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A model of health care provider decision making about HPV vaccination in adolescent males
Vaccine 33 (2015) 4081–4086
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
A model of health care provider decision making about HPV vaccination in adolescent males Andreia B. Alexander ∗ , Candace Best, Nathan Stupiansky, Gregory D. Zimet Section of Adolescent Medicine, Department of Pediatrics, Indiana University School of Medicine, 410 West 10th Street, HS 1001, Indianapolis, IN 46202, United States
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Article history: Received 24 March 2015 Received in revised form 16 June 2015 Accepted 22 June 2015 Available online 2 July 2015 Keywords: Human papillomavirus Health care provider Male Qualitative research Vaccine Adolescent
a b s t r a c t Introduction: In the U.S., HPV vaccination of adolescent males remains low, despite the recommendation for routine vaccination. Although research has highlighted that health care provider (HCP) recommendation is very influential in HPV vaccine uptake, research on this topic in the male population is lacking. Accordingly, we used a qualitative approach to identify HCP knowledge, attitudes, and behaviors regarding adolescent male HPV vaccination, one year, after routine vaccination of adolescent males was recommended. Method: A total of 20 U.S. pediatric HCPs participated in 20–30 min interviews about knowledge, attitudes, and practices regarding male HPV vaccination. Interviews were audio-recorded, transcribed and, analyzed using inductive content analysis. Results: The providers had been in practice for 1–35 years, 75% were female, and 75% were White. Opinions on HPV vaccination were shaped by knowledge/perception of the risks and benefits of vaccination. Although all providers frequently offered HPV vaccine to male patients, the strength and content of the offer varied greatly. Vaccination opinions determined what issues were emphasized in the vaccine offer (e.g., stressing herd immunity, discussing prevention of genital warts), while adolescent age influenced if and how they pitched their vaccine offer (e.g., HPV as a STI). Most providers agreed with the ACIP recommendations, however, several expressed that providers’ preexisting opinions might remain unchanged despite the recommendations. Consistent with the literature on determinants of HPV vaccination, providers believed that their own recommendation was a major factor in a family’s decision to vaccinate. Barriers to vaccination included the “newness” and sexual nature of the vaccine, lack of insurance coverage, and the vaccine not being mandated. Conclusions: Providers’ opinions about, and approaches to offering, HPV vaccination to males were highly variable. Interventions designed to improve male HPV vaccination should focus on helping providers to routinely recommend the vaccine to all of their eligible patients, both males and females. Published by Elsevier Ltd.
1. Introduction Human papillomavirus (HPV) has been identified as a necessary cause of genital warts, virtually all cervical cancers, many other anogenital cancers, and increasing numbers of cancers of the oropharynx [1]. The quadrivalent HPV vaccine (HPV4) was licensed in the U.S. for 9- to 26-year-old males in 2009 [2] and the Centers for Disease Control and Prevention’s (CDC) Advisory Committee on
∗ Corresponding author. Tel.: +1 973 9729261; fax: +1 973 972 9268. E-mail addresses: [email protected] (A.B. Alexander), [email protected] (C. Best), [email protected] (N. Stupiansky), [email protected] (G.D. Zimet). http://dx.doi.org/10.1016/j.vaccine.2015.06.085 0264-410X/Published by Elsevier Ltd.
Immunization Practices (ACIP) issued a routine recommendation for males in 2011 [3]. Although HPV vaccination has proven to be effective and safe, vaccination rates remain suboptimal in the U.S., especially for males [4,5]. Most published research on factors associated with HPV vaccine uptake in adolescents has focused on females [6–8]. These studies have found that public insurance status, Hispanic race, lower family income, having received flu vaccine, increased perceived vaccine effectiveness, peer acceptance, and anticipated inaction regret, were associated with increased vaccine uptake or uptake intent in males [6–10]. While some variation exists between the factors associated with male and female vaccine uptake, health care provider recommendation is a primary factor for HPV vaccination of both males
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and females [11,12]. However, many of the studies of males were conducted prior to implementation of the ACIP routine recommendation [13–15]. Although health care provider recommendation is very influential, research on this topic in adolescent males, post-routine ACIP recommendation, is lacking. This information is needed to better understand the nature of provider recommendation/nonrecommendation and could be used to guide development of interventions aimed at improving provider vaccination of males. Accordingly, the purpose of this study is to identify health care provider knowledge, attitudes, and practices regarding adolescent male HPV vaccine recommendation, post-routine recommendation by the ACIP. As little is known about these factors, a qualitative approach was taken.
2. Methods 2.1. Procedures Participants were a convenience sample of 20 pediatric physicians (general and adolescent) working in primary care clinics with relatively high vaccination rates serving primarily lower income families in a Midwestern city. A total of 28 providers were contacted via email and asked to participate in a 20–30 min interview about their opinions and practices related to HPV vaccination of males. A total of 20 (71.4%) responded and interviews were conducted either in person, in a private room at the provider’s clinic/research office or via telephone. Each participant was compensated with a $20 gift card. Interviews were conducted after the 2011 ACIP recommendation for routine HPV vaccination of males. Written informed consent for this study was waived and the study was approved by the Institutional Review Board at the author’s institution.
Table 1 Demographics. Demographic
n
%
Gender Female Male
15 5
75 25
Race White Black Hispanic
15 4 1
75 20 5
5 3 9 3
25 15 45 15
1 4 3 12
5 20 15 60
Years practicing pediatrics 1–5 years 6–10 years 10–20 years 21+ years % of Active patient population Male <20% 21–30% 31–40% 41–50%
until no new themes or changes to the model were detected. Disagreement between researchers was resolved through discussion. 3. Results 3.1. Sample The 20 providers were mostly female (n = 15) and White (n = 15), and had been practicing pediatrics from 1 to 35 years (see Table 1 for more detailed information). Overall there were no notable differences in responses by gender or race. 3.2. Model of provider recommendation
2.2. Data collection Prior to each interview, participants completed a demographic questionnaire. Semi-structured interviews were conducted by the primary author using an inductive approach based in grounded theory to avoid making assumptions, allowing for a model of decision making to emerge from the data. Interviews focused on practices regarding HPV vaccination for males. Topics included HPV vaccine knowledge, presentation of vaccine to patients, opinions about the need for male vaccination, risks, benefits, barriers, patient decision making, and school vaccination. Interviews were audio-recorded and transcribed. After each interview, the interviewer completed detailed field notes intended to document relevant information not captured on the audiorecording. The research team agreed that the data reached theoretical saturation upon completion of 20 interviews [16]. 2.3. Analysis Data were evaluated via inductive content analysis [17], which is utilized when little is known about a topic. The process includes open coding, creating categories, and abstraction of concepts, and tends to move from very specific to more general. The primary and secondary author read and openly coded four randomly chosen interviews identifying emerging issues, concepts, and themes surrounding the knowledge, opinions, and practices of health care providers regarding the HPV vaccine. The researchers then came together and discussed their individual codes and created a consensus list of preliminary codes. The researchers read through and coded the remaining 16 interviews separately and developed an initial model, which was readjusted throughout the process of coding
After examining providers’ knowledge, attitudes, and practices around male HPV vaccination, a model of provider recommendation emerged (Fig. 1). Below is an overview of the model, followed by a more detailed description of model components. We found that providers’ knowledge and perception of the risks and benefits of the HPV vaccine for males influenced their opinions on male vaccination. Their opinions on male vaccination then determined the nature of their vaccine offer. While this was true for most providers, there were exceptions. For example, although one provider felt anal and penile cancer prevention were clear benefits of HPV vaccination in males, he felt uncomfortable discussing these cancers with parents and adolescent males. Additionally, he believed parents and adolescents would be equally uncomfortable discussing these cancers. Several other providers who acknowledged prevention of male cancers as a benefit of vaccination felt this was not an important benefit because the incidence of these cancers is low. As a result, these providers said that they did not discuss male cancers when offering HPV vaccine to males. All providers agreed that their HPV vaccination offer influenced, at least partially, family vaccination decisions. For most providers, the age of the adolescent determined whether or not they would offer the vaccine and the components included in their vaccine offer. For example, a few providers stated that they never offer the vaccine to any males younger than age 11, while other providers were willing to vaccinate at age 9. Furthermore, for some, the age of the male patient would determine whether or not they would discuss the sexually transmitted nature of the virus. Many providers felt the age of the adolescent influenced how families made the decision to vaccinate. Most providers stated that the older the adolescent, the more likely the adolescents’ opinion was included in vaccination discussions and considered in vaccination initiation.
