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Providers’ time spent and tools used when discussing the HPV vaccine with parents of adolescents
Vaccine 34 (2016) 6217–6222
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
Providers’ time spent and tools used when discussing the HPV vaccine with parents of adolescents Amanda F. Dempsey ⇑, Steven Lockhart, Elizabeth J. Campagna, Jennifer Pyrzanowski, Juliana Barnard, Sean T . O’ Leary Adult and Child Consortium for Outcomes Research and Dissemination Science Program, Children’s Hospital Colorado and University of Colorado, 13199 East Montview Blvd, Suite 300, Aurora, CO 80045, United States
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Article history: Received 28 July 2016 Received in revised form 21 October 2016 Accepted 28 October 2016 Available online 10 November 2016 Keywords: Human papillomavirus Vaccine delivery Communication
a b s t r a c t Objectives: Little is known about HPV vaccine communication tools currently used by primary care providers of adolescents, or how such tools impact the quality of HPV vaccine recommendations, which some have defined as using a ‘‘presumptive” communication style, continuing to offer vaccines despite resistance, and strongly recommending vaccines at the appropriate ages. We surveyed primary care providers to assess their current use of HPV vaccine communication tools, and how these related to their HPV vaccine recommendation quality. Study Design: Cross sectional survey of 183 pediatrics and family medicine primary care providers in the Denver metro area. Results: Response rate was 82% (n = 150). Most (59%) providers used a presumptive vaccine recommendation >75% of the time, and 76% reported continuing to offer the HPV vaccine even after parent refusal. However, less than two-thirds of providers ‘‘strongly” recommended the vaccine to 11–12 year olds (60% for females, 55% for males, p = 0.02). The HPV vaccine information sheet from the Centers from Disease Control and Prevention was the most frequently used communication tool during clinical visits (64% used at least 75% of the time) and directing parents to preferred websites was the most frequently used between-visit communication tool (21% used >50% of visits). Use of tools was not associated with any measure of HPV vaccine recommendation quality but was associated with longer HPV vaccine discussion times. Conclusions: Providers use only limited types of adolescent HPV vaccine communication tools, and frequently do not use preferred vaccine communication strategies. Better engagement with existing HPV vaccine communication tools, and/or the creation of new tools may be needed to enhance providers’ ability to provide high quality HPV vaccine recommendations. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction Compared to the tetanus-diphtheria-acellular pertussis (Tdap) and meningococcal (MCV) vaccines, utilization of the human papilAbbreviations: HPV, human papillomavirus; Tdap, Tetanus-diphtheria-acellular pertussis vaccine; CDC, Centers for Disease Control and Prevention; MD, medical doctor; DO, doctor of osteopathy; NP, nurse practitioner; PA, physician’s assistant; COMIRB, Colorado Multi-Institutional Review Board. ⇑ Corresponding author at: Adult and Child Consortium for Outcomes Research and Dissemination Science (ACCORDS) Program, Children’s Hospital Colorado and University of Colorado, Anschutz Medical Campus, 13199 East Montview Blvd, Suite 300, Aurora, CO 80045, United States. E-mail addresses: [email protected] (A.F. Dempsey), Steven. [email protected] (S. Lockhart), [email protected] (E.J. Campagna), [email protected] (J. Pyrzanowski), Juliana.barnard@ ucdenver.edu (J. Barnard), Sean.O’[email protected] (Sean T . O’ Leary). http://dx.doi.org/10.1016/j.vaccine.2016.10.083 0264-410X/Ó 2016 Elsevier Ltd. All rights reserved.
lomavirus (HPV) vaccine among adolescents lags substantially. As of 2015 only 62.8% of 13–17 year old females and 49.8% of males, had initiated the three dose series, and only 41.9% and 28.1%, respectively, had completed it [1]. These levels are far below the Healthy People 2020 target goal of 80% vaccine coverage [2] – levels reached or nearly reached by Tdap and MCV. Low utilization of HPV vaccines leaves many adolescents at unnecessary risk for developing HPV-related diseases such as cervical and anal cancers and HPV-associated head and neck cancers. [3]. Numerous studies demonstrate the important influence that a provider’s recommendation can have on adolescent HPV vaccine uptake [4–10]. Research shows that when a strong recommendation is provided, the likelihood of the vaccine being given can increase as much as 5 fold [5]. Unfortunately, increasing numbers of studies also demonstrate that providers often discuss the HPV
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vaccine differently than other adolescent vaccines, which can lead parents to view the HPV vaccine as less important, safe, or necessary. [7,11,12]. In response to this, numerous organizations have called for tools and interventions to improve the way providers communicate with patients and their parents about adolescent HPV vaccination, operating under the notion that if effective tools were available and used, adolescent HPV vaccine utilization would increase [13–15]. To be effective, such tools need to enable providers to communicate about HPV vaccines effectively with parents, but in a time efficient manner. [16] Gilkey and colleagues have suggested that focusing on the ‘‘quality” of provider recommendations, which they operationalize as recommending the vaccine strongly, routinely, for the preferred age range (11–12 years), and on the same day as the appointment [12], may be a good starting place for interventions. Studies from provider communication regarding childhood vaccines further suggest that promoting a ‘‘presumptive” communication style (i.e. ‘‘it’s time to get vaccines”) may also be a preferred strategy compared to a participatory one (i.e. ‘‘do you want to get vaccines?”), and that many parents who initially refuse vaccines will change their minds if a provider continues to use a presumptive communication style during the visit [17]. Vaccine communication tools can take many forms including print, video and web-based. To our knowledge, there is no prior research describing HPV vaccine communication tools currently used by providers, or how these tools may impact clinical practice in terms of time spent discussing vaccines or providers’ quality of HPV vaccine recommendations. To address this knowledge gap, we surveyed primary care providers that were enrolled in a large, cluster-randomized trial of an HPV vaccine communication toolkit. This survey was done prior to the trial to provide a baseline assessment of the length of time providers spent discussing HPV vaccine during visits, the baseline quality of these providers’ HPV vaccine recommendations, and providers’ HPV vaccine communication tool use. We hypothesized that, (1) as in other studies [12], many providers would report low quality HPV vaccine recommendation practices; (2) that recommendation quality would be positively associated with the number of communication tools used; and (3) that as additional tools were used (especially those given outside of the clinical visit – i.e. mailed information sheets ahead of the appointment), the time providers spent personally discussing HPV vaccines during visits would decrease.
