ABSTRACT
We described the relative contributions of parental intention and provider recommendation style to HPV and meningococcal vaccine receipt. Parent-child dyads that were eligible for both meningococcal and HPV vaccines participated in pre-visit surveys and consented to audio recording of their clinical interactions with healthcare providers related to vaccination. Surveys were analyzed for parent and child demographics and parental intention to vaccinate children with HPV and/or meningococcal vaccines. Audio recordings were analyzed for provider recommendation style, defined as indicated (provider stated vaccine was due at that visit) or not, and for child receipt of vaccines. Linear and logistic regression models were used to determine the relative contributions of parental intention and provider recommendation style to vaccine receipt. 56 parents/child dyads participated. 79% of children received HPV vaccines, and 93% received meningococcal vaccines. After controlling for demographic variables, parental intention did not differ by vaccine type. However, providers were less likely to use an indicated recommendation for HPV than for meningococcal vaccine. After controlling for demographic factors, parental intention, and provider recommendation style, vaccine type (HPV or meningococcal) was no longer associated with vaccine receipt Differences that were previously attributed to vaccine-specific factors may be explained by parents’ and providers’ roles in vaccine receipt. These findings suggest that interventions and policy recommendations regarding adolescent vaccination should focus on increasing parental demand for vaccines and ensuring that providers present all vaccines as the medical standard of care.
KEYWORDS: HPV Vaccine, meningococcal vaccine, parental intention, provider recommendation
Introduction
Current literature regarding adolescent vaccination indicates that both parental intention to vaccinate1-4 and provider vaccine presentation5-7 contribute substantially to whether or not a child receives a vaccine. Both parents’ pre-existing attitudes about vaccination and the words that providers use when discussing vaccines determine whether children receive vaccines at their medical visits. As such, both have been identified as targets for public health interventions to increase vaccination rates.
Three vaccines are currently recommended at ages 11–12: the tetanus, diphtheria, and pertussis booster (Tdap), the meningococcal vaccine, and the Human Papillomavirus (HPV) vaccine. The vast majority of children receive Tdap and meningococcal vaccines as recommended, but HPV vaccination rates are frequently 20% lower – even though national guidelines recommend that children receive all three vaccines at the same visit.8 Parents appear to have more hesitations about the HPV vaccine, including apprehension about vaccinating against a sexually transmitted infection and safety concerns largely based on unsubstantiated stories that are widely promulgated on social media.2,9-12 Providers are also more hesitant when recommending the HPV vaccine,13,14 in part because they anticipate negative responses from parents to their recommendations, especially because the vaccine protects against a sexually transmitted disease.15-17 In contrast, meningococcal vaccines have received little media attention and are generally perceived as widely accepted by both providers and parents.
While research has identified both parental intention and provider recommendation as points of potential public health intervention,18-21 little is known about their relative contributions to the receipt of different adolescent vaccines at the same visit and therefore their efficacy as targets for intervention. In this study, we compare the HPV and meningococcal vaccines to examine the contributions of parental intention and provider recommendation style to the receipt of the two vaccines. Studying the relationships of parental intention and provider recommendation with different vaccines within the same visit presents a unique opportunity for understanding their relative contributions to vaccine receipt and to identify how best to increase vaccination rates.
Results
Descriptive statistics
The children in this study were 32% White, 39% Hispanic, 18% Black and 11% Other (Table 1). Household income ranged from less than $25,000 to more than $200,000; 38% of families had an income of less than $25,000, 21% had an income between $25,001 and $50,000, and 29% had a household income greater than $50,001. Seven people did not report their household incomes. More than half of the parents (55%) reported having attended at least some college. Most of the parents/guardians who accompanied the children were female (79%), while participating children were more evenly split at 57% male and 43% female.
Table 1.