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Fig. 1. Model of health care provider HPV vaccine offer.
Table 2 Model themes. Model component
Major theme(s) (n out of 20)
Minor theme(s) (n out of 20)
Benefits
Prevention against genital warts [14] Prevention of male-to-female HPV transmission [14]
Prevention of penile, oral, anal, and/or unidentified cancers [9] Increase provider-patient-family communication [3] Cost effectiveness of male vaccination [2] Decreased worldwide burden of disease [2] Improving male sexual responsibility [1]
Risks
Safe [20] Low side effect profile [20] Increased pain compared to other vaccines [9] Syncope [10]
Local reactions at injection site [6] Potential for systemic symptoms [5] Allergic reactions [3] Parental fears of sexual disinhibition [1] Concerns for reports of chronic fatigue and pain [1] Potential for more serious side effects [2] Patient’s blaming vaccination with a coincidental condition [2]
Opinions
Good, safe, and effective intervention [16] Both males and females should be vaccinated [9]
Not important in males/more important in females [7] Herd immunity [4]
Offer
Offered in conjunction with other vaccines [18] Additional time spent explaining the HPV vaccine [15] Eliciting information from family [7] Prevention of genital warts [14] Prevention of cervical cancer [12] Males getting vaccinated protects future partners [11] Prevents STI [8] 3 doses needed [7] Personal recommendation to get vaccinated [11]
Varying levels of recommendation for vaccination [20] ACIP recommendation [7] Should be given before sexual debut [6] Prevention of anal cancers [3] Side effects [3] Stress cancer prevention/avoid genital warts discussion [5] Stress genital warts prevention/avoid anal cancer discussion [9]
Age
Vaccinating younger adolescents [9–10-year-old] [3] Vaccinating 11 years or older [10] Vaccinating older adolescents 16 years or older [10]
Gauge family readiness [8] Spread out adolescent vaccine schedule [5] Avoid discussing sex, STIs with younger adolescents [3] Avoid discussing anal cancers with younger adolescents [3]
Barriers
Not mandated for school attendance [10] Lack of insurance coverage by private insurers [9] Social anxiety around teen sexuality [8] Males not completing 3-dose series [7] Not all physicians offering/recommending vaccination [6] New vaccine [4]
Adolescents receiving too many immunizations during ages 11–12 [5] Lack of awareness by providers and families [4] Media reports of adverse side effects [4] Physicians failing to offer the vaccine [6] Poor clinic attendance among adolescent males [3] Vaccination less relatable for males than for females [2]
ACIP Recommendation
Opinion Beneficial [13] Would initiate insurance coverage [5] Knowledge Routine recommendation [11] Adolescents—unsure about upper age limit [14] Genital wart prevention [18] Channel of information Newsletters/emails from the American Academy of Pediatrics [8] Newsletters/emails from CDC [6]
Opinion Unsure of rationalization of recommendation [3] Increase physician offering/recommending vaccine [5] Limited impact on provider behavior [4] Knowledge Unaware of the recommendation [2] Confusion around which male cancers were included in vaccine indications [3] Channel of information Office discussions with colleagues [1] Formal meetings within practice [3]
Decision
Provider recommendation important [15] Decision made by parents [19]
1. Adolescent input with older adolescents [7] 2. Adolescent input with more cognitively mature adolescents [6]
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Table 3 Example quotes for each model component. Model component
Example quote
Benefits
“There are no direct benefits to you [the male patient] (Female, White).” “Well, preventing genital warts and spread of the virus to partners, rising health care costs from treatment of the genital warts and then patient discomfort, relieving that. . .The treatment for warts is rather costly. Once the warts have been established. The modalities are painful. Patients usually have to get repeat treatments. And so, all those things add to the costs of the treatment, where if we can prevent it then we would negate that cost factor (Female, Black).”
Risks
“Well, I’ve heard the really bad things that some of the people say on TV and attribute it to getting the shot. And so, it always makes me think, you know, well, even though it may be just a miniscule percentage chance of something like that happening, like some, some weird allergic reaction, or something weird that occurs after giving a shot, I always worry about that.” (female, black) “I think the biggest risk right now myself is people get the vaccine and something develops thinking it’s a vaccine’s fault (Female, White).”
Opinions
“I mean it is a sexually transmitted disease. It is something that boys could get. And so, why would we just focus on girls? I don’t want my son having genital warts. (Female, White)” “It depends on whose perspective you’re looking at. Because herd immunity is just as important as sort of the individual entity. It just depends on what perspective you’re taking. So, for me as the healthcare provider I think it’s important for everybody because the more people we immunize, the more people are protected. Overall. If you you’re talking about it on an individual basis, like the person [male] in front of me, it’s going be less important than if you’re a girl in front of me (Male, White).”
Offer
“[I do not discuss genital warts because] I always think cancer is a scarier term for people. You know, they’re like, warts I can deal with that, whatever (Female, White).” “You know, I didn’t [include cancer in my offer] because I probably just omit it from my own, you know, not having that little piece of my knowledge bank (Male, Black).” “Well, for cancers, it’s a tough one for males. Because the cancers that we are talking about are primarily, I mean, there’s some penile cancers, but the rates are so low, we’re talking about anogenital cancers, and it’s very difficult to talk about sexual orientation in an 11 year old when they haven’t made up their mind. You know? But generally, I focus on genital warts with young men (Female, White).”
Age
“I don’t really feel like talking about genital warts to a 9-year old. And I think they should understand what the benefit is of the vaccine. So, usually I bring it up when those 6th grade vaccines are going. But again, if I don’t feel like that, if it’s going make everybody uncomfortable, I wait until 12 or 13 (Female, White).”
Barriers
“I ask everybody if they’ve had all of their HPV shots and they’ll either say, ‘Yes,’ or ‘I’m part way through the series,’ or they’ll say, ‘No, my doctor said I didn’t need it yet.’ Or, ‘My doctor said it was too new.’ Or, ‘My doctor wasn’t sure that it would be good for me’ (Female, White).”
