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Responding to critiques of the Canadian PrEP guidelines: Increasing equitable access through a nurse-led active-offer PrEP service (PrEP-RN).

HIV pre-exposure prophylaxis (PrEP) is the use of HIV medications by HIV-negative persons to prevent HIV acquisition from future potential or known exposures to this virus. Multiple studies have demonstrated its efficacy in this regard. In 2017, to help increase the use of PrEP in Canada, clinical practice guidelines were published. These summarized the available literature and made recommendations for men who have sex with men (MSM), persons who engage in injection drugs use (IDU), and heterosexual persons. Recently, arguments were made to suggest that these guidelines are not inclusive of other minority populations in Canada, including persons of African, Caribbean, and Black (ACB) descent and Indigenous persons. In this article, we review these critiques, and overview our approach to risk assessments for PrEP. Specifically, we detail the clinical procedures of our nurse-led PrEP clinic in Ottawa (entitled PrEP-RN). Lastly, we present preliminary uptake data for PrEP-RN, and discuss their meaning.

KEY WORDS: HIV, nursing, PrEP, risk assessment

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HIV transmission in Canada continues to unequally affect specific groups, particularly men who have sex with men (MSM), persons who use injection drugs (IDU), and individuals from regions where HIV is endemic, including Indigenous persons and persons of African, Caribbean, and Black (ACB) descent (PHAC, 2018). According to national estimates, 2,165 (range: 1,200 to 3,150) cases of HIV were diagnosed in Canada in 2016 (most recent year of available data). This figure constitutes a slight rise from 1,960 (range: 1,270 to 2,670) in 2014, although this increase might relate to more testing over the same time (PHAC, 2018). Of incident cases, 52.5% were MSM, 11.3% IDU, and 33.2% heterosexual persons (PHAC, 2018). ACB accounted for 41.7% of the heterosexual exposures (Bourgeois et al., 2018). In Ontario, while only 5% of the population is ACB, these men and women account for 26% of new HIV diagnoses (OHESI, 2017). For prevalent cases, 51.9% were MSM, 17.4% IDU, and 32.6% heterosexual persons, of whom 46% of were from HIV endemic countries (PHAC, 2018).

To inform local prevention efforts, we categorized HIV diagnoses reported to our health unit from January 1, 2011 to December 31, 2014 as less than or greater than 12 months from infection; as some of these infections would have been previously diagnosed and then reported to our health unit when the person entered Ontario (e.g., during immigration screening), we stratified these cases based on if people knew they were HIV-positive (Friedman, O'Byrne, & Roy, 2017). We were able to classify 62% of cases using these parameters (Friedman et al., 2017).

Our data showed that in Ottawa, during these four years, 70.9% (n = 66/93) of HIV diagnoses among persons unaware they were HIV-positive--regardless of whether the infection was acquired more or less than 12 months ago--were in MSM, 7.5% (n = 7/93) were in IDU, 3.2% (n = 3/93) were in MSMIDU (people with both risk factors), and 21.5% (n = 20/93) were in ACB (Friedman et al., 2017). MSM, IDU, and ACB thus accounted for 95.5% of HIV diagnoses among persons unaware they were HIV-positive in our city. A notable finding was that, for ACB, 80% (n = 16/20) of diagnoses among people unaware of being HIV-positive involved those whose infections were likely acquired more than 12 months ago, compared to 18% (n = 12/66) in MSM and 0% in IDU (Friedman et al., 2017). This highlights that, while MSM accounted for most new HIV diagnoses in Ottawa during 2011-2014, HIV infections among ACB remained undiagnosed for a longer period (Friedman et al., 2017). Ongoing data collection show these trends continue.

While efforts to address ongoing HIV transmission have historically focused on having persons eschew practices that transmit HIV (e.g., condomless anal or vaginal sex), they now include having HIV-negative persons use HIV medication before and after potential exposures (Tan et al., 2017). For this, HIV-negative persons take Emtricitabine/Tenofovir DF 200/300mg (the only medication currently approved in Canada for PrEP) daily or as needed, following the on-demand protocol established in one study (Tan et al., 2017). Known as pre-exposure prophylaxis (PrEP), data suggest that, when taken as prescribed with appropriate clinical monitoring and condom use, PrEP can prevent HIV acquisition by up to 96% in MSM (Tan et al., 2017). One study among IDU identified a 74% reduction in HIV incidence, although it is difficult to interpret PrEP efficacy from this study because injection drug use, drug equipment sharing, and sexual contact with more than one partner all decreased during the study (Tan et al., 2017). Meanwhile, studies among males and females with opposite sex partners yielded mixed results. Among the effective studies, risk reduction ranged from 62% to 96% (Tan et al., 2017). The FEMPrEP and VOICE studies, in contrast, did not show any reductions in HIV incidence among participants using PrEP (Tan et al., 2017). The reasons for such discrepancies in findings might be variable serum levels of PrEP, suggesting that participants in some studies were not taking medication (Tan et al., 2017).

In November 2017, to help nurses, nurse practitioners, and physicians provide PrEP to their patients who might be at-risk for HIV, the first Canadian guidelines about PrEP were released in the Canadian Medical Association Journal (Tan et al., 2017), with a clinical update in June 2018 (Tan & Hull, 2018). These guidelines recommended clinical parameters for PrEP assessment, prescription, and monitoring. Also included were details about who should use PrEP. These recommendations were consensus statements built using the GRADE principles of guideline development. Known limitations of this method are that they are restricted to what is known from published evidence, and subsequent agreement in interpretation among the panel (1) who produces the guidelines (Feder, Eccles, Grol, Griffiths, & Grimshaw, 1999; Woolf, Grol, Hutchinson, Eccles, & Grimshaw, 1999).