VARIABLE | Percentage | N = 56 |
---|---|---|
Child’s Race/Ethnicity (n = 56) | ||
Black | 17.86% | 10 |
Hispanic | 39.29% | 22 |
Other | 10.71% | 6 |
White | 32.14% | 18 |
Child’s Sex (n = 56) | ||
Female | 42.86% | 24 |
Male | 57.14% | 32 |
Child’s Age (Years) (n = 56) | ||
11–12 | 80.36% | 45 |
13–14 | 16.07% | 9 |
15+ | 3.57% | 2 |
Parent’s Race/Ethnicity (n = 56) | ||
Black | 17.86% | 10 |
Hispanic | 37.50% | 21 |
Other | 7.14% | 4 |
White | 37.50% | 21 |
Parent’s Sex (n = 56) | ||
Female | 78.57% | 44 |
Male | 21.43% | 12 |
Parent’s Age (Years) (n = 53) | ||
Mean: 41.30 | ||
Standard deviation: 7.21 | ||
Range: 29–60 | ||
Parent’s Education (n = 56) | ||
Less than high school | 21.43% | 12 |
High school or GED | 23.21% | 13 |
Associate’s degree/some college | 41.07% | 23 |
Bachelor’s degree | 7.14% | 4 |
Graduate or professional degree | 7.14% | 4 |
Household Income (n = 49) | ||
Less than $25,000 | 37.50% | 21 |
$25,001-$50,000 | 21.43% | 12 |
$50,001-$75,000 | 10.71% | 6 |
$75,001-$100,000 | 14.29% | 8 |
Greater than $100,000 | 3.57% | 2 |
Prior to the medical visit, about 45% of parents indicated that they were likely or very likely to vaccinate against HPV, about 38% were undecided, and about 18% were unlikely or very unlikely (Table 2). For the meningococcal vaccine, about 57% of parents were likely or very likely to vaccinate, about 32% were undecided, and 11% were unlikely or very unlikely. Sixty-six percent of parent-child dyads received an indicated presentation for the HPV vaccine compared to 91% receiving an indicated presentation for the meningococcal vaccine. After speaking with medical providers, 79% of parents agreed to HPV vaccination and 93% agreed to meningococcal vaccination for their child at that visit.
Table 2.
VARIABLE | Percentage | N = 56 |
---|---|---|
Parent’s Intent to Vaccinate Prior to the Visit (n = 56) | ||
HPV | ||
Very likely | 21.43% | 12 |
Likely | 23.21% | 13 |
Undecided | 37.50% | 21 |
Unlikely | 10.71% | 6 |
Very unlikely | 7.14% | 4 |
meningococcal | ||
Very likely | 26.79% | 15 |
Likely | 30.36% | 17 |
Undecided | 32.14% | 18 |
Unlikely | 5.36% | 3 |
Very unlikely | 5.36% | 3 |
Provider’s Vaccine Presentation (n = 56) | ||
HPV | ||
Indicated | 66.07% | 37 |
Elective | 26.79% | 15 |
Contraindicated | 7.14% | 4 |
Meningococcal | ||
Indicated | 91.07% | 51 |
Elective | 7.14% | 4 |
Contraindicated | 1.79% | 1 |
Child Received Vaccine at Visit (n = 56) | ||
HPV | ||
Yes | 78.57% | 44 |
No | 21.43% | 12 |
Meningococcal | ||
Yes | 92.86% | 52 |
No | 7.14% | 4 |
After adjusting for child and parent sex and parent education, parental intention to vaccinate was not significantly different for the HPV and meningococcal vaccines (Table 3). The random effects linear regression model adjusted for demographic variables indicates that the mean parental intention score was 3.674 for the meningococcal vaccine on a scale from 1 (very unlikely) to 5 (very likely). In comparison, the parental intention score for HPV vaccine was 0.286 lower, but the difference was not statistically significant (95% CI −0.623–0.087; p = 0.136; Table 3). In contrast, providers were nearly four times more likely to present the HPV vaccine as elective or contraindicated compared to the meningococcal vaccine (Table 4). The logistic regression model adjusted for demographic variables indicated a risk ratio of 3.82 (95% CI 1.68–6.75), indicating that providers were less likely to use effective vaccine presentations for HPV compared to meningococcal vaccines.
Table 3.
