Introduction

The human papillomavirus (HPV) is the most common sexually transmitted infection (STI) worldwide and is a cause of anogenital cancers [1]. Among gay, bisexual, and other men who have sex with men (GBM), the prevalence of high risk HPV (potentially cancer-causing HPV) in the anal canal remains high, with one Canadian study documenting these infections in 67.6% of HIV-positive and 51.7% of HIV-negative GBM participants [2]. Consequently, despite great advances in HIV treatment and care, the incidence of HPV-associated anal cancers continues to increase among HIV-positive GBM [3–4], with rates approximately 100-fold that of the general population [5–6]. Fortunately, HPV vaccination has proven efficacy in preventing both anogenital warts (condyloma) in males and anal pre-cancers (anal intraepithelial neoplasia; AIN) in GBM up to the age of 26 [7].

In 2006, the quadrivalent HPV vaccine (Gardasil) was first approved by Health Canada for females aged 9 to 26, covering the most common wart-causing HPV types (i.e., HPV-6 and -11) and the most common high risk or oncogenic types (i.e., HPV-16 and -18) [8]. The following year it was provided at no cost to girls between the ages of 9 and 13 across Canada. In 2010, approval was expanded to include males aged 9 to 26 and in 2012, Canada’s National Advisory Committee on Immunization (NACI) recommended the quadrivalent HPV vaccine for all males who have sex with males who are age nine years and older [9]. However, only in 2016 did the province of Ontario expand its coverage of HPV vaccination to include boys aged 9 to 13 years, as part of the universal school-based program, and GBM up to 26 years of age as part of a targeted program [10]. The HPV vaccine was made freely available to boys in other provinces across Canada prior to this time, and this change in policy occurred after substantive pressure from community activists, doctors, and researchers across Ontario [11].

In 2015, Health Canada approved a 9-valent vaccine (Gardasil-9), which adds five additional oncogenic types to the quadrivalent (helping to protect against anal cancer caused by HPV types 16, 18, 31, 33, 45, 52, and 58 in addition to genital warts caused by HPV types 6 and 11) [8]. However, currently only the quadrivalent vaccine is covered under provincial insurance programs. Without insurance, the out of pocket cost for all three doses of the quadrivalent HPV vaccine is around $420 CAD [12] and approximately $560 CAD for all three doses of the 9-valent Gardasil vaccine [13].

A post-hoc analysis of vaccine benefit in a cohort study of GBM aged 26 years and older demonstrated efficacy in preventing anal condylomas [14]. Studies with HIV-positive adult males [15] and boys [16] suggest that it is both immunogenic and safe in these populations, with a subsequent study in the same HIV-positive adult male population demonstrating persistent immunity over two years later [17]. One fundamental question that has remained unanswered is the utility of HPV vaccination for those who are older (i.e., >26 years) and those with known prior exposure to HPV. For example, in the United Kingdom it has been recommended that some GBM up to the age of 45 could benefit from HPV vaccination, including men living with HIV, despite previous probable HPV infection [18].

Moreover, despite the high prevalence of anal canal HPV in HIV-positive GBM, one Canadian study demonstrated that no individual had all 9 HPV types covered by the 9-valent vaccine [19], suggesting that some benefit could be derived from vaccination particularly for oncogenic strains 16 and 18. Further, a retrospective analysis of AIN recurrence rates in GBM, found that those who were vaccinated had a 50% reduction in AIN recurrence after ablative therapy (i.e. the surgical removal of anal cancer precursors or anal dysplasia) [20].

Much of the research on HPV vaccine uptake among GBM has been quantitative and has indicated that many GBM had very limited awareness of HPV’s cancer risks for GBM, but maintain a strong willingness to become vaccinated once informed of the effectiveness of the vaccine [21–24]. Some studies have also pointed to concerns with side effects [23], stigmatization [20], and vaccine effectiveness [20, 25]. HIV-positive GBM have been shown to have similar awareness and vaccine acceptability levels as HIV-negative men, and have also indicated increased levels of worry of the risks of HPV-related illness [26]. Qualitative research with GBM in North America and the United Kingdom has produced similar findings, demonstrating that GBM often report a willingness to be vaccinated despite limited awareness and understanding of HPV risks [27–28].

