequitable levels of PrEP awareness and uptake among women,3,21,22 an effect amplified by the widespread adoption and endorsement of these criteria at the state level. The US Preventive Services Task Force, a national panel of experts, recently released drafted recommendations for PrEP that parallel the CDC recommended indications criteria for women at risk due to heterosexual activity31; if left unrevised, these recommendations would further reinforce the more restrictive of the CDC criteria, according to which only 1.5% of our sample was eligible.

Nationwide, the CDC originally estimated that 468,000 US women were strong candidates for PrEP because of heterosexual activity based on the 2014 recommended indications criteria.32 In 2018, they revised that number to 177,000 women based on an alternative estimation approach.33 Our results imply that both of these estimates drastically misrepresent the number of women who could actually benefit from PrEP. Such underestimation may skew providers' perceptions about women's need for PrEP and, in so doing, reduce the frequency with which PrEP is offered to women within the health care system. It may also lead to broader deprioritization for PrEP for women, discouraging allocation of funding and other resources to initiatives aimed at enhancing women's access. Ongoing evaluation and improvement of CDC eligibility criteria is crucial to ensuring that women's HIV prevention needs are not overlooked in clinical practices and public health policies.

ACKNOWLEDGMENTS

The authors thank the Connecticut Planned Parenthood patients who generously contributed their time and effort by participating in this study. The authors are grateful to Ms. Susan Lane for her help with data collection and other facets of the study.

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Keywords:

HIV; pre-exposure prophylaxis; eligibility determination; clinical decision-making; patient care; women

Supplemental Digital Content

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