2. Methods 2.1. Study overview and population From February to April of 2014, we conducted a cross sectional survey of medical providers (medical doctors/doctors of osteopathy [MD/DO], nurse practitioners [NPs], and physicians assistants [PAs]) from 16 primary care practices (6 private pediatric offices, 6 public pediatric offices [(i.e. Federally qualified health centers [FQHC] or FQHC-like practices] and 4 private family medicine offices) in the Denver metro area that served adolescent patients and were enrolled in our clinical trial. Paper surveys were distributed for completion to each of the practices prior to practices being randomized into intervention and control groups of a cluster-randomized trial (trial ongoing, ClinicalTrials.gov 024456077; https://clinicaltrials.gov/ct2/show/NCT02456077? term=NCT02456077&rank=1) of an HPV vaccine provider communication toolkit. The survey was presented during study orientation meetings that explained the overall purpose of the project (to improve provider communication about HPV vaccines) and also included a brief discussion of what might constitute a ‘‘communi-
cation tool” being used currently or in the future by the practice. Surveys collected ‘‘baseline” measures of physician HPV vaccine communication practices. All study activities were approved by the Colorado Multi-Institutional Review Board (COMIRB-protocol # 13-2785). No incentives for participation were provided. 2.2. Outcome measures A primary outcome measure was the ‘‘quality” of providers’ recommendations for HPV vaccines. At the time of data collection, there were no publications providing metrics to assess this outcome. Therefore, for this study, recommendation quality was assessed using three questions. The first queried how often providers ‘‘inform parents of eligible adolescents that I recommend HPV vaccine for their child and only discuss it further if they refuse or have questions,” which was used as a proxy measure for the ‘‘presumptive” recommendation style suggested by some studies as a preferred communication strategy for vaccine discussions [17]. The highest response choice on a 4-point Likert scale, ‘‘most of the time (>75%),” was defined as a high quality recommendation (other response choices included ‘‘often (51–75%),” ‘‘sometimes (26– 50%),” and ‘‘rarely/never (0–25%)”). The second measure queried providers about how often they ‘‘continued to recommend the vaccine during at least one other visit despite parental refusal” with the same response choice (most of the time (>75%)) defined as a high quality recommendation. The third measure assessed providers’ current practices for recommending the HPV vaccine to 11–12 year old male and female patients. The response choice ‘‘strongly recommend the vaccine” was defined as a high quality recommendation (other response choices included ‘‘recommend the vaccine, but not strongly,” ‘‘make no recommendation,” or ‘‘recommend against the vaccine.”). Time personally spent discussing HPV vaccines during clinical visits was assessed for two scenarios: ‘‘discussing the HPV vaccine with parents who have substantial concerns about the vaccine,” and ‘‘discussing the HPV vaccine for the first time with typical parents.” This was compared to time spent discussing Tdap vaccines, which is required for school entry in Colorado, among typical parents. Response choices included ‘‘no time or someone else discusses the vaccine,” ‘‘1–4 min,” ‘‘5–9 min,” ‘‘10–14 min,” ‘‘15–19 min,” and ‘‘20+ min.” Some categories were later collapsed due to a skewed distribution of the results. The frequency of various communication tools used during (n = 4 tools assessed) or between (n = 5 tools assessed) visits was assessed using the same 4-point Likert scale as described above. Two separate lists of specific tools that might be used during or between visits was provided along with a write in category for other tools not included on the list. Expert input and review of the published literature was used to create the list of communication tools assessed. Based on the distribution of results, a dichotomous variable was created for the use of each tool in order to generate a tool count where yes = most of the time/often/sometimes (26–100%) and no = rarely/never (0–25%). A during- or between-visit tool count was then calculated by summing positive responses for each individual. Association of during- and betweenvisit tools counts with the three measures of high quality HPV vaccine recommendations and categorical responses to time spent discussing vaccines (described above) was explored with tool counts assessed as both an ordinal and continuous variable. Since conclusions from both analyses were the same, only continuous variable tool count results are presented. 2.3. Associated variables Several demographic and clinical characteristics were examined for their association with the various outcome measures described
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above. These included provider gender, health care degree (MD/ DO, NP, or PA), years at the practice, practice specialty (Pediatrics or Family Medicine), and type of practice (Public or Private). 2.4. Data analysis Descriptive statistics were generated for all survey questions. Associations between the various outcome measures and potential predictor variables were assessed using Chi-square or student’s ttests as appropriate. All reported p-values are from two-sided tests. Missing values have been excluded. All analyses were performed in SASÒ software version 9.4 (SAS Institute Inc., Cary, NC, USA) or STATA version 12 (StataCorp, College Station, Texas). 3. Results There were 150 respondents out of 183 eligible yielding an 82% response rate. One provider was removed from the analysis because they did not answer the primary outcomes questions leaving a final sample size of 149 respondents representing 16 practices. As shown in Table 1, most participants were MD/DO trained and female. Provider quality of HPV vaccine recommendations is shown in Table 2. A majority (59%) of providers indicated they used a presumptive vaccine recommendation style > 75% of the time. Additionally, 76% of respondents reported continuing to offer the HPV vaccine at subsequent visits after parent refusal. However, less than two-thirds of providers ‘‘strongly” recommended the vaccine for 11–12 year old patients overall, with differences by patient gender (60% females, 55% males, p = 0.02). For both patient genders, providers were significantly more likely to strongly recommend the HPV vaccine to parents with adolescents 13 years or older compared to parents of 11–12 year olds (p < 0.001 for all comparisons). In univariate analysis, strongly recommending the HPV vaccine to 11–12 year old boys and girls was significantly associated with pediatric specialty compared to family medicine (58% vs 32%, p = 0.03), and working in a public vs. private setting (54% vs 46%, p < 0.01), but not with provider degree, gender, or years in practice. Less than 12% of providers reported strongly recommending the HPV vaccine to 9–10 year olds of either gender. HPV vaccine discussions were significantly longer for HPV vaccine-hesitant parents than ‘‘typical” parents (Fig. 1), with 65% Table 1 Provider characteristics. Characteristic
% (n)a N = 149
Provider type MD/DO Nurse practitioner Physician assistant
64% (96) 15% (22) 21% (31)
Gender Male Female
22% (33) 78% (115)
Specialty Pediatrics Family medicine
87% (130) 13% (19)
Practice setting Pediatrics – public Pediatrics – private Family Medicine – private
36% (54) 51% (76) 13% (19)
Years in practice 0–5 years 6–10 years >10 years
43% (63) 19% (28) 39% (57)
Missing values have been excluded when < 5%. a Percentages may not sum to 100 due to rounding.