In this issue of the Canadian Journal of Human Sexuality, Nelson et al. (2019) criticize these guidelines, using the keyword "racism" and stating that they were "a recipe for increasing racial and gender disparities in HIV infection". Nelson et al.'s (2019) main argument is that ACB in Canada account for a sizeable number of new HIV infections each year, and yet were not identified in the guidelines as a priority target population. We agree with Nelson et al. (2019) about the importance of HIV prevention, including PrEP, among ACB (who account for many new HIV diagnosis in our local area, and who appear to be diagnosed late).

With a general goal to build on the work of Nelson et al. (2019) and further engage with the literature on HIV care, we propose an in-depth analysis of their commentary. As such, in this article, we review the current Canadian PrEP guidelines (focusing on the clinical indications for PrEP, not the nursing/medical care associated with providing PrEP), and then discuss Nelson et al.'s (2019) commentary, highlighting their key arguments and providing insights into the areas that we feel require clarifications and further analysis. Lastly, we present our nurse-led PrEP clinic in Ottawa (entitled PrEP-RN, for PrEP-Registered Nurse), and show how we assess peoples need for PrEP--in keeping with the analysis and arguments presented in this paper.

A REVIEW OF THE CANADIAN PrEP GUIDELINES

From the Canadian guidelines (Tan et al., 2017), there is a strong recommendation to provide PrEP to MSM and transgendered males who both (1) engage in condomless anal sex (penetrative or receptive) and (2) have an additional risk factor, such as diagnosed sexually transmitted infections (STIs), recurrent use of HIV post-exposure prophylaxis (PEP), an "HIV-positive partner with substantial risk of transmissible HIV", or a HIRIMSM score [greater than or equal to] 11. The HIRI-MSM calculates risk based on individual and group-level risk factors, specifically age, number of male sex partners, number of male sex partners with whom a person engaged in anal sex, number of sex partners who were HIV-positive, and drug use (Tan et al., 2017).

Importantly, the focus on "substantial risk of transmissible HIV" among HIV-positive partners reflects the virtually non-transmissible nature of a supressed viral load (Rodger et al., 2016), but that there is a difference between when this viral suppression is known versus reported (Conroy, Gamarel, Neilands, Dilworth et al., 2016). In the guidelines, the word "believed" differentiates this situation from when clinicians "know" based on clinical records (Tan et al., 2017). For example, while Rodger et al. (2016) found a transmission rate of 0% among persons with known viral suppression, Conroy, Gamarel, Neilands, Sauceda et al. (2016; Conroy, Gamarel, Neilands, Dilworth et al., 2016) found discrepancies between beliefs about viral load and its actual levels. Conroy, Gamarel, Neilands, Sauceda et al. (2016) stated that, among 236 male couples, "92.4% [of the HIV-positive partners] reported they were virally supressed at the last clinic visit, [while only] 62.4% were actually virally suppressed as indicated by blood tests, and 77.8% of their partners reported they believed their HIV-positive partner was virally supressed" (p.e32). Moreover, in Rodger et al.'s (2016) study, where the transmission rate was 0%, the authors excluded 5.5% (n = 55/1004) of participants from analysis because their viral levels exceeded 200 copies/ mL. The guidelines thus highlight the need to differentiate between laboratory values and self-report, but that, if viral suppression is present, then the probability of HIV transmission is "low but nonzero" (Tan et al., 2017, p. E1449).

For IDU, there is a weak recommendation for those who "share injection drug paraphernalia with persons with a non-negligible risk of HIV infection", with non-negligible risk defined as "HIV-positive with a viral load > 40copies/mL, HIV-status unknown but from a population with high HIV prevalence, [and] HIV-positive and believed to have a viral load < 40 copies/mL, with concomitant STIs" (Tan et al., 2017, p. E1450). This recommendation exclusively applies to injection drug paraphernalia, to the exclusion of other equipment, such as crack pipes.

For "heterosexual exposure", there is a strong recommendation for PrEP in serodiscordant relationships wherein there is "a substantial risk of having transmissible HIV", which is defined as an HIV-positive person with a viral load > 40 copies/ mL, or a person of unknown HIV status from a population with high HIV prevalence compared to the general population; the clinical update specifies that most studies use a viral load of 200 copies/mL (Tan et al., 2017, p. E1450). The appendix to the guideline specifies that this serodiscordance must be known, meaning that the second item about prevalence does not apply (Tan et al., 2018). The appendix also specifies, however, that, "[wjhen considering PrEP for heterosexual adults on the basis of having multiple or unknown-status partners, practitioners must make decisions on a case-by case basis, using local epidemiologic data and patient-reported risk behaviours [and] exposures in the partner" (Tan et al., 2018, p. 15). Thus, while the guidelines are prescriptive about who qualifies for PrEP, they respond to local epidemiologic data and patient risk factors. Nonetheless, they only explicitly recommend PrEP for MSM with behavioural risk factors (condomless sex and an STI diagnosis or PEP use), I DU who share drug equipment with HIV-positive partners who are not virally supressed or of unknown status, and heterosexuals in known serodiscordant relationships who engage in condomless sex with HIV-positive partners who are not virally supressed.

