Implementation and Evaluation of a School-Based Human Papillomavirus Vaccination Program in Rural Kentucky Robin C. Vanderpool, DrPH,1 Patrick J. Breheny, PhD,2 Peggy A. Tiller, RN, BSN,3 Carol A. Huckelby3 Amy D. Edwards, RN, MSN,3 Kristi D. Upchurch, RN,3 Cynthia A. Phillips, RN,3 Christine F. Weyman, MD, PhD3 Introduction: Human papillomavirus (HPV) vaccination rates remain marginal across the U.S., including Kentucky, a state recognized for increased HPV-related cancer burden. School-based HPV immunization programs may be a viable approach to improving vaccination initiation and completion rates among youth. Therefore, the purpose of this study was to design, implement, and evaluate a school-based HPV vaccination program conducted in rural south-central Kentucky. Methods: Guided by evidence-based approaches to increasing immunization rates, the practical expertise of school nursing staff, and a detailed study protocol, academic and health department– based investigators implemented an HPV vaccination project in two high schools during the 2012– 2013 academic year; data were analyzed in 2013–2014. Rates of returned parental consent forms, parental consent/declination, and HPV vaccination rates were documented. Results: At the beginning of the school year, all 935 students at the two schools were given HPV vaccination parental consent forms. Five hundred eleven students returned consent forms (55% return rate), and 447 of these students were HPV vaccine naïve (87%). Of these students, 315 (70%) initiated the vaccine series, with 276 (62%) completing the entire three-dose series, so that 88% of students initiating the vaccine series successfully completed the series. In estimating rates for the entire school body, 45% of students had received all three doses by the end of the project. Conclusions: Despite study design limitations, results of this project provide further evidence about school-based immunization programs as an effective strategy for improving HPV vaccination rates among Kentucky and U.S. adolescents. (Am J Prev Med 2015;49(2):317–323) & 2015 American Journal of Preventive Medicine
Introduction
T
o aid in the prevention of human papillomavirus (HPV)-related diseases, including genital warts and cervical cancer, the Advisory Committee on Immunization Practices (ACIP) currently recommends the threedose HPV vaccine for male and female 11- and 12-year-olds and catch-up vaccination for unvaccinated female youth From the 1Department of Health Behavior, College of Public Health, University of Kentucky, Lexington, Kentucky; 2Department of Biostatistics, College of Public Health, University of Iowa, Iowa City, Iowa; and 3Lake Cumberland District Health Department, Somerset, Kentucky Address correspondence to: Robin C. Vanderpool, DrPH, Department of Health Behavior, University of Kentucky College of Public Health, 2365 Harrodsburg Road, Suite A230, Lexington KY 40504. E-mail: robin@ kcr.uky.edu. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2015.05.001
& 2015 American Journal of Preventive Medicine
aged 13–26 years and unvaccinated male youth aged 13–21 years.1,2 However, HPV vaccination rates remain marginal across the country. Nationally, in 2013, 57% of adolescent girls had received Dose 1, and only 38% completed the three-dose series.3 Only 35% of adolescent boys received Dose 1 in 2013, and only 14% completed the full series.3 Kentucky, a state recognized for increased HPV-related cancer burden,4–6 remains below national estimates in terms of HPV vaccination. In 2013, 48% of female adolescents received Dose 1 and 27% completed the full series. Only 19% and 11% of male adolescents received Dose 1 and 2, respectively, representing some of the lowest male HPV vaccination rates in the country.3 Initiation and completion of the HPV vaccine remains an obvious public health challenge,7,8 requiring innovative strategies and partnerships. An evidence-based strategy for increasing adolescent immunization rates is the offering of vaccines in school
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settings. Other countries have achieved impressive increases in adolescent HPV vaccination rates by using schools as the primary delivery method for vaccination.14,17–25 In the U.S., however, HPV vaccination policies vary, and school-based vaccination initiatives often require partnerships among public health departments, school officials, and academic researchers.13,26–28 Notably, school-based services can immunize significant numbers of adolescents by removing barriers related to access to health care, cost, separate medical appointments, parental time away from work, student absenteeism, transportation, and parental presence.8,9,12,13,26,29–31 Moreover, school programs can provide students, parents, and school administration with vaccine education.8,10,32–34 However, school immunization programs are not without challenges. For example, obtaining school leadership support and parental consent may prove difficult; education of school personnel is required; billing for services when children are ineligible for the Vaccines for Children (VFC) program is problematic; developing and maintaining vaccination tracking systems is necessary for medical record keeping and project evaluation purposes; and sustainability is challenging.15,26,29,32,33,35 Similar to most states, Kentucky currently lacks a statewide mandate requiring HPV vaccination for school entry. However, health agencies may proactively provide HPV vaccination in school settings with the support of school leadership. One such agency is the Lake Cumberland District Health Department (LCDHD), a regional public health department covering ten medically underserved counties in rural south-central Kentucky. Although population-based HPV vaccination rates are not available in Kentucky owing to limitations of the Kentucky Immunization Registry (i.e., voluntary data contributions from local health departments and VFC providers, and non-mandatory reporting of HPV vaccination), internal health department records suggested adolescent HPV vaccination rates in the region were lower than state and national estimates. From a socioeconomic perspective, in 2011, the percentage of children eligible for free or reduced-price meals in each county ranged from 61% to 76% across the district,36 serving as a proxy measure for the number of VFC-eligible students. Given these factors and the fact that the health department is one of the few HPV vaccination providers in the district, LCDHD partnered with faculty from the University of Kentucky (UK) to design, implement, and evaluate the impact of a school-based HPV vaccination program on vaccine initiation and completion among students in two high schools during the 2012–2013 school year. The purpose of this article is to describe the program’s systematic approach and methods, present findings, and discuss the strengths and limitations of the project.