ACIP Recommendation
“I think that it’s not [the recommendation] for providers who weren’t sure of the HPV vaccine. I don’t think the fact that now they say it’s [for] males it’s going to increase the vaccine if they’re not sure about the vaccine. If they are not sure about the vaccine, they’re not going to give it to girls or boys. And if you’re sure of the vaccine now you can say, hey, your insurance company’s going to pay for this vaccine that cost $600 a pop (Female, White).” “I do. Because if I think about my [medical practice] partners, two of them just follow recommendations without really looking into it too much. . .I’m not the person to discuss all those recommendations. I like to check the evidence behind the recommendation. . .With HPV for boys, I’m not convinced because all of the evidence that I have don’t benefit for my patient. It’s just not convincing me (Female, White).”
Decision
“Yeah, it’s a big deal. I think it depends a little bit on where they are in their cognitive maturity. Some 11, 12 year-olds are further along in making those decisions. There are some parents who leave it up to their child at age 14, 15. You know, and that’s interesting to me. I think it should be probably a mutual decision. (Female, White)” “I really do think that getting vaccinated is like getting a CBC checked, or your cholesterol checked, is very much a function of the physician’s recommendations. And so, I think, sometimes in private practice they are not recommending it as much as we are in academic medicine (Female, White)”
Most providers identified barriers to vaccination (e.g., “newness” of the vaccine, STI prevention) that influenced their offer and/or the decision of families to vaccinate. Similarly, many providers felt that logistical barriers (e.g., lack of insurance coverage, non-mandated school vaccination) strongly influenced families opting for non-vaccination for their sons. Interestingly, there was substantial variation in how providers felt that the ACIP’s recommendation for routine male vaccination would affect vaccination rates. Most believed that the preexisting opinions of individual providers would impact how they perceived the ACIP recommendation, which would then influence their vaccine offer (or non-offer). For example, if providers had a positive opinion about male vaccination, then they may add the ACIP recommendation to their offer in order to increase the “sell-ability” of the vaccine. Likewise, most interviewees believed that providers holding a negative opinion about male vaccination would not change their offer to include the latest recommendation and/or would
not increase their frequency of male vaccine offers. A breakdown of model components and example quotes can be found in Tables 2 and 3, respectively.
3.2.1. Benefits The most frequently reported benefits of HPV vaccination in males were prevention against genital warts (n = 14) and prevention of male to female HPV transmission (n = 14). While all of these providers felt that protection of females was an important aspect of male HPV vaccination, there was much more variation in beliefs about the importance of the prevention of genital warts, with some providers believing prevention of genital warts was important to personal health (n = 5) and for decreasing health care costs (n = 2), and others feeling that emphasis should only be placed on cancer prevention (n = 9). Other benefits listed by providers can be found in Table 2
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Although penile, anal, and/or oral cancer prevention were considered benefits of male HPV vaccination (n = 9), these were mentioned by only a few providers (ranging from five for penile cancer to two for anal cancers). When asked why cancer prevention was not listed as a benefit for males, providers stated: (1) they did not know about the cancer indication (n = 3), (2) they knew that cancer prevention was indicated but did not know the specifics (n = 8), or (3) they did not feel the incidence of these cancers was high enough to be considered a benefit (n = 7).
3.2.2. Risks All of the providers agreed that the vaccine was safe and had a low side effects profile. The most frequently mentioned risks were increased pain compared to other vaccinations (n = 9) and syncope (mostly in females) (n = 10). Other risks mentioned can be found in Table 2.
3.2.3. Opinion Most providers viewed HPV vaccine as good, safe, and effective (n = 16). Although many believed males and females should be vaccinated equally (n = 9), several did not believe that vaccination was as important for males (n = 7). Some providers saw male vaccination as an important intervention primarily to establish herd immunity (n = 4).
3.2.4. Offer Most providers stated they offered the vaccine to their male patients in conjunction with other routine adolescent vaccines (n = 18), but spent additional time explaining HPV vaccination for two main reasons: (1) its recent availability for males and (2) families’ lack of awareness about male HPV vaccination. Oftentimes, providers would begin their offer by eliciting HPV vaccine information from the family (n = 7), then would describe the specifics about the vaccine. The most frequently mentioned components of the vaccine offer were that: (1) the vaccine was used to prevent genital warts (n = 14) and cervical cancer (n = 12), (2) males should receive the vaccine in order to prevent future partners from being infected (n = 11), (3) the vaccine was used to prevent an STI (n = 8), and (4) the adolescent would need a series of three doses (n = 7). The majority of the providers concluded their offer with a personal recommendation that the adolescent male receive the vaccine (n = 11). However, only five (25%) physicians in this study actually stated that they strongly recommend the vaccine to their male patients with another six (30%) stating they recommend the vaccine, but not strongly. While many providers mentioned genital warts in their vaccine offer, some who worked with younger adolescents left it out completely due to its sexual nature (n = 5). In these instances, providers stressed cancer prevention in order to avoid this discussion. Conversely, most of the providers who spoke about genital warts excluded any discussion of anal cancers (n = 9). The most common reasons identified for this exclusion included provider discomfort and the perceived discomfort among families.
3.2.5. Age Providers were evenly split about vaccinating young adolescents. Half were comfortable vaccinating 11–12-year-old males (n = 10), with some willing to start as young as age nine (n = 3). The remaining providers were more reluctant to vaccinate young adolescent males (n = 10). Many of these providers noted the difficulty in explaining HPV vaccination to parents of younger adolescents because of the perception that parents are not ready to discuss sex or STIs.
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3.2.6. Barriers The most commonly reported barriers included the vaccine not being mandated for school attendance (n = 10), perceived lack of insurance coverage by private insurers (n = 9), anxiety around teen sexuality [8], males not coming back to complete the three dose series (n = 7), not all physicians offering/recommending the vaccine (n = 6), and the vaccine being too new (n = 4). Less commonly reported barriers can be found in Table 2. 3.2.7. ACIP recommendation Most providers agreed that the latest ACIP recommendation was beneficial (n = 13), with only a few providers questioning why the ACIP added a routine HPV vaccination for males (n = 3). Most of the variation came with respect to the effect the recommendation would have on male vaccination and providers’ knowledge about HPV vaccine and its recommendations for use. Most providers knew that the 2011 ACIP recommendation included routine HPV vaccination for males (n = 11). However, some were unaware about this “new” recommendation (up to a year after the recommendation had been released) (n = 2). Providers were knowledgeable that the vaccine should be given to adolescents, but were unclear on the specifics. For example, some knew that it could be given as young as age 9 (n = 5), but others did not. Likewise, most knew that it was routinely recommended for 11 and 12 year-olds (n = 18). Nevertheless, the majority did not know the upper age limit of the recommendation (n = 14). Most providers understood that the vaccine was indicated to prevent genital warts (n = 18), however, there was quite a bit of confusion around which male HPV-related cancers were included in the vaccination indications. Most providers became aware of the latest recommendation via newsletters and emails from the American Academy of Pediatrics and/or the CDC (n = 8). Others were informed during office discussions with colleagues or formal meetings (n = 3). 