Table 2 Provider recommendation quality for HPV vaccination of adolescents. Recommendation characteristic % Who uses presumptive style Most of the time (>75% of the time) Often (51%–75% of the time) Sometimes (26%–50% of the time) Rarely or never (0%–25% of the time)
% (n)a N = 149 59% (86) 23% (34) 14% (20) 3% (5)
% Who continues to offer the vaccine at subsequent visits after initial refusal Most of the time (>75% of the time) 76% (1 1 2) Often (51%–75% of the time) 16% (23) Sometimes (26%–50% of the time) 7% (11) Rarely or never (0%–25% of the time) 1% (2) % Who strongly recommends HPV vaccine to. . . 9–10 year old girls 9–10 year old boys 11–12 year old girls 11–12 year old boys 13–15 year old girls 13–15 year old boys 16–17 year old girls 16–17 year old boys
11% (16) 8% (12) 60% (89) 55% (82) 90% (133) 84% (125) 93% (138) 85% (126)
Missing values have been excluded when < 5%. a Percentages may not sum to 100 due to rounding.
percent of providers reporting spending 5 or more minutes discussing HPV vaccines with hesitant parents compared to only 13% reporting this length of discussion with typical parents (p < 0.001). Significantly more providers reported long (5+ min) discussions with both HPV vaccine-hesitant and typical parents compared with Tdap (p < 0.001 for all comparisons). Vaccine information sheets were the most commonly used communication tool for HPV vaccines during the clinical encounter, being used most of the time by 64% of providers. Use of other tools during the visit was infrequent (Table 3). Similarly, few providers used HPV vaccine communication tools between visits. Encouraging parents to access information about the vaccine after the visit was the most common between visit tool used, reported as being used often, or most of the time by 17%, and 4% of providers, respectively. Reminder notices for completion of the HPV vaccine series among those who had initiated it were the second most common between visit tool used, but this tool was used often or most of the time by only 18% of providers. For vaccine refusing parents, providers indicated they frequently (most of the time – 48%, often – 24%) gave parents educational materials at the end of the visit to further consider regarding HPV vaccination. In contrast with our hypothesis, increased numbers of tools used during or between visits was associated with a longer time spent discussing HPV vaccines. Providers who spent P 5 min discussing HPV vaccines with typical parents used significantly more tools during and between visits than providers spending less than 5 min in this discussion (mean number of during visit tools 2.6 vs. 1.9, p = 0.01; mean number of between visit tools 1.5 vs. 1.0, p = 0.04). A similar pattern was found when discussing the HPV vaccine with hesitant parents, but this result was only statistically significant for tools used between visits (mean number of tools between visits 1.2 vs. 0.8, p = 0.02; mean number of tools during visits 2.1 vs 1.8, p = 0.12). Also, contrary to our hypotheses, the number of tools used during or between visits was not associated with any of the three measures of provider recommendation quality (data not shown). 4. Discussion In one of the first studies to document the use of communication tools for HPV vaccination in primary care, we found that while
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Time Spent Discussing HPV and Tdap Vaccines with Parents
100%
86%
86%
80% 57%
60% 35%
40% 20% 0%
13%
12% 1%
2%
0%
No me spent/someone else discusses
1-4 minutes
HPV Vaccine - typical parents
5-9 minutes
0%
8%
0%
10+ minutes
HPV vaccine - hesitant parents
Tdap vaccine - typical parents Fig. 1. Percentage of respondents reporting time spent discussing HPV vaccines with ‘typical’ parents (blue) and ‘hesitant’ parents (red); and discussing Tdap vaccines with ‘typical’ parents (green). Missing values have been excluded when < 5%. All 2-way, between vaccine comparisons are statistically significant (<0.001).
Table 3 HPV vaccination communication tools used by providers during or between visits.
Tools used during visits CDC Vaccine information Sheets Educational materials created by vaccine manufacturers Educational materials from an outside resources such as CDC, state health department etc. Educational materials created by your office
Most of the time (>75%)% (n)
Often (51%–75%)% (n)
Sometimes (26%–50%)% (n)
Rarely/Never (0–25%)% (n)
64% (94) 5% (8) 8% (12)
10% (14) 5% (7) 10% (14)
16% (23) 22% (33) 39% (57)
11% (16) 68% (100) 44% (64)
5% (7)
5% (8)
12% (18)
78% (114)
Tools used between visits Sending information about HPV vaccination with patients appointment reminder Encouraging parents to access information about the vaccine online
3% (5)
0%
2% (3)
94% (136)
2% (3)
2% (3)
9% (13)
87% (126)
before the scheduled visit Encouraging parents to access information about the vaccine online
4% (6)
17% (25)
30% (44)
49% (71)
2% (3)
1% (2)
5% (7)
92% (131)
10% (14)
8% (11)
11% (15)
71% (100)
(office or other website) after scheduled visits Sending reminder notices to parents whose adolescents have not yet started the vaccine series Sending reminder notices to parents whose adolescents have started but not yet completed the vaccine series
Missing values have been excluded and are < 5% with the exception of ‘‘Parents whose adolescent has started but not yet completed the vaccine series are sent reminder notices” where missing responses = 6.4% (n = 9). ⁄ Percentages may not sum to 100 due to rounding.
a majority of providers surveyed used at least one communication tool during the visit, and a substantial minority used at least one tool between visits, use of tools was not associated with decreased time spent discussing the HPV vaccine, nor was it associated with the likelihood that a provider would give a high quality recommendation for the HPV vaccine. These findings, which were contrary to our hypotheses, suggest that better engagement with current tools and/or new HPV vaccine communication tools may be needed to promote providers’ ability to effectively communicate about HPV vaccines with parents of adolescents. In this study, a high proportion of providers reported spending more than five minutes discussing the HPV vaccine during clinical encounters with vaccine hesitant parents. Given that clinical appointments typically last only 10–20 min, spending such time discussing HPV vaccines means that discussions about other important and recommended adolescent health topics are less likely to be addressed [18]. Anticipation of long HPV vaccine discussions also likely causes some providers to forgo the HPV vaccine discussion altogether in order to focus on other issues [11,19]. We
found that increasing numbers of communication tools used was associated with longer HPV vaccine discussion times, rather than shorter, suggesting that the tools currently being used by these providers may not be time efficient, and in fact, may be adding to the time spent discussing the vaccine. A possible solution would be to increase the use of communication tools before or between visits – a strategy that was used by only a small minority of providers in our study. If done effectively, conveying information about HPV (or other vaccines) prior to the visit could answer many parents’ questions and concerns, potentially freeing up time during the clinical encounter to focus on other topics. This concept is supported by results from a concomitant survey of parents we performed from the same clinical sites as the providers in this study, in which a high proportion indicated they were open to receiving various forms of HPV vaccine information prior to the adolescent’s visit [20]. However, it is important not to disregard an alternative hypothesis to explain our results – that tool use did not cause longer visits, but rather that providers already willing to invest a substantial amount of time in the HPV vaccine discussion may also
