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Review

Provider communication about HPV vaccination: A systematic review

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Pages 1454-1468 | Received 26 Oct 2015, Accepted 03 Dec 2015, Published online: 08 Apr 2016

abstract

Background. Improving HPV vaccination coverage in the US will require healthcare providers to recommend the vaccine more effectively. To inform quality improvement efforts, we systematically reviewed studies of provider communication about HPV vaccination. Methods. We searched MEDLINE, CINAHL, EMBASE, and POPLINE in August 2015 to identify studies of provider communication about HPV vaccination. Results. We identified 101 qualitative and quantitative studies. Providers less often recommended HPV vaccine if they were uncomfortable discussing sex, perceived parents as hesitant, or believed patients to be low risk. Patients less often received recommendations if they were younger, male, or from racial/ethnic minorities. Despite parents' preference for unambiguous recommendations, providers often sent mixed messages by failing to endorse HPV vaccine strongly, differentiating it from other vaccines, and presenting it as an “optional” vaccine that could be delayed. Conclusion. Interventions are needed to help providers deliver effective recommendations in the complex communication environment surrounding HPV vaccination.

Introduction

Improving the delivery of human papillomavirus (HPV) vaccine is a public health priority in the United States.Citation1,2 Despite national guidelines for the routine administration of HPV vaccine to 11- and 12-year-old adolescents, only 40% of girls and 22% of boys completed the 3-dose series in 2014.Citation3 These persistently low levels of coverage have prompted a rapid growth in the research literature on determinants of HPV vaccination, and this work has consistently highlighted the powerful influence of healthcare providers' communication. Adolescents who receive a provider's recommendation have substantially higher odds of initiating HPV vaccination compared to those who do not.Citation4-7 However, around half of age-eligible adolescents do not receive recommendations.Citation8-10 Furthermore, a growing body of research suggests that those recommendation adolescents do receive are weaker than recommendations for other adolescent vaccines, such as tetanus, diphtheria, and acellular pertussis (Tdap) and meningococcal vaccines.Citation11,12 Understanding and improving provider communication, particularly with regard to recommendations, is imperative to increasing HPV vaccination coverage.

To inform quality improvement efforts in this area, we systematically reviewed the literature on provider communication about HPV vaccination. We organized our review using the classic communication constructs of source (where a message originates), audience (the receiver), message (what is communicated), channel (the medium used to convey the message), and context (where and when communication occurs).Citation13,14 With regard to source and audience, our aims were to understand which providers are preferred sources of information, identify factors associated with the delivery and receipt of recommendations, and characterize the communication roles played by patients and parents in clinical decision making. We additionally sought to assess provider communication about HPV vaccination in terms of message content and style, as well as channels used to educate about HPV vaccination in clinical settings. Finally, we aimed to describe the context of HPV vaccine communication to understand how policy environments, clinical systems, and health communication interventions facilitate or constrain communication.

Methods

We searched four databases (MEDLINE, CINAHL, EMBASE, and POPLINE) in August 2015 to identify studies related to provider communication about HPV vaccination. Searches varied by database, but all used combinations of terms related to HPV, vaccination, and communication. For example, we conducted a search of MEDLINE using the following terms: (“Papillomavirus Vaccines”[mesh] OR ((hpv[tiab] OR papilloma[tiab] OR papillomavirus[tiab]) AND (vaccin*[tiab] OR immuniz*[tiab])) OR gardasil[tiab]) AND (“Health Communication”[mesh] OR “Physician-Patient Relations”[Mesh] OR communicat*[tiab] OR recommend*[tiab] OR deci*[tiab]). We identified additional studies by soliciting in-press and unpublished papers from research groups publishing in this area and by checking reference lists of papers included in our review.

We reviewed studies for inclusion using a two-step process. First, one author (MBG) reviewed paper titles and abstracts to identify relevant studies, and another (ALM) checked these determinations. Second, we conducted full-text reviews of identified studies. In this step, one author (MBG or ALM) further assessed each study's eligibility and coded eligible studies using an abstraction form. The other author checked the data. For each step, authors resolved questions and disagreements in coding through discussion.