3.2.8. Decision There was very little variation regarding the decision process about male vaccination. Most providers believed that their recommendation was one of the most important factors in the family’s decision (n = 15). This was evident in the reported percentage of males who accepted HPV vaccination. Providers who stated they recommended or strongly recommended the vaccine reported a 70–90% vaccination uptake, while providers who stated that they offered, but did not recommend the vaccine reported a vaccination rate of 25–50%. Providers agreed that parents were the primary decision-makers around vaccination (n = 19). In the cases when adolescents had input into the decision, it was most likely to involve an older adolescent (n = 8). 4. Discussion Although we were able to describe an overall model of provider offer, there was great variation within each of the components of the model, despite the fact that these providers were from the same or similar practice groups. This variability suggests that the decision to offer and recommend HPV vaccination is dependent on physician knowledge or lack of knowledge about, and opinions on, the risks and benefits associated with the vaccine. One of the most heterogeneous findings was with regard to prevention of HPV-related cancers that affect males, with some providers having no/inaccurate knowledge of current indications and others having accurate knowledge. Providers who were more knowledgeable about HPV-related cancers were also more likely to provide a strong recommendation for the vaccine. As provider recommendation is one of the strongest predictors of HPV vaccine uptake [11–14], future research should be conducted to determine
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effective interventions to increase physician knowledge about cancer-prevention indications for HPV vaccination. A second area of heterogeneity was comfort with discussion about HPV vaccine as STI prevention. While some providers were personally uncomfortable discussing HPV outcomes, such as anogenital warts, others believed that families would be uncomfortable with such a discussion, especially in younger adolescents. This set of findings is consistent with previous research, which shows that few pediatricians engage in meaningful discussions about sexual health with their adolescent patients [18]. Not surprisingly, providers were more comfortable discussing sexual health issues with older adolescents (>15-years-old). Overall, the providers considered physician recommendation to be the strongest determining factor in parent approval of vaccinating their children. However, despite an overall general positive opinion about male HPV vaccination, most providers did not provide strong recommendations for vaccination. It appears that most of the providers believed that male vaccination had a role in protecting female partners, but were less convinced of its direct benefits for their male patients, a finding consistent with research conducted prior to ACIP’s routine recommendation [19]. This finding may explain, at least in part, why U.S. male vaccination initiation rates since the ACIP routine recommendation have only reached 34.6% [4]. Finally, many of our respondents felt the latest ACIP recommendation would not have a major effect on provider recommendations; that a provider’s preexisting personal opinion of HPV vaccination would remain the principal determining factor. It is not clear to what extent this opinion is supported by data, but the slow progress in HPV vaccination rates of females and males, despite the strong routine ACIP recommendation, suggests that health care providers have not fully embraced the ACIP guidelines. 4.1. Limitations While the qualitative design of this study allowed us to examine in-depth information about health care provider knowledge, attitudes, and practices around HPV vaccination, there are a number of limitations. Although a sample size of 20 interviews was adequate for this qualitative research study, it limits the generalizability of these findings, which may not be applicable to different groups of health care providers. Additionally, while this study provides a good starting point to understanding male HPV vaccination, the data collection sites were clinics with high adolescent vaccination rates and high proportions of patients on state funded insurance programs. Research conducted in clinics with lower vaccination rates as well as those with higher proportions of patients using private insurance will help elucidate the full range of issues surrounding providers and male HPV vaccination. 5. Conclusion Overall, providers had a positive opinion about HPV vaccine and offered it to most of their male patients. There was substantial variability across providers in terms of knowledge about the benefits of HPV vaccination for males, comfort with discussing sexual issues with adolescents and their families, and whether or not the provider recommended the vaccine. The results of this study may help to inform the development and evaluation of interventions for physicians to increase vaccine uptake and may inform future,
larger scale, research in diverse settings to gain a better understanding of physician knowledge, attitudes, and practices around HPV vaccination in general and of males in particular. Acknowledgments This study was supported by Merck & Co., Inc. through an investigator-initiated grant (MISP #38094). Its contents are the sole responsibility of the authors and do not reflect the official view of Merck & Co., Inc. Conflict of interest statement: Gregory Zimet and Nathan Stupiansky have been investigators on investigator-initiated research funded by Merck & Co. In the last year, Gregory Zimet served as a consultant to Merck & Co., Inc. References [1] Center for Disease Control and Prevention. Human Papillomavirus 2014 [cited 2014 July 3]. Available from http://www.cdc.gov/std/hpv/ [2] US Food and Drug administration [cited 2014 July 3].Available from Approval Letter—Gardasil; 2009 http://www.fda.gov/BiologicsBloodVaccines/Vaccines/ ApprovedProducts/ucm186991.htm [3] Centers for Disease Control and Prevention. Recommendations on the use of quadrivalent human papillomavirus vaccine in males—. Advisory Committee on Immunization Practices (ACIP); 2011. Report No.: Contract No.: 50. [4] Elam-Evans LD, Yankey D, Jeyarajah J, Singleton JA, Curtis CR, MacNeil J, et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years—United States, 2013. MMWR 2014;63:625–33. [5] Pierre-Victor D, Mukherjee S, Bahelah R, Madhivanan P. Human papillomavirus vaccine uptake among males 11–26 years in United States: findings from the National Health and Nutrition Examination Survey, 2011-2012. Vaccine 2014;32(49):6655–8. [6] Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among US adolescents: a systematic review of the literature. JAMA Pediatr 2014;168(1):76–82. [7] Etter DJ, Zimet GD, Rickert VI. Human papillomavirus vaccine in adolescent women: a 2012 update. Curr Opin Obstet Gynecol 2012;24(5):305–10. [8] Rambout L, Tashkandi M, Hopkins L, Tricco AC. Self-reported barriers and facilitators to preventive human papillomavirus vaccination among adolescent girls and young women: A systematic review. Prev Med 2014;58:22–32. [9] Alexander AB, Stupiansky NW, Ott MA, Herbenick D, Reece M, Zimet GD. Parentson decision-making about human papillomavirus vaccination: a qualitative analysis. BMC Pediatr 2012;12(1):192. [10] Alexander AB, Stupiansky NW, Ott MA, Herbenick D, Reece M, Zimet GD. What parents and their adolescent sons suggest for male HPV vaccine messaging. Health Psychol 2014;33(5):448. [11] Lau M, Lin H, Flores G. Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health. Vaccine 2012;30(20):3112–8. [12] Rosenthal S, Weiss T, Zimet G, Ma L, Good M, Vichnin M. Predictors of HPV vaccine uptake among women aged 19–26: importance of a physician’s recommendation. Vaccine 2011;29(5):890–5. [13] Reiter PL, McRee A-L, Pepper JK, Gilkey MB, Galbraith KV, Brewer NT. Longitudinal predictors of human papillomavirus vaccination among a national sample of adolescent males. Am J Public Health 2013;103(8):1419–27. [14] Gilkey MB, Moss JL, McRee AL, Brewer NT. Do correlates of HPV vaccine initiation differ between adolescent boys and girls? Vaccine 2012;30:5928–34. [15] Malo TL, Giuliano AR, Kahn JA, Zimet GD, Lee J-H, Zhao X, et al. Physicians’ human papillomavirus vaccine recommendations in the context of permissive guidelines for male patients: a national study. Cancer Epidemiol Biomarkers Prev 2014;23(10):2126–35. [16] Sandelowski M. Sample size in qualitative research. Res Nurs Health 1995;18(2):179–83. [17] Elo S, Kyngäs H. The qualitative content analysis process. J Adv Nurs 2008;62(1):107–15. [18] Alexander SC, Fortenberry JD, Pollak KI, Bravender T, Davis JK, Østbye T, et al. Sexuality talk during adolescent health maintenance visits. JAMA Pediatr 2014;168:163–9. [19] Perkins RB, Clark JA. Providers’ attitudes toward human papillomavirus vaccination in young men challenges for implementation of 2011 recommendations. Am J Men’s Health 2012;6(4):320–3. [20] Centers for Disease Control and Prevention. National and state vaccination coverage among adolescents aged 13–17 years—United States; 2013. Report No.: Contract No.: 34.