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be those more interested in using tools during this discussion. In either case, provider acceptance of communication tools for HPV vaccines is likely to be influenced by their ease of use, their ability to make visits more efficient, and by their ability to result in increased HPV vaccination rates. Our larger trial on the provider communication toolkit will be able to address each of these important outcomes. In this study, three-quarters of providers reported continuing to offer the vaccine to reluctant parents, yet only 59% reported using a presumptive recommendation style. Prior research [17] demonstrated that use of a presumptive style for communicating about vaccines for parents of children age 1–19 months was associated with a significantly less vaccine resistance compared to a participatory style (26% vs. 83%). These findings are intriguing, and suggest that a presumptive style may be a preferred approach when discussing vaccines with parents. More research is needed to understand whether a provider’s communication style affects parents’ vaccination attitudes, and also whether a presumptive communication style is associated with higher vaccine acceptance for adolescent vaccines specifically. In a national study of provider HPV vaccine recommendation quality, Gilkey et al. found that 73% reported recommending the vaccine as ‘‘very or extremely important” for 11–12 year olds. In our study, this outcome was slightly less common with only 60% of providers reporting strongly recommending the HPV vaccine for 11–12 year old females, and only 55% for males. These results are consistent with our corresponding parent study in which only 39% of parents indicated that their adolescent’s provider ‘‘very strongly” recommended the HPV vaccine at their adolescent’s most recent check-up and 34% indicated their provider ‘‘somewhat strongly” recommended it [20]. While differences in our study’s results to that of Gilkey’s national study could be explained by regional differences in parent or provider attitudes, or by differences in how the outcome was assessed, both sets of data indicate ongoing reluctance by a substantial proportion of providers to strongly recommend the HPV vaccine to 11–12 year olds. This reluctance is concerning given that HPV vaccination preferably at age 11–12 has been a national recommendation for nearly a decade, and that vaccination levels continue to be low [1,21,22]. These results are consistent with prior research demonstrating that parental hesitance for HPV vaccination is common, especially for younger adolescents [23,24], and Gilkey’s study in which 47% of providers believed that parents perceived the HPV vaccine to be of little or no importance for 11–12 year olds [12]. With consistently low rates of HPV vaccine uptake among adolescents nationally, interventions to improve use of the vaccine are needed. Among the many barriers to HPV vaccination that have been described, changing providers’ HPV vaccine recommendation practices may be a potentially ‘‘fixable” one [7,25,26]. Indeed, several medical organizations have recently begun to focus on training providers on how to make high quality HPV vaccine recommendations for their adolescent patients [14,25,27,28]. Research in the future will need to examine how these strategies impact HPV vaccination rates, and also whether such strategies have any negative impact on clinical efficiency. Findings from this study should be interpreted in light of several limitations. First, although our sample was heterogeneous with regard to provider training, specialty, and clinic type, the sample was small and regional. Thus, findings from this study may not be generalizable to other geographic locations. Second, while we used expert input and published literature to create the list of HPV vaccine communication tools assessed in this study, this list is likely not exhaustive. Some providers may effectively use other HPV vaccine communication tools that were not assessed in this study. Mitigating this concern somewhat is the opportunity that providers had in the study to report in a free text space ‘‘other”
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communication tools used– few were listed and those that listed were similar to the tool categories queried directly. Additionally, in this survey we did not assess ‘‘how” tools were used, which is likely to vary substantially between providers, although we did capture this information from a subset of providers in qualitative interviews that were also part of the baseline assessment in the larger trial study (unpublished data). Finally, our measures of tool use, quality of HPV vaccine recommendations, and time spent discussing the HPV vaccine may be subject to recall bias as we did not observe these outcomes prospectively. Relatedly, social desirability bias could have led providers to overestimate how frequently they were engaging in recommended immunization practices and using communication tools. However, the consistency of our findings with a concomitant survey of parents from these providers’ offices, and with national data on provider HPV vaccine recommendation strategies is reassuring. 5. Conclusions Many providers spend a significant amount of time discussing HPV vaccines with hesitant parents, yet fail to give high quality HPV vaccine recommendations. Moreover, providers currently use few tools between visits to convey HPV vaccine information to parents, and when communication tools are used either during or between visits, they are associated with longer HPV vaccine discussion times. Better engagement with existing tools and/or new tools that are effective at improving provider HPV vaccine recommendation quality, and are also time efficient, are needed to increase adolescent HPV vaccination levels. Funding This work was supported by the Centers for Disease Control and Prevention (5U01 IP 000801-03). The opinions expressed in this manuscript do not necessarily reflect those of the funding agency. References [1] Reagan-Steiner S et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years - United States, 2015. MMWR Morb Mortal Wkly Rep 2016;65(33):850–8. [2] Koh HK, Blakey CR, Roper AY. Healthy People 2020: a report card on the health of the nation. JAMA 2014;311(24):2475–6. [3] Viens LJ et al. Human papillomavirus-associated cancers - United States, 2008– 2012. MMWR Morb Mortal Wkly Rep 2016;65(26):661–6. [4] Rahman M et al. Provider recommendation mediates the relationship between parental human papillomavirus (HPV) vaccine awareness and HPV vaccine initiation and completion among 13- to 17-year-old U.S. adolescent children. Clin Pediatr (Phila) 2015;54(4):371–5. [5] Ylitalo KR, Lee H, Mehta NK. Health care provider recommendation, human papillomavirus vaccination, and race/ethnicity in the US National Immunization Survey. Am J Public Health 2013;103(1):164–9. [6] Lau M, Lin H, Flores G. Factors associated with human papillomavirus vaccineseries initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health. Vaccine 2012;30 (20):3112–8. [7] Gilkey MB et al. Provider communication and HPV vaccination: the impact of recommendation quality. Vaccine 2016. [8] Rickert VI et al. The role of parental attitudes and provider discussions in uptake of adolescent vaccines. Vaccine 2015;33(5):642–7. [9] Clark SJ et al. Parent perception of provider interactions influences HPV vaccination status of adolescent females. Clin Pediatr (Phila) 2015. [10] Rand CM et al. Patient-provider communication and human papillomavirus vaccine acceptance. Clin Pediatr (Phila) 2011;50(2):106–13. [11] Gilkey MB et al. Physician communication about adolescent vaccination: how is human papillomavirus vaccine different? Prev Med 2015;77:181–5. [12] Gilkey MB et al. Quality of physician communication about human papillomavirus vaccine: findings from a national survey. Cancer Epidemiol Biomarkers Prev 2015. [13] Center for Disease Control and Prevention, N.C.f.I.a.R.D., Health Communications Office, You are the Key to HPV Cancer Prevention: Communicating about HPV. 2014 Sept 30, 2014]; Available from:.
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[14] National Cancer Institute, President’s Cancer Panel Annual Report, Accelerating HPV Vaccine Uptake: Urgency for Action to Prevent Cancer. A Report to the President of the United States from the President’s Cancer Panel. 2014: Bethesda, MD. [15] American Academy of Pediatrics. Give a strong recommendation for HPV vaccine to increase uptake. 2015 1/15/16]; Available from:
[21] Markowitz LE et al. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2007;56(RR-2):1–24. [22] Reagan-Steiner S et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years - United States, 2014. MMWR Morb Mortal Wkly Rep 2015;64(29):784–92. [23] Beachler DC et al. HPV vaccination initiation after the routine-recommended ages of 11–12 in the United States. Papillomavirus Res 2016;2:11–6. [24] Darden PM et al. Reasons for not vaccinating adolescents: national immunization survey of teens, 2008–2010. Pediatrics 2013;131(4):645–51. [25] Zimet GD. Health care professionals and adolescent vaccination. A call for intervention research. Hum Vaccine Immunother 2014;10(9):2629–30. [26] Zimet GD. ‘‘A day late and a dollar short”: physicians and HPV vaccination. Cancer Epidemiol Biomarkers Prev 2015. [27] Committee National Vaccine Advisory. Assessing the state of vaccine confidence in the United States: recommendations from the National Vaccine Advisory Committee. Pub Health Rep 2015;130:573–95. [28] Stokley S et al. Adolescent vaccination: recommendations from the National Vaccine Advisory Committee. Am J Prev Med 2009;36(3) [278–9 e6].
