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Importance of a team approach to recommending the human papillomavirus vaccination

Holly B. Fontenot, PhD, RN, WHNP-BC (Associate Professor)1, Melanie L. Kornides, ScD, RN, FNP-BC (Research Fellow)2, Annie-Laurie McRee, DrPH (Assistant Professor)3, & Melissa B. Gilkey, PhD (Assistant Professor)4

ABSTRACT Background and purpose: Few studies have examined human papillomavirus (HPV) vaccine communication in the context of the health care team. Methods: In 2016, the investigators conducted a national, online survey of U.S. parents who reported having dis- cussed HPV vaccination with their adolescent’s health care team. Multivariable logistic regression assessed asso- ciations between HPV vaccine initiation ($1 dose) and having: 1) discussed HPV vaccination with multiple team members and 2) received congruent recommendations about HPV vaccination. Conclusions: Of the 795 parents in the sample, about half (52%) reported discussing HPV vaccination with multiple team members, including nurse practitioners, nurses, and physicians. Most reported receiving congruent recom- mendations for (76%) or against (12%) HPV vaccination; few (12%) received mixed recommendations. Parents who discussed HPV vaccination with multiple team members had greater odds of series initiation (odds ratio [OR] = 2.34, 95% CI: 1.61–3.40), whereas those who received mixed versus congruent recommendations for HPV vaccination had lower odds of vaccination (OR = 0.56, 95% CI: 0.33–0.95). Implications for practice: Findings suggest that a coordinated team approach to recommendations may encourage HPV vaccination. Nurse practitioners are well positioned to facilitate coordination efforts within their clinical practices. Keywords: Adolescent health; human papillomavirus infections/prevention and control; human papillomavirus vaccine.

Journal of the American Association of Nurse Practitioners 30 (2018) 368–372, © 2018 American Association of Nurse Practitioners

DOI# 10.1097/JXX.0000000000000064

Introduction Human papillomavirus (HPV) is the most common sexually transmitted infection in the United States (U.S.) and causes multiple cancers in men and women. Human papilloma- virus vaccine has been available for first-line prevention of HPV-related diseases for over a decade, yet HPV vaccina- tion coverage is not on target to meet national goals (U.S. Department of Health and Human Services, 2014). Cover- age is especially low for men, younger adolescents, and

those living in certain geographic areas (Reagan-Steiner et al., 2016). Research, primarily among physicians, has established health care providers’ communication as a key determinant of vaccination uptake; youth who do, versus do not, receive a recommendation for HPV vaccina- tion have 5 to 23 times the odds of being vaccinated (Bartlett & Peterson, 2011; Holman et al., 2014; Lau, Lin, & Flores, 2012; Rahman, Laz, McGrath, & Benson, 2014; Ylitalo, Lee, & Mehta, 2012). However, despite national guidelines for routine vaccination at ages 11 or 12 years (Reagan-Steiner et al., 2016), many physicians report that they do not strongly and consistently deliver HPV vaccine recommendations for their age-eligible patients (Daley et al., 2006; Gilkey, Malo, Shah, Hall, & Brewer, 2015; Gilkey et al., 2015; Lau et al., 2012; Malo et al., 2014; Vadaparampil et al., 2011, 2013, 2014).

Other health care team members, in addition to physicians, likely play an important role in recommending HPV vaccination, and yet to date, we have only a limited understanding of the role of nurse practitioners, nurses, and others or of how teams work together to counsel

1WF Connell School of Nursing, Boston College, Chestnut Hill, Massachusetts, 2Department of Population Medicine, Harvard Medical School & Harvard Pilgrim Health Care Institute, Boston, Massachusetts, 3Department of Pediatrics, University of Minnesota, Minneapolis, Minnesota, 4Department of Health Behavior, Universityof North Carolina Gillings School of Global Public Health, Chapel Hill, North Carolina Correspondence: HollyB. Fontenot, PhD, RN, WHNP-BC, WF Connell School of Nursing, Boston College, 140 Commonwealth Ave, Chestnut Hill, MA 02467. Tel: 617-552-1846; Fax: 617-552-0745; E-mail: [email protected] Received: 15 November 2017; revised: 30 March 2018; accepted 4 April 2018

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parents on this topic (Gilkey & McRee, 2016). In one recent study, over half of the physicians reported that at least one other health care team member, including a nurse prac- titioner, physician assistant, and/or nurse, discussed HPV vaccine or made the initial HPV vaccination recommen- dation (Malo et al., 2016). Little is known about how often parents speak with multiple health care team members about vaccination or whether all team members commu- nicate similar messages about HPV vaccination. Using data from a national sample of parents of adolescents, this study sought to assess the following: 1) the prevalence of discussing HPV vaccination with multiple providers on an adolescent’s health care team; 2) the prevalence of re- ceiving a congruent recommendation for HPV vaccination during the health care visit; and 3) associations between these factors and HPV vaccine initiation. By considering a team approach to vaccine communication, this study provides novel data about possible roles for nurses and nurse practitioners in HPV vaccination, which currently is underexplored in vaccine research.

