In the United States, more than 14 million people. Communicating with Families About HPV Vaccines. Clinical Review. Amanda Dempsey, MD, PhD, MPH

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1 Clinical Review Communicating with Families About HPV Vaccines Amanda Dempsey, MD, PhD, MPH Abstract Objective: To provide evidence-based guidance on strategies that are likely or unlikely to be successful in navigating HPV vaccine conversations with patients and parents. Methods: Nonsystematic review of the literature. Results: This review highlights some of the most recent innovations in provider HPV vaccine communication and describes provider communication strategies that have been found to improve adolescent vaccination rates in rigorous scientific studies. Promising strategies for which additional research is needed and strategies that probably do not work are also described. Conclusion: By understanding what works, what may work, and what not to do when it comes to communicating with families about HPV vaccines, providers can be better prepared for maximizing the impact they can have on adolescent HPV vaccination rates. Key words: human papillomavirus; vaccine hesitancy; health communication; parents; immunization. In the United States, more than 14 million people newly acquire genital human papillomavirus (HPV) annually, and 75 million Americans are infected at any given time [1]. As the most common sexually transmitted disease, more than 80% of sexually active U.S. adults are estimated to be infected with HPV by the age of 50 [1,2]. Although the majority of infections are silent and resolve without clinical sequelae, a proportion of infected individuals will go on to develop HPV-related diseases. In women, these include cervical cancer and pre-cancer (ie, abnormal Pap smears); cancers of the vagina, vulva, anus, and oropharynx; and genital warts [3]. Males also bear a high burden of HPV-related disease in the form of penile, anal, and oropharyngeal cancers, as well as genital warts [3]. While once thought of as primarily a woman s disease [4], recent research demonstrates men are also significantly impacted by HPV particularly in the form of oropharyngeal cancers, which are 2 to 3 times more common in men than in women [5]. In fact, it is estimated by the year 2020 more men will die of HPV-related oropharyngeal cancer than women will die of cervical cancer [6,7]. The combined cost of HPV-associated cancers and other conditions is estimated to be $8 billion per year in the United States [8 11]. HPV Vaccines Effective HPV vaccines have been available for females aged 9 to 26 years since 2006 (bivalent and quadrivalent vaccines) and for males aged 9 to 26 since 2010 (quadrivalent vaccine only) [12]. These vaccines have been shown in clinical trials to be highly efficacious in preventing HPV infection, cervical pre-cancer, and anal, vaginal, penile, and vulvar cancers caused by the HPV types covered in the vaccine [2]. Although their effectiveness against head and neck cancer has not been studied in clinical trials, most experts believe that these vaccines will also provide protection against at least a proportion of these cancers [13,14]. In 2015 the U.S. Food and Drug Administration approved licensure of a 9-valent HPV vaccine that will soon replace the quadrivalent vaccine in the U.S. market [15]. The 9-valent vaccine is licensed for both males and females aged 9 to 26 and is expected to prevent an even higher proportion of HPV-related cancers than earlier HPV vaccines due to the protection against 5 additional oncogenic HPV types [15]. Despite the potential of HPV vaccines to drastically reduce the incidence of HPV-related cancers and other diseases, these vaccines are not being as widely used in the United States as was hoped. The most recent national data from 2015 demonstrates that only 41.9% of girls and 28.1% of boys have received all 3 doses recommended in the HPV vaccine series [16]. This level of vaccine From the University of Colorado Denver, Aurora, CO. Vol. 24, No. 3 March 2017 JCOM 123

2 HPV Vaccine Communication utilization is significantly lower than the Healthy People 2020 goal of 80% coverage [17], and also significantly lower than that of other developed countries such as Australia and the United Kingdom, which have achieved vaccination levels of ~70% among their target adolescent populations [18,19]. In the future, these low vaccination levels will likely be mitigated somewhat by the recent approval from the FDA and recent recommendation from the Advisory Committee on Immunization Practices (ACIP) for only 2 doses of the 9-valent HPV vaccine (spaced 6 to 12 months apart) for adolescents less than 15 years of age [20,21]. Three doses are still recommended for those aged 15 to 26 years. Provider Communication About HPV Vaccines How providers communicate with parents and patients about HPV vaccines is a key influential factor driving current U.S. adolescent HPV vaccination levels [22,23]. Numerous studies demonstrate that a provider s recommendation generally has the largest impact on whether or not an adolescent receives the vaccine, even above that of parent factors such as attitudes and beliefs about the vaccine and patient characteristics such as age and insurance status [23 31]. Moreover, parents consistently cite their adolescent s provider as one of the most trusted and impactful resources for obtaining vaccine information [22,32]. Unfortunately, research also shows that providers often fail to adequately recommend the HPV vaccine for their patients, especially for 11 to 12 year olds for whom the vaccine is preferentially recommended [33,34]. For example, in a national study of parents done in 2013, not being recommended by a provider was one of the top 5 reasons parents of males and of females aged 11 to 17 gave for not getting their adolescent vaccinated against HPV [35]. Supporting this also is a 2014 study of 776 pediatricians and family medicine providers nationally, in which Gilkey and colleagues found that more than 1 out of 4 providers did not highly endorse the HPV vaccine for 11 to 12 year olds despite this having been the recommended practice from ACIP for the prior 8 years for girls and 4 years for boys. This is in comparison to the other adolescents vaccines that were reported in the same study as being endorsed highly by these providers > 95% of the time [36]. Recognizing that providers HPV vaccine recommendations are often suboptimal, researchers have begun to define what components comprise high-quality HPV vaccine recommendations. This has been operationalized by one research group as (1) timeliness routinely recommending the vaccine starting when the patient is 12 years; (2) consistency recommending the vaccine for all eligible adolescents as opposed to an approach based on providers perception of their patients risk for HPV infection; (3) urgency recommending that the vaccine be given on the same day the vaccine is being discussed, rather than offering the option of getting it at a future visit; and (4) strength using language that clearly conveys that the provider believes the vaccine is very important for the adolescent to receive. A national study of primary care providers done in 2014 examined how frequently these quality components were implemented [37]. The results were startling and discouraging. Nearly half of providers (49%) reported they usually recommended that 11 to 12 year olds get the vaccine at a later visit, 41% used a risk-based approach for deciding when to recommend the vaccine, 27% did not tell the parents the vaccine was very or extremely important, and a large proportion did not start routinely recommending the vaccine before the age of 13 (39% for male patients and 25% for females) [37]. Much research has now accumulated to explain the underlying reasons why providers may not give consistent and high-quality HPV vaccine recommendations to all eligible adolescents [22]. Issues such as providers own knowledge about HPV-related diseases, personal beliefs about the vaccine s safety and necessity, concern that a discussion about the vaccine will necessitate a discussion about adolescent sexuality with the parent, belief that parents will not want their child vaccinated if asked, perceptions that a provider can adequately select those patients most in need of HPV vaccination, and concern that raising the vaccine discussion with vaccine-hesitant parents will result in prolonged discussions have have been shown to impact whether and how providers communicate about HPV vaccination during clinical visits [22,36 45]. Now that these barriers have been defined and described, there is a great need to use this knowledge to develop and evaluate interventions that help to mitigate these barriers and improve providers vaccine communication abilities. Such interventions are needed not only for HPV, but for all vaccines [46,47]. Possible Strategies for Helping Providers Communicate About HPV Vaccines Communicating with families about HPV vaccines can take many forms [22]. These include strategies such 124 JCOM March 2017 Vol. 24, No. 3

3 Clinical Review as passive communication via posters or information posted in the clinic; active, practice-based strategies such as vaccination reminders sent by text, , or phone; and interpersonal communication strategies between a provider and a patient or their parent. The scope of this article focuses on interpersonal communication and reviews 4 novel, recently developed, evidence-based interpersonal communication strategies that have been shown to improve vaccination rates for HPV specifically, and 2 additional strategies that show promise but have not been evaluated for HPV vaccines in particular (Table). Two additional communication techniques that were found in research studies not to improve vaccination rates are also presented. This information can assist providers in understanding what works, what may work, and what not to do when talking to families about HPV vaccination. Before discussing these interventions, it is worth noting that several of the passive and active strategies have been shown in clinical trials to improve adolescent HPV vaccination rates. Although these are beyond the scope of this article, inclusion of these strategies should certainly be considered by any practice as a mechanism to increase vaccination levels, especially given that the most successful interventions to improve vaccination levels consist of multiple components [48]. Also useful is a recently described taxonomy of vaccine communication interventions that provides additional perspective on the scope and complexity of interventions to improve vaccine delivery [49]. There are several well-written review articles that describe interventions that focus on passive and active strategies at the practice or community level [50 52]. Interpersonal Communication Strategies Shown to Increase HPV Vaccination Presumptive Communication One of the first studies to examine the specific way in which providers communicate about vaccines focused not on HPV but rather on young childhood vaccines. In 2013 Opel and colleagues performed a study in which they taped clinical encounters between a pediatrician and a parent of a child aged 1 to 19 months [53]. Of the 111 encounters