Abstract
Objective
Anal cancer and other diseases caused by human papillomavirus (HPV) are more common among people who are HIV-positive. To understand the potential role of HIV status in HPV prevention efforts, we examined HPV-related knowledge, attitudes, and beliefs among HIV-positive and HIV-negative gay men.
Materials and Methods
In January 2009, we interviewed a national sample of 247 adult gay men from the United States that included an oversample of HIV-positive men.
Results
Status of HIV was not associated with most beliefs about HPV-related diseases (i.e., genital warts, oral cancer, and anal cancer); however, HIV-positive men had higher worry about and perceived likelihood of these diseases. Most men correctly believed that HIV increases risk of HPV-related diseases, yet 29% to 42% still did not. Relatively few men believed that HPV vaccine works in males or that physicians are allowed to give it to men. Acceptability of the HPV vaccine was high and not associated with HIV status (78% of HIV-positive men vs 74% of HIV-negative men; adjusted odds ratio = 1.48; 95% confidence interval = 0.67–3.27).
Conclusions
The high acceptability of HPV vaccine, relatively low knowledge of how HIV increases risk for HPV-related diseases, and misperceptions about HPV vaccine can inform HPV prevention efforts for gay men. The few differences by HIV status suggest that HPV prevention programs may be able to use similar approaches with both HIV-negative and HIV-positive gay men.
Keywords: human papillomavirus, vaccine, acceptability, gay men
Infection with HIV increases risk of persistent human papillomavirus (HPV) infection and related diseases, including genital warts, cervical cancer, and anal cancer [1–3]. Men who have sex with men have markedly high rates of HPV-related disease including anal cancer, mainly attributable to the high prevalence of HPV infection [4–6] and HIV infection [7, 8]. The advent of highly active antiretroviral therapy has not reduced the high incidence of HPV-related cancers in HIV-infected individuals [9, 10].
Given gay men’s elevated risk for HPV-related diseases, primary prevention efforts such as HPV vaccination and secondary prevention strategies such as anal cancer screening may be particularly beneficial to them [11]. Since the approval of a quadrivalent HPV vaccine (HPV4) for females in 2006 [12], interest in expanding vaccine coverage to males has steadily increased [13–16]. In October 2009, the US Food and Drug Administration approved HPV4 for use by males aged 9 to 26 years [17], although off-label usage would permit men older than 26 years to receive the vaccine as well. Infection with HPV often happens soon after sexual debut, but it is unlikely that sexually active adult men have been exposed to all 4 HPV types present in the quadrivalent vaccine [18]. To understand the role that HIV status may play in HPV prevention efforts, we examined HPV-related knowledge, attitudes, and beliefs in a national sample of gay men.
METHODS
Participants and Procedures
In January 2009, we hired a company to survey men from a national panel of US households for our UNC Men’s Health Study. The company previously composed the panel using list-assisted random dialing, which provided a probability sample of US households with telephones [19]. In addition to 874 self-identified gay, bisexual, and heterosexual men from the panel whom we invited to participate in our study, we invited an oversample of 19 HIV-positive men. Of 893 potential participants, 233 (26%) did not respond to the invitation and 37 (4%) did not complete a survey. Compared with participants, nonparticipants were younger and more likely to be non-white, report a household income of less than $60,000 per year, and not have a college degree (all p < .05). Participants and nonparticipants were equally likely to be living with a spouse or partner.
We report here on 188 HIV-negative and 59 HIV-positive gay men. We did not include 301 heterosexual and 75 bisexual men in this analysis because of these groups’ very low prevalence of HIV (n = 6 and n = 2, respectively). Participants were predominantly non-Hispanic, white men (83%), most of whom had college degrees (59%) and health insurance (87%). Six percent reported living in rural areas. Larger proportions of HIV-positive men than HIV-negative men reported 2 or more sexual partners or a nonmonogamous regular partner in the past year (72% vs 53%, p = .03). Status of HIV was not associated with race/ethnicity, education, or insurance status in this national sample. Men positive for HIV were older than men negative for HIV (mean age = 51 vs 47 y, p < .01). Larger proportions of HIV-positive men than HIV-negative men reported 50 or more lifetime sex partners (66% vs 33%, p < .01), a previous sexually transmitted infection (66% vs 26%, p < .01), and current unemployment (37% vs 14%, p < .01). The institutional review board at the University of North Carolina approved the study.