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
A model of health care provider decision making about HPV vaccination in adolescent males Andreia B. Alexander ∗ , Candace Best, Nathan Stupiansky, Gregory D. Zimet Section of Adolescent Medicine, Department of Pediatrics, Indiana University School of Medicine, 410 West 10th Street, HS 1001, Indianapolis, IN 46202, United States
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Article history: Received 24 March 2015 Received in revised form 16 June 2015 Accepted 22 June 2015 Available online 2 July 2015 Keywords: Human papillomavirus Health care provider Male Qualitative research Vaccine Adolescent
a b s t r a c t Introduction: In the U.S., HPV vaccination of adolescent males remains low, despite the recommendation for routine vaccination. Although research has highlighted that health care provider (HCP) recommendation is very influential in HPV vaccine uptake, research on this topic in the male population is lacking. Accordingly, we used a qualitative approach to identify HCP knowledge, attitudes, and behaviors regarding adolescent male HPV vaccination, one year, after routine vaccination of adolescent males was recommended. Method: A total of 20 U.S. pediatric HCPs participated in 20–30 min interviews about knowledge, attitudes, and practices regarding male HPV vaccination. Interviews were audio-recorded, transcribed and, analyzed using inductive content analysis. Results: The providers had been in practice for 1–35 years, 75% were female, and 75% were White. Opinions on HPV vaccination were shaped by knowledge/perception of the risks and benefits of vaccination. Although all providers frequently offered HPV vaccine to male patients, the strength and content of the offer varied greatly. Vaccination opinions determined what issues were emphasized in the vaccine offer (e.g., stressing herd immunity, discussing prevention of genital warts), while adolescent age influenced if and how they pitched their vaccine offer (e.g., HPV as a STI). Most providers agreed with the ACIP recommendations, however, several expressed that providers’ preexisting opinions might remain unchanged despite the recommendations. Consistent with the literature on determinants of HPV vaccination, providers believed that their own recommendation was a major factor in a family’s decision to vaccinate. Barriers to vaccination included the “newness” and sexual nature of the vaccine, lack of insurance coverage, and the vaccine not being mandated. Conclusions: Providers’ opinions about, and approaches to offering, HPV vaccination to males were highly variable. Interventions designed to improve male HPV vaccination should focus on helping providers to routinely recommend the vaccine to all of their eligible patients, both males and females. Published by Elsevier Ltd.
1. Introduction Human papillomavirus (HPV) has been identified as a necessary cause of genital warts, virtually all cervical cancers, many other anogenital cancers, and increasing numbers of cancers of the oropharynx [1]. The quadrivalent HPV vaccine (HPV4) was licensed in the U.S. for 9- to 26-year-old males in 2009 [2] and the Centers for Disease Control and Prevention’s (CDC) Advisory Committee on
∗ Corresponding author. Tel.: +1 973 9729261; fax: +1 973 972 9268. E-mail addresses: [email protected] (A.B. Alexander), [email protected] (C. Best), [email protected] (N. Stupiansky), [email protected] (G.D. Zimet). http://dx.doi.org/10.1016/j.vaccine.2015.06.085 0264-410X/Published by Elsevier Ltd.
Immunization Practices (ACIP) issued a routine recommendation for males in 2011 [3]. Although HPV vaccination has proven to be effective and safe, vaccination rates remain suboptimal in the U.S., especially for males [4,5]. Most published research on factors associated with HPV vaccine uptake in adolescents has focused on females [6–8]. These studies have found that public insurance status, Hispanic race, lower family income, having received flu vaccine, increased perceived vaccine effectiveness, peer acceptance, and anticipated inaction regret, were associated with increased vaccine uptake or uptake intent in males [6–10]. While some variation exists between the factors associated with male and female vaccine uptake, health care provider recommendation is a primary factor for HPV vaccination of both males
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and females [11,12]. However, many of the studies of males were conducted prior to implementation of the ACIP routine recommendation [13–15]. Although health care provider recommendation is very influential, research on this topic in adolescent males, post-routine ACIP recommendation, is lacking. This information is needed to better understand the nature of provider recommendation/nonrecommendation and could be used to guide development of interventions aimed at improving provider vaccination of males. Accordingly, the purpose of this study is to identify health care provider knowledge, attitudes, and practices regarding adolescent male HPV vaccine recommendation, post-routine recommendation by the ACIP. As little is known about these factors, a qualitative approach was taken.
2. Methods 2.1. Procedures Participants were a convenience sample of 20 pediatric physicians (general and adolescent) working in primary care clinics with relatively high vaccination rates serving primarily lower income families in a Midwestern city. A total of 28 providers were contacted via email and asked to participate in a 20–30 min interview about their opinions and practices related to HPV vaccination of males. A total of 20 (71.4%) responded and interviews were conducted either in person, in a private room at the provider’s clinic/research office or via telephone. Each participant was compensated with a $20 gift card. Interviews were conducted after the 2011 ACIP recommendation for routine HPV vaccination of males. Written informed consent for this study was waived and the study was approved by the Institutional Review Board at the author’s institution.
Table 1 Demographics. Demographic
n
%
Gender Female Male
15 5
75 25
Race White Black Hispanic
15 4 1
75 20 5
5 3 9 3
25 15 45 15
1 4 3 12
5 20 15 60
Years practicing pediatrics 1–5 years 6–10 years 10–20 years 21+ years % of Active patient population Male <20% 21–30% 31–40% 41–50%
until no new themes or changes to the model were detected. Disagreement between researchers was resolved through discussion. 3. Results 3.1. Sample The 20 providers were mostly female (n = 15) and White (n = 15), and had been practicing pediatrics from 1 to 35 years (see Table 1 for more detailed information). Overall there were no notable differences in responses by gender or race. 3.2. Model of provider recommendation
2.2. Data collection Prior to each interview, participants completed a demographic questionnaire. Semi-structured interviews were conducted by the primary author using an inductive approach based in grounded theory to avoid making assumptions, allowing for a model of decision making to emerge from the data. Interviews focused on practices regarding HPV vaccination for males. Topics included HPV vaccine knowledge, presentation of vaccine to patients, opinions about the need for male vaccination, risks, benefits, barriers, patient decision making, and school vaccination. Interviews were audio-recorded and transcribed. After each interview, the interviewer completed detailed field notes intended to document relevant information not captured on the audiorecording. The research team agreed that the data reached theoretical saturation upon completion of 20 interviews [16]. 2.3. Analysis Data were evaluated via inductive content analysis [17], which is utilized when little is known about a topic. The process includes open coding, creating categories, and abstraction of concepts, and tends to move from very specific to more general. The primary and secondary author read and openly coded four randomly chosen interviews identifying emerging issues, concepts, and themes surrounding the knowledge, opinions, and practices of health care providers regarding the HPV vaccine. The researchers then came together and discussed their individual codes and created a consensus list of preliminary codes. The researchers read through and coded the remaining 16 interviews separately and developed an initial model, which was readjusted throughout the process of coding
After examining providers’ knowledge, attitudes, and practices around male HPV vaccination, a model of provider recommendation emerged (Fig. 1). Below is an overview of the model, followed by a more detailed description of model components. We found that providers’ knowledge and perception of the risks and benefits of the HPV vaccine for males influenced their opinions on male vaccination. Their opinions on male vaccination then determined the nature of their vaccine offer. While this was true for most providers, there were exceptions. For example, although one provider felt anal and penile cancer prevention were clear benefits of HPV vaccination in males, he felt uncomfortable discussing these cancers with parents and adolescent males. Additionally, he believed parents and adolescents would be equally uncomfortable discussing these cancers. Several other providers who acknowledged prevention of male cancers as a benefit of vaccination felt this was not an important benefit because the incidence of these cancers is low. As a result, these providers said that they did not discuss male cancers when offering HPV vaccine to males. All providers agreed that their HPV vaccination offer influenced, at least partially, family vaccination decisions. For most providers, the age of the adolescent determined whether or not they would offer the vaccine and the components included in their vaccine offer. For example, a few providers stated that they never offer the vaccine to any males younger than age 11, while other providers were willing to vaccinate at age 9. Furthermore, for some, the age of the male patient would determine whether or not they would discuss the sexually transmitted nature of the virus. Many providers felt the age of the adolescent influenced how families made the decision to vaccinate. Most providers stated that the older the adolescent, the more likely the adolescents’ opinion was included in vaccination discussions and considered in vaccination initiation.