NELSON ET AL.'S CRITIQUE

In this issue of the Canadian Journal of Human Sexuality, Nelson et al. (2019) critique the Canadian PrEP guidelines. In brief, these authors argue that, while guidelines in general can structure care, they can also restrict it. Nelson et al. (2019) asserted that the Canadian PrEP guidelines, specifically, undermine access to PrEP because they are not sensitive to the parameters surrounding HIV transmission among ACB communities and women. The outcome is that these guidelines could (unintentionally) limit access for these persons. While not listed in their title or main points, Nelson et al. (2019) mention that their assertion extends to Indigenous persons in Canada. As with Nelson et al. (2019), we find it important to engage critically with the tools that guide our practice, and address their effects, irrespective of intention. We will now discuss these authors' points in more detail.

First, Nelson et al. (2019) noted that the Canadian guidelines differs from the Health Canada approved PrEP indication for Emtricitabine/Tenofovir DF 200/300mg, which is to "prevent the risk of sexually acquired HIV-1 infection in adults at high risk". The product monograph then defines "high risk" as "when a partner is known to be HIV-positive, or if a person has sex within a high prevalence area or network and/or has one of: inconsistent or no condom use; STI diagnosis; exchange sex; illicit drug use or alcohol dependence; incarceration; partners of unknown HIV-status with any of the foregoing factors" (Gilead, 2018, p. 4). Based on available epidemiologic data (Canadian, from Toronto and our Ottawa data), ACB communities fulfill the "high prevalence network" criterion. As an extension, per the product monograph, ACB men and women should be offered PrEP if they fulfill any other criterion, such as condomless sex, an STI diagnosis, etc. This, however, is not in the guidelines; instead, these men and women require a known serodiscordant sexual partner who has a viral load > 40 copies/ mL, which requires that partners disclose their HIV-positive status, and that information about the partner's viral load is known (Tan et al., 2017). As Nelson et al. (2019) aptly noted, obtaining this information is not always possible, especially in relationships involving money or resources (e.g., sex trade work, survival sex, exchange sex), illicit drug use, and/or gender power dynamics--which are precisely the parameters listed in the product monograph, but not the guidelines (Gilead Sciences, 2018; Tan et al., 2017).

Nelson et al. (2019), moreover, highlighted that, because the Health Canada approved factors of illicit drug use and incarceration are not equally distributed within the population (Malakieh, 2018), current Canadian PrEP recommendations may exacerbate inequities among marginalized populations by not including the risk factors specific to these groups. To explain further, with incarceration being a known risk factor for HIV acquisition, and with the rates of incarceration being higher among ACB and Indigenous populations in Canada (Malakieh, 2018; Owusu-Bempah, 2014), Nelson et al. (2019) argued that to ignore these risk factors is to overlook items that greatly contribute to ongoing HIV transmission among these groups. Different factors affect HIV transmission within diverse groups, but to not include those that affect ACB and Indigenous groups, for example, could limit PrEP access to these persons (Nelson et al., 2019).

In analyzing the guidelines regarding the above-mentioned criticism, the online appendix notes that, while specific indications exist for MSM, IDU and male-female exposures (as noted above), this does not mean persons who do not fulfill these parameters should not receive PrEP (Tan et al., 2017). Providers, instead, should rely on local epidemiologic correlates and patient specific factors. This means that the guidelines should be considered indications for use, not exclusion criteria for others who might benefit from PrEP, such as ACB, Indigenous persons, and women. In this regard, Nelson et al. (2019) speak to the limits of guidelines, but equally engage in the common misunderstanding about their use: that is, guidelines summarize available evidence, and, as a result, remain silent about practice issues that are not yet well documented in the literature (Guyatt, Schunemann, Djulbegovic, & Akl, 2015). In other words, if Canadian PrEP guidelines are silent about a specific population subgroup this does not mean they should not receive PrEP. This is a common misconception that a lack of evidence for or in support of certain practices is equivalent to being evidence against their use (Altman & Bland, 1995). The guidelines do not say to not provide PrEP to these persons, just that the available evidence for PrEP among them is limited.

Such a limitation in knowledge about ACB communities and PrEP are thus codified in, and propagated by, the guidelines. As Woolf et al. (1999) stated, "scientific evidence about what to recommend is often lacking, misleading, or misinterpreted, [and] even when the data are certain, recommendations for or against interventions will involve subjective value judgements when the benefits are weighed against the harms" (p. 529). These are known shortcomings of GRADE developed guidelines (Guyatt et al., 2015), and are aptly critiqued by Nelson et al. (2019).

Although guidelines are not necessarily built with the intention to exclude by summarizing available evidence, they may do so in practice (Woolf et al., 1999). On that note, we share Nelson et al.'s (2019) concerns with respect to the application of guidelines in practice and their effects. To explain, as described by Woolf et al. (1999), guidelines may restrict PrEP to only those persons explicitly listed in the guidelines because, for example, prescribers who are less familiar with PrEP may follow the published recommendations without considering--or even knowing--the details that warrant individual tailoring of the guidelines; e.g., incarceration, engaging in sex trade work, etc. Such lack of familiarity, moreover, may be common in primary care, where providers are generalists and may only have a few patients in their practices who would benefit from PrEP (Turner, Roepke, Wardell, & Teitleman, 2018). As such, the guidelines may restrict access to groups not listed as "indicated" for PrEP in the guidelines (although they are in the product monograph), especially among primary care providers who may follow the guidelines explicitly.