Methods Participants and procedures The investigators conducted a cross-sectional, national survey of parents of adolescents (aged 11–17 years) in Sep- tember 2016. Participants were members of the Knowledge Panel, an online, nationally representative panel of 55,000 U.S. adults, maintained by the survey research company GfK for measurement of public opinion, attitudes, and behav- iors. The panel was constructed through list-assisted address-based sampling with phone call follow-ups for nonresponsive households (GfK, 2016). Panelists received points exchangeable for small cash payments from the company as an incentive for completing surveys. Eligible participants were those who reported ever having discussed HPV vaccine with one or more members of their adoles- cent’s health care team (n = 795). Electronic informed con- sent was obtained. The survey’s response rate was 59% using AAPOR Formula 4 (The American Association for Public Opinion Research, 2016). The Institutional Review Board of Harvard Pilgrim Health Care Institute approved the study protocol. Additional details are reported elsewhere (Kor- nides, McRee, & Gilkey, 2018).

Measures and analysis Demographics included information on parents (race/ ethnicity; educational attainment), adolescents (age at the time of first provider discussion about HPV vaccination; age at the time of survey; biologic sex), and households (annual income; geographic location). Age at the time of first dis- cussion was subtracted from age at the time of survey to calculate time since first discussion about HPV vaccine.

The survey assessed parents’ first experience talking with their adolescent’s health care team about HPV

vaccination. Parents reported if they discussed HPV vacci- nation with multiple members of the health care team (including physicians, nurse practitioners, physician assis- tants, nurses, and medical assistants). They also reported on the recommendation(s) received from the health care team. Responses were categorized to indicate whether parents received only recommendation(s) for HPV vacci- nation; only recommendation(s) against HPV vaccination; or recommendations both for and against HPV vaccination. The outcome measure was parents’ self-report of adoles- cents’ initiation of HPV vaccination ($1 dose).

Descriptive statistics were used to characterize the sample. A multivariable logistic regression model assessed associations between HPV vaccine initiation and: 1) discussion with multiple team members and 2) recommendation(s) received from the health care team. The model adjusted for the following demographic vari- ables associated with HPV vaccine initiation in bivariate analyses (p < .10): child age at the survey, time since first discussion about HPV vaccine, parent educational at- tainment, and parent race/ethnicity. Analyses were con- ducted using Stata 14.2 (College Station, TX), with statistical significance set at p < .05.

Results The total sample included 795 parents reporting from all regions of the U.S. (Table 1). Over one-third of the parents had a high school degree or less, and most were non- Hispanic whites (68%), Hispanic (19%), or non-Hispanic blacks (9%). Parents reported on similar proportions of adolescent children by sex (51% males) and age (mean: 14.2, SD 1.9). About two-thirds (69%) of the adolescents had initiated HPV vaccination at the time of the survey.

Human papillomavirus vaccine discussions About half of the parents (52%, n = 410) reported discus- sing HPV vaccination with more than one member of the adolescent’s health care team during their initial dis- cussion. Over three-quarters of the parents (76%, n = 606) reported receiving only recommendation(s) for HPV vac- cination from the health care team. Fewer reported re- ceiving only recommendation(s) against HPV vaccination (12%, n = 92) or reported receiving recommendations both for and against vaccination (12%, n = 97).

Associations with human papillomavirus vaccine initiation In the multivariable model, parents who spoke with multiple team members had 2.34 (p < .001; 95% CI: 1.61–3.40) times the adjusted odds of HPV vaccine initia- tion compared with parents who only spoke with one team member (Table 2). Parents who reported receiving only recommendation(s) against HPV vaccination or mixed recommendations (i.e., both for and against) had

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lower odds of HPV vaccine initiation (OR = 0.56 and OR = 0.44, respectively) as compared to parents who only re- ceived recommendation(s) for HPV vaccination.

Discussion and conclusion Discussion The importance of a physician’s recommendation has been established as a key determinant of HPV vaccine uptake, but to date, few studies have sought to con- textualize HPV vaccine communication within the broader health care team (Bartlett & Peterson, 2011;

Holman et al., 2014; Lau et al., 2012; Rahman, Laz, McGrath, & Berenson, 2014; Reagan-Steiner et al., 2015). In this national study, we found that parents who discussed HPV vaccination with more than one health care team member had greater odds of vaccinating their child as compared to parents who only discussed it with one team member. In this way, our findings suggest that communication with other members of the health care team (nurses, medical assistants, and others) may be important for amplifying recom- mendations delivered by the primary care provider (physician, nurse practitioner, or physician assistant). About half of the parents in our sample reported dis- cussing HPV vaccination with multiple health care team members. Although we were unable to differen- tiate by provider type, previous studies have found improved patient outcomes among primary care patients receiving care from multidisciplinary teams that included registered nurses (Fiscella, Mauksch, Bodenheimer, & Salas, 2017; Mundt, et al., 2016). Similarly, we believe that nurse practitioners are well positioned to lead future HPV vaccine communication initiatives that engage other providers and staff because of their advanced training in leadership, quality improvement, health delivery systems and practice-based inquiry improvement, and evidence- based practice (NONPF, 2017). Future research should explore this promising approach to improving coverage.