Methods School Participation The LCDHD invited four area high schools to participate in the project; area middle schools were not considered for the program because of limited community and parental support for HPV vaccination among preadolescents in the region, despite this age group being ideal candidates for vaccination. Two high schools—located in the same rural-designated county—agreed to participate in the program. One of the high schools serves the county seat (i.e., city school district) and had a student enrollment of 222, including 29 minority students, whereas the other high school serves the broader county (i.e., county school district) and had a student enrollment of 713, with 26 minority students. Although the two schools differed in total enrollment, the schools were comparable in the number of minority students and the percentage of students eligible for free or reduced-price meals (65% and 70%, respectively), and their school nurses were LCDHD employees.
Intervention Components and Logistics Guided by evidence- and practice-based strategies, the program involved multiple components to impact vaccination rates and reduce known immunization barriers.11 First, the nurses recommended including HPV educational materials and parental consent forms in students’ back-to-school packets. Nurses also used the high schools’ “One Call” telephone reminder system to contact all parents/guardians listed in the schools’ student records database during the first month of school to inform them about the program and encourage return of consent forms; the phone system also was used to remind parents about their child’s subsequent receipt of Doses 2 and 3. Additionally, nurses delivered HPV information to students and parents through an informational booth at school orientation, classroom settings, newspaper articles, school website postings, and special events (e.g., football games). Grant-funded incentives were used to increase student participation, including T-shirts, pizza and sub sandwich parties, and prize drawings. Students helped to design small media materials; for example, students designed posters and banners emblazoned with the student-coined slogan “Spread the Word, Not the Disease: Get Your Vaccine.” Lastly, a community advocate who had lost her daughter to cervical cancer at age 22 years was invited to speak to the students at a special event. In terms of programmatic logistics, staff developed a protocol that outlined a project timeline; recruitment procedures; processes for consent form tracking; eligibility criteria for vaccination (e.g., parental consent, no clinical contraindications) and VFC status; vaccination tracking procedures; a scheduling algorithm for delivering the three-dose series (at 0, 2, and 6 months); student retention strategies; procedures for documenting adverse vaccine reactions and other student/parental concerns; and plans to send home an updated vaccination record at the end of the school year. Related to the study timeline, the majority of students could be vaccinated with all three doses of HPV4 (Gardasil) during the school year (versus summer months, when students are more transient).37 Dose 1 would be available through December 1, 2012, allowing for 4 months of vaccine initiation (August–November); the majority of students were subsequently vaccinated with Doses 1 and 2 in the fall of 2012 and Dose 3 in the winter of 2013. Nurses facilitated grade-specific immunization clinics during the school day, providing advanced notice to school administration. Finally, similar to other school immunization programs,26 staff determined that all students would www.ajpmonline.org
Vanderpool et al / Am J Prev Med 2015;49(2):317–323 be able to participate in the program and secured extra vaccine stock for students who were ineligible for VFC (e.g., private insurance). This inclusion criterion was an important component of the project given the fact that during the project period, school nurses in Kentucky were not allowed to bill private insurance companies. If the vaccine had only been given to VFC-eligible children, staff were concerned that (C Weyman, LCDHD, personal communication, 2014) (1) the project could have increased the stigma of low-SES adolescents as candidates for a sexually transmitted disease (prevention) vaccine; and (2) school leadership would not have approved project participation if all students were not offered the opportunity to be vaccinated.
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All procedures were approved by the Kentucky Cabinet for Health and Family Services’ IRB.
Data Collection All 935 students at the two intervention schools were given a parental consent form in August 2012. Of those, 511 (54.7%) returned the form (Figure 1). Sex and grade for nearly all of the 935 students were known (Table 1). For students who returned forms, the nurses were able to document each student’s vaccination consent status, reason for declination (if available), VFC status, insurance type, and HPV vaccination status (Table 1). For students receiving consent to be vaccinated, the date of HPV vaccine administration for each dose was recorded as well as any vaccination side effects (e.g., syncope) or reasons for incomplete vaccination during the project period (e.g., pregnancy).