Second, regarding practice implications, Nelson et al. (2019) highlighted the need to offer PrEP to ACB who are diagnosed with STIs. They supported this assertion by reporting how, in their research in Toronto, while STIs were a risk factor for HIV acquisition among MSM "(OR = 2.9, 95% CI 0.6, 13.3, p < .01)", they were a greater risk factor among heterosexual ACB men "(OR = 79.9, 95% CI 11.5, 555.7, p < .01)" (p. 2). In reviewing the supporting reference, it is important to note that Nelson et al.'s article containing the research data was listed as "submitted" (not published or accepted) and did not specify which STIs they discussed. As a result, we are left to wonder if they meant to include all bacterial STIs (gonorrhea, chlamydia, syphilis), any STI diagnosis (so the previous list plus herpes and warts), or limit their analysis to a single STI (e.g., syphilis exclusively). We suspect these authors meant syphilis because they then discussed it shortly thereafter. However, ambiguity remains regarding the stage of syphilis the authors refer to, and we can only assume Nelson et al. (2019) meant infectious syphilis and not late latent syphilis, which also disproportionately affects ACB. Building their point on unpublished data makes it difficult to assess their assertion. (2)

Nevertheless, based on the high rates of HIV and infectious syphilis co-infection in Canada (Chouhdri, Miller, Sandhu, Leon, & Aho, 2018; PHO, 2015), we think the relationship Nelson et al. (2019) discussed is unsurprising. PrEP should likely be considered for anyone diagnosed with infectious syphilis because, with elevated co-infection rates (Chouhdri et al., 2018; PHO, 2015), a syphilis diagnosis signals that a person may be having sex within a network of elevated HIV prevalence. In Canada, infectious syphilis is also most commonly diagnosed in MSM (Choudhri et al., 2018), reinforcing that this infection is a proxy measure for high HIV prevalence in a persons sexual network. This finding may apply beyond MSM and ACB communities, but further research is needed.

Also needing more research is if this logic applies to gonorrhea and/or chlamydia, or if the link is limited to infectious syphilis. Knowing that gonorrhea and chlamydia induce localized cellular responses, which increase a person's biologic susceptibility to HIV due to an increased presence of HIV target cells and localized inflammatory responses (Mayer 8c Venkatesh, 2011; Ward & Ronn, 2010), it might be worthwhile to consider PrEP for persons with these STIs as well, especially if the infection(s) were detected rectally. Being localized infections, these STIs are only acquired at sites of sexual contact, and thus identify condomless sex involving the anatomical location(s) where the infection(s) was/were detected. Evidence from Vancouver identified an HIV incidence rate of 4.6 per 100 person-years for those diagnosed with rectal gonorrhea, signalling that rectal bacterial infections should likely warrant discussions about PrEP with persons in groups with high HIV prevalence (Hull, Edward, & Kelley, 2017).

Third, Nelson et al. (2019) highlighted important subcultural differences among ACB, compared to other populations affected by HIV, which makes their indications for PrEP unique. For example, they (2019) reported that ACB MSM are less likely to disclose same sex partners to healthcare professionals, compared to white MSM. While providers' lack of inquiry about sexual orientation undermines disclosure among ACB MSM, whatever the cause, the outcome is that providers may not offer PrEP to these men because they have no indication according to the guidelines; they are not known to either be MSM or to have partners diagnosed with HIV. This last point is important, as Nelson et al. (2019) reported that many ACB women who were diagnosed with HIV in Toronto were unaware their partners were HIV-positive. The problem is that the woman (and possibly both partners) were unaware of the serodiscordance in their relationships, meaning these women would not be indicated for PrEP using the Canadian PrEP guidelines. In contrast, according to the product monograph for Emtricitabine/Tenofovir DF 200/300mg, these women warrant PrEP (Gilead Sciences, 2018), which is appropriate considering elevated HIV prevalence among ACB (compared to the general population) and sexual practices that can transmit HIV.

After making this excellent point, Nelson et al. (2019) indiscriminately applied this logic to all women. They (2019) argued that PrEP "would finally enable women to exert control over their [HIV] prevention--independent of their male partner" (p. 2). While we endorse efforts to achieve prevention and empowerment among women, we respectfully disagree with Nelson et al.'s (2019) use of ACB women as a justification for why all women warrant PrEP. HIV prevalence among ACB, compared to the general population, is different (OHESI, 2017). The prevalence among the entire Canadian population is 0.2% (PHAC, 2015), compared to 11.1% among MSM and IDU in Ottawa (PHAC, 2011), with prevalence estimates among ACB not established but assumed to be similarly elevated. With a 36-fold difference in prevalence between high prevalence groups and the entire population in Ottawa (and greater differences having been identified in Toronto and Montreal, PHAC, 2011), it is important to remember that PrEP is not without risks or side effects. Emtricitabine-Tenofovir DF 200/300mg can affect kidney function, which is why renal tests are performed every three months for people using PrEP (Tan et al., 2017). Nelson et al. (2019) raised a good point about women, but did so without considerations that the use and provision of any medication is always a risk-benefit analysis. While Nelson et al. (2019) highlighted the benefits, they did not appear to consider the risks associated with their recommendation. As such, while the logic of providing PrEP to persons within networks of high HIV prevalence applies to ACB women, it may not for all women in Canada. Further research needs to explore this point.