Measures
The UNC Men’s Health Study survey is available online: http://www.unc.edu/~ntbrewer/hpv.htm. We adapted items from the Carolina HPV Immunization Measurement and Evaluation Project [20, 21] and cognitively tested the survey with 28 gay and bisexual men to confirm that the meaning we intended for the items corresponded to how participants understood them. We refined the items and further tested the survey via in-depth interviews with 8 gay and heterosexual men.
We assessed perceived knowledge of HPV-related disease by asking, “How much would you say you know about [genital warts, oral cancer, or anal cancer]?” (3 items, 1 = “nothing at all” to 4 = “quite a lot,” α = 0.73). We used similar multi-item scales to assess worry about HPV-related diseases (3 items, 1 = “not at all” to 4 = “quite a lot,” α = 0.56) and perceived severity about HPV-related diseases (3 items, 1 = “not at all” to 4 = “quite a lot,” α = 0.55). The survey asked men if they thought HIV increased, decreased, or had no effect on the chances of getting genital warts, oral cancer, and anal cancer. We then provided men a brief statement about HPV (“HPV is a common sexually transmitted disease (STD) that can cause genital warts and cervical cancer. HPV also causes anal cancer and may cause oral and penile cancer”). The survey asked men if they had ever heard of HPV vaccine before the survey. Among those who reported hearing about HPV before the survey, the survey inquired about attitudes toward HPV vaccine, including whether they thought HPV vaccine works in males, whether HPV vaccine is only for women, and whether physicians are allowed to give HPV vaccine to men.
After giving a more detailed description of HPV vaccine (“Researchers recently found that the HPV vaccine protects men from getting most genital warts. Researchers are also studying whether the HPV vaccine protects men against HPV-related cancers. Although the vaccine is not yet approved for men, some doctors are already giving HPV vaccine to men using a legal loophole called ‘off-label use’”), the survey measured how willing men would be to get it were it approved for use in males, using 5 survey items, each accompanied by a 5-point response scale that ranged from 1 = “definitely not willing” to 5 = “definitely willing” (α = 0.97). To facilitate comparisons with the existing HPV vaccine acceptability literature, and because these data were skewed, we created a dichotomous summary willingness variable, classifying men who responded “probably willing” or “definitely willing” on at least 3 of the 5 items as willing to receive HPV vaccine.
The survey measured perceived likelihood of developing HPV-related diseases (genital warts and oral, anal, or penile cancer) without vaccination (4 items, 1 = “no chance” to 5 = “certain I will get disease,” α = 0.82) and perceived effectiveness of HPV vaccine against the same diseases (4 items, 1 = “no protection” to 5 = “complete protection,” α = 0.94). The survey measured perception of possible barriers to receipt of HPV vaccine: short-term pain or discomfort, long-term adverse effects, cost of the vaccine, and difficulty finding a health care provider who would provide HPV vaccine to males (4 items, 1 = “not at all” to 5 = “extremely,” α = 0.64). The survey measured anticipated regret if they chose not to get vaccinated and later developed an HPV-related disease (genital warts; HPV infection that could lead to cancer; 2 items, 1 = “not at all” to 4 = “quite a lot,” α = 0.85). We also asked whether participants believed their health care provider would recommend they get the vaccine if it were approved for males.
We asked participants about sexual behaviors relevant to HPV infection, including age at first intercourse, total number of lifetime sexual partners, previous diagnoses of sexually transmitted infections, and number and type of sexual partners in the last year. Participants reported total number of lifetime sexual partners, but because these data were positively skewed, we created a 4-level categorical variable (≤4 partners, 5–19 partners, 20–49 partners, and ≥ 50 partners). We created a categorical variable to describe sexual risk in the past year: none (0 sexual partners), low risk (1 mutually monogamous regular sexual partner), and high risk (≥2 sexual partners or a nonmonogamous regular sexual partner). We ascertained HIV status via respondent self-report.