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Fig. 1. Model of health care provider HPV vaccine offer.
Table 2 Model themes. Model component
Major theme(s) (n out of 20)
Minor theme(s) (n out of 20)
Benefits
Prevention against genital warts [14] Prevention of male-to-female HPV transmission [14]
Prevention of penile, oral, anal, and/or unidentified cancers [9] Increase provider-patient-family communication [3] Cost effectiveness of male vaccination [2] Decreased worldwide burden of disease [2] Improving male sexual responsibility [1]
Risks
Safe [20] Low side effect profile [20] Increased pain compared to other vaccines [9] Syncope [10]
Local reactions at injection site [6] Potential for systemic symptoms [5] Allergic reactions [3] Parental fears of sexual disinhibition [1] Concerns for reports of chronic fatigue and pain [1] Potential for more serious side effects [2] Patient’s blaming vaccination with a coincidental condition [2]
Opinions
Good, safe, and effective intervention [16] Both males and females should be vaccinated [9]
Not important in males/more important in females [7] Herd immunity [4]
Offer
Offered in conjunction with other vaccines [18] Additional time spent explaining the HPV vaccine [15] Eliciting information from family [7] Prevention of genital warts [14] Prevention of cervical cancer [12] Males getting vaccinated protects future partners [11] Prevents STI [8] 3 doses needed [7] Personal recommendation to get vaccinated [11]
Varying levels of recommendation for vaccination [20] ACIP recommendation [7] Should be given before sexual debut [6] Prevention of anal cancers [3] Side effects [3] Stress cancer prevention/avoid genital warts discussion [5] Stress genital warts prevention/avoid anal cancer discussion [9]
Age
Vaccinating younger adolescents [9–10-year-old] [3] Vaccinating 11 years or older [10] Vaccinating older adolescents 16 years or older [10]
Gauge family readiness [8] Spread out adolescent vaccine schedule [5] Avoid discussing sex, STIs with younger adolescents [3] Avoid discussing anal cancers with younger adolescents [3]
Barriers
Not mandated for school attendance [10] Lack of insurance coverage by private insurers [9] Social anxiety around teen sexuality [8] Males not completing 3-dose series [7] Not all physicians offering/recommending vaccination [6] New vaccine [4]
Adolescents receiving too many immunizations during ages 11–12 [5] Lack of awareness by providers and families [4] Media reports of adverse side effects [4] Physicians failing to offer the vaccine [6] Poor clinic attendance among adolescent males [3] Vaccination less relatable for males than for females [2]
ACIP Recommendation
Opinion Beneficial [13] Would initiate insurance coverage [5] Knowledge Routine recommendation [11] Adolescents—unsure about upper age limit [14] Genital wart prevention [18] Channel of information Newsletters/emails from the American Academy of Pediatrics [8] Newsletters/emails from CDC [6]
Opinion Unsure of rationalization of recommendation [3] Increase physician offering/recommending vaccine [5] Limited impact on provider behavior [4] Knowledge Unaware of the recommendation [2] Confusion around which male cancers were included in vaccine indications [3] Channel of information Office discussions with colleagues [1] Formal meetings within practice [3]
Decision
Provider recommendation important [15] Decision made by parents [19]
1. Adolescent input with older adolescents [7] 2. Adolescent input with more cognitively mature adolescents [6]
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Table 3 Example quotes for each model component. Model component
Example quote
Benefits
“There are no direct benefits to you [the male patient] (Female, White).” “Well, preventing genital warts and spread of the virus to partners, rising health care costs from treatment of the genital warts and then patient discomfort, relieving that. . .The treatment for warts is rather costly. Once the warts have been established. The modalities are painful. Patients usually have to get repeat treatments. And so, all those things add to the costs of the treatment, where if we can prevent it then we would negate that cost factor (Female, Black).”
Risks
“Well, I’ve heard the really bad things that some of the people say on TV and attribute it to getting the shot. And so, it always makes me think, you know, well, even though it may be just a miniscule percentage chance of something like that happening, like some, some weird allergic reaction, or something weird that occurs after giving a shot, I always worry about that.” (female, black) “I think the biggest risk right now myself is people get the vaccine and something develops thinking it’s a vaccine’s fault (Female, White).”
Opinions
“I mean it is a sexually transmitted disease. It is something that boys could get. And so, why would we just focus on girls? I don’t want my son having genital warts. (Female, White)” “It depends on whose perspective you’re looking at. Because herd immunity is just as important as sort of the individual entity. It just depends on what perspective you’re taking. So, for me as the healthcare provider I think it’s important for everybody because the more people we immunize, the more people are protected. Overall. If you you’re talking about it on an individual basis, like the person [male] in front of me, it’s going be less important than if you’re a girl in front of me (Male, White).”
Offer
“[I do not discuss genital warts because] I always think cancer is a scarier term for people. You know, they’re like, warts I can deal with that, whatever (Female, White).” “You know, I didn’t [include cancer in my offer] because I probably just omit it from my own, you know, not having that little piece of my knowledge bank (Male, Black).” “Well, for cancers, it’s a tough one for males. Because the cancers that we are talking about are primarily, I mean, there’s some penile cancers, but the rates are so low, we’re talking about anogenital cancers, and it’s very difficult to talk about sexual orientation in an 11 year old when they haven’t made up their mind. You know? But generally, I focus on genital warts with young men (Female, White).”
Age
“I don’t really feel like talking about genital warts to a 9-year old. And I think they should understand what the benefit is of the vaccine. So, usually I bring it up when those 6th grade vaccines are going. But again, if I don’t feel like that, if it’s going make everybody uncomfortable, I wait until 12 or 13 (Female, White).”
Barriers
“I ask everybody if they’ve had all of their HPV shots and they’ll either say, ‘Yes,’ or ‘I’m part way through the series,’ or they’ll say, ‘No, my doctor said I didn’t need it yet.’ Or, ‘My doctor said it was too new.’ Or, ‘My doctor wasn’t sure that it would be good for me’ (Female, White).”
ACIP Recommendation
“I think that it’s not [the recommendation] for providers who weren’t sure of the HPV vaccine. I don’t think the fact that now they say it’s [for] males it’s going to increase the vaccine if they’re not sure about the vaccine. If they are not sure about the vaccine, they’re not going to give it to girls or boys. And if you’re sure of the vaccine now you can say, hey, your insurance company’s going to pay for this vaccine that cost $600 a pop (Female, White).” “I do. Because if I think about my [medical practice] partners, two of them just follow recommendations without really looking into it too much. . .I’m not the person to discuss all those recommendations. I like to check the evidence behind the recommendation. . .With HPV for boys, I’m not convinced because all of the evidence that I have don’t benefit for my patient. It’s just not convincing me (Female, White).”