Fourth, Nelson et al. (2019) raised issue with the fact that the guidelines discuss heterosexual exposure, versus the practices of vaginal and anal sex. This distinction is important because, as written, the guidelines conflate sexual orientation with sexual practices, when studies highlight that these two items are not interchangeable. For example, data from England show that many women who define as "lesbian" have had, and continue to have, male partners, albeit infrequently (Diamant, Schuster, McGuigan, & Lever, 1999). Adding to this is that women who had female and male partners had higher rates of diagnosed STIs and unplanned pregnancy (Mercer et al., 2007). This emphasizes that the important consideration for PrEP is not how one self-defines or identifies, but what one does sexually and with whom. While not raised by Nelson et al. (2019), we, furthermore, think that the term "relationship" is ambiguous, as the risk of HIV transmission relates to sexual contact, not relationships per se. We, consequently, feel Table 4 in the Canadian PrEP guidelines--while written for PEP--is preferable, although we must disclose that we may only think this because it is based on our work on risk assessments for PEP (O'Byrne, MacPherson, Roy, & Kitson, 2015). This table makes the risk assessment a combination of group prevalence and risk practices, and aligns with what we do in Ottawa.

THE OTTAWA MODEL: PrEP-RN

At this point, we turn our attention to our local PrEP clinic and detail our clinical procedures and preliminary findings. We do this to detail our approach to HIV risk assessments, which differ from the Canadian PrEP guidelines, and which we feel addresses some of the excellent issues that Nelson et al. (2019) aptly raised about the current Canadian PrEP guidelines.

To begin, on August 6th, 2018, we started offering provider-driven PrEP, which we entitled PrEP-RN (for registered nurse). Unique to our project is that it is wholly nurse-led and nurserun, in contrast to other models which are physician driven with nurses providing care within their PrEP care delivery models. We established this project as a research project, which the Ontario HIV Treatment Network (OHTN) funded. Data collection was prospective observational, and involved data extraction from patients' files. The Research Ethics Boards at the University of Ottawa and Ottawa Public Health approved data collection for PrEP-RN.

As part of this study, nurses who work for Ottawa Public Health began actively offering PrEP to persons with risk factors for HIV acquisition; this differs from many current PrEP programs, in which patients self-select for PrEP and seek services when they feel "at risk" for HIV. In our program, nurses offer PrEP to patients with risk factors for HIV acquisition, and do so irrespective of patients' perception of HIV risk. Also unique to our program is that these referrals are undertaken not only by nurses in the STI clinic, but also by public health nurses who follow-up on STIs from across the City of Ottawa. To explain further, in Ontario, by law, positive test results for gonorrhea, chlamydia, syphilis, and HIV are reportable to local public health units, whether they are untaken in STI clinics, hospital settings, or primary care clinics (Ontario, 1990). After being reported, public health nurses review these results to ensure patients are notified of their infections and treated correctly; these nurses also undertake follow-up with persons who could have been exposed to these STIs (i.e., "contacts") to ensure notification and testing (Ontario, 1990). Because these infections are risk factors for HIV, we use them as part of our risk assessment for PrEP. These public health nurses are thus a key component of PrEP-RN.

PrEP Risk Assessments

The HIV risk assessments for PrEP that our clinic and public health nurses undertake differ from the Canadian PrEP guidelines. Rather than following specific guideline statements for identifiable groups, we determine patients' risk of HIV acquisition based on their practices (sexual and drug use) and the HIV prevalence in their sexual or drug use networks. In combination, we use these two factors to determine risk and need for PrEP, and we do so to surmount what Woolf et al. (1999) noted as major limitation of guidelines: "What is best for patients overall, as recommended in guidelines, may be inappropriate for individuals" (p. 529). We thus make an assessment for each patient using a two-part risk assessment, which we detail now.

First, to determine risk practices, we use self-report and STI diagnosis, including site of these infections, where applicable (e.g., rectal versus oral versus urethral versus cervical infections for gonorrhea and chlamydia). Using self-reported sexual practices, we use Table 1 from the Canadian PrEP guidelines, which details a hierarchy of practices that transmit HIV, to determine the possibility of HIV transmission based on patients' practices (Tan et al., 2017). From this, condomless anal and vaginal sex and needle sharing are high risk (without differentiation for receptive versus insertive), oral sex is low risk, and manual contact is no risk (Tan et al., 2017). Acknowledging that patients may be reluctant to (or outright not) disclose same sex behaviour, condomless sex, drug use, etc., we also use clinical judgment (Petroll & Mosack, 2011). For example, we would assess that patients with a urethral or rectal gonococcal infection, who report 100% condom use, at least occasionally engaged in condomless sex. We also acknowledge the important point raised by Nelson et al. (2019) that disclosure about same sex male partners is less common among ACB men. Moreover, we draw on Vancouver data, which highlighted the following HIV incidence rates per 100-person years: 4.6 for rectal gonorrhea; 17.0 for concurrent rectal gonorrhea and syphilis (Hull et al., 2017). Self-reported behaviour and STI diagnoses thus constitute the first aspect of our assessment to determine each patients risk of HIV transmission were exposure to occur.

Second, to determine a persons probability of exposure, we stratify patients based on the estimated HIV prevalence in their networks. MSM, IDU, ACB, and persons from regions where HIV is endemic are considered high prevalence. We also consider regional rates of HIV among Indigenous persons, which are known to be high in certain areas of Canada (e.g., Saskatchewan). Anyone not belonging to these groups is considered low prevalence. We also use diagnoses of infectious syphilis to estimate probability of exposure. Knowing, for example, the high rates of syphilis and HIV co-infection, we consider a syphilis diagnosis to indicate a high HIV prevalence network. We similarly use a history of recent incarceration or of engaging in sex trade work, and the location of sexual practices (e.g., gay bathhouses), to name a few items, to estimate HIV prevalence. Because HIV prevalence is often higher in the foregoing groups and locations, we consider a history that includes these items to indicate that patients likely belong to high prevalence networks. Lastly, while we consider sexual contact with a person known to be HIV-positive to potentially be high-risk, we do not consider persons who are HIV-positive with a known suppressed viral load to be high risk. Instead, we focus on contacts with persons newly diagnosed with HIV, and for up to 12 months after diagnosis, as this is the average time it takes from diagnosis to viral suppression for almost all persons. We also acknowledge, as detailed above, the difference between "known" and "believed" viral suppression, noting that there can be a small discrepancy between these two states. Following the Canadian PrEP guidelines, for persons with suspected--but not known--HIV viral suppression, we consider the risk of transmission low but non-negligible and accept that risk is possible.