Eligible studies were those that used data from a US sample to report quantitative or qualitative findings related to provider communication about HPV vaccination. We defined “provider communication” to include in-person dialog among patients, parents, and providers as well as the use of educational materials or other communication interventions in a clinical setting. For the purposes of this study, “clinical settings” included primary care practices or clinics, school-based health clinics, public health department clinics that deliver vaccines, and pharmacies. We limited our review to studies with US samples to account for the unique practice and policy environments that influence HPV vaccination in this country. Excluded studies were those that reported on: only the association between receiving a provider recommendation and HPV vaccine uptake; message framing without an explicitly stated clinical context; communication in settings, such as dental offices, that do not stock HPV vaccine; reminder/recall interventions; or quality improvement interventions that did not evaluate changes in provider communication.

Results

The search yielded 2,175 unduplicated articles, 101 of which met eligibility criteria and were included in our review (, ). Most studies (67%) were quantitative, primarily using cross-sectional survey designs. About one-third (33%) of included studies used qualitative or mixed methods. Only one study examined recorded dialog among providers, patients, and parents. A majority of studies were conducted with either health care providers (53%) or with parents (42%); about one-quarter included adolescents or young adults (25%). Most studies focused on communication about HPV vaccination for only adolescent girls (53%) with fewer focusing on either boys specifically (11%) or on both boys and girls (36%).

Figure 1. Flow diagram of included and excluded articles.

Figure 1. Flow diagram of included and excluded articles.

Table 1. Characteristics of included studies.

Source

Preferences in communication source by provider type

Studies that compared sources of HPV vaccine communication found a preference for talking with physicians versus other providers.Citation15-17 For example, far more parents viewed physicians than nurses as helpful for making decisions about HPV vaccination.Citation16 Similarly, only about one-third of young adults were comfortable getting HPV vaccine from a nurse or medical assistant without first talking with a doctor.Citation15 Qualitative studies suggested that these communication preferences were based on the perception that physicians were most knowledgeable about vaccines as well as patients' social and medical histories.Citation17-20 However, two studies indicated that preferences for talking with a physician about HPV vaccination lessened after initial discussions; respondents were more open to communicating with other providers or office staff for follow-up.Citation15,21 The extent to which parent and patient preferences are currently being met is unknown; however, one recent study found that about half of physicians in a national sample did not make the initial HPV vaccine recommendation for patients in their practice, but rather relied on a nurse practitioner, medical assistant, or other provider to do so.Citation22

Variation in recommendations by provider factors

Studies of variation in HPV vaccine recommendations by provider factors focused on providers' knowledge, perceptions, and professional characteristics. Evidence on whether HPV-related knowledge influenced providers' communication about HPV vaccination was mixed, but suggested a modest association overall. Several quantitative studies found that knowledge was associated with recommendation intention and behavior.Citation23-26 Qualitative studies further supported the hypothesis that knowledge informed provider communication, with incomplete knowledge of HPV-attributable cancers in males identified as a key barrier to HPV vaccine recommendations for boys.Citation27,28 However, other studies found no association between providers' knowledge and their HPV vaccine recommendations.Citation29-31

Studies assessed a wide range of provider perceptions and their relationship to HPV vaccine recommendations, with the most important perceptions being those related to discomfort talking about sex, parental hesitancy, and the role of professional organizations. Discomfort talking about sex or sexually transmitted infections was associated with providing less frequent and lower-quality HPV vaccine recommendations,Citation27,32-34 as was believing that talking about sex was a prerequisite to HPV vaccination.Citation29,35,36 Perceptions of parental hesitancy toward HPV vaccination were also negatively associated with communication; providers who perceived parents as unsupportive less often recommended or intended to recommend HPV vaccine.Citation12,29,33,35,37-39 Conversely, providers who perceived professional organizations as influential more often recommended or intended to recommend the vaccine.Citation23-25,37,40-43

Other frequently studied perceptions included those related to providers' confidence in HPV vaccine and their own abilities to discuss it. For example, providers who perceived high HPV vaccine efficacy consistently reported more positive recommendation intentions and behaviors.Citation29,32,37,44,45 In contrast, no studies found a correlation between providers' perceptions of HPV vaccine safety and their recommendation behaviors, perhaps because concerns about safety were relatively uncommon.Citation27,32,36,38,44,45 In terms of providers' perceptions of themselves, self-efficacy to communicate about HPV vaccine was associated with recommending and intending to recommend the vaccine.Citation12,26,46 Interestingly, providers who viewed themselves as “early adopters” were also more likely to recommend HPV vaccine.Citation30,45,47