To the best of our knowledge, there is currently no published qualitative research that focuses exclusively on the HPV vaccination practices of GBM living with HIV in Canada. In this article, we explore HPV vaccination barriers and hesitancy among HIV-positive gay men in Canada. We conducted in-depth qualitative interviews with gay men living with HIV as part of the HPV Screening and Vaccine Evaluation (HPV-SAVE) Study. HPV-SAVE investigated HPV and anal cancer screening for gay men living in Toronto, Ottawa, and Vancouver. As part of this work, we have examined variable methods to anal cancer screening (i.e. cytology [anal Pap smears] and HPV testing) and treatment options (via a trial comparing ablative treatment to surveillance alone for anal dysplasia/pre-cancerous lesions) for HIV-positive gay men and other men who have sex with men. Participants were interviewed after undergoing anal cancer screening via cytology (i.e., anal Pap test) from their primary care doctors in Toronto. Our objective was to inductively examine participants’ narrative accounts of their knowledge, experiences, and perceptions related to HPV and the HPV vaccine in order to understand the production and organization of HPV health literacy and vaccine uptake.

Methods

Between November 2016 and July 2017 we conducted 25 in-depth, semi-structured qualitative interviews [29] with gay men living with HIV in Toronto. 24 out of 25 study participants we interviewed identified as gay, leading us to use this language to describe our sample. However, one participant did indicate both “Two-Spirit” and “Don’t know” on their sociodemographic questionnaire (See Table 1). When quoting this participant we have specifically recognized the way in which he identified.

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Table 1. Characteristics of interview participants.

https://doi.org/10.1371/journal.pone.0207953.t001

Prior to beginning the study, a community advisory board (CAB) was formed. The CAB was composed of members living with HIV, community health policy advocates, early career academics, physicians, and researchers with statistical and epidemiological expertise. The CAB met quarterly and informed the qualitative study design, interview question development, recruitment strategies, and the interpretation of preliminary findings.

Qualitative study participants were purposively recruited from a subsample of men who took part in the larger HPV-SAVE study and who indicated a willingness to be contacted for additional research activities. These participants were initially contacted by phone or email and drawn from three participating primary care clinics and one outpatient infectious disease clinic in Toronto. We recruited participants who were at various stages of the anal cancer screening process, including those who had different anal Pap results, treatment experiences, and HPV vaccination histories. We iteratively reviewed our data to inform our purposive sampling strategy following the principle of theoretical saturation [30]. See Table 1 for a summary of key participant information including HPV vaccination history and socio-demographic information.

With the exception of one interview conducted by phone for accommodation reasons, all interviews were conducted in-person at the University of Toronto in a private meeting room. Under the supervision of the first author (DG), the qualitative interviews were conducted by the second author (MG) who is a postdoctoral research fellow and a trained qualitative researcher. Participants provided informed written consent prior to the interview. Interviews were approximately an hour in length, ranging between 30–75 minutes. Participants received a $30 CAD honorarium. The study received ethics approval from the University of Toronto HIV Research Ethics Board.

The following key domains were explored: (1) general awareness and understanding of HPV and anal cancer risks; (2) social and cultural contexts informing HPV and sexual health related decision-making; (3) motivations and experiences related to anal cancer screening; (4) other anal and gastrointestinal disease and STI treatment experiences; and (5) knowledge, perceptions and experiences related to the HPV vaccine. While this last interview domain is the primary focus of the analysis presented in this paper, we draw upon the interviews in their entirety given that in most instances the HPV vaccine was discussed by participants earlier on in the interview and connected to other key interview questions, including men’s HPV knowledge and anal cancer screening motivations. Interviews were audio recorded, transcribed verbatim, and reviewed for accuracy.

QSR NVivo 11 qualitative software was used to code transcripts following Grounded Theory [30–31]. As Charmaz explains, Grounded Theory is a set of methods that “consist of systematic, yet flexible guidelines for collecting and analyzing qualitative data to construct theories ‘grounded’ in the data themselves” [32]. Using an iterative, constant comparative method [33], we systematically reviewed and coded transcripts as interviews were completed. We wrote codes for sections or units of texts, and created memos that expanded upon sections of coded text and described relationships across the codes. Because our qualitative coding was conducted concurrently with the data collection process, we were able to iteratively refine our interview guide and explore emergent themes in subsequent interviews [34–35].

Results

Cost and perspectives on policy

Only a few participants reported being aware that the HPV vaccine is freely available to men in Ontario who are 26 years old and under. When informed about coverage, most said they saw this as important even if they were not able to benefit personally from this recent shift in coverage. Some men, however, did express discontentment over previous and current strategies governing HPV vaccination coverage. For example, one participant argued that the previous approach focusing only on cisgender girls and women was an example of the government being “sexist” and described the issue of HPV among gay men with a high degree of urgency: “Like, this is not something we should be playing around with. This is something that should've been done a long time ago, because too many people’s lives depend on it now (31 years old, vaccinated).