Decision
“Yeah, it’s a big deal. I think it depends a little bit on where they are in their cognitive maturity. Some 11, 12 year-olds are further along in making those decisions. There are some parents who leave it up to their child at age 14, 15. You know, and that’s interesting to me. I think it should be probably a mutual decision. (Female, White)” “I really do think that getting vaccinated is like getting a CBC checked, or your cholesterol checked, is very much a function of the physician’s recommendations. And so, I think, sometimes in private practice they are not recommending it as much as we are in academic medicine (Female, White)”
Most providers identified barriers to vaccination (e.g., “newness” of the vaccine, STI prevention) that influenced their offer and/or the decision of families to vaccinate. Similarly, many providers felt that logistical barriers (e.g., lack of insurance coverage, non-mandated school vaccination) strongly influenced families opting for non-vaccination for their sons. Interestingly, there was substantial variation in how providers felt that the ACIP’s recommendation for routine male vaccination would affect vaccination rates. Most believed that the preexisting opinions of individual providers would impact how they perceived the ACIP recommendation, which would then influence their vaccine offer (or non-offer). For example, if providers had a positive opinion about male vaccination, then they may add the ACIP recommendation to their offer in order to increase the “sell-ability” of the vaccine. Likewise, most interviewees believed that providers holding a negative opinion about male vaccination would not change their offer to include the latest recommendation and/or would
not increase their frequency of male vaccine offers. A breakdown of model components and example quotes can be found in Tables 2 and 3, respectively.
3.2.1. Benefits The most frequently reported benefits of HPV vaccination in males were prevention against genital warts (n = 14) and prevention of male to female HPV transmission (n = 14). While all of these providers felt that protection of females was an important aspect of male HPV vaccination, there was much more variation in beliefs about the importance of the prevention of genital warts, with some providers believing prevention of genital warts was important to personal health (n = 5) and for decreasing health care costs (n = 2), and others feeling that emphasis should only be placed on cancer prevention (n = 9). Other benefits listed by providers can be found in Table 2
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Although penile, anal, and/or oral cancer prevention were considered benefits of male HPV vaccination (n = 9), these were mentioned by only a few providers (ranging from five for penile cancer to two for anal cancers). When asked why cancer prevention was not listed as a benefit for males, providers stated: (1) they did not know about the cancer indication (n = 3), (2) they knew that cancer prevention was indicated but did not know the specifics (n = 8), or (3) they did not feel the incidence of these cancers was high enough to be considered a benefit (n = 7).
3.2.2. Risks All of the providers agreed that the vaccine was safe and had a low side effects profile. The most frequently mentioned risks were increased pain compared to other vaccinations (n = 9) and syncope (mostly in females) (n = 10). Other risks mentioned can be found in Table 2.
3.2.3. Opinion Most providers viewed HPV vaccine as good, safe, and effective (n = 16). Although many believed males and females should be vaccinated equally (n = 9), several did not believe that vaccination was as important for males (n = 7). Some providers saw male vaccination as an important intervention primarily to establish herd immunity (n = 4).
3.2.4. Offer Most providers stated they offered the vaccine to their male patients in conjunction with other routine adolescent vaccines (n = 18), but spent additional time explaining HPV vaccination for two main reasons: (1) its recent availability for males and (2) families’ lack of awareness about male HPV vaccination. Oftentimes, providers would begin their offer by eliciting HPV vaccine information from the family (n = 7), then would describe the specifics about the vaccine. The most frequently mentioned components of the vaccine offer were that: (1) the vaccine was used to prevent genital warts (n = 14) and cervical cancer (n = 12), (2) males should receive the vaccine in order to prevent future partners from being infected (n = 11), (3) the vaccine was used to prevent an STI (n = 8), and (4) the adolescent would need a series of three doses (n = 7). The majority of the providers concluded their offer with a personal recommendation that the adolescent male receive the vaccine (n = 11). However, only five (25%) physicians in this study actually stated that they strongly recommend the vaccine to their male patients with another six (30%) stating they recommend the vaccine, but not strongly. While many providers mentioned genital warts in their vaccine offer, some who worked with younger adolescents left it out completely due to its sexual nature (n = 5). In these instances, providers stressed cancer prevention in order to avoid this discussion. Conversely, most of the providers who spoke about genital warts excluded any discussion of anal cancers (n = 9). The most common reasons identified for this exclusion included provider discomfort and the perceived discomfort among families.
3.2.5. Age Providers were evenly split about vaccinating young adolescents. Half were comfortable vaccinating 11–12-year-old males (n = 10), with some willing to start as young as age nine (n = 3). The remaining providers were more reluctant to vaccinate young adolescent males (n = 10). Many of these providers noted the difficulty in explaining HPV vaccination to parents of younger adolescents because of the perception that parents are not ready to discuss sex or STIs.
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3.2.6. Barriers The most commonly reported barriers included the vaccine not being mandated for school attendance (n = 10), perceived lack of insurance coverage by private insurers (n = 9), anxiety around teen sexuality [8], males not coming back to complete the three dose series (n = 7), not all physicians offering/recommending the vaccine (n = 6), and the vaccine being too new (n = 4). Less commonly reported barriers can be found in Table 2. 3.2.7. ACIP recommendation Most providers agreed that the latest ACIP recommendation was beneficial (n = 13), with only a few providers questioning why the ACIP added a routine HPV vaccination for males (n = 3). Most of the variation came with respect to the effect the recommendation would have on male vaccination and providers’ knowledge about HPV vaccine and its recommendations for use. Most providers knew that the 2011 ACIP recommendation included routine HPV vaccination for males (n = 11). However, some were unaware about this “new” recommendation (up to a year after the recommendation had been released) (n = 2). Providers were knowledgeable that the vaccine should be given to adolescents, but were unclear on the specifics. For example, some knew that it could be given as young as age 9 (n = 5), but others did not. Likewise, most knew that it was routinely recommended for 11 and 12 year-olds (n = 18). Nevertheless, the majority did not know the upper age limit of the recommendation (n = 14). Most providers understood that the vaccine was indicated to prevent genital warts (n = 18), however, there was quite a bit of confusion around which male HPV-related cancers were included in the vaccination indications. Most providers became aware of the latest recommendation via newsletters and emails from the American Academy of Pediatrics and/or the CDC (n = 8). Others were informed during office discussions with colleagues or formal meetings (n = 3). 3.2.8. Decision There was very little variation regarding the decision process about male vaccination. Most providers believed that their recommendation was one of the most important factors in the family’s decision (n = 15). This was evident in the reported percentage of males who accepted HPV vaccination. Providers who stated they recommended or strongly recommended the vaccine reported a 70–90% vaccination uptake, while providers who stated that they offered, but did not recommend the vaccine reported a vaccination rate of 25–50%. Providers agreed that parents were the primary decision-makers around vaccination (n = 19). In the cases when adolescents had input into the decision, it was most likely to involve an older adolescent (n = 8). 4. Discussion Although we were able to describe an overall model of provider offer, there was great variation within each of the components of the model, despite the fact that these providers were from the same or similar practice groups. This variability suggests that the decision to offer and recommend HPV vaccination is dependent on physician knowledge or lack of knowledge about, and opinions on, the risks and benefits associated with the vaccine. One of the most heterogeneous findings was with regard to prevention of HPV-related cancers that affect males, with some providers having no/inaccurate knowledge of current indications and others having accurate knowledge. Providers who were more knowledgeable about HPV-related cancers were also more likely to provide a strong recommendation for the vaccine. As provider recommendation is one of the strongest predictors of HPV vaccine uptake [11–14], future research should be conducted to determine