Studies assessing the relationship between provider characteristics and HPV vaccine recommendations most often focused on clinical specialty and demographics. Most studies found that pediatricians reported more positive HPV vaccine recommendation practices than family physiciansCitation9,11,12,30,33,48-51 or other types of providers.Citation12,32 Other studies failed to find variation in recommendations by specialty,Citation23,34-36,40,52,53 but several of these studies did not include pediatricians.Citation34,52,53 Most studies did not find variation in HPV vaccine recommendations by provider sex,Citation9,23,30,36,39,44,47-49,54 but those that did most often favored female providers.Citation24,25,29,33,53 Similarly, most studies did not find variation in HPV vaccine recommendations by provider age or years in practice,Citation30,33,36,47,49 although a few did with mixed results.Citation9,24,50 Studies assessing provider race/ethnicity suggested that minority status was associated with recommending HPV vaccine.Citation9,30,32,34

Studies of clinic or practice-level characteristics focused on the composition of patient populations in terms of race/ethnicity, insurance type, and geographic location. Providers who served a higher proportion of Hispanic patients reported more often recommending or intending to recommend HPV vaccine for boys,Citation23,30 but not girls.Citation23,32 In contrast, one study reported a negative association between seeing a higher proportion of non-Hispanic Black patients and recommending HPV vaccine.Citation32 Studies of providers with higher participation in Medicaid or the Vaccines for Children program found that this participation was associated with more positive HPV vaccine recommendation practicesCitation9,23,30,33-35 or no effect.Citation29,44,48 Provider recommendations did not vary substantially by national region,Citation30,33-35,39,44 but providers practicing in urban areas more often reported recommending HPV vaccine than those in rural or suburban ones.Citation34,37,44,46

Audience

Variation in recommendations by patient factors

Studies assessing patient factors associated with receiving an HPV vaccine recommendation most often examined patient demographics and providers' perceptions of patients' risk of HPV infection. A consistent finding for adolescent patients was that providers' recommendation intentions and behavior improved with patient age, such that recommendations were stronger and more frequent for older adolescents than for those in the target age range of 11–12 years old.Citation9,22-25,27,29,33,35,37,38,40,42,44,51-53,55-60 Relatively few providers recommended or intended to recommend HPV vaccination for younger patients, ages 9 and 10.Citation22,23,27,35,40,51,59 These recommendation practices corresponded with the preferences of parents, who tended to favor communicating with providers about HPV vaccination in their adolescents' teenage vs. preteen years.Citation16,19,61 Among studies focusing on young adult patients, provider recommendations declined slightly in frequency for patients in their twenties.Citation35,41,56,62 Two studies suggested that a minority of providers continued to recommend HPV vaccine for older adults, ages 27 and over, who fell outside of the recommended age range for catch up vaccination.Citation52,63

Provider communication was consistently associated with patients' sex such that providers' recommendation intentions and behavior were more supportive of HPV vaccination for girls versus boys.Citation10,12,24,25,29,33,37,44,55,57,58,60,64,65 For example, the 2014 NIS-Teen found that 64% of age-eligible girls had received a provider recommendation compared to just 42% of boys.Citation10 All but one study examining patients' race/ethnicity suggested disparities in provider communication with parents of African American and Hispanic adolescents less often discussing HPV vaccine with a provider or receiving HPV recommendations than parents of non-Hispanic White adolescents.Citation7,64,66-70 This pattern of findings is concerning given that both quantitative and qualitative studies suggested that provider recommendations were especially influential among parents from racial/ethnic minority backgrounds.Citation19,69,71-73