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
Providers’ time spent and tools used when discussing the HPV vaccine with parents of adolescents Amanda F. Dempsey ⇑, Steven Lockhart, Elizabeth J. Campagna, Jennifer Pyrzanowski, Juliana Barnard, Sean T . O’ Leary Adult and Child Consortium for Outcomes Research and Dissemination Science Program, Children’s Hospital Colorado and University of Colorado, 13199 East Montview Blvd, Suite 300, Aurora, CO 80045, United States
a r t i c l e
i n f o
Article history: Received 28 July 2016 Received in revised form 21 October 2016 Accepted 28 October 2016 Available online 10 November 2016 Keywords: Human papillomavirus Vaccine delivery Communication
a b s t r a c t Objectives: Little is known about HPV vaccine communication tools currently used by primary care providers of adolescents, or how such tools impact the quality of HPV vaccine recommendations, which some have defined as using a ‘‘presumptive” communication style, continuing to offer vaccines despite resistance, and strongly recommending vaccines at the appropriate ages. We surveyed primary care providers to assess their current use of HPV vaccine communication tools, and how these related to their HPV vaccine recommendation quality. Study Design: Cross sectional survey of 183 pediatrics and family medicine primary care providers in the Denver metro area. Results: Response rate was 82% (n = 150). Most (59%) providers used a presumptive vaccine recommendation >75% of the time, and 76% reported continuing to offer the HPV vaccine even after parent refusal. However, less than two-thirds of providers ‘‘strongly” recommended the vaccine to 11–12 year olds (60% for females, 55% for males, p = 0.02). The HPV vaccine information sheet from the Centers from Disease Control and Prevention was the most frequently used communication tool during clinical visits (64% used at least 75% of the time) and directing parents to preferred websites was the most frequently used between-visit communication tool (21% used >50% of visits). Use of tools was not associated with any measure of HPV vaccine recommendation quality but was associated with longer HPV vaccine discussion times. Conclusions: Providers use only limited types of adolescent HPV vaccine communication tools, and frequently do not use preferred vaccine communication strategies. Better engagement with existing HPV vaccine communication tools, and/or the creation of new tools may be needed to enhance providers’ ability to provide high quality HPV vaccine recommendations. Ó 2016 Elsevier Ltd. All rights reserved.
1. Introduction Compared to the tetanus-diphtheria-acellular pertussis (Tdap) and meningococcal (MCV) vaccines, utilization of the human papilAbbreviations: HPV, human papillomavirus; Tdap, Tetanus-diphtheria-acellular pertussis vaccine; CDC, Centers for Disease Control and Prevention; MD, medical doctor; DO, doctor of osteopathy; NP, nurse practitioner; PA, physician’s assistant; COMIRB, Colorado Multi-Institutional Review Board. ⇑ Corresponding author at: Adult and Child Consortium for Outcomes Research and Dissemination Science (ACCORDS) Program, Children’s Hospital Colorado and University of Colorado, Anschutz Medical Campus, 13199 East Montview Blvd, Suite 300, Aurora, CO 80045, United States. E-mail addresses: [email protected] (A.F. Dempsey), Steven. [email protected] (S. Lockhart), [email protected] (E.J. Campagna), [email protected] (J. Pyrzanowski), Juliana.barnard@ ucdenver.edu (J. Barnard), Sean.O’[email protected] (Sean T . O’ Leary). http://dx.doi.org/10.1016/j.vaccine.2016.10.083 0264-410X/Ó 2016 Elsevier Ltd. All rights reserved.
lomavirus (HPV) vaccine among adolescents lags substantially. As of 2015 only 62.8% of 13–17 year old females and 49.8% of males, had initiated the three dose series, and only 41.9% and 28.1%, respectively, had completed it [1]. These levels are far below the Healthy People 2020 target goal of 80% vaccine coverage [2] – levels reached or nearly reached by Tdap and MCV. Low utilization of HPV vaccines leaves many adolescents at unnecessary risk for developing HPV-related diseases such as cervical and anal cancers and HPV-associated head and neck cancers. [3]. Numerous studies demonstrate the important influence that a provider’s recommendation can have on adolescent HPV vaccine uptake [4–10]. Research shows that when a strong recommendation is provided, the likelihood of the vaccine being given can increase as much as 5 fold [5]. Unfortunately, increasing numbers of studies also demonstrate that providers often discuss the HPV
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vaccine differently than other adolescent vaccines, which can lead parents to view the HPV vaccine as less important, safe, or necessary. [7,11,12]. In response to this, numerous organizations have called for tools and interventions to improve the way providers communicate with patients and their parents about adolescent HPV vaccination, operating under the notion that if effective tools were available and used, adolescent HPV vaccine utilization would increase [13–15]. To be effective, such tools need to enable providers to communicate about HPV vaccines effectively with parents, but in a time efficient manner. [16] Gilkey and colleagues have suggested that focusing on the ‘‘quality” of provider recommendations, which they operationalize as recommending the vaccine strongly, routinely, for the preferred age range (11–12 years), and on the same day as the appointment [12], may be a good starting place for interventions. Studies from provider communication regarding childhood vaccines further suggest that promoting a ‘‘presumptive” communication style (i.e. ‘‘it’s time to get vaccines”) may also be a preferred strategy compared to a participatory one (i.e. ‘‘do you want to get vaccines?”), and that many parents who initially refuse vaccines will change their minds if a provider continues to use a presumptive communication style during the visit [17]. Vaccine communication tools can take many forms including print, video and web-based. To our knowledge, there is no prior research describing HPV vaccine communication tools currently used by providers, or how these tools may impact clinical practice in terms of time spent discussing vaccines or providers’ quality of HPV vaccine recommendations. To address this knowledge gap, we surveyed primary care providers that were enrolled in a large, cluster-randomized trial of an HPV vaccine communication toolkit. This survey was done prior to the trial to provide a baseline assessment of the length of time providers spent discussing HPV vaccine during visits, the baseline quality of these providers’ HPV vaccine recommendations, and providers’ HPV vaccine communication tool use. We hypothesized that, (1) as in other studies [12], many providers would report low quality HPV vaccine recommendation practices; (2) that recommendation quality would be positively associated with the number of communication tools used; and (3) that as additional tools were used (especially those given outside of the clinical visit – i.e. mailed information sheets ahead of the appointment), the time providers spent personally discussing HPV vaccines during visits would decrease.