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effective interventions to increase physician knowledge about cancer-prevention indications for HPV vaccination. A second area of heterogeneity was comfort with discussion about HPV vaccine as STI prevention. While some providers were personally uncomfortable discussing HPV outcomes, such as anogenital warts, others believed that families would be uncomfortable with such a discussion, especially in younger adolescents. This set of findings is consistent with previous research, which shows that few pediatricians engage in meaningful discussions about sexual health with their adolescent patients [18]. Not surprisingly, providers were more comfortable discussing sexual health issues with older adolescents (>15-years-old). Overall, the providers considered physician recommendation to be the strongest determining factor in parent approval of vaccinating their children. However, despite an overall general positive opinion about male HPV vaccination, most providers did not provide strong recommendations for vaccination. It appears that most of the providers believed that male vaccination had a role in protecting female partners, but were less convinced of its direct benefits for their male patients, a finding consistent with research conducted prior to ACIP’s routine recommendation [19]. This finding may explain, at least in part, why U.S. male vaccination initiation rates since the ACIP routine recommendation have only reached 34.6% [4]. Finally, many of our respondents felt the latest ACIP recommendation would not have a major effect on provider recommendations; that a provider’s preexisting personal opinion of HPV vaccination would remain the principal determining factor. It is not clear to what extent this opinion is supported by data, but the slow progress in HPV vaccination rates of females and males, despite the strong routine ACIP recommendation, suggests that health care providers have not fully embraced the ACIP guidelines. 4.1. Limitations While the qualitative design of this study allowed us to examine in-depth information about health care provider knowledge, attitudes, and practices around HPV vaccination, there are a number of limitations. Although a sample size of 20 interviews was adequate for this qualitative research study, it limits the generalizability of these findings, which may not be applicable to different groups of health care providers. Additionally, while this study provides a good starting point to understanding male HPV vaccination, the data collection sites were clinics with high adolescent vaccination rates and high proportions of patients on state funded insurance programs. Research conducted in clinics with lower vaccination rates as well as those with higher proportions of patients using private insurance will help elucidate the full range of issues surrounding providers and male HPV vaccination. 5. Conclusion Overall, providers had a positive opinion about HPV vaccine and offered it to most of their male patients. There was substantial variability across providers in terms of knowledge about the benefits of HPV vaccination for males, comfort with discussing sexual issues with adolescents and their families, and whether or not the provider recommended the vaccine. The results of this study may help to inform the development and evaluation of interventions for physicians to increase vaccine uptake and may inform future,
larger scale, research in diverse settings to gain a better understanding of physician knowledge, attitudes, and practices around HPV vaccination in general and of males in particular. Acknowledgments This study was supported by Merck & Co., Inc. through an investigator-initiated grant (MISP #38094). Its contents are the sole responsibility of the authors and do not reflect the official view of Merck & Co., Inc. Conflict of interest statement: Gregory Zimet and Nathan Stupiansky have been investigators on investigator-initiated research funded by Merck & Co. In the last year, Gregory Zimet served as a consultant to Merck & Co., Inc. References [1] Center for Disease Control and Prevention. Human Papillomavirus 2014 [cited 2014 July 3]. Available from http://www.cdc.gov/std/hpv/ [2] US Food and Drug administration [cited 2014 July 3].Available from Approval Letter—Gardasil; 2009 http://www.fda.gov/BiologicsBloodVaccines/Vaccines/ ApprovedProducts/ucm186991.htm [3] Centers for Disease Control and Prevention. Recommendations on the use of quadrivalent human papillomavirus vaccine in males—. Advisory Committee on Immunization Practices (ACIP); 2011. Report No.: Contract No.: 50. [4] Elam-Evans LD, Yankey D, Jeyarajah J, Singleton JA, Curtis CR, MacNeil J, et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years—United States, 2013. MMWR 2014;63:625–33. [5] Pierre-Victor D, Mukherjee S, Bahelah R, Madhivanan P. Human papillomavirus vaccine uptake among males 11–26 years in United States: findings from the National Health and Nutrition Examination Survey, 2011-2012. Vaccine 2014;32(49):6655–8. [6] Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among US adolescents: a systematic review of the literature. JAMA Pediatr 2014;168(1):76–82. [7] Etter DJ, Zimet GD, Rickert VI. Human papillomavirus vaccine in adolescent women: a 2012 update. Curr Opin Obstet Gynecol 2012;24(5):305–10. [8] Rambout L, Tashkandi M, Hopkins L, Tricco AC. Self-reported barriers and facilitators to preventive human papillomavirus vaccination among adolescent girls and young women: A systematic review. Prev Med 2014;58:22–32. [9] Alexander AB, Stupiansky NW, Ott MA, Herbenick D, Reece M, Zimet GD. Parentson decision-making about human papillomavirus vaccination: a qualitative analysis. BMC Pediatr 2012;12(1):192. [10] Alexander AB, Stupiansky NW, Ott MA, Herbenick D, Reece M, Zimet GD. What parents and their adolescent sons suggest for male HPV vaccine messaging. Health Psychol 2014;33(5):448. [11] Lau M, Lin H, Flores G. Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health. Vaccine 2012;30(20):3112–8. [12] Rosenthal S, Weiss T, Zimet G, Ma L, Good M, Vichnin M. Predictors of HPV vaccine uptake among women aged 19–26: importance of a physician’s recommendation. Vaccine 2011;29(5):890–5. [13] Reiter PL, McRee A-L, Pepper JK, Gilkey MB, Galbraith KV, Brewer NT. Longitudinal predictors of human papillomavirus vaccination among a national sample of adolescent males. Am J Public Health 2013;103(8):1419–27. [14] Gilkey MB, Moss JL, McRee AL, Brewer NT. Do correlates of HPV vaccine initiation differ between adolescent boys and girls? Vaccine 2012;30:5928–34. [15] Malo TL, Giuliano AR, Kahn JA, Zimet GD, Lee J-H, Zhao X, et al. Physicians’ human papillomavirus vaccine recommendations in the context of permissive guidelines for male patients: a national study. Cancer Epidemiol Biomarkers Prev 2014;23(10):2126–35. [16] Sandelowski M. Sample size in qualitative research. Res Nurs Health 1995;18(2):179–83. [17] Elo S, Kyngäs H. The qualitative content analysis process. J Adv Nurs 2008;62(1):107–15. [18] Alexander SC, Fortenberry JD, Pollak KI, Bravender T, Davis JK, Østbye T, et al. Sexuality talk during adolescent health maintenance visits. JAMA Pediatr 2014;168:163–9. [19] Perkins RB, Clark JA. Providers’ attitudes toward human papillomavirus vaccination in young men challenges for implementation of 2011 recommendations. Am J Men’s Health 2012;6(4):320–3. [20] Centers for Disease Control and Prevention. National and state vaccination coverage among adolescents aged 13–17 years—United States; 2013. Report No.: Contract No.: 34.