Providers more often recommended HPV vaccination for patients they perceived to be at higher risk for HPV infection. Studies found that providers prioritized HPV vaccination for subpopulations including sexually active adolescents, males who might have same sex partners, and adolescents of lower socioeconomic status.Citation19,33,38,44,74 Similarly, some providers based their HPV vaccine recommendations on risk-related factors such as the results of a Pap or HPV test, number of sexual partners, or relationship status.Citation52,58,75 Ironically, providers in one qualitative study acknowledged that their ability to accurately assess whether adolescents were sexually active was limited.Citation38

Communication roles

Studies of parents' and adolescents' communication roles in clinical settings consistently found that a parent, most often the mother, was responsible for making the ultimate decision about HPV vaccination.Citation4,18-20,71,74,76-78 However, the extent to which parents communicated about HPV vaccination beyond giving consent varied, with qualitative studies suggesting that parents from racial/ethnic minorities or with lower socioeconomic status were less likely to be engaged by providers and more likely than parents from more socially privileged backgrounds to defer to providers' advice.Citation19,71,73,74,77 Parents were also more likely to follow providers' advice without question when they received a strong, unambiguous recommendation.Citation38,74,77

Findings on adolescents' role in clinical communication about HPV vaccination were also mixed. Some studies emphasized their lack of participation, particularly in the case of younger adolescents.Citation4,19,74,78,79 Indeed, some parents indicated a preference for vaccinating in the preteen years specifically because they viewed adolescents as having little say during this time.Citation18,80 In contrast, other studies found that adolescents did play a role in communication and decision-making in clinical settings, one which increased with age, maturity, and social privilege.Citation18,27,71,73,76,80 For some parents, the desire to maximize adolescents' role was even a reason for delaying HPV vaccination.Citation80 Studies suggested that parent-adolescent decisions were largely concordant and that most dyads ultimately reached agreement about the vaccination decision, but they sometimes looked to providers for guidance in the case of initial disagreement.Citation76,81 Interestingly, one qualitative study noted that adolescents' participation in medical dialog was often subtle and included non-verbal forms of communication such as nods, suggesting that adolescents' communication role could be easy to overlook.Citation76

Message

Content

Studies of the preferred and actual content of provider communication about HPV vaccination focused on prevention topics, vaccine safety, and vaccination logistics. Of these, content related to prevention featured most prominently, with parents and adolescents most often wanting providers to discuss the specific diseases HPV vaccine prevents and its efficacy.Citation18,21,82,83 In correspondence with preferred content, prevention of cancer, genital warts, and sexually transmitted infections (STIs) constituted the major topics of actual HPV vaccine communication. Almost all providers reported mentioning cancer prevention when they discussed HPV vaccination.Citation33,59 However, studies of girls suggested that providers placed a higher priority on cancer prevention Citation17,29,35,38,40,81 than studies of boys.Citation22,27,29,40,76 For girls, discussions centered on cervical cancer prevention, and included genital warts and STIs less often.Citation35,38,40,79,81 For boys, prevention topics were more varied with the prevention of genital warts and STIs featuring as or more prominently than the prevention of cancer;Citation22,27,29,76 cancer topics included cervical cancer prevention for future partners and, less frequently, the prevention of male cancers in patients themselves.Citation22,27,29,40,76 Several qualitative studies found that some providers chose to discuss cancer, but not genital warts or STIs, so as to avoid talking about sex;Citation27,59 however, a quantitative study found that, for boys, very few providers discussed one without the other.Citation22 Although two studies sought to assess the association between the prevention content and HPV vaccine acceptance, results were inconclusive.Citation60,84

Content about safety and side effects featured somewhat less prominently in studies of provider communication about HPV vaccination. Qualitative studies suggested that some parents and adolescents prioritized safety and side effects as important topics for discussion,Citation19,21,38,61,82 but studies of actual content suggested that such communication was fairly limited.Citation27,79,82 For example, one qualitative study of parents and their adolescent sons found that most recalled that their providers had told them HPV vaccination was generally safe, but few reported receiving information or asking questions about specific side effects.Citation76

Topics related to provider communication about the logistics of HPV vaccination were varied. Parents reported a preference for being informed of: the number of doses needed to complete the vaccine series; the vaccine's availability for boys; cost; and the recommended timing of administration.Citation21 With regard to timing, some parents expressed a particular interest in the rationale for vaccinating adolescents in their preteen years vs. later.Citation18,21,38 In contrast to these preferences, several studies indicated deficiencies in provider communication about how to complete the 3 dose series.Citation27,76,81,85 Fewer studies assessed actual content in terms of the availability of HPV vaccine for boys, cost, and timing.Citation22,76