Another participant described having a very strong interest in being vaccinated but was prohibited entirely by the costs. He vocalized very strong critiques against the current health policies restricting free access to gay men and other men who have sex with men:

I think the government's being short-sighted, that covering things like this is, in the long run, a far smarter thing to do. You pay a couple of hundred bucks for a vaccine or you pay thousands of dollars for someone's chemotherapy treatment. It's just, the math is ridiculous on these things. (53 years old, not vaccinated)

When informed about coverage for boys and men, including younger gay men, he also vocalized frustration: “Yeah, but again, why under 26? I mean, that's ridiculous. It's… very frustrating.”

Discussion

Our interviews were an opportunity to qualitatively investigate HPV vaccine decision-making among older HIV-positive gay men in Toronto, Ontario, Canada. Among the participants we interviewed, men reported no significant degrees of resistance to the general idea of being vaccinated for HPV. The majority of participants did not express significant concerns about side effects, vaccine efficacy, or the necessity of being vaccinated. When presented with the evidence on HPV-associated cancer risk for GBM, most participants became interested in vaccination. Despite this, the majority of the men in our sample have not been vaccinated for HPV, and many remained undecided about vaccination, even after they had been screened for anal cancer as part of their engagement in the HPV-SAVE Study.

Two primary factors appeared to have facilitated a degree of vaccine hesitancy or reluctance among our participants. The first was a primary lack of risk perception and health literacy about HPV cancer risks for men, including gay men. The association between HPV, women, and cervical cancer played a significant role in shaping our participants’ interpretation of themselves as being at risk for HPV and the limited information they had about HPV and anal cancer. Even when participants were aware of HPV risks, for many, these gendered associations made HPV less of a priority. Some participants remained hesitant about the HPV vaccine even after they had received abnormal cytology and histology test results and were undergoing treatment for anal dysplasia. All participants who articulated that HPV vaccination was not strongly recommended or encouraged for them by their primary health care provider said that they decided not to be vaccinated. Our research supports the findings of previous studies that have found physicians’ recommendations to be highly correlated with an increased likelihood of patients accepting to be vaccinated for HPV [24], underscoring the importance of receiving clear recommendations from primary health care providers.

The second primary factor that led to vaccine hesitancy or reluctance was the price/out of pocket expense of the vaccine. Participants’ decision-making processes regarding vaccination appeared to be frequently shaped by cost. In men’s narrative accounts, risk perception and cost appeared to inform men’s decisions both independently and co-constitutively. Sometimes participants reported not pursuing active questioning about the HPV vaccine with their physician, even when they had the resources and insurance to pay for it, as they did not consider themselves to be at high risk. Other participants expressed concerns about the significant costs of the vaccine, but their strong sense of individual risk perception appeared to make them decide that vaccination was the right health decision for them. However, some patients who considered themselves to be at a significant risk and the vaccine to be a valuable intervention, remained reluctant or hesitant due to the cost. Finally, some participants explained that they understood themselves to be at risk of HPV-related illnesses but they were unclear if they would benefit from vaccination, having likely been infected with HPV already. This is despite the fact that the NACI recommends vaccination for all GBM over the age of 9 [9].

As such, notwithstanding their noted acceptability of vaccination (i.e., the idea/principle of getting vaccinated in general) reluctance remained in relation to HPV vaccination. Viewed in this way, our participants appeared to be closer to the “acceptance” end of the vaccine hesitancy continuum [36], with a number of interrelated obstacles preventing vaccination. Our analysis points to a variety of interrelated structurally produced vaccine hesitancies. Rather than a property of individuals refusing vaccination, conceptualizing the production of vaccine hesitancy in this way elucidates how social systems—i.e. media, health promotion campaigns, public policy, physician recommendations—serve to create environments and knowledge systems in which people are less likely to become vaccinated due to dominant discursive frames of risk and persistent resource barriers to biomedical interventions.

Given these structurally produced hesitancies in our sample, it was evident that a clear and strong recommendation by a physician was a primary facilitator to be vaccinated. This poses challenges for physicians who have to balance communicating the possible benefits of vaccination with respecting how their patients’ decision-making may be constrained by finances. However, physicians should be mindful not to communicate the vaccine as being less essential because of the costs. Physicians serving HIV-positive patients should readdress the issue of vaccination annually, to see if a patient’s financial situation has changed, and to clarify the benefits of vaccination.