Variable | Coefficient* | Robust Standard Error | P-Value | 95% Confidence Interval |
---|---|---|---|---|
Vaccine Type (Reference = Meningococcal vaccine) | ||||
HPV | −0.268 | 0.177 | 0.136 | −0.623–0.087 |
Child Sex (Reference = Male) | ||||
Female | −0.121 | 0.246 | 0.625 | −0.614–0.372 |
Parent Sex (Reference = Male) | ||||
Female | −0.016 | 0.240 | 0.947 | −0.497–0.465 |
Parent Education (Reference = High school or less) | ||||
Some college or greater | 0.125 | 0.248 | 0.617 | −0.372–0.622 |
Meningococcal Vaccine Intention Score | 3.674 | 0.283 | 0.000 | 3.108–4.240 |
Observations | 112 | 112 | 112 | 112 |
*The reference intention score is 3.674 out of 5 on a scale ranging from very unlikely to very likely to receive the meningococcal vaccine at the current visit. Coefficients represent the increment in the intention score associated with the variable; they are calculated by adding the coefficient to the reference score. For example, the average parental intention for HPV vaccine was 3.674 + (−0.268) = 3.406.
The model is adjusted for vaccine type (HPV vs. meningococcal) child sex (female vs. male), parent sex (female vs. male) and parental education (high school or less vs. > high school).
Interpretation: After adjusting for child and parent sex and parent education, parents were similarly likely to intend to vaccinate their children with the HPV and meningococcal vaccines.
Table 4.
Variable | Risk Ratio | 95% Confidence Interval | p-value |
---|---|---|---|
HPV Vaccine Presentation | 3.82 | 1.68, 6.75 | 0.002 |
Child Sex (Female) | 1.18 | 0.49, 2.63 | 0.704 |
Parent Sex (Female) | 1.10 | 0.36, 2.93 | 0.854 |
Parent education (>High School) | 0.74 | 0.29, 1.75 | 0.52 |
*The reference group is provider presentation for meningococcal vaccination for male children with a male parent with an education level of high school or less.
Interpretation: We estimated a logistic regression model of provider presentation of vaccine as elective or contraindicated vs. indicated on vaccine type, child sex, parent sex, and parent education. Model estimates were used to obtain risk ratios associated with each covariate. The risk ratio of 3.82 for HPV vaccination indicates that providers were 3.82 times more likely to present HPV vaccination as elective or contraindicated than meningococcal vaccination.
The final adjusted logistic regression model displayed in Table 5 examines HPV and meningococcal vaccine receipt adjusted for presentation and parental intention to vaccinate as well as the demographic covariates of child sex, parent sex, and parent education level. In Model 1, after adjusting for demographic variables alone, children were 17% less likely to receive the HPV than the meningococcal vaccine (risk ratio [RR] 0.83; 95% CI 0.53–0.99). However, in Model 2, after adjusting for parental intention and provider presentation style, children’s likelihood of receiving HPV and meningococcal vaccines did not differ significantly (RR 0.96; 95% 0.68–1.05). In Model 2, each one-point increase in parental intention score was associated with a 5% increase in the likelihood of vaccination (RR 1.05; 95% CI 1.03–1.07). In contrast, non-indicated provider presentation was associated with half the vaccination rate of indicated presentations (RR 0.52, 95% CI 0.15–0.90).
Table 5.
Variable | Model 1 Risk Ratio and 95% CI |
Model 2 Risk Ratio and 95% CI |
---|---|---|
HPV Vaccine Received | 0.83 (0.53 to 0.99) | 0.96 (0.68 to 1.05) |
Child Sex (Female) | 0.90 (0.66 to 1.01) | 0.80 (0.42 to 1.00) |
Parent Sex (Female) | 0.94 (0.63 to 1.05) | 0.93 (0.51 to 1.05) |
Parent Education (>High School) | 0.89 (0.63 to 1.02) | 0.76 (0.35 to 0.99) |
Parental Intention | 1.05 (1.03 to 1.07) | |
Provider Presentation | 0.52 (0.15, 0.90) |
Note: We estimated two models of receipt of vaccination with different combination of covariates.
Model 1: Adjusted for child sex, parent sex and parent education level.
Model 2: Adjusted for child sex, parent sex, parent education level, provider presentation of vaccine, and parental intention to vaccine
Interpretation: When adjusting for demographic variables only, children are less likely to receive HPV vaccination than meningococcal vaccination (Model 1). After additionally adjusting for provider presentation and parental intention (Model 2), receipt of HPV and meningococcal vaccines are equally likely.