Style

Studies of communication style focused on four areas: 1) recommendation strength; 2) recommendation quality; 3) the framing of HPV vaccine in relation to other adolescent vaccines; and 4) collaborative communication. First, with regard to recommendation strength, quantitative studies consistently found an association between the extent to which providers endorsed the importance of HPV vaccine and parents' positive perceptions of HPV vaccine,Citation60,86 their intention to get their children vaccinated,Citation60,87 and adolescents' receipt of HPV vaccine.Citation60,87-89 Qualitative studies also found strong provider endorsement to be uniquely influential on parents' HPV vaccination decisions.Citation27,38,74,77 Unfortunately, these same studies suggested that providers often failed to strongly endorse HPV vaccine.Citation11,27,38,44,47,60,86,87,89,90 For example, one national study found that only about two-thirds of parents who received HPV vaccine recommendations perceived a high level of provider endorsement.Citation60

Building on the notion of recommendation strength, a second series of studies found that recommendation quality, or the extent to which providers delivered guideline-consistent recommendations, was also associated with HPV vaccination. In addition to strength of endorsement, these studies assessed the quality indicators of timeliness (i.e., routinely recommending HPV vaccine by age 12 versus later), consistency (using a routine versus risk-based approach to recommendations), and urgency (recommending same-day vaccination). A national study of primary care physicians found that half reported 2 or more lower-quality recommendation practices.Citation33 A corresponding survey of parents found that those who received high- versus low-quality recommendations had more often initiated HPV vaccination for their adolescents and had less often refused or delayed the vaccine.Citation60

A third area of communication style centered on understanding how providers communicated about HPV vaccine in relation to other vaccines; qualitative studies identified two main approaches in this regard. In one, providers framed HPV vaccine as one of several vaccines in the routine schedule, avoided drawing special attention to it, and offered their strong endorsement.Citation38,74 Providers using this approach reported low levels of parental hesitancy and high levels of vaccine uptake.Citation38,74 In the other approach, providers distinguished HPV vaccine from other adolescent vaccines by presenting it as an “optional” vaccine which was not required for school; this approach often involved a more lengthy discussion of risks and benefits as well as obtaining parental consent separately from, not along with, other vaccines.Citation38,74,77,79,91 Providers using the second approach reported higher levels of parental hesitancy and vaccine refusal or delay, but nevertheless felt obligated to mention the absence of school entry requirements for HPV vaccine and offer the option to delay vaccination in order to more closely coincide with sexual debut.Citation38,74 Providers who presented HPV vaccine as optional expressed the hope that this open-ended communication style would foster trust with vaccine hesitant parents, thereby encouraging the acceptance of other adolescent vaccines in the short term as well as HPV vaccine in the long term.Citation38 Unfortunately, some parents who delayed HPV vaccination with the intention of getting it later reported that they never followed-up to do so.Citation38,91

The extent to which providers adhere to these overall approaches of aligning HPV vaccine with or distinguishing it from other vaccines is unknown. However, the existing literature consistently supported the assertion that providers often communicated about HPV vaccine differently from other vaccines in discrete ways. Quantitative and qualitative studies found that providers spent longer talking about HPV vaccine than other vaccines,Citation11,27,35,74,76,84 endorsed HPV vaccine less strongly than Tdap and meningococcal vaccines,Citation11,12,22,74,87 and often presented HPV vaccine as an “optional” vaccine vs. one that was “routine” or “required.”Citation12,22,38,74,79,91 Finally, one study found that, among providers with a preferred order for discussing adolescent vaccines, over two-third preferred to discuss HPV vaccine last.Citation11