2. Methods 2.1. Study overview and population From February to April of 2014, we conducted a cross sectional survey of medical providers (medical doctors/doctors of osteopathy [MD/DO], nurse practitioners [NPs], and physicians assistants [PAs]) from 16 primary care practices (6 private pediatric offices, 6 public pediatric offices [(i.e. Federally qualified health centers [FQHC] or FQHC-like practices] and 4 private family medicine offices) in the Denver metro area that served adolescent patients and were enrolled in our clinical trial. Paper surveys were distributed for completion to each of the practices prior to practices being randomized into intervention and control groups of a cluster-randomized trial (trial ongoing, ClinicalTrials.gov 024456077; https://clinicaltrials.gov/ct2/show/NCT02456077? term=NCT02456077&rank=1) of an HPV vaccine provider communication toolkit. The survey was presented during study orientation meetings that explained the overall purpose of the project (to improve provider communication about HPV vaccines) and also included a brief discussion of what might constitute a ‘‘communi-
cation tool” being used currently or in the future by the practice. Surveys collected ‘‘baseline” measures of physician HPV vaccine communication practices. All study activities were approved by the Colorado Multi-Institutional Review Board (COMIRB-protocol # 13-2785). No incentives for participation were provided. 2.2. Outcome measures A primary outcome measure was the ‘‘quality” of providers’ recommendations for HPV vaccines. At the time of data collection, there were no publications providing metrics to assess this outcome. Therefore, for this study, recommendation quality was assessed using three questions. The first queried how often providers ‘‘inform parents of eligible adolescents that I recommend HPV vaccine for their child and only discuss it further if they refuse or have questions,” which was used as a proxy measure for the ‘‘presumptive” recommendation style suggested by some studies as a preferred communication strategy for vaccine discussions [17]. The highest response choice on a 4-point Likert scale, ‘‘most of the time (>75%),” was defined as a high quality recommendation (other response choices included ‘‘often (51–75%),” ‘‘sometimes (26– 50%),” and ‘‘rarely/never (0–25%)”). The second measure queried providers about how often they ‘‘continued to recommend the vaccine during at least one other visit despite parental refusal” with the same response choice (most of the time (>75%)) defined as a high quality recommendation. The third measure assessed providers’ current practices for recommending the HPV vaccine to 11–12 year old male and female patients. The response choice ‘‘strongly recommend the vaccine” was defined as a high quality recommendation (other response choices included ‘‘recommend the vaccine, but not strongly,” ‘‘make no recommendation,” or ‘‘recommend against the vaccine.”). Time personally spent discussing HPV vaccines during clinical visits was assessed for two scenarios: ‘‘discussing the HPV vaccine with parents who have substantial concerns about the vaccine,” and ‘‘discussing the HPV vaccine for the first time with typical parents.” This was compared to time spent discussing Tdap vaccines, which is required for school entry in Colorado, among typical parents. Response choices included ‘‘no time or someone else discusses the vaccine,” ‘‘1–4 min,” ‘‘5–9 min,” ‘‘10–14 min,” ‘‘15–19 min,” and ‘‘20+ min.” Some categories were later collapsed due to a skewed distribution of the results. The frequency of various communication tools used during (n = 4 tools assessed) or between (n = 5 tools assessed) visits was assessed using the same 4-point Likert scale as described above. Two separate lists of specific tools that might be used during or between visits was provided along with a write in category for other tools not included on the list. Expert input and review of the published literature was used to create the list of communication tools assessed. Based on the distribution of results, a dichotomous variable was created for the use of each tool in order to generate a tool count where yes = most of the time/often/sometimes (26–100%) and no = rarely/never (0–25%). A during- or between-visit tool count was then calculated by summing positive responses for each individual. Association of during- and betweenvisit tools counts with the three measures of high quality HPV vaccine recommendations and categorical responses to time spent discussing vaccines (described above) was explored with tool counts assessed as both an ordinal and continuous variable. Since conclusions from both analyses were the same, only continuous variable tool count results are presented. 2.3. Associated variables Several demographic and clinical characteristics were examined for their association with the various outcome measures described
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above. These included provider gender, health care degree (MD/ DO, NP, or PA), years at the practice, practice specialty (Pediatrics or Family Medicine), and type of practice (Public or Private). 2.4. Data analysis Descriptive statistics were generated for all survey questions. Associations between the various outcome measures and potential predictor variables were assessed using Chi-square or student’s ttests as appropriate. All reported p-values are from two-sided tests. Missing values have been excluded. All analyses were performed in SASÒ software version 9.4 (SAS Institute Inc., Cary, NC, USA) or STATA version 12 (StataCorp, College Station, Texas). 3. Results There were 150 respondents out of 183 eligible yielding an 82% response rate. One provider was removed from the analysis because they did not answer the primary outcomes questions leaving a final sample size of 149 respondents representing 16 practices. As shown in Table 1, most participants were MD/DO trained and female. Provider quality of HPV vaccine recommendations is shown in Table 2. A majority (59%) of providers indicated they used a presumptive vaccine recommendation style > 75% of the time. Additionally, 76% of respondents reported continuing to offer the HPV vaccine at subsequent visits after parent refusal. However, less than two-thirds of providers ‘‘strongly” recommended the vaccine for 11–12 year old patients overall, with differences by patient gender (60% females, 55% males, p = 0.02). For both patient genders, providers were significantly more likely to strongly recommend the HPV vaccine to parents with adolescents 13 years or older compared to parents of 11–12 year olds (p < 0.001 for all comparisons). In univariate analysis, strongly recommending the HPV vaccine to 11–12 year old boys and girls was significantly associated with pediatric specialty compared to family medicine (58% vs 32%, p = 0.03), and working in a public vs. private setting (54% vs 46%, p < 0.01), but not with provider degree, gender, or years in practice. Less than 12% of providers reported strongly recommending the HPV vaccine to 9–10 year olds of either gender. HPV vaccine discussions were significantly longer for HPV vaccine-hesitant parents than ‘‘typical” parents (Fig. 1), with 65% Table 1 Provider characteristics. Characteristic
% (n)a N = 149
Provider type MD/DO Nurse practitioner Physician assistant
64% (96) 15% (22) 21% (31)
Gender Male Female
22% (33) 78% (115)
Specialty Pediatrics Family medicine
87% (130) 13% (19)
Practice setting Pediatrics – public Pediatrics – private Family Medicine – private
36% (54) 51% (76) 13% (19)
Years in practice 0–5 years 6–10 years >10 years
43% (63) 19% (28) 39% (57)
Missing values have been excluded when < 5%. a Percentages may not sum to 100 due to rounding.