Discussion
The analyses reported here address an important knowledge gap: quantifying the relative contributions of parental intention and provider recommendation style to vaccine receipt within the same visit. Previous studies of parents have largely relied on surveys to analyze intentions and recommendations, and providers in particular have been asked about their perceptions and experiences as a whole rather than in regards to specific visits.15,16,21 We add to the literature by using prospectively collected survey data and audio recordings of visits, which decreases reliance on parents’ and providers’ memories of past conversations. We are further able to compare the parental intention and provider presentation style for HPV and meningococcal vaccines within the same visit, thus limiting potential differences in conversations based on characteristics of unique parents, patients, and providers.
Interestingly, we did not find significant differences in parental intention to receive HPV compared with meningococcal vaccines, nor did intention vary by patient demographic characteristics. However, providers were four times more likely to give an ineffective recommendation for HPV compared to meningococcal vaccination – irrespective of patient demographics. Together with literature on providers’ perceptions of parental barriers, these results suggest that providers’ perceptions of parents’ intentions, rather than parents’ actual intentions, may be a more significant factor in the depression of vaccination rates.13,22,23 Finally, we found that it was the parents’ intentions and the providers’ recommendations that accounted for observed differences in HPV and meningococcal vaccination rates. This indicates that both public education around vaccine benefits and targeted provider education on effective recommendations may be crucial to improving vaccination rates, independent of vaccine type. Though educational interventions aimed at parents have generally shown limited impact,24 one recent study indicated benefit to educating parents through tailored videos during medical visits.25 Culturally tailored interventions also show promise, though more research is needed.26-28 In the era of social media, respected public health organizations with an online presence aimed at parents are also important for changing perceptions.29
In the U.S., HPV vaccine initiation rates are approximately 20% lower than meningococcal vaccination rates, although both vaccines are recommended for co-administration at the ages of 11–12.8 State-by-state differences in HPV and meningococcal vaccination rates range from <10% to 30%;8 the gap in our study, at 14%, falls within this range. Many studies have examined vaccine type and patient demographic information such as sex, age, and race/ethnicity to better understand reasons for disparities in vaccination rates.2,8,30 While data on parental knowledge and attitudes are mixed, provider recommendation is crucial to parental acceptance of HPV and other vaccinations.6,15,31-33 Studies have indicated a role for training providers in effective communication techniques,5,34 with less impact noted for parent education.35 Our analysis supports a stronger role for provider recommendation, but indicate that parental intentions around vaccination also contribute to vaccine utilization. Therefore both could be targets for vaccination efforts.
This study is limited by a small sample size and limited geographic sampling area. Although we believe our sample is representative of the patients in the recruitment sites, replication of our analysis using alternative sampling methods would help assess potential sampling errors. As the role of covariates on the outcomes (i.e., effect size) may differ across subpopulations served by differed providers, further study of patients from other sites is needed In addition, data were insufficient to include provider demographics in the analyses. We chose to compare HPV and meningococcal vaccines because both were recommended for adolescents per the national vaccine schedule, and therefore covered by insurance or federally subsidized, yet neither was required for middle or high school entry in the states where our recruitment sites were located. However, additional unmeasured factors may affect vaccine receipt, and analysis of different vaccines could yield different results.
Conclusion
After accounting for parental intention and provider presentation style, vaccine type does not significantly affect vaccine receipt. We found that differences that were previously attributed to vaccine-specific factors may be explained by parents’ and providers’ roles in vaccine receipt. These findings suggest that interventions and policy recommendations regarding adolescent vaccination should focus on increasing parental demand for vaccines and ensuring that providers present all vaccines as the medical standard of care.
Data and methods
Setting, recruitment, and eligibility
As part of a multi-site intervention study, we recruited participants for surveys and audio recordings of clinical interactions at eight urban and suburban pediatric and family medicine clinics in the Northeastern United States between May 2015 and March 2018. Patient populations were racially, ethnically, and socioeconomically diverse. Study protocols, including patient and provider recruitment, audio recording, survey collection, and qualitative data analysis have been described previously.7 The institutional review boards of both Boston University Medical Center and Harvard University approved this study.
Parent-child dyads were eligible for inclusion if the parent spoke English or Spanish and the child was due to start the HPV vaccine series. Providers were eligible if they were seeing an eligible parent-child dyad. Almost all eligible providers (98.5%; n = 132 of 134) and 80% of eligible parent-child dyads (n = 208 of 261) agreed to participate in the larger study. For this analysis, we limited the sample to parent-child pairs that met the following criteria: 1) children were eligible for both their first HPV and meningococcal vaccines, 2) parent-child pairs indicated in the pre-visit survey their intentions to vaccinate for both the HPV and meningococcal vaccines, and 3) providers initiated discussion about both the HPV and meningococcal vaccines. We then excluded one more parent-child pair because the parent’s education level, which was a covariate in our analyses, was missing, resulting in a sample size of fifty-six parent-child pairs spread across thirty-nine of the participating providers.