Once we obtained this information about the two parts of our risk assessment (risk practices and HIV prevalence), we plot these items on a two-dimensional risk matrix. See Figure 1. On the x-axis, we mark patients' risk practices; on the y-axis, we note the probability of HIV exposure. On this matrix, as prevalence increases (either because a patient belongs to an identifiable network, or because she/he/they has/ have an associated risk factor, such as syphilis, incarceration, or illicit drug use, which are factors associated with elevated HIV incidence and prevalence, or they are known HIV contacts), the probability of HIV exposure increases. If these factors are present, the patient moves up the y-axis. For possibility of HIV transmission, we use patients' reported practices, locations of detected STIs, and clinical judgment, which we mark along the x-axis. Vaginal and anal sex, for example, are high risk. We then plot the intercept of the lines from the y- and x-axes to stratify the patient as high, medium, or low risk.

Anyone classified as high-risk warrants PrEP, whereas those classified as low risk do not. Classification for these groups is simple: the benefits of PrEP outweigh the risks for the high-risk group, and the opposite is true for the low risk group. The medium risk group, in contrast, requires further assessment and counselling about risks, benefits, and preferences. Patients in this group also warrant an assessment of their risk tolerance. While one person may be low risk based on our assessment approach, s/he/they may have a low risk tolerance and may want PrEP to appease concerns about HIV acquisition. We feel, in opposition to the Canadian guidelines, that such persons should be offered PrEP, provided that the prescribing clinician obtains informed consent. If the patient consents knowing the risks, then PrEP should be provided because, as Nelson et al. (2019) noted, PrEP can "enable women to exert control over their prevention" (p. 2). We feel Nelson et al.'s (2019) point can be extended to any person who engages in receptive sexual contact (vaginal and/or anal), and applies to women, MSM, and transgendered persons.

This risk matrix identifies seven categories of patients. See Table 1. PrEP is warranted in the first three, case-by-case decisions need to be made for the fourth category, PrEP is likely not needed for the fifth category, and PrEP is not required for the sixth and seventh categories.

Category 1 includes people who engaged in practices that can transmit HIV with HIV-positive persons who have viral loads > 40 copies/mL. This is the highest risk scenario. Category 2 is people in high prevalence groups who have diagnosed STIs (syphilis, rectal gonorrhea or chlamydia) or PEP use. This group includes people with the highest objective risk indicators of HIV acquisition after known exposures. Category 3 is persons in high prevalence groups who engage in condomless anal or vaginal sex. PrEP is indicated for this group, which includes people with elevated probabilities of exposure (based on prevalence) who engage in practices that could transmit HIV, were they exposed. Category 4 is persons who belong to networks with high HIV prevalence, but who do not engage in practices that can transmit HIV due to, for example, condom use or avoiding such practices. We also include persons with known HIV-positive partners whose viral loads are believed to be supressed in this group. In these cases, while transmission is unlikely, it could occur due to condom malfunction (e.g., breakage or slippage), or if there is a discrepancy between what the persons believes or reports about their viral load and their actual viral load; in such cases, as has been seen in the published literature, the person may be incorrect in their beliefs about having a suppressed viral load. Category 5 includes persons who are known contacts of people who are HIV-positive with confirmed viral loads < 40 copies/mL. This is a low risk scenario, which does not warrant PrEP. Category 6 is persons who engage in practices that can transmit HIV within networks with low HIV prevalence. Although transmission could occur, exposure is improbable. While PrEP could be considered for these patients, it should be based on patient preference and risk tolerance. Lastly, category 7 is persons who do not engage in practices that transmit HIV and who belong to low prevalence groups. These patients do not need PrEP, and would be exposed to potential harms from PrEP without any possible benefits.

Case Examples

In their article, Nelson et al. (2019) used two examples to determine the sensitivity of the Canadian PrEP guidelines to detect risk of HIV acquisition among ACB populations and women. We now use these cases, plus two of our own, to demonstrate the outcomes of our risk matrix.

To begin, the first of Nelson et al.'s (2019) examples was an ACB man who reports condomless vaginal sex and is diagnosed with syphilis (which, as noted above, we assume is infectious syphilis). This man does not qualify for PrEP according to the Canadian guidelines, although he does fulfill the indications for PrEP in the medication monograph (Gilead Sciences, 2018). Using our risk matrix, this patient likewise qualifies for PrEP. Based on condomless vaginal sex, we consider him to have high risk practices, and, while his partners are female, his diagnosis of infectious syphilis raises his probability of HIV exposure to high risk. Figure 2a plots these two points, and circles the intercept in the high risk area of the matrix, showing that he warrants PrEP.