Similar to other studies (Gilkey & McRee, 2016; Gilkey, Malo, et al., 2015; Gilkey, Moss, et al., 2015; Malo et al., 2016), our findings suggest that improvement of HPV vaccine recommendations is needed to achieve Healthy People 2020 goals. In this national sample, nearly 1 in four parents of age-eligible children re- ceived a recommendation against vaccination from at least one team member. Previous research among health providers has noted barriers to HPV vaccine recommendation including the following: financial concerns, knowledge gaps, perceived parental con- cerns or negative attitudes toward vaccination, and preferences for vaccinating older and female adoles- cents (Holman et al, 2014). In addition, communication style and content may play a role in parental percep- tion of the recommendation received. Provider am- bivalence in vaccine recommendations, perception of parental hesitancy, and risk-based approaches to prescribing may all contribute to failure to provide strong and timely HPV vaccine recommendations (Henrikson, Tuzzio, Gilkey, & McRee, 2016; McRee, Gilkey, & Dempsey, 2014). Last, despite the low levels of incongruent recommendations for HPV vaccination (overall 12%), findings indicate that receiving these mixed messages from health care team members is po- tentially as detrimental to vaccine uptake as receiving only

Table 1. Sample characteristics (n = 795) n (%)

Child characteristics

Sex

Male 407 (51) Female 388 (49)

Age in years (mean, [SD]) 14.2 (1.9)

Time in years from first HPV vaccine discussion (mean, [SD])

2.1 (1.6)

HPV vaccine initiation ($1 dose)

No 245 (31) Yes 550 (69)

Parent characteristics

Educational attainment

High school degree or less 311 (39) Some college, no degree 192 (24) College degree or more 292 (37)

Race/ethnicity

Non-Hispanic white 538 (68) Non-Hispanic black 70 (9) Hispanic 150 (19) Other 37 (5)

Household characteristics

Annual income

<$35,000 156 (20) $35,000—$74,999 217 (27) $$75,000 422 (53)

Region in United States.

Northeast 152 (19) Midwest 196 (25) South 262 (33) West 185 (23)

Note: HPV = human papillomavirus.

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a recommendation against vaccination. This association further highlights the importance of interventions that engage the entire health care team.

This study is strengthened by a large national sample and the inclusion of novel questions about the influence of recommendations from multiple health care team mem- bers instead of physicians alone. Limitations include a cross-sectional design and parental report of commu- nication and adolescents’ HPV vaccination status. In ad- dition, the survey did not assess the role of different provider types and their communication styles. As a result, we are limited in our understanding of the specific influ- ences of nurse practitioners and nurses as compared to other types of health care providers. Future research should aim to identify the vaccine practices of these types of health care team members, as well as factors associated with their HPV vaccine communication and recommendations.

Conclusion and practice implications Understanding the larger context of parent communica- tion with multiple and diverse members of the health care team is important for increasing HPV vaccination coverage. Future research is needed to examine vaccine knowledge, beliefs, and communication behaviors of all members of the health care team including nurses and nurse practitioners. Having this foundational information is necessary to 1) ensure that all members give a con- gruent recommendation for HPV vaccination and 2) build effective vaccine communication interventions, consid- ering parent and patient experience with multiple health care team members.

Health care practices should examine system-, team-, and provider-level approaches to providing multiple positive HPV vaccine recommendations at the same visit and over time. Health care teams should consider clinical in-service trainings to ensure that all members of the team are educated about HPV and HPV vaccination, as well as understand the importance of building a comprehensive communication strategy that promotes multiple opportunities to provide HPV vac- cine recommendations to patients and families. Given their transdisciplinary training and perspective, nurse practitioners are well positioned to lead these efforts and affect change in HPV vaccination rates in their practices.

Competing interests: The authors report no conflicts of interest.

Funding: This study was supported by a Grant from the National Cancer Institute (K22 CA186979 for Melissa B. Gilkey and L40 CA220702 for Melanie L. Kornides).

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Table 2. Correlates of HPV vaccine initiation HPV Vaccine Initiation ($1 Dose)

n/N

Multivariable

% OR 95% CI

Discussed HPV vaccine with multiple members of the health care team

No 234/385 61 1 Yes 316/410 77 2.34 1.61–3.40*

Recommendation(s) received from the health care team

For HPV vaccination only 440/606 73 1 Against HPV vaccination only 45/92 49 0.44 0.27–0.72** Both for and against HPV vaccination 65/97 67 0.56 0.33–0.95***

Note: Model adjusted for child’s age, time (years) from first discussion, parent’s educational attainment, parent’s race/ethnicity. CI = confidence interval; HPV = human

papillomavirus; OR = odds ratio.

*p < .001.

**p < .01.

***p < .05.

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