Table 2 Provider recommendation quality for HPV vaccination of adolescents. Recommendation characteristic % Who uses presumptive style Most of the time (>75% of the time) Often (51%–75% of the time) Sometimes (26%–50% of the time) Rarely or never (0%–25% of the time)
% (n)a N = 149 59% (86) 23% (34) 14% (20) 3% (5)
% Who continues to offer the vaccine at subsequent visits after initial refusal Most of the time (>75% of the time) 76% (1 1 2) Often (51%–75% of the time) 16% (23) Sometimes (26%–50% of the time) 7% (11) Rarely or never (0%–25% of the time) 1% (2) % Who strongly recommends HPV vaccine to. . . 9–10 year old girls 9–10 year old boys 11–12 year old girls 11–12 year old boys 13–15 year old girls 13–15 year old boys 16–17 year old girls 16–17 year old boys
11% (16) 8% (12) 60% (89) 55% (82) 90% (133) 84% (125) 93% (138) 85% (126)
Missing values have been excluded when < 5%. a Percentages may not sum to 100 due to rounding.
percent of providers reporting spending 5 or more minutes discussing HPV vaccines with hesitant parents compared to only 13% reporting this length of discussion with typical parents (p < 0.001). Significantly more providers reported long (5+ min) discussions with both HPV vaccine-hesitant and typical parents compared with Tdap (p < 0.001 for all comparisons). Vaccine information sheets were the most commonly used communication tool for HPV vaccines during the clinical encounter, being used most of the time by 64% of providers. Use of other tools during the visit was infrequent (Table 3). Similarly, few providers used HPV vaccine communication tools between visits. Encouraging parents to access information about the vaccine after the visit was the most common between visit tool used, reported as being used often, or most of the time by 17%, and 4% of providers, respectively. Reminder notices for completion of the HPV vaccine series among those who had initiated it were the second most common between visit tool used, but this tool was used often or most of the time by only 18% of providers. For vaccine refusing parents, providers indicated they frequently (most of the time – 48%, often – 24%) gave parents educational materials at the end of the visit to further consider regarding HPV vaccination. In contrast with our hypothesis, increased numbers of tools used during or between visits was associated with a longer time spent discussing HPV vaccines. Providers who spent P 5 min discussing HPV vaccines with typical parents used significantly more tools during and between visits than providers spending less than 5 min in this discussion (mean number of during visit tools 2.6 vs. 1.9, p = 0.01; mean number of between visit tools 1.5 vs. 1.0, p = 0.04). A similar pattern was found when discussing the HPV vaccine with hesitant parents, but this result was only statistically significant for tools used between visits (mean number of tools between visits 1.2 vs. 0.8, p = 0.02; mean number of tools during visits 2.1 vs 1.8, p = 0.12). Also, contrary to our hypotheses, the number of tools used during or between visits was not associated with any of the three measures of provider recommendation quality (data not shown). 4. Discussion In one of the first studies to document the use of communication tools for HPV vaccination in primary care, we found that while
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Time Spent Discussing HPV and Tdap Vaccines with Parents
100%
86%
86%
80% 57%
60% 35%
40% 20% 0%
13%
12% 1%
2%
0%
No me spent/someone else discusses
1-4 minutes
HPV Vaccine - typical parents
5-9 minutes
0%
8%
0%
10+ minutes
HPV vaccine - hesitant parents
Tdap vaccine - typical parents Fig. 1. Percentage of respondents reporting time spent discussing HPV vaccines with ‘typical’ parents (blue) and ‘hesitant’ parents (red); and discussing Tdap vaccines with ‘typical’ parents (green). Missing values have been excluded when < 5%. All 2-way, between vaccine comparisons are statistically significant (<0.001).
Table 3 HPV vaccination communication tools used by providers during or between visits.
Tools used during visits CDC Vaccine information Sheets Educational materials created by vaccine manufacturers Educational materials from an outside resources such as CDC, state health department etc. Educational materials created by your office
Most of the time (>75%)% (n)
Often (51%–75%)% (n)
Sometimes (26%–50%)% (n)
Rarely/Never (0–25%)% (n)
64% (94) 5% (8) 8% (12)
10% (14) 5% (7) 10% (14)
16% (23) 22% (33) 39% (57)
11% (16) 68% (100) 44% (64)
5% (7)
5% (8)
12% (18)
78% (114)
Tools used between visits Sending information about HPV vaccination with patients appointment reminder Encouraging parents to access information about the vaccine online
3% (5)
0%
2% (3)
94% (136)
2% (3)
2% (3)
9% (13)
87% (126)
before the scheduled visit Encouraging parents to access information about the vaccine online
4% (6)
17% (25)
30% (44)
49% (71)
2% (3)
1% (2)
5% (7)
92% (131)
10% (14)
8% (11)
11% (15)
71% (100)
(office or other website) after scheduled visits Sending reminder notices to parents whose adolescents have not yet started the vaccine series Sending reminder notices to parents whose adolescents have started but not yet completed the vaccine series
Missing values have been excluded and are < 5% with the exception of ‘‘Parents whose adolescent has started but not yet completed the vaccine series are sent reminder notices” where missing responses = 6.4% (n = 9). ⁄ Percentages may not sum to 100 due to rounding.