This qualitative analysis complements emergent quantitative findings on HPV vaccination with HIV-positive men in Ontario [37]. For example, among 678 men interviewed using a structured questionnaire, many had either not heard of HPV (20%) or had heard the term but did not know what it was (25%). Among men familiar with the term (n = 398), only 51% knew that HPV can cause anal cancer and 56% knew that people with HIV are at higher risk for cancers caused by HPV. Many thought their chance of getting HPV was zero (19%) or low (36%). Sixty-three percent had heard of the HPV vaccine and 44% knew that it was recommended for males, but only 13% reported that a health professional discussed the vaccine with them and 6% were vaccinated. Men said that they would be likely/very likely to get vaccinated if it were offered free of charge (81%), if they had to co-pay $30/dose (59%), or pay full price (18%).

Our work also complements international epidemiological literature that has found limited awareness of HPV vaccine availability for men [17, 25], the belief that HPV is predominately a risk for cervical cancer among cisgender women [38], and a limited understanding of anal cancer risks [17–18, 20], as persistent barriers to vaccination. This quantitative research has also underscored that the costs of the HPV vaccine are major impediments to vaccine uptake [17–18, 24, 39].

Our analysis is subject to several limitations. We exclusively focused on HIV-positive GBM. These men may have different understandings of the necessity of the HPV vaccine than HIV-negative GBM, because they are at higher risk for HPV associated cancers [31]. Our participants also tended to be older (mean age of 50.4 years old), white, and identified as gay males. We did not interview any transgender males. Our participants were also recruited from a clinical trial on anal Pap testing and thus the participants may be more active in their health care than the general GBM population. Nonetheless, that we found vaccine hesitancy and low awareness of the HPV vaccine among a group of highly active health seekers, may indicate just how significant the problem may be across a more generalized population of GBM.

Conclusion

Public health policy and health promotion strategies in Canada have facilitated vaccine hesitancy among HIV-positive men at risk for HPV associated cancers. In Canada, the lack of coverage for HPV vaccination among HIV-positive men of all age groups, and health promotion strategies and media having focused on cisgender girls and women, have played a role in producing vaccine hesitancy among men who are at significant risk for anal cancer–especially GBM living with HIV. Fortunately, current health promotion and media efforts are focusing more on boys and men, and several Canadian provinces currently have “high-risk” HPV vaccination programs for males [40].

Improving access and uptake of HPV vaccination requires addressing both persistent financial barriers to access as well as increasing HPV health literacy levels among men and healthcare providers [41] particularly by reframing the long-standing gendered associations of HPV and emphasizing vaccination as part of a holistic safer sex strategy. The feminization of HPV and HPV vaccine messages shaped the knowledge base of our participants, leading many to think that the HPV vaccine was not relevant for them. Men’s accounts of the gendered messages of HPV demonstrate that once an association has been strongly communicated about a particular health concern, people may interpret and process new knowledge through this established frame. Even though policies and messaging of a health risk may change over time, the initial gendered associations communicated can play a strong role in shaping how individuals process new health messages and programs. However, while the feminization of HPV related cancers has undoubtedly played a role in these men’s risk perceptions of HPV and the importance of HPV vaccination, it did not appear to serve as a permanent or insurmountable barrier to men’s health decision-making. Increasing HPV vaccination among HIV-positive GBM in Ontario and across Canada will require the commitment of well-informed health care providers who provide clear recommendations along with continued public health, governmental, and community efforts to remove barriers to access.

Supporting information

Acknowledgments

The authors acknowledge and thank study participants for sharing their experiences. They also recognize the significant contributions of the HPV-SAVE Community Advisory Board members, including: Robert Reinhard, Evan Collins, Len Tooley, Owen McEwen, David McLay, Llewelyn Goddard, and Jordan Prosper. The authors also thank the other members of the HPV-SAVE Team, including: Jason Brunetta, Owen McEwen, Rupert Kaul, Paul MacPherson, Janet Raboud, Anita Rachlis, Alberto Severini, Darrell Tan, Jill Tinmouth, and Joel Palefsky.

HPV-SAVE is funded by the Canadian Institutes of Health Research (CIHR), the Canadian HIV Trials network (CTN), and the Ontario HIV Treatment Network (OHTN).