Statistical Analysis
Analyses compared HIV-negative and HIV-positive gay men’s beliefs about HPV, HPV-related diseases, and HPV vaccine. As preliminary analyses identified demographic differences by HIV status, multivariate analyses controlled for age, number of lifetime sex partners, previous diagnosis of sexually transmitted infections, and employment status. We used multivariate linear regression to examine the association of HIV status with continuous outcomes (e.g., beliefs about HPV-related diseases), and multivariate logistic regression to examine differences in dichotomous outcomes (e.g., knowledge that HIV increases chances of getting HPV-related diseases and willingness to receive HPV vaccine). For multi-item scales that were associated with HIV status, we conducted post hoc tests, using individual scale items as outcomes. We examined the associations of knowledge, attitudes, and beliefs with willingness to receive HPV vaccine in multivariate logistic regressions separately for HIV-negative and HIV-positive men, reporting adjusted odds ratios (aORs) and 95% confidence intervals (95% CIs). We analyzed data using SPSS 17.0 (SPSS, Inc, Chicago, IL). All statistical tests were 2-tailed, using a critical α of 0.05.
RESULTS
Status of HIV was not related to the perceived knowledge of HPV-related diseases, perceived severity of HPV-related diseases, or anticipated regret if they declined HPV vaccine and later developed HPV-related disease (Table 1). Men positive for HIV worried more about HPV-related diseases and had higher perceived likelihood of HPV-related diseases. In post hoc analyses, HIV-positive men had greater worry about genital warts and anal cancer and had higher perceived likelihood of genital warts than HIV-negative men (all p < .01). Although most men believed that HIV increases risk of HPV-related diseases, HIV status was unrelated to beliefs that HIV infection increases risk of these diseases (Table 2).
Table 1.
Beliefs About HPV-Related Diseases and HPV Vaccine
| HIV-negative men, mean (SD) | HIV-positive men, mean (SD) | p | |
|---|---|---|---|
| HPV-related diseases | |||
| Perceived knowledgea | 1.81 (0.61) | 1.95 (0.74) | .50 |
| Perceived severitya | 3.33 (0.63) | 3.32 (0.61) | .93 |
| Worrya | 1.48 (0.47) | 1.83 (0.69) | <.01 |
| Perceived likelihoodb | 2.17 (0.50) | 2.37 (0.58) | <.01 |
| Anticipated regreta | 3.47 (0.77) | 3.41 (0.83) | .14 |
| HPV vaccine | |||
| Perceived effectivenessb | 3.08 (0.79) | 3.10 (0.84) | .98 |
| Perceived barriersb | 2.62 (0.79) | 2.52 (0.88) | .73 |
HIV-negative men, n = 188. HIV-positive gay men, n = 59. Analyses controlled for age, number of lifetime sex partners, previous diagnoses of sexually transmitted infection, and employment status.
Four-point response scales ranged from “not at all” or “nothing at all” (coded as 1) to “quite a lot” (coded as 4).
Five-point response scales ranged from “no chance,” “no protection,” or “not at all” (coded as 1) to “certain I will get [disease],” “complete protection,” or “extremely” (coded as 5).
Table 2.
Beliefs About HIV and HPV Vaccine
| HIV-negative men, % (n) | HIV-positive men, % (n) | p | |
|---|---|---|---|
| HIV increases risk of | |||
| Genital warts | 60 (112) | 71 (42) | .45 |
| Oral cancer | 58 (109) | 59 (35) | .61 |
| Anal cancer | 61 (115) | 66 (39) | .97 |
| HPV vaccine | |||
| Heard of it | 76 (143) | 75 (44) | .64 |
| Had somewhat or mostly positive opinions of ita | 71 (101) | 77 (34) | .30 |
| Is only for womena | 59 (85) | 43 (19) | .03 |
| Works in malesa | 20 (28) | 27 (12) | .59 |
| Doctors are allowed to give it to mena | 17 (24) | 23 (10) | .37 |
| Doctor would recommend it | 34 (63) | 53 (31) | .06 |
| Willing to receive it | 74 (139) | 78 (46) | .33 |
HIV-negative men, n = 188. HIV-positive gay men, n = 59. Analyses controlled for age, number of lifetime sex partners, previous diagnoses of sexually transmitted infection, and employment status.
Asked of HIV-negative (n = 143) and HIV-positive (n = 44) men who had heard of HPV vaccine before survey.