Study data
This study focused on self-reported parent and child demographic data and parental intention scores from pre-visit surveys, provider recommendation styles from audio recordings, and vaccine receipt, as noted in audio recordings and post-visit surveys. Demographic information included parent and child age, race, sex, and country of origin; parent education level and preferred language (English or Spanish), and household income. Parental intention to vaccinate was measured by asking parents to assess their likelihood of accepting HPV and meningococcal vaccination at the current visit rated on five-level Likert scales ranging from very unlikely to very likely.
Provider vaccine presentation style was determined through qualitative analysis of audio recordings as described previously.7 Briefly, provider presentations were coded as ‘indicated’ if they clearly recommended that vaccination should occur at that visit, e.g. “Your child is due for vaccines today.” Presentations were coded as ‘elective’ if providers were non-directive and framed vaccination as optional, e.g. “If you want to start today, you can, or you can wait until next year.” In rare cases, providers recommended that vaccination be delayed to a future visit; this was coded as ‘contraindicated.’
Statistical analysis
We first investigated patient and parent demographic factors associated with a) parental intention for children to receive the HPV and/or meningococcal vaccines, and b) provider recommendation style for both vaccines. We then investigated the effects of patient and parent demographics, parental intention, and provider recommendation style on the receipt of HPV and meningococcal vaccines.
To perform these analyses, we developed an analytic data set with two observations per patient, one for HPV vaccine and another for meningococcal vaccine outcomes. We estimated multivariate linear and logistic regression models to measure the adjusted differences in the three outcomes between the vaccine types. We specified random effects at the patient level for each model to account for clustering of the two observations for each patient.36 For instance, for the outcome of parental intention to vaccinate, we estimated a random effects linear regression model with an indicator of vaccine type and patient demographics as covariates. The coefficient for the HPV vaccine type indicates the adjusted difference in parental intention to vaccinate compared to the meningococcal vaccine. For the other two outcomes – provider presentation style and receipt of vaccination, both of which are dichotomous, we estimated analogous logistic regression models. For the outcome of receipt of vaccination we estimated a broader model that also included parental intention to vaccinate and provider presentation style as covariates. This gives the difference in likelihood of receipt of each vaccination type after adjusting for these two additional covariates. We report 95% confidence level for the estimates. All estimation was performed using Stata version 14.1.37
We performed preliminary analyses to determine the final form of the key covariates (continuous vs. categorical vs. dichotomous) (results not shown). First, we compared incorporating parental education as a continuous versus dichotomous variable (high school graduate or less vs. at least some college); as no substantive differences were noted, the dichotomous variable was retained for simplicity of presentation. Second, we treated parental intention Likert scores as continuous (very unlikely to unlikely to undecided to likely to very likely) in all statistical models because we found systematic increasing/decreasing association using categorical specifications. Third, we explored how to categorize provider presentation. Our prior work showed that ‘indicated’ vaccine presentations were associated with higher likelihood of vaccination than ‘elective’ or ‘contraindicated’ presentations.7 We found no difference in the results using all three presentation categories vs. using a dichotomous ‘indicated’ vs. ‘not indicated’ measure, so the dichotomous measure was retained for simplicity of presentation. Finally, we adjust for child’s sex, parent’s sex, and parental education in all models. We include child’s sex because the HPV vaccine is predominantly known as the vaccine that protects against cervical cancer, which exclusively affects females, so parents of male children may approach vaccination differently from parents of female children.38 Parent’s sex is included because husbands often defer to their wives when making medical decisions about their children.39 We include parental education because highly educated parents are more likely to question vaccine recommendations.40,41 We also tested different combinations of demographic variables, and confirmed that adjusting for the above variables gave the best-fit models. Parallel analyses including patient age (9 to 17) as a covariate indicated that age was not significantly associated with any of the outcome measures, nor did it affect the other covariate estimates; therefore, we have reported findings without patient age as a covariate.