A fourth area of communication style considered the extent to which providers engaged parents and patients in discussion about HPV vaccination. For example, one series of quantitative studies assessed “collaborative” communication based on parental reports of whether they discussed HPV vaccination with a provider, whether they received enough time to make a decision, and whether providers played a role in decision making. These studies found that collaborative communication was associated with HPV vaccine uptake.Citation92 However, traditionally underserved groups, such as parents of Hispanic and non-privately insured adolescents, were less likely to report collaborative communication, which adversely affected HPV vaccination coverage for these groups.Citation93 Qualitative research generally supported the finding that providers were less likely to engage non-English speaking parents or parents from disadvantaged backgrounds in HPV vaccine-related communication.Citation73,76 Subgroup differences aside, a quantitative analysis of transcribed medical encounters found that providers were verbally dominant in discussions about HPV vaccination, speaking over three-quarters of the words spoken, taking longer turns than parents, and using on average more than 11 technical terms per visit.Citation79 All studies that assessed who initiated HPV vaccine conversations found in favor of providers; parents and patients brought up the topic only rarely and preferred that providers initiate the discussion.Citation76,77,79,87,91,94-97

Decisional timeframe

Both qualitative and quantitative studies found that parents often preferred not to make an immediate decision about HPV vaccination during discussions with a provider, but rather wished to decide later after thinking more about the issue and getting more information.Citation12,16,18,73,74,79,80 Studies suggested that providers may contribute to extending the timeframe for HPV vaccination decision making, given that many gave parents a choice about when to vaccinate or, even at times, actively suggested delay.Citation33,38,60,74,77,91 For example, a national survey of physicians found that only about half usually recommended same-day vaccination for 11- and 12-year-old patients.Citation33

Satisfaction

No studies examined parents' and patients' satisfaction with provider communication about HPV as a primary focus; however, a few reported on certain aspects of parent satisfaction, such as receiving adequate time and informational support. For example, most parents participating in the 2010 NIS-Teen reported that their daughters' providers did give them enough time to discuss HPV vaccine; however, this perception was less common among parents of unvaccinated versus vaccinated daughters.Citation4 One small study found that most parents who discussed HPV vaccination with a provider reported receiving adequate information on prevention topics.Citation84 In contrast, qualitative studies with parents from racial/ethnic minority backgrounds suggested some degree of dissatisfaction with HPV vaccine communication, with some parents reporting too little information, limited opportunities to ask questions, or ambiguous recommendations.Citation61,71,77,78,98,99 For these parents, the perception that providers were withholding information was a source of confusion that introduced doubt about the value of HPV vaccination, discouraged vaccine acceptance, and in some cases undercut parents' trust in providers.Citation61,71,77,78,98,99 Parents emphasized their desire for clear, unambiguous messages from providers about the importance of HPV vaccination.Citation38,71,77,99

Channel

Relatively few studies assessed modes of clinical communication about HPV vaccination beyond provider dialog, but those that did focused primarily on written materials. Written brochures and fact sheets, such as the CDC's Vaccine Information Sheet,Citation12,87,100-103 and postersCitation87,100 were commonly used in traditional primary care settings to support provider communication about HPV vaccination. In studies examining preferred materials, both parents and providers favored brief written materials,Citation12,16,87,94,100,101,103 with parents additionally expressing interest in websites.Citation87,103 Parents and providers across several studies voiced the need for educational materials that were tailored to parents' cultural background, language preference, and literacy level.Citation12,43,94,99,101,104 Given concerns about literacy, some providers suggested video as a promising educational channel,Citation43,94 but only a minority of parents viewed informational videos as helpful.Citation16 Notably, no studies examined educational materials designed specifically for adolescent patients themselves.

Context

Visit type

Studies assessing visit type found that almost all providers who discussed HPV vaccination used well-child visits to do so, whereas only about three-quarters used school physicals, and about half used camp or sports physicals.Citation17,22 Fewer providers reported discussing HPV vaccine during visits for acute care, even when patients' complaints were mild.Citation11,22,41,63,105 Providers perceived communicating about HPV vaccination to be difficult in the context of acute care, with concerns including the lack of time or fear that parents might blame the vaccine if the child's illness worsened.Citation11,59 Despite avoiding HPV vaccine communication during acute care visits, some providers acknowledged that such visits were sometimes their only contact with adolescents, particularly older adolescents who they perceived as less likely to make well-child visits.Citation59,73,85