recorded, 50% of parents were classified as vaccine hesitant. Parents were aware they were being taped but not aware that the overall purpose of the study was to examine providers communication related to vaccination. The researchers found that providers generally used one of 2 communication styles to introduce the vaccine discussion. The first, called the presumptive style, assumed Table. Possible Strategies for Communicating with Familes about HPV Vaccines Tested and found useful for HPV specifically Presumptive communication style Motivational interviewing Personalized communication Focus on cancer prevention Tested and found useful for other vaccines, but not tested for HPV specifically Helping parents create specific plans for vaccination Treating all vaccines discussed the same Tested for other vaccines but not found useful Presenting myths and facts Fear appeals Untested possibilities for the future Leveraging technology Using psychological "levers" Serious video games that parents would agree to vaccination and presented the vaccines as routine (ie, We have to do some shots today ). The second style, called participatory, was more parentoriented and used language suggesting shared decisionmaking (ie, So what do you want to do about shots today? ). The study showed that the odds of resisting the provider s vaccine recommendations were significantly higher when providers used a participatory approach than a presumptive one, suggesting that even small changes in language can have a major impact on the likelihood of vaccination. However, given the study design, causality between providers recommendation style and parents vaccination decisions could not be delineated. In 2015 Moss and colleagues performed a study that examined the use of these 2 communication styles with regard to HPV vaccination [54]. This study used data from the 2010 National Immunization Survey Teen, a national survey on childhood vaccination that includes provider verification of vaccines given [16]. Researchers categorized provider vaccine communication styles into provider-driven, which was similar to the presumptive style described Opel, and patient-driven, which was similar to Opel s permissive style. Parents who received a more provider-driven style of HPV vaccine recommendation were far more likely to have allowed their adolescent to be vaccinated than those receiving patient-driven recommendations [54]. Further supporting this communication approach are results from a qualitative study done by Vol. 24, No. 3 March 2017 JCOM 125

4 HPV Vaccine Communication Hughes and colleagues in which triads of mothers, adolescents, and providers were interviewed after a preventive care visit to assess the communication that occurred regarding HPV vaccination [39]. Providers communication style was categorized into 1 of 3 groups: paternalistic (clinician makes the vaccination decision and communicates this to the family); informed (patient and family gathers information from the clinician and other sources to reach a vaccination decision); and shared (medical and personal information is exchanged between the provider and family and then a decision is reached jointly). Providers who typically adopted the paternalistic approach perceived that they had the highest success in convincing parents to vaccinate a perception that was confirmed in quantitative assessments of vaccination status among adolescents in the study sample [39]. Our own research demonstrates that learning and implementing a presumptive/paternalistic HPV vaccine recommendation style is easy for primary care providers to do and is perceived as often shortening the time taken during clinical visits to discuss the vaccine [55,56]. Thus, providers should consider opening the HPV vaccine conversation using this approach, and then turning to some of the other communication techniques described below when met with parental resistance or questions. Motivational Interviewing A second communication technique that seems effective for promoting HPV vaccination, especially for vaccine hesitant parents, is motivational interviewing. Motivational interviewing describes a communication technique in which the provider leverages a parents or patients intrinsic motivation to engage in a preferred health behavior [57]. Motivational interviewing was originally developed to combat substance abuse [58,59] but has subsequently been successfully applied to a number of other health issues [60 64]. There is growing interest from public health and medical providers in using this technique for increasing vaccination [39,65 68]. Our research group performed a large, cluster-randomized controlled trial of 16 pediatric and family medicine clinics to examine the impact of a provider communication toolkit on adolescent HPV vaccine series initiation and completion [50,69]. The toolkit consisted of motivational interviewing training for providers related to HPV vaccination and training on 3 tangible resources providers could also use with parents an HPV fact sheet, an HPV vaccine decision aid, and an educational website. Results from the study demonstrated that motivational interviewing was the toolkit component most widely utilized by providers and was also perceived as being the most useful. More importantly, HPV vaccine series initiation levels were significantly higher among adolescents in practices receiving the toolkit than in control practices. There was no impact on HPV vaccine series completion (unpublished results). The usefulness of motivational interviewing for vaccination is further supported by a small study in which community pharmacists receiving