Three-quarters of gay men (76%) had heard of HPV vaccine before the survey. Status of HIV was not associated with higher vaccine awareness (Table 2). Among men who had heard of HPV vaccine before the survey (n = 187), a high proportion reported somewhat or mostly positive opinions of it (72%), yet few thought that HPV vaccine worked in males (21%) or that physicians were allowed to give HPV vaccine to men (18%), with no differences by HIV status. Most HIV-negative men (59%) believed HPV vaccine was only for women compared with less than half of HIV-positive men (43%). Somewhat more HIV-positive men than HIV-negative men thought their physicians would recommend HPV vaccine if approved for use in males, but the difference was not statistically significant (53% vs 34%, p = .06). Among those who had heard of the vaccine, HIV-negative and HIV-positive men reported equivalent levels of perceived HPV vaccine effectiveness and perceived barriers to receiving HPV vaccine (Table 1).
When the vaccine’s protection against HPV-related disease was not specified, 37% of men were “probably willing” and 23% of men were “definitely willing” to receive it. More men said they were “definitely willing” to get the vaccine when the protection it could offer against HPV-related cancers was specified. The dichotomous summary measure showed similar high willingness to receive HPV vaccine among HIV-positive and HIV-negative men (78% and 74%, respectively; aOR = 1.49, 95% CI = 0.67–3.29; see Table 2).
Higher willingness to receive HPV vaccine was associated with higher perceived effectiveness of the vaccine, belief that a physician would recommend the vaccine, and anticipated regret over developing HPV-related disease after declining vaccination among both HIV-positive and HIV-negative men (Table 3). Higher perceived likelihood of HPV-related diseases was associated with higher acceptability of HPV vaccine only for HIV-negative men. Higher perceived severity of HPV-related disease and lower perceived barriers to getting HPV vaccine were associated with higher acceptability of HPV vaccine only for HIV-positive men.
Table 3.
Correlates of Willingness to Receive HPV Vaccine
| HIV-negative men, aOR (95% CI) | HIV-positive men, aOR (95% CI) | |
|---|---|---|
| HPV-related diseases | ||
| Perceived knowledge | 0.99 (0.56–1.78) | 1.09 (0.45–2.65) |
| Perceived severity | 1.45 (0.88–2.41) | 3.19 (1.06–9.65)a |
| Worry | 2.31 (0.99–5.35) | 1.59 (0.55–4.61) |
| Perceived likelihood | 2.76 (1.23–6.22)a | 3.14 (0.88–11.23) |
| Anticipated regret | 3.33 (2.05–5.43)b | 2.37 (1.10–5.13)a |
| Believed HIV increases risk of | ||
| Genital warts | 1.07 (0.54–2.11) | 0.44 (0.08–2.44) |
| Oral cancer | 0.76 (0.39–1.52) | 0.81 (0.20–3.25) |
| Anal cancer | 1.01 (0.50–2.01) | 0.66 (0.15–2.93) |
| HPV vaccine | ||
| Perceived effectiveness | 4.15 (2.35–7.34)b | 6.05 (1.74–21.11)a |
| Perceived barriers | 0.88 (0.58–1.36) | 0.30 (0.11–0.78)a |
| Heard of it | 0.78 (0.35–1.74) | 0.50 (0.09–2.73) |
| Had somewhat or mostly positive opinion of itc | 1.72 (0.75–3.91) | 4.60 (0.62–34.05) |
| Is only for womenc | 0.96 (0.44–2.09) | 0.35 (0.07–1.71) |
| Works in malesc | 2.30 (0.72–7.34) | 7.27 (0.71–74.88) |
| Doctors are allowed to give it to menc | 1.47 (0.50–4.29) | 3.13 (0.32–30.53) |
| Doctor would recommend itc | 5.94 (2.20–16.03)b | 28.53 (3.07–264.84)a |
HIV-negative men, n = 188. HIV-positive gay men, n = 59. Analyses controlled for age, number of lifetime sex partners, previous diagnosis of sexually transmitted infections, and employment status.
p < .05.
p < .001.
Asked of HIV-negative (n = 143) and HIV-positive (n = 44) men who had heard of HPV vaccine before survey.
DISCUSSION
Human papillomavirus–related diseases are a pressing health concern for gay men, especially HIV-infected men. We found few differences in HPV-related beliefs and attitudes by HIV status. Most men correctly believed that HIV increases risk of HPV-related diseases, yet many still did not. Overall perceived knowledge of HPV-related diseases was low. These findings indicate a need for further education about HPV-related diseases, especially among HIV-positive men who are at increased risk for these diseases compared with HIV-negative men.