Funding Statement
This work was supported by an American Cancer Society Research Scholar Grant [grant number 128607-RSG-15-150-01-CPHPS]. No commercial support was obtained.
Acknowledgments
The authors would like to acknowledge Sara Waugh for her early contributions to the project.
Disclosure of potential conflicts of interest
The authors have no financial relationships relevant to this article to disclose.
Non-standard abbreviations
Human Papillomavirus (HPV)
References
- 1.Barnack JL, Reddy DM, Swain C.. Predictors of parents’ willingness to vaccinate for human papillomavirus and physicians’ intentions to recommend the vaccine. Womens Health Issues. 2010;20(1):28–34. doi: 10.1016/j.whi.2009.08.007. [DOI] [PubMed] [Google Scholar]
- 2.Perkins RB, Lin M, Silliman RA, Clark JA, Hanchate A. Why are u.s. Girls getting meningococcal but not human papilloma virus vaccines? Comparison of factors associated with human papilloma virus and meningococcal vaccination among adolescent girls 2008 to 2012. Womens Health Issues. 2015;25(2):97–104. doi: 10.1016/j.whi.2014.12.005. [DOI] [PubMed] [Google Scholar]
- 3.Mohammed KA, Vivian E, Loux TM, Arnold LD. Factors associated with parents’ intent to vaccinate adolescents for human papillomavirus: findings from the 2014 national immunization survey–teen. Prev Chronic Dis [Internet]. 2017;14 [accessed. 2018 October 4]. http://www.cdc.gov/pcd/issues/2017/16_0314.htm. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Perkins RB, Pierre-Joseph N, Marquez C, Iloka S, Clark JA. Why do low-income minority parents choose human papillomavirus vaccination for their daughters? J Pediatr. 2010;157:617–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Brewer NT, Hall ME, Malo TL, Gilkey MB, Quinn B, Lathren C. Announcements versus conversations to improve HPV vaccination coverage: a randomized trial. Pediatrics. 2017;139:1. doi: 10.1542/peds.2016-1764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Hirth JM, Fuchs EL, Chang M, Fernandez ME, Berenson AB. 2019. Variations in reason for intention not to vaccinate across time, region, and by race/ethnicity, NIS-Teen (2008–2016). Vaccine. 2019. Jan 21;37(4):595–601. doi: 10.1016/j.vaccine.2018.12.017. Epub 2018 Dec 21 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Fenton AT, Eun TJ, Clark JA, Perkins RB. 2018. Indicated or elective? The association of providers' words with HPV vaccine receipt. Hum Vaccin Immunother. 2018;14(10):2503–2509. doi: 10.1080/21645515.2018.1480237. Epub 2018 Jun 28 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Walker TY, Elam-Evans LD, Yankey D, Markowitz LE, Williams CL, Mbaeyi SA, Fredua B, Stokley S. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years - United States, 2017. MMWR Morb Mortal Wkly Rep. 2018;67(33):909–17. doi: 10.15585/mmwr.mm6731e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Dorell C, Yankey D, Kennedy A, Stokley S. Factors that influence parental vaccination decisions for adolescents, 13 to 17 years old: national immunization survey-teen, 2010. Clin Pediatr (Phila). 2013;52(2):162–70. doi: 10.1177/0009922812468208. [DOI] [PubMed] [Google Scholar]
- 10.Kasting ML, Shapiro GK, Rosberger Z, Kahn JA, Zimet GD. Tempest in a teapot: A systematic review of HPV vaccination and risk compensation research. Hum Vaccin Immunother. 2016;12(6):1435–50. doi: 10.1080/21645515.2016.1141158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Ernst K, Shelby A. Social media in the exam room: stories of human papillomavirus disease and prevention. Acad Pediatr. 2018;18(2):S19–20. doi: 10.1016/j.acap.2017.05.002. [DOI] [PubMed] [Google Scholar]
- 12.Faasse K, Porsius JT, Faasse J, Martin LR. Bad news: the influence of news coverage and Google searches on Gardasil adverse event reporting. Vaccine. 2017;35:6872–78. [DOI] [PubMed] [Google Scholar]