motivational interviewing training for adult vaccination reported significantly higher patient readiness to receive vaccines following their interaction with the pharmacist than those who did not receive the training [70]. Finally, Perkins et al performed a cluster randomized controlled trial that evaluated the impact of a provider-focused intervention on adolescent HPV vaccination rates. The intervention included frequent provider support meetings, education on HPV infection and vaccination, feedback on providers individual HPV vaccination rates, provider incentives, and basic motivational interviewing principles with vaccinehesitant parents. HPV vaccination series initiation and completion rates were significantly higher in intervention practices than controls, and this effect was sustained for at least 6 months after the active intervention period was over [67]. However, it was unknown how much the motivational interviewing contributed to these results. Based on the above information, and the long history of success of motivational interviewing for improving patient compliance with other recommended health behaviors, this technique appears to have a reasonable evidence base and should be considered for communicating with families that express resistance to HPV vaccination. Personalized Communication Parents reasons for not having their adolescent vaccinated against HPV are often complex and multifactorial [71,72]. Personalized approaches are needed to account for each parent s unique informational needs, beliefs, and prior experiences [65]. Unfortunately, given the short amount of time allotted for clinical visits, it is often difficult to provide adequate information to parents during these encounters [73 75]. Indeed, concern about prolonged HPV vaccine discussions has been identified as an important barrier for providers that cause some to forgo recommending the vaccine [36,75]. One potential solution to this issue is to leverage technology in the form of web-based interventions that use 126 JCOM March 2017 Vol. 24, No. 3

5 Clinical Review software to tailor materials to each individual s unique informational needs. Feasibility for this idea comes from the knowledge that many parents already use the web to research health issues related to their children [76], and that doctors offices are increasingly using patient portals and other web-based resources to help parents prepare for upcoming visits, especially those focused on health maintenance [77,78]. Tailored messaging interventions have been shown across populations and health issues to generally result in superior adherence with health behaviors when compared to untailored controls [79 82]. Several researchers have thus begun exploring whether such a personalized communication strategy may be similarly effective for adolescent HPV vaccination [50,83 85]. As an example, Maertens and colleagues used communitybased participatory research techniques to develop a webbased tailored messaging intervention for Latinos regarding HPV vaccination [86]. A subsequent randomized controlled trial of the intervention in over 1200 parents of adolescents and young adults demonstrated that the intervention improved participants intentions to vaccinate compared to usual care [87], and among adolescents, higher HPV vaccine series initiation levels (unpublished data). Although additional work is needed to understand the feasibility of implementing such an intervention more broadly, additional support for the usefulness of a tailored messaging approach comes from a study of female university students that demonstrated higher HPV vaccination intentions after exposure to tailored information compared to untailored information. However, the impact on actual HPV vaccine utilization was not measured in the study [84]. Contrasting results were found in a different study of university students where researchers failed to find an impact of message tailoring on HPV vaccination utilization. However, this study was limited by a low response rate (~50%) to the follow up survey where vaccination status was assessed, and also by overall low levels of HPV vaccine initiation among the entire study sample (8%) [85]. Given the low number of studies in this area, and some conflicting data, additional research is needed to better understand the impact of personalized communication on HPV vaccination levels. However, results from these studies suggest that a modest benefit may be achieved with this approach, especially if coupled with other, evidence-based, clinic-level interventions to promote vaccination (eg, vaccine reminders, extended office hours), as is suggested by the Task Force on Community Preventive Services [48]. Focusing Communication on Cancer Prevention HPV vaccines are unique in that they are only 1 of 2 vaccines for cancer prevention (the other being hepatitis B). Provider and parent surveys suggest that while most providers do mention cancer prevention when discussing HPV vaccines [40,88,89], this may be more commonly done with female patients than males [22]. Focusing on cancer prevention rather than sexual transmissibility is a communication technique suggested by the Centers for Disease Control and Prevention (CDC) as many parents cite this aspect of the vaccine as one of the most compelling reasons for vaccinating [45,90]. CDC s You are the Key program [91] uses cancer prevention as a central theme in their physician and patient communication materials, based on significant prior market research on the acceptability and impact of such messages among parents and providers. In 2016 Malo and colleagues tested the potential impact of brief