Prevention of HPV-related disease is emerging as a public health priority for gay men and people who are HIV-positive; however, HPV vaccination may have some limitations for these groups. Studies have shown that HPV vaccination prevents persistent infection with HPV types associated with most anal cancers [22], is an effective tool for preventing genital warts in men, and may prevent other HPV-related diseases as well. Ideally, HPV vaccine would be administered before sexual debut and exposure to HPV [12]. Most men in our study were older than the age recommended for HPV vaccination (9–26 y). Many participants reported high numbers of sexual partners, suggesting that many gay men (including those who were HIV-positive) had likely already been exposed to at least one type of HPV. However, they may not have been exposed to all types present in HPV vaccine [5] and thus may potentially receive some benefit. The National Health and Nutrition Examination Survey found that only 2% of men aged 14 to 59 years (sexual orientation not specified) had antibodies to 2 types of HPV and fewer than 1% had antibodies to all 4 types [18], although antibody prevalence for any HPV type increased continually from age 14 to 59 years, indicating ongoing acquisition of HPV infection. Even with these potential limitations, HPV vaccine is one of our most promising tools for primary prevention of HPV-related disease and may confer benefits even after sexual debut or exposure to a single HPV type.
The relatively high HPV vaccine acceptability that we found is consistent with previous studies that found high acceptability among college-aged men [23]. Although HIV infection is a risk factor for many HPV-related diseases, it may not prompt greater uptake of HPV vaccine. In our study, HPV vaccine acceptability did not differ between HIV-negative and HIV-positive gay men. Most men had heard of HPV vaccine and held somewhat or mostly positive opinions of it, but few believed HPV vaccine works in males or that physicians are allowed to give it to men.
If delivering HPV vaccine to gay men becomes a public health priority, targeted interventions to modify attitudes identified in this study may be helpful. We identified 3 factors, namely, perceived effectiveness of HPV vaccine, belief that a physician would recommend HPV vaccine, and anticipated regret if they declined HPV vaccine and later developed HPV-related disease, that might serve as leverage points to increase acceptability of HPV vaccine, regardless of HIV status.
This study’s strengths include use of a national panel, with equivalent sampling frames for HIV-positive and HIV-negative gay men. The cross-sectional design, however, precludes inferences about causality. These findings will need to be confirmed using data on HPV vaccine uptake now that the US Food and Drug Administration has approved the quadrivalent HPV vaccine for males aged 9 to 26 years. Cost-effectiveness analyses should continue during the initial period of delivering HPV vaccine to males to increase our understanding of the benefits of vaccinating gay men. Models of male HPV vaccination have previously found modest to low cost-effectiveness; however, these models have generally examined HPV-related outcomes only for women [24, 25]. Future analyses should include HPV-related diseases among men, such as genital warts and anal cancer, as well as the potential benefit of herd immunity to gay men—if any— because of vaccination of heterosexuals and women. Comparison of the benefits of HPV vaccine, a primary prevention strategy, to anal cancer screening, a secondary prevention strategy, could further elucidate the individual and joint contributions of these efforts in helping prevent anal cancer. Although our analyses controlled for age and other demographic variables, future research will need to confirm the generalizability of our findings to young men (the population for whom HPV vaccine was approved), men of color, and men with lower education levels. The comparability of the findings from this national study to results from studies of these specific and often higher-risk samples of gay men is not yet known.
These findings offer early insight into gay men’s HPV-related knowledge, attitudes, and beliefs. The high acceptability of HPV vaccine, relatively low knowledge of how HIV increases risk for HPV-related diseases, and misperceptions about HPV vaccine may be helpful when planning HPV prevention efforts. The few differences between HIV-negative and HIV-positive men suggest that HPV prevention programs may be able to use similar approaches with both HIV-negative and HIV-positive gay men.
Acknowledgments
This study was supported in part by research grants from the Investigator-Initiated Studies Program of Merck & Co, Inc, the American Cancer Society (MSRG-06-259-01-CPPB), and the Cancer Control Education Program at Line-berger Comprehensive Cancer Center (grant no. R25 CA57726).
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