a majority of providers surveyed used at least one communication tool during the visit, and a substantial minority used at least one tool between visits, use of tools was not associated with decreased time spent discussing the HPV vaccine, nor was it associated with the likelihood that a provider would give a high quality recommendation for the HPV vaccine. These findings, which were contrary to our hypotheses, suggest that better engagement with current tools and/or new HPV vaccine communication tools may be needed to promote providers’ ability to effectively communicate about HPV vaccines with parents of adolescents. In this study, a high proportion of providers reported spending more than five minutes discussing the HPV vaccine during clinical encounters with vaccine hesitant parents. Given that clinical appointments typically last only 10–20 min, spending such time discussing HPV vaccines means that discussions about other important and recommended adolescent health topics are less likely to be addressed [18]. Anticipation of long HPV vaccine discussions also likely causes some providers to forgo the HPV vaccine discussion altogether in order to focus on other issues [11,19]. We
found that increasing numbers of communication tools used was associated with longer HPV vaccine discussion times, rather than shorter, suggesting that the tools currently being used by these providers may not be time efficient, and in fact, may be adding to the time spent discussing the vaccine. A possible solution would be to increase the use of communication tools before or between visits – a strategy that was used by only a small minority of providers in our study. If done effectively, conveying information about HPV (or other vaccines) prior to the visit could answer many parents’ questions and concerns, potentially freeing up time during the clinical encounter to focus on other topics. This concept is supported by results from a concomitant survey of parents we performed from the same clinical sites as the providers in this study, in which a high proportion indicated they were open to receiving various forms of HPV vaccine information prior to the adolescent’s visit [20]. However, it is important not to disregard an alternative hypothesis to explain our results – that tool use did not cause longer visits, but rather that providers already willing to invest a substantial amount of time in the HPV vaccine discussion may also
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be those more interested in using tools during this discussion. In either case, provider acceptance of communication tools for HPV vaccines is likely to be influenced by their ease of use, their ability to make visits more efficient, and by their ability to result in increased HPV vaccination rates. Our larger trial on the provider communication toolkit will be able to address each of these important outcomes. In this study, three-quarters of providers reported continuing to offer the vaccine to reluctant parents, yet only 59% reported using a presumptive recommendation style. Prior research [17] demonstrated that use of a presumptive style for communicating about vaccines for parents of children age 1–19 months was associated with a significantly less vaccine resistance compared to a participatory style (26% vs. 83%). These findings are intriguing, and suggest that a presumptive style may be a preferred approach when discussing vaccines with parents. More research is needed to understand whether a provider’s communication style affects parents’ vaccination attitudes, and also whether a presumptive communication style is associated with higher vaccine acceptance for adolescent vaccines specifically. In a national study of provider HPV vaccine recommendation quality, Gilkey et al. found that 73% reported recommending the vaccine as ‘‘very or extremely important” for 11–12 year olds. In our study, this outcome was slightly less common with only 60% of providers reporting strongly recommending the HPV vaccine for 11–12 year old females, and only 55% for males. These results are consistent with our corresponding parent study in which only 39% of parents indicated that their adolescent’s provider ‘‘very strongly” recommended the HPV vaccine at their adolescent’s most recent check-up and 34% indicated their provider ‘‘somewhat strongly” recommended it [20]. While differences in our study’s results to that of Gilkey’s national study could be explained by regional differences in parent or provider attitudes, or by differences in how the outcome was assessed, both sets of data indicate ongoing reluctance by a substantial proportion of providers to strongly recommend the HPV vaccine to 11–12 year olds. This reluctance is concerning given that HPV vaccination preferably at age 11–12 has been a national recommendation for nearly a decade, and that vaccination levels continue to be low [1,21,22]. These results are consistent with prior research demonstrating that parental hesitance for HPV vaccination is common, especially for younger adolescents [23,24], and Gilkey’s study in which 47% of providers believed that parents perceived the HPV vaccine to be of little or no importance for 11–12 year olds [12]. With consistently low rates of HPV vaccine uptake among adolescents nationally, interventions to improve use of the vaccine are needed. Among the many barriers to HPV vaccination that have been described, changing providers’ HPV vaccine recommendation practices may be a potentially ‘‘fixable” one [7,25,26]. Indeed, several medical organizations have recently begun to focus on training providers on how to make high quality HPV vaccine recommendations for their adolescent patients [14,25,27,28]. Research in the future will need to examine how these strategies impact HPV vaccination rates, and also whether such strategies have any negative impact on clinical efficiency. Findings from this study should be interpreted in light of several limitations. First, although our sample was heterogeneous with regard to provider training, specialty, and clinic type, the sample was small and regional. Thus, findings from this study may not be generalizable to other geographic locations. Second, while we used expert input and published literature to create the list of HPV vaccine communication tools assessed in this study, this list is likely not exhaustive. Some providers may effectively use other HPV vaccine communication tools that were not assessed in this study. Mitigating this concern somewhat is the opportunity that providers had in the study to report in a free text space ‘‘other”
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communication tools used– few were listed and those that listed were similar to the tool categories queried directly. Additionally, in this survey we did not assess ‘‘how” tools were used, which is likely to vary substantially between providers, although we did capture this information from a subset of providers in qualitative interviews that were also part of the baseline assessment in the larger trial study (unpublished data). Finally, our measures of tool use, quality of HPV vaccine recommendations, and time spent discussing the HPV vaccine may be subject to recall bias as we did not observe these outcomes prospectively. Relatedly, social desirability bias could have led providers to overestimate how frequently they were engaging in recommended immunization practices and using communication tools. However, the consistency of our findings with a concomitant survey of parents from these providers’ offices, and with national data on provider HPV vaccine recommendation strategies is reassuring. 5. Conclusions Many providers spend a significant amount of time discussing HPV vaccines with hesitant parents, yet fail to give high quality HPV vaccine recommendations. Moreover, providers currently use few tools between visits to convey HPV vaccine information to parents, and when communication tools are used either during or between visits, they are associated with longer HPV vaccine discussion times. Better engagement with existing tools and/or new tools that are effective at improving provider HPV vaccine recommendation quality, and are also time efficient, are needed to increase adolescent HPV vaccination levels. Funding This work was supported by the Centers for Disease Control and Prevention (5U01 IP 000801-03). The opinions expressed in this manuscript do not necessarily reflect those of the funding agency. References [1] Reagan-Steiner S et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years - United States, 2015. MMWR Morb Mortal Wkly Rep 2016;65(33):850–8. [2] Koh HK, Blakey CR, Roper AY. Healthy People 2020: a report card on the health of the nation. JAMA 2014;311(24):2475–6. [3] Viens LJ et al. Human papillomavirus-associated cancers - United States, 2008– 2012. MMWR Morb Mortal Wkly Rep 2016;65(26):661–6. [4] Rahman M et al. Provider recommendation mediates the relationship between parental human papillomavirus (HPV) vaccine awareness and HPV vaccine initiation and completion among 13- to 17-year-old U.S. adolescent children. Clin Pediatr (Phila) 2015;54(4):371–5. [5] Ylitalo KR, Lee H, Mehta NK. Health care provider recommendation, human papillomavirus vaccination, and race/ethnicity in the US National Immunization Survey. Am J Public Health 2013;103(1):164–9. [6] Lau M, Lin H, Flores G. Factors associated with human papillomavirus vaccineseries initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health. Vaccine 2012;30 (20):3112–8. [7] Gilkey MB et al. Provider communication and HPV vaccination: the impact of recommendation quality. Vaccine 2016. [8] Rickert VI et al. The role of parental attitudes and provider discussions in uptake of adolescent vaccines. Vaccine 2015;33(5):642–7. [9] Clark SJ et al. Parent perception of provider interactions influences HPV vaccination status of adolescent females. Clin Pediatr (Phila) 2015. [10] Rand CM et al. Patient-provider communication and human papillomavirus vaccine acceptance. Clin Pediatr (Phila) 2011;50(2):106–13. [11] Gilkey MB et al. Physician communication about adolescent vaccination: how is human papillomavirus vaccine different? Prev Med 2015;77:181–5. [12] Gilkey MB et al. Quality of physician communication about human papillomavirus vaccine: findings from a national survey. Cancer Epidemiol Biomarkers Prev 2015. [13] Center for Disease Control and Prevention, N.C.f.I.a.R.D., Health Communications Office, You are the Key to HPV Cancer Prevention: Communicating about HPV. 2014 Sept 30, 2014]; Available from:
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[14] National Cancer Institute, President’s Cancer Panel Annual Report, Accelerating HPV Vaccine Uptake: Urgency for Action to Prevent Cancer. A Report to the President of the United States from the President’s Cancer Panel. 2014: Bethesda, MD. [15] American Academy of Pediatrics. Give a strong recommendation for HPV vaccine to increase uptake. 2015 1/15/16]; Available from:
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