messages related to HPV vaccination, including cancer prevention messages, among a national sample of 776 medical providers and 1504 parents of adolescents [92]. In addition to their potential to motivate parents to vaccination, associations between parental endorsement of each message and their adolescent s vaccination status were also examined. The cancer prevention messages were among those most highly endorsed by both parents and providers as being motivating for parents to get their adolescent vaccinated. More importantly, among parents these endorsements were associated with a significantly higher likelihood of the adolescent having been vaccinated against HPV. Interestingly, one of the briefest messages in the study, I [the physician] strongly believe in the importance of this cancer preventing vaccine for [child s name], was perceived as the most persuasive message by parents. Further support for the positive impact of framing HPV vaccines primarily as cancer prevention comes from another national study of 1495 parents of 11 to 17 year olds that examined 3 measures of quality of their adolescent provider s HPV vaccine recommendation, and the relationship between recommendation quality and likelihood of adolescent HPV vaccination [40]. The 3 quality indicators assessed included providing information about cancer prevention, encouraging the vaccine strongly, and recommending it be given on the same day as it was being discussed. While 49% of parents reported receiving no HPV vaccine recommendation from their adolescents provider, of those that did, 86% received a cancer prevention message. Parents who had been given high quality recommendations that included either 2 or 3 of the Vol. 24, No. 3 March 2017 JCOM 127

6 HPV Vaccine Communication quality indicator measures had over 9 times the odds of vaccine series initiation and 3 times the odds of vaccine series follow through than those who had not received any recommendation, and also significantly higher odds of vaccination than parents who had received low quality recommendations (ie, included only 1 indicator). Taken together, these results suggest that focusing discussions about HPV vaccines on their ability to prevent cancer is likely to be persuasive for some parents. Strategies That Are Promising But Not Thoroughly Tested Helping Parents Create Vaccination Plans A recent commentary suggested that instead of focusing on changing beliefs or educating parents and patients about the need for a given vaccine, perhaps a better way to craft interventions for increasing vaccination is to focus on structuring the environment to make vaccination easy [93,94]. Examples of this include strategies such as extended office hours and making the vaccine available in other locations such as schools and pharmacies, both of which have been shown in some populations and settings to improve vaccine utilization [48,95]. One aspect of structuring a vaccine-conducive environment that relates to provider communication is helping parents create implementation intentions for future vaccination visits. In its most obvious form, this would mean providers provide office resources that facilitate making an appointment for the next dose in the HPV vaccine series during a clinic visit where the first dose was provided. But such an approach could also potentially extend to parents who are on the fence about the vaccine to make an appointment before the parent leaves the office with an unvaccinated child to either re-discuss the vaccine in the future or to actually start the vaccine series. Support for such a strategy comes primarily from the social sciences, which suggest that implementation intentions work by increasing attention to specific cues to action, making it more likely that that the cue will be acted upon [96 98]. Creating implementation intentions has been shown to be helpful for improving adherence with a variety of health behaviors [99 105], and there is a growing evidence base related to how implementation intentions may facilitate vaccination specifically. For example Vet and colleagues performed a randomized controlled trial among 616 men who have sex with men with either strong or weak intentions to receive the hepatitis B vaccine [106]. Half of the participants were asked to create an implementation intention plan where they described when, where and how they would obtain the vaccine. Those in the control arm were not given this prompt. Regardless of whether their initial vaccination intention was weak or strong, those who had been asked to create an implementation plan had more than double the likelihood of actually getting the vaccine than participants who did not receive the implementation plan prompt. Similarly, a study of influenza vaccination rates among corporate employees found that those who were asked to write down the day and time they planned to go to employee health to get the free vaccine were somewhat more likely (4% higher) to be vaccinated than those who did not receive this prompt [107]. In addition, a study of elderly individuals found that influenza vaccination rates were significantly higher among those who had received action instructions on how, when and where to get the vaccine than those who did not [108]. These studies suggest that helping parents craft a definitive follow-up plan regarding vaccination could have a significant impact on vaccination rates particularly for vaccines like HPV that require multiple doses. Treating all Adolescent Vaccines the Same Prior research has demonstrated that providers often communicate differently about HPV vaccines than other adolescent vaccines such as