Statistical Analysis
Figure 1. Study design, sample sizes, and outcomes. August 2015
The primary analysis focused on the 447 students who returned the consent form and had not received any doses of the vaccine (i.e., HPV vaccine naïve). Of these 447 unvaccinated students, 329 (74%) received consent to be vaccinated (Figure 1). We considered rates of initiation (students who received at least one dose of the vaccine) and completion (students who received all three doses of the vaccine). A Bayesian approach to inference was taken, with uniform priors for initiation and completion rates, and 95% Credible Intervals (roughly speaking, the Bayesian equivalent of a Confidence Interval) were calculated from the posterior distribution for all vaccination rates of interest. The analysis of initiation and completion rates among consenting students was straightforward based on the conjugate relationship between the binomial data and uniform prior. Measures of significance (p) comparing rates between various groups are based on posterior predictive p-values for the null model.38 Estimation of schoolwide initiation and completion rates was less straightforward, as the number of vaccinated students in the entire student population was unknown. Corresponding to the study time frame, we estimated this number based on 2012 national adolescent
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Table 1. Characteristics of Students From Participating High Schools According to Consent Response Rate (N¼935) Non-responders
Responders
n¼424 (%)
n¼511 (%)
Female
210 (50)
240 (47)
Male
211 (50)
271 (53)
Characteristic Sex
Missing
3
Grade 9
109 (26)
142 (28)
10
123 (29)
128 (25)
11
113 (27)
116 (23)
12
79 (19)
124 (24)
Missing
1
Insurance status Insured
114 (22)
Medicaid/KCHIP
182 (36)
No insurance
22 (4)
Underinsured
28 (5)
Unknown Prior doses (baseline)
165 (32) a
0
447 (87)
1
9 (2)
2
5 (1)
3
50 (10)
a
Number of doses of the HPV vaccine that the student received prior to the start of the intervention. HPV, human papillomavirus; KCHIP, Kentucky Children’s Health Insurance Program.
HPV vaccination rates reported by CDC.39 Uncertainty about this number was carried through to all subsequent calculations and is reflected in the width of the 95% CIs. We also conducted separate analyses of male and female students based on the historic rollout of the vaccine (i.e., ACIP issued initial HPV vaccination guidance for female patients in 2007 and for male patients in 2010) and the marked differences in HPV vaccination rates between male and female Kentucky adolescents. All analyses were carried out in 2013– 2014 using R, version 3.2.0, and the UK Office of Research Integrity approved all de-identified secondary data analyses.
observed between the two schools in terms of initiation, completion, or consent. We first documented the vaccine status of the 511 students who returned consent forms: Fifty (10%) had already completed the HPV vaccine series; 14 (3%) had initiated the series (i.e., Doses 1, 2, or both); and 447 (87%) were considered HPV vaccine naïve (Figure 1). Of the vaccine-naïve students, 315 (70%) initiated the series (i.e., received at least one dose), with 276 (62%) completing all three doses (Figure 1). Stated differently, 88% of students initiating the series as part of the school-based program successfully completed all three doses. Furthermore, of the 14 students who had previously initiated the vaccine series, 12 (86%) completed it (Figure 1).
Initiation and Completion The primary purpose of this study was to measure the initiation and completion rates among students participating in the school-based program. The percentages reported in the previous section (70% initiation, 62% completion) overstate the success of the program because they do not account for the 424 students who did not return a consent form (and thus were not vaccinated by the school program). Although the number of nonresponding vaccine-naïve students is unknown, we estimate it as described in the Methods section and properly account for the uncertainty in this estimate when presenting CIs for initiation and completion. Table 2 presents estimates and 95% CIs for the number of students who completed at least one (“initiation”) and all three (“completion”) HPV vaccine doses. We estimate that at the beginning of the academic year, only 14% of students had received all three doses of the HPV vaccine. As part of the school program, 36% of eligible students (i.e., those who were not already vaccinated) were vaccinated; as a result, 45% of students had received all Table 2. Overall HPV Vaccination (Initiation and Completion) Rates
Time points Baselinea Vaccinated Final
Results Summary Statistics Data from the two high schools were combined to present overall vaccination initiation and completion rates for the project; no significant differences were
c
b
Initiation (1 dose)
Completion (3 doses)
Rate, % (95% CI)
Rate, % (95% CI)
24 (20, 27)
14 (12, 17)
44 (40, 48)
36 (33, 39)
57 (53, 61)
45 (42, 49)
a
Baseline, percentage of students vaccinated prior to the start of the intervention. b Vaccinated, percentage of eligible students vaccinated during the intervention period (i.e., those who were not already vaccinated). c Final, percentage of students vaccinated by the end of the intervention period. CI, credible interval; HPV, human papillomavirus.
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three doses by the end of the project. We did not observe any significant differences between grades in terms of either initiation or completion. Stratifying the analysis by sex revealed that female students were far more likely than male students to have already received the vaccine at the outset of the program, although the percentage of eligible students initiating vaccination and completing all three doses during the study was similar for both sexes (Table 3).
Discussion Findings suggest that the program was successful in improving HPV vaccination initiation and completion rates among adolescents in two rural Kentucky high schools. Specifically, of the HPV vaccine–naïve students receiving consent to be vaccinated, 96% initiated the series and 84% completed the full regimen. Moreover, almost 90% of students who started the vaccine series completed it, demonstrating the feasibility of using school-based vaccination programs to successfully navigate adolescents from initiation through series completion during an academic year.9 These findings are comparable to a school-based HPV vaccine