- 13.Rosen BL, Shepard A, Kahn JA. US health care clinicians’ knowledge, attitudes, and practices regarding human papillomavirus vaccination: a qualitative systematic review. Acad Pediatr. 2018;18:S53–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Rutten LJF, Sauver JL St, Beebe TJ, Wilson PM, Jacobson DJ, Fan C, Breitkopf CR, Vadaparampil ST, Jacobson RM. Clinician knowledge, clinician barriers, and perceived parental barriers regarding human papillomavirus vaccination: association with initiation and completion rates. Vaccine. 2017;35(1):164–69. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Gilkey MB, Malo TL, Shah PD, Hall ME, Brewer NT. Quality of physician communication about human papillomavirus vaccine: findings from a national survey. Cancer Epidemiol Biomarkers Prev. 2015;24(11):1673–79. doi: 10.1158/1055-9965.EPI-15-0326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Vadaparampil ST, Kahn JA, Salmon D, Lee JH, Quinn GP, Roetzheim R, Bruder K, Malo TL, Proveaux T, Zhao X, et al. Missed clinical opportunities: provider recommendations for HPV vaccination for 11–12 year old girls are limited. Vaccine. 2011;29(47):8634–41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Perkins RB, Clark JA, Apte G, Vercruysse JL, Sumner JJ, Wall-Haas CL, Rosenquist AW, Pierre-Joseph N. Missed opportunities for HPV vaccination in adolescent girls: a qualitative study. Pediatrics. 2014;134(3):e666–674. doi: 10.1542/peds.2014-0442. [DOI] [PubMed] [Google Scholar]
- 18.Tom A, Robinett H, Buenconsejo-Lum L, et al. Promoting and providing HPV vaccination in Hawaii: barriers faced by health providers. J Community Health. 2016;41(5):1069–77. doi: 10.1007/s10900-016-0183-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Kulczycki A, Qu H, Shewchuk R. Recommend, but also discuss: different patterns of physician-perceived barriers to discussing HPV vaccination and their association with vaccine administration in 11–12 year-old girls. Matern Child Health J. 2016;20(12):2539–47. doi: 10.1007/s10995-016-2079-9. [DOI] [PubMed] [Google Scholar]
- 20.Javaid M, Ashrawi D, Landgren R, Stevens L, Bello R, Foxhall L, Mims M, Ramondetta L. Human papillomavirus vaccine uptake in Texas pediatric care settings: a statewide survey of healthcare professionals. J Community Health. 2017;42(1):58–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among US adolescents: a systematic review of the literature. JAMA Pediatr. 2014;168(1):76–82. doi: 10.1001/jamapediatrics.2013.2752. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Perkins RB, Clark JA. Providers’ perceptions of parental concerns about HPV vaccination. J Health Care Poor Underserved. 2013;24(2):828–39. doi: 10.1353/hpu.2013.0080. [DOI] [PubMed] [Google Scholar]
- 23.Healy CM, Montesinos DP, Middleman AB. Parent and provider perspectives on immunization: are providers overestimating parental concerns? Vaccine. 2014;32(5):579–84. doi: 10.1016/j.vaccine.2013.11.076. [DOI] [PubMed] [Google Scholar]
- 24.Beavis AL, Levinson KL. Preventing cervical cancer in the United States: barriers and resolutions for HPV vaccination. Front Oncol [Internet] 2016;6 [accessed 2019 February 5];http://journal.frontiersin.org/article/10.3389/fonc.2016.00019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Dixon BE, Zimet GD, Xiao S, Tu W, Lindsay B, Church A, Downs SM. An educational intervention to improve HPV vaccination: a cluster randomized trial. Pediatrics. 2019;143:1. doi: 10.1542/peds.2018-1457. [DOI] [PubMed] [Google Scholar]
- 26.Galbraith KV, Lechuga J, Jenerette CM, Moore LAD, Palmer MH, Hamilton JB. Parental acceptance and uptake of the HPV vaccine among African-Americans and Latinos in the United States: a literature review. Soc Sci Med. 2016;159:116–26. doi: 10.1016/j.socscimed.2016.04.028. [DOI] [PubMed] [Google Scholar]