the tetanus-diphtheria-pertussis (Tdap) and meningococcal (MCV) vaccines [22,36]. Providers often tend to discuss the HPV vaccine last among these 3 vaccines, provide weaker endorsements of the vaccine, and pre-emptively give much more detail about the HPV compared to the other vaccines, even in the absence of a parent s request for additional information [36,39,41]. The CDC and the American Academy of Pediatrics now suggest putting HPV at the beginning or middle of the list of vaccines recommended to the adolescent (ie, HPV, Tdap and MCV ), and treating all recommended vaccines equivalently in terms of the level of detail provided to parents in the absence of a parent s request for more information [109,110]. Through these suggestions have face validity, their specific impact on HPV vaccination rates, and on patient and provider satisfaction with the visit have yet to be evaluated. Strategies that Probably Don t Work Presenting Myths and Facts Research related to promoting other vaccines provides insight into communication activities that probably would not work well for promoting HPV vaccination. A JCOM March 2017 Vol. 24, No. 3

7 Clinical Review study by Nyhan and colleagues examined the impact of 2 different messages related to influenza vaccines on participants beliefs about the vaccine s safety and intentions to get vaccinated [111]. One group received information to correct the commonly held belief that influenza vaccine can cause the flu while the other received information about the risks associated with contracting an influenza infection. While the correction of myths did improve participants perceptions of the vaccine s safety, information about influenza dangers did not. Neither message impacted intentions to vaccinate in the study subjects overall. However, in sub-analyses the correction of myths actually decreased intentions to vaccinate among those with high baseline levels of concern about the vaccine s side effects that is, among those most concerned that the flu vaccine can give someone the flu, correcting this myth actually decreased the likelihood that they would receive the vaccine. Similar findings have been reported in other studies related to vaccination [ ], and suggest that the threat generated by providing information opposing a person s beliefs may actually entrench these beliefs further as part of the threat response a phenomenon known as attitude polarization [115]. These results also are consistent with the concept of negativity bias, which posits that negative information influences people s risk perceptions more than positive information, and that the more strongly a risk is attempted to be negated, the lower the effectiveness and perceived trust of the information [116]. Using Fear Appeals One tactic that has been suggested by some as a way to promote vaccination is to provide graphic depictions of the possible sequelae of vaccine-preventable diseases. The thought behind this idea is that because vaccination is so successful, most parents will have never experienced significant impacts from vaccine preventable diseases that, in the past, had been a major motivator for parents to vaccinate. Thus, in order to counter beliefs about controversial issues like vaccination, highly emotionally compelling and engaging information may be especially useful. This is a common tactic used by anti-vaccination groups to spread their own messages [117]. However, several studies suggested that using fear appeals (aka scare tactics) such as this to promote vaccination can actually have a negative effect on vaccination intentions. For example, in a 2011 study of a nationally representative sample of parents of children < 18 years, 4 different message formats were tested for their impact on parental intentions to vaccinate a future child with the measlesmumps-rubella vaccine (MMR) [113]. Message formats included correcting the misinformation that MMR causes autism, presenting information on MMR-related disease risk, providing a dramatic narrative about a child endangered by measles, and showing pictures of infants affected by these diseases. Counter to the study s hypotheses, the dramatic narrative message actually increased parents perceptions that MMR vaccines had serious side effects, and the pictures increased parents belief that the MMR vaccine could cause autism. These counterintuitive results are consistent with other studies that have examined the impact of message framing on adults vaccination intentions for HPV and influenza [108,118,119]. Taken together, fear appeals seem unlikely to sway many hesitant parents towards HPV vaccination. Looking Into the Future Moving forward, additional interventions to improve providers ability to communicate with families about HPV vaccination will undoubtedly be developed. A major area of interest in this regard is leveraging the power of technology and the internet, including using social media, mobile technologies, and online interventions to augment the provider/parent interaction that occurs during the clinical visit [50,120]. Web-based approaches have the benefit of generally being low cost and easy to disseminate to large populations. Such interventions have already been developed for a number of other health issues, some of which have proven effective [121,122]. However, use of the internet to promote healthy behaviors in general, and vaccination specifically, is still in its infancy. There is still much to be learned about how to create effective web-based tools, how to engage patients with them, and how to assess their impact on health outcomes [123]. Another interesting area for future research is identifying psychological levers to motivate parents vaccination intentions [94]. One example is focusing on using parents values (ie, protecting my child from harm) as an intervention target rather than beliefs or attitudes. This is because values tend to be inherent and static over time, compared to beliefs and attitudes, which are subject to change depending on the context [124]. Prior research has shown that interventions that leverage values rather than facts can be an effective way to overcome beliefs that are highly emotional or controversial, and that individuals are more likely to trust sources and individuals Vol. 24, No. 3 March 2017 JCOM 129