Barriers to communication

Studies assessing barriers to provider communication about HPV vaccination considered both policy- and clinic-level factors. Although providers reported being highly motivated to follow practice guidelines, many perceived guidelines for HPV vaccine administration to be complex and unclear; indeed, providers with this perception recommended HPV vaccination less often.Citation27,34,59,106 Providers also perceived the lack of school entry requirements for HPV vaccination as a barrier to making strong recommendations because of the implicit assertion that HPV vaccine was less important than Tdap and other recommended vaccines.Citation9,11,41,63,74 Other studies suggested that policies requiring parental consent prior to HPV vaccine administration to minors may be a barrier to direct communication with adolescents.Citation107,108

In terms of barriers related to the clinical environment, studies most often identified deficiencies in scheduling as limiting provider communication about HPV vaccination. Providers identified patient reminder/recall as critical to their efforts to recommend HPV vaccination, but many reported that they did not use these systems, and instead relied on patients to initiate scheduling.Citation11,43,59,85,94 Finally, providers reported that time constraints in the clinical encounter were also a barrier to HPV vaccine communication.Citation9,11,12,35,41,45,59,63

Interventions to improve communication

Only two studies evaluated the impact of interventions on providers' HPV vaccine communication. One study tested a multi-component, clinic-based intervention that included provider education and provider alerts in patients' electronic medical records; parents of adolescent patients who attended intervention clinics were more likely to discuss HPV vaccination with a provider, but were no more likely to receive a strong recommendation.Citation109 A second study evaluated a social marketing campaign that included public service announcements and the provision of clinic-based educational materials to parents of adolescents; most providers who participated reported that the campaign made them more likely to discuss and recommend HPV vaccination.Citation100

Discussion

Findings from this systematic review of over 100 quantitative and qualitative studies suggest that healthcare providers face a highly complex communication environment when discussing HPV vaccination in clinical settings. First, the audience for clinical communication is not uniform; studies noted that patients could present with or without their parents and that expectations about the communication roles accorded to each of these parties shifted with patients' age and maturity, as well as with parents' preferences.Citation18,27,71,73,76,80 In addition to age, patients' sex added complexity to communication, with providers offering different prevention messages to boys and girls.Citation17,22,27,29,35,38,40,76,81 Second, at the interpersonal level, many providers perceived parents as being unsupportive of HPV vaccination, a view which hindered guideline-consistent delivery of recommendations.Citation12,29,33,35,37-39 Third, studies consistently documented a challenging policy context, including unclear practice guidelines and a lack of school entry requirements for HPV vaccination.Citation11,27,34,59,74 Finally, participants across several studies perceived clinical systems as unconducive to communication due to factors such as time constraints and deficiencies in reminder/recall systems.Citation11,43,59,85,94 In these ways, an audience with dynamic communication needs came together with unsupportive interpersonal, policy, and clinical contexts to create challenges for effective HPV vaccine communication.

Given these complexities, it is perhaps not surprising that the research literature documented shortcomings in provider communication about HPV vaccination. Communication practices such as describing HPV vaccine as “optional,” differentiating it from other adolescent vaccines, failing to endorse it strongly, and recommending delayed vs. same-day vaccinationCitation33,38,60,75 were common and likely compromised providers' ability to deliver HPV vaccine according to national guidelines. Although some providers expressed the hope that merely offering, rather than strongly endorsing, HPV vaccine would honor parents' preferences and earn their trust,Citation38 the findings of this review suggest that this view is likely misguided. Rather, qualitative research suggests that parents found open-ended communication ambiguous, frustrating and worrying, leading them to delay HPV vaccination for their adolescents.Citation61,71,77,78,98,99 Instead of encouraging shared decision making, mixed messages appeared to lead to a “default” communication style in which neither providers nor parents engaged in the decision-making process.Citation110