- 27.Cruz DMRI, Tsark JAU, Chen JJ, Albright CL, Braun KL. Human papillomavirus (HPV) vaccination motivators, barriers, and brochure preferences among parents in multicultural Hawai‘i: a qualitative study. J Cancer Educ. 2017;32(3):613–21. doi: 10.1007/s13187-015-0901-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Joseph NP, Bernstein J, Pelton S, Belizaire M, Goff G, Horanieh N, Freund KM. Brief client-centered motivational and behavioral intervention to promote HPV vaccination in a hard-to-reach population: a pilot randomized controlled trial. Clin Pediatr (Phila). 2016;55(9):851–59. doi: 10.1177/0009922815591885. [DOI] [PubMed] [Google Scholar]
- 29.Reiter PL, Gerend MA, Gilkey MB, Perkins RB, Saslow D, Stokley S, Tiro JA, Zimet GD, Brewer NT. Advancing human papillomavirus vaccine delivery: 12 priority research gaps. Acad Pediatr. 2018;18(2S):S14–6. doi: 10.1016/j.acap.2017.04.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Perkins RB, Brogly SB, Adams WG, Freund KM. Correlates of human papillomavirus vaccination rates in low-income, minority adolescents: a multicenter study. J Womens Health (Larchmt). 2012;21(8):813–20. doi: 10.1089/jwh.2011.3305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Perkins RB, Clark JA. What affects human papillomavirus vaccination rates? A qualitative analysis of providers’ perceptions. Womens Health Issues. 2012;22(4):e379–86. doi: 10.1016/j.whi.2012.04.001. [DOI] [PubMed] [Google Scholar]
- 32.Perkins RB, Chigurupati NL, Apte G, Vercruysse J, Wall-Haas C, Rosenquist A, Lee L, Clark JA, Pierre-Joseph N. Why don't adolescents finish the HPV vaccine series? A qualitative study of parents and providers. Hum Vaccin Immunother. 2016. Jun 2;12(6):1528–35. doi: 10.1080/21645515.2015.1118594. Epub 2016 Jan 25 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Opel DJ, Robinson JD, Heritage J, Korfiatis C, Taylor JA, Mangione-Smith R. Characterizing providers’ immunization communication practices during health supervision visits with vaccine-hesitant parents: a pilot study. Vaccine. 2012;30(7):1269–75. doi: 10.1016/j.vaccine.2011.12.129. [DOI] [PubMed] [Google Scholar]
- 34.Perkins RB, Zisblatt L, Legler A, Trucks E, Hanchate A, Gorin SS. Effectiveness of a provider-focused intervention to improve HPV vaccination rates in boys and girls. Vaccine. 2014. [Internet] http://www.ncbi.nlm.nih.gov/pubmed/25448095. [DOI] [PubMed] [Google Scholar]
- 35.Kaufman J, Ryan R, Walsh L, Horey D, Leask J, Robinson P, Hill S. Face-to-face interventions for informing or educating parents about early childhood vaccination. Cochrane Database Syst Rev [Internet] 2018. [accessed. 2018 November1]. http://doi.wiley.com/10.1002/14651858.CD010038.pub3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Twisk J. Applied longitudinal data analysis for epidemiology: a practical guide, 2nd ed. Cambridge, UK: Cambridge University Press; 2013. [Google Scholar]
- 37.StataCorp Stata statistical software: release 14. College Station (TX): StataCorp LP; 2016. [Google Scholar]
- 38.Perkins RB, Apte G, Marquez C, Porter C, Belizaire M, Clark JA, Pierre-Joseph N. Factors affecting human papillomavirus vaccine use among white, black and latino parents of sons. Pediatr Infect Dis J. 2013;32(1):e38–44. doi: 10.1097/INF.0b013e31826f53e3. [DOI] [PubMed] [Google Scholar]
- 39.Wall G, Arnold S. How involved is involved fathering?: an exploration of the contemporary culture of fatherhood. Gender Soc. 2007;21(4):508–27. doi: 10.1177/0891243207304973. [DOI] [Google Scholar]
- 40.Mendel-Van Alstyne JA, Nowak GJ, Aikin AL. What is ‘confidence’ and what could affect it?: A qualitative study of mothers who are hesitant about vaccines. Vaccine. 2018;36(44):6464–72. doi: 10.1016/j.vaccine.2017.09.007. [DOI] [PubMed] [Google Scholar]
- 41.Swaney SE, Burns S. Exploring reasons for vaccine-hesitancy among higher-SES parents in Perth, Western Australia. Health Promot J Aust [Internet] 2018. [accessed. 2018 November26]. http://doi.wiley.com/10.1002/hpja.190. [DOI] [PubMed] [Google Scholar]