8 HPV Vaccine Communication with shared values than those without [125], suggesting that this may be a useful way to motivate parents toward vaccinating their children. Self-affirmation is another example of a psychological lever that has a significant evidence base from the social science literature as a helpful tool for moving patients towards a desired health behavior [126,127], but it has not been extensively applied to the field of vaccination. Researchers in the field of vaccine delivery are increasingly recognizing the potential value of these unique intervention approaches [101, ], and it may be fruitful in the future to more closely examine the efficacy of interventions that target things like values, self-affirmation or other psychological levers to change parents HPV vaccination behaviors. A final notable area for intervention research related to HPV vaccination is the use of video games. Although not likely to be used directly during patient visits, this strategy could be conceptualized as a potential way to augment the information conveyed to a parent by a provider directly during a clinical encounter. A meta-analysis from 2016 identified 16 different serious video games that were used to train and educate users about specific vaccine preventable diseases (usually influenza, none for HPV) and the need for vaccination [135]. In many of them, the objective of the game was to protect a virtual community from a vaccine preventable disease and/or manage outbreaks. Only 2 of the games evaluated outcomes in the short term (ie, at the time the game was being played). None have evaluated longer-term impacts such as vaccination intention or utilization. In the era of plugged in parents and adolescents, video games represent a unique but understudied mechanism for helping providers communicate, albeit indirectly, with families about the need for vaccination. Imagine providing a prescription to an HPV-vaccine hesitant family to go play Zombie Wars HPV! One would expect the curiosity factor alone would result in significant engagement with this intervention tool. Conclusion With persistently lagging HPV vaccination rates among U.S. adolescents, there is a growing need for effective interventions to improve adolescent HPV vaccine utilization. How providers communicate with families is one of the most influential factors in parents vaccination decisions. Emerging research is beginning to delineate potentially effective communication techniques such as presumptive approaches to making the vaccine recommendation, framing the vaccine as cancer preventing, and using motivational interviewing and personalized messaging when met with parental vaccine resistance. Moving forward the list of evidence-based interventions to improve providers HPV vaccine communication is likely to grow, and to increasingly leverage technology based solutions. However, given the complexities of the vaccination decision [136] and the ever growing spread of vaccine hesitancy [137], it is unlikely that a single intervention approach will be effective for getting adolescent HPV vaccine levels up to the national goal of 80% coverage. As has been recognized in the past, the most effective interventions for HPV vaccination in the future are likely to be multicomponent, including not only provider communication strategies but also clinic-, community-, and parent-level interventions [48]. Corresponding author: Amanda Dempsey, MD, PhD, MPH, East Montview Blvd, Suite 300, Aurora, CO 80045, amanda.dempsey@ucdenver.edu. Financial disclosures: None reported. REFERENCES 1. Centers for Disease Control and Prevention. Genital HPV infection - CDC fact sheet Accessed 26 Jun 2012 at 2. Markowitz LE, Dunne EF, Saraiya M, et al. Quadrivalent human papillomavirus vaccine: Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2007;56(RR-2): Viens LJ, Henley SJ, Watson M, et al. Human papillomavirusassociated cancers - United States, MMWR Morb Mortal Wkly Rep 2016;65: Daley EM, Vamos CA, Zimet GD, et al. The feminization of HPV: Reversing gender biases in US human papillomavirus vaccine policy. Am J Public Health 2016;106: Rettig EM, D Souza G. Epidemiology of head and neck cancer. Surg Oncol Clin North Am 2015;24: Louie KS, Mehanna H, Sasieni P. Trends in head and neck cancers in England from 1995 to 2011 and projections up to Oral Oncol 2015;51: Mehanna H, Beech T, Nicholson T, et al. Prevalence of human papillomavirus in oropharyngeal and nonoropharyngeal head and neck cancer--systematic review and meta-analysis of trends by time and region. Head Neck 2013;35: Chesson HW, Markowitz LE, Hariri S, et al. The impact and cost-effectiveness of nonavalent HPV vaccination in the United States: Estimates from a simplified transmission model. Hum Vaccin Immunother 2016;12: Insinga RP, Glass AG, Rush BB, et al. The health care costs of cervical human papillomavirus-related disease. Am J Obstet 130 JCOM March 2017 Vol. 24, No. 3

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