As their second example, Nelson et al. (2019) discussed an ACB woman who engages in condomless vaginal sex with a single male partner and is diagnosed with an STI; again, Nelson et al. (2019) did not specify which infection was identified, and we would consider, for example a diagnosis of infectious syphilis to signal higher risk than pharyngeal chlamydia. According to the Canadian guidelines, PrEP would not be indicated for this woman because she is not in a known serodiscordant relationship. Using our risk matrix, as with example 1, this woman would qualify for PrEP, albeit with a lower level of risk than the first example. See Figure 2b for this case.

Building on Nelson et al.'s (2019) case examples, we now further evaluate our risk matrix using two additional examples, the first of which is a white 17-year-old Canadian born female with male partners who does not use condoms for vaginal sex and is diagnosed with chlamydia. Based on our matrix, this female would be low risk and would not warrant PrEP because, although the possibility of HIV transmission would be high based on condomless vaginal sex, were she to be exposed, the prevalence of HIV among these women and their male partners is sufficiently low (at 0.2%) that her probability of HIV exposure is very low. When plotted, this female is low risk, and, based on a review of the risks and benefits of PrEP (renal damage and regular follow-up versus possibility of exposure), she would not warrant PrEP. See Figure 3.

To complete our analysis, we add a final example: a 34-yearold female sex trade worker who reports exclusive condom use for vaginal and anal sex. She would be high risk for HIV exposure based on sex work, but mid-range risk for sexual practices, related to condom use. When plotted on our matrix, she is medium risk. See Figure 4. Notably, this situation needs to be considered case-by-case, recognizing the power and economic dynamics that influence condom use in sex trade work (Argento et al., 2016). Based on these factors, we would offer PrEP to this patient.

What is useful about this risk matrix is that it is not restricted to specific indications about particular groups, such as are written in the Canadian PrEP guidelines. Instead, it assesses risk practices (with variance based on clinical judgment) considering a persons probability of exposure (using known prevalence estimates and other factors associated with elevated HIV prevalence, such as incarceration and sex trade work). We feel this matrix is sensitive to the need for PrEP among diverse groups, and can be used by clinicians when performing assessments. We also feel this matrix addresses some issues Nelson et al. (2019) raised about the Canadian PrEP guidelines.

PrEP-RN: Preliminary Uptake Data

As part of PrEP-RN, we offered PrEP to anyone who falls within the first three categories in Table 1. During the first four months of PrEP-RN (from August 6, 2018 through December 5, 2018), we offered PrEP to 163 patients, 159 of whom were male, 1 who was trans-male, and 3 who were female. The average age of these patients was 33.3 years. Within this group, none were Indigenous, and approximately 10 were ACB.

Of these 163 people to whom we offered PrEP, 103 fell within the first two risk categories of HIV contacts, and members of a high HIV prevalence group with an STI diagnosis or PEP use. The remaining 60 patients were in categories 3 and 4 (high prevalence and vaginal or anal sex, with or without condoms). Of those within the first two categories, 12 were ineligible (already HIV-positive or on PrEP). Of the 91 patients who were eligible, 40 (44%) agreed to PrEP and 51 (56%) declined it. Then, 38 of the referred patients presented for PrEP. This shows that, of the 91 persons who were eligible, 100% (n = 91/91) were referred, 44% (n = 40/91) accepted a PrEP referral, and 41.8% (n = 38/91) presented for care. Figure 5 overviews the PrEP cascade.

Among those who accepted and declined PrEP, the numbers and percentages were similar based on risk profiles, save those who our nurses deemed at high risk based on clinical judgment. More of such persons declined PrEP. See Table 2. Notably, one person who was diagnosed with infectious syphilis was diagnosed with HIV at his one-month follow-up PrEP assessment.

These findings show that PrEP-RN is a viable strategy for PrEP delivery to persons at high risk for HIV acquisition. Nurses were able to identify and offer PrEP to persons who were high risk based on our risk matrix (i.e., categories 1 through 3). This is important, as economic analyses suggest PrEP would reduce costs overall when targeted appropriately (Cambiano et al., 2018).

Interestingly though, the uptake rate for PrEP in our first four months of implementation was only 44% overall, suggesting that barriers to PrEP are not only a lack of access (related to prescribers and cost of medication), but also a lack of perceived need by persons in high prevalence groups and among those who are HIV contacts. For example, of the 35 persons to whom we offered PrEP after a diagnosis of infectious syphilis, only 45.7% agreed to a referral, despite an HIV incidence rate of 3.6 per 100-person year in Vancouver, and other PrEP studies showing a 1 in 20 seroconversion rate among persons diagnosed with infectious syphilis (Pathela, Braunstein, Blank, Shepard, & Schillinger, 2015; Solomon et al., 2014). As noted by Grulich et al. (2018), while PrEP can be effective for HIV prevention at the individual level simply though its use, for population level prevention effects to occur, PrEP roll-out should be "rapid, targeted, and high-coverage" (p.e629). Our preliminary results suggest that, while PrEP-RN fulfills the rapid and targeted components, it does not achieve high-coverage, based on the finding that over half of these high-risk persons declined PrEP.

Future efforts thus need to focus on increasing access to healthcare and PrEP medications, and on interventions for patients to appreciate the utility of PrEP for their HIV prevention. Such campaigns should target all high prevalence groups, including MSM, IDU, and ACB communities. Indigenous communities should be included as well. It is particularly important that efforts are made to expand PrEP beyond white MSM to ensure inclusion of persons who are members of the other groups in Canada who are disproportionately affected by HIV transmission.