Findings also provide evidence of communication disparities in terms of who receives a provider recommendation for HPV vaccination. More specifically, parents of younger adolescents, males, and adolescents from racial and ethnic minorities less often received recommendations. This pattern of findings is concerning given that HPV vaccination is more effective when administered to preteens versus older adolescents and may be especially beneficial for traditionally underserved populations who experience a disproportionate burden of cervical cancer later in life.Citation111 Although HPV vaccination coverage among adolescents from racial and ethnic minorities tends to be on par with or higher than coverage for non-Hispanic Whites, eliminating communication disparities could raise coverage for these high priority populations even higher. Studies also indicate that many providers used risk-based approaches to recommending HPV vaccine, prioritizing the vaccine for adolescents they perceived as likely to be sexually active.Citation33,52,74,75 Such risk-based strategies have been shown to be ineffective given the extremely high prevalence of HPV infection and the difficulty of accurately predicting adolescents' sexual debut.Citation112

In terms of implications for clinical practice, this review highlights several promising approaches for communicating about HPV vaccination (). More specifically, quality improvement efforts aimed at strengthening provider communication about HPV vaccination should emphasize the need to say HPV vaccination is important, recommend same-day vaccination, and deliver routine recommendations to all 11- and 12-year-old patients.Citation38,74 Other promising strategies include emphasizing cancer prevention benefits and discussing HPV vaccine at the same time and in the same way as other recommended adolescent vaccines.

Table 2. Promising practices for recommending HPV vaccination in clinical settings.

This review suggests opportunities for additional research, particularly in the areas of communication source and audience, by raising questions about the relative roles of parents, patients, and providers in HPV vaccine communication. The extent to which parents wish to engage in communication about HPV vaccination—or the impact of their engagement on their HPV vaccination decisions—is largely unknown and warrants further study. In the case of patients, the findings of this review suggests that the communication role of adolescents is under-represented in the research literature, particularly given that several studies found that adolescents can have a positive influence on HPV vaccine decision making.Citation4,76 In the case of providers, this review found that, although parents preferred to communicate with physicians, other providers, including nurse practitioners and medical assistants, were often responsible for delivering recommendations. Given this discordance, more research is needed to understand what impact the source of HPV vaccine recommendations has on uptake and how to delegate communication roles among the care team to maximize efficiency.

It is noteworthy that our search identified only two studies that sought to measure the impact of interventions on provider communication about HPV vaccination.Citation100,109 Additional intervention research is urgently needed to evaluate approaches for supporting effective provider communication and to prospectively evaluate the impact of those interventions on HPV vaccine uptake. Message testing to understand the impact of providers' communication content on parents' HPV vaccine decision making and satisfaction could be especially useful. Although the broader literature on message framing has yield mixed results as to the benefits of gain- versus loss-framed messages,Citation113-115 other areas of potential importance include the relative influence of different prevention messages in terms of disease types and number of diseases,Citation116-118 the length or amount of content delivered, and cognitive versus affective approaches to conveying HPV vaccine-related information.

Strengths of this systematic review include the use of two coders and a standardized form to perform data abstraction across databases in multiple fields of study. Limitations include this review's reliance on studies that most often used relatively weak, cross-sectional designs, convenience samples, and self-reported measures of providers' recommendation behavior and adolescents' vaccination status. Although our narrative analytic approach was well-suited to the aims of this study and the variable quality of the available evidence, future studies should seek to use rigorous study designs to assess the impact of specific communication practices, such as the delivery of provider recommendations, on HPV vaccine uptake. Finally, we acknowledge that this review is limited in its primary focus on provider dialog; related literatures in other areas such as the use of reminder/recall and message faming are also relevant to understanding clinical communication about HPV vaccination.

Conclusion

Improving provider communication is one of the most highly prioritized goals in the national movement to increase HPV vaccination coverage.Citation2 This review identifies promising communication practices, such as strongly endorsing HPV vaccine and using routine approaches to delivering recommendations, that can inform quality improvement efforts and potentially reduce communication disparities that currently limit HPV vaccine recommendations for younger adolescents, males, and racial/ethnic minorities. At the same time, this review suggests that providers face substantial barriers to communicating about HPV vaccination due to challenging interpersonal, clinical, and policy contexts. Interventions are needed to support providers in recommending HPV vaccination effectively and efficiently in the highly complex communication environment surrounding HPV vaccination.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Acknowledgments

The authors wish to thank Jane Carpenter for providing administrative support.

Funding

This study was supported by a career development award from the National Cancer Institute (K22 CA186979). The funder did not play a role in study design, data analysis, report writing, or the decision to submit the article for publication.

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