CLOSING REMARKS

PrEP is now an efficacious component of the HIV prevention armamentarium, and recent Canadian guidelines detail how it should be prescribed and monitored, in addition to who should be considered for PrEP. Notably, the indications in the Canadian guidelines differ from the Health Canada approved indications listed in the product monograph for Emtricitabine-Tenofovir DF 200/300mg (the only drug approved in Canada for PrEP). In reviewing these differences, Nelson et al. (2019) aptly noted that the Canadian guidelines do not have specific indications for ACB communities and women. These authors raised the same point for Indigenous persons in Canada.

Building on Nelson et al.'s (2019) work, our goal was to further engage with the literature on HIV care, and present an in-depth analysis of their paper. As such, we reviewed the current Canadian PrEP guidelines, and, considering Nelson et al.s (2019) arguments, engaged in three main discussion and clarification points. First, Nelson et al.'s (2019) critique was premised on the assumption that a lack of indication within the Canadian guidelines constitutes an exclusion criterion in practice. We clarified the general purpose of practice guidelines and that a lack of indication does not denote exclusion, while agreeing with Nelson et al.'s (2019) critique regarding guideline application in practice and possible negative effects when applied to specific subgroups of the population where data are lacking. Second, Nelson et al.'s (2019) critique is further premised on an analysis of PrEP indications that is presented without explicit consideration of mitigating risks associated with any pharmacologic intervention. In effect, the proposed assessment does not capture the complexities of using medication for prevention purposes. All medications have risks and side effects, and these must be considered as part of any analysis of pharmacologic interventions. Such analyses should apply to all interventions. Third, Nelson et al. (2019) used their argument about ACB women to assert that all women in Canada might warrant PrEP. This likely over-extends the utility of PrEP (and consequently undermines their arguments), and does so by using a group of high prevalence to justify PrEP among many women of low prevalence; an argument that extends back into our previous point of contention, which is that benefits and risks must be considered in any discussion of PrEP and HIV prevention.

To make applicable the critique we bring to Nelson et al. (2019) work, we then provided an overview of, and initial uptake about, a practice model (our Ottawa-based PrEP-RN clinic), which operates in ways that addresses many of Nelson et al.'s (2019) concerns about the current Canadian PrEP guidelines. In our practice model, rather than focusing on specific indications for identifiable populations, a two-dimensional risk matrix is used to assess a patient's probability of HIV exposure (based on group prevalence) and his/her/their specific risk practices for HIV transmission (sexual and injection drug use practices); an approach that proves to be inclusive of "invisible" subgroups in the guidelines (includes ACB communities) to better define eligibility for PrEP. In brief, despite our differences in the interpretation of guideline use and application, we think that Nelson et al. (2019) raised important points that warrant further investigation, dialogue, and debate, as they have potential real-life impact for persons in Canada. We thank these authors for bringing their critique forward and engaging both clinicians and researchers on this topic.

Correspondence concerning this article should be sent to Patrick O'Byrne, School of Nursing, University of Ottawa, 451 Smyth Road, Ottawa, ON K1H 8M5, Canada. E-mail: pjobyrne@uottawa.ca

doi:10.3138/cjhs.2018-0050

NOTES

(1) O'Byrne was a member of this panel and co-authored the Canadian guidelines in question. His involvement was to chair the working group about assessment and provision of PEP.

(2) It was later clarified verbally with the authors that the intention was to speak of infectious syphilis.

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Patrick O'Byrne (1,2), Lauren Orser (1), Jean Daniel Jacob (1), Andree Bourgault (2), and Soo Ryun Lee (2)

(1) School of Nursing, University of Ottawa, Ottawa, ON

(2) Sexual Health Clinic, Ottawa Public Health, Ottawa, ON

Caption: Figure 1. PrEP risk matrix

Caption: Figure 2. High risk matrix

Caption: Figure 3. Low risk assessment

Caption: Figure 4. Medium risk assessment
Table 1. Risk Categories for PrEP

Category                     Group                     Risk

1           HIV contact (of an HIV-positive person    High
            with transmissible HIV) who engages in
            practices that transmit HIV

2           Member of high HIV prevalence group       High
            with diagnosed STI or PEP use

3           Member of high HIV prevalence group       High
            and condomless anal or vaginal sex

4           Member of high HIV prevalence group       Medium
            and condoms for anal or vaginal sex

5           HIV contact (of an HIV-positive person    Low
            with non-transmissible HIV)

6           Member of low HIV prevalence group        Low
            and condomless anal or vaginal sex

7           Member of low HIV prevalence group        Low
            with condoms

Table 2. Risk Factors

                            Accepted     Declined    Ineligible
                              PrEP         PrEP       for PrEP

HIV contact                 5 (12.5%)   5 (9.8%)     8 (66.6%)

PEP use                     4 (10%)     6 (11.8%)    2 (16.7%)

Gonorrhea or Chlamydia      3 (7.5%)    3 (5.9%)     0
(rectal infection or LGV)

Syphilis                    16 (40%)    19 (37.2%)   2 (16.7%)

Clinical judgment           6 (15%)     12 (23.5%)   0

Multiple risk factors       6 (15%)     6 (11.8%)    0
(of above)

Totals (n = 103)            40          51           12

Figure 5. The PrEP care cascade

Eligible    91
Referred    91
Accepted    40
Presented   38

Note: Table made from bar graph.
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Author:O'Byrne, Patrick; Orser, Lauren; Jacob, Jean Daniel; Bourgault, Andree; Lee, Soo Ryun
Publication:The Canadian Journal of Human Sexuality
Article Type:Report
Geographic Code:1CANA
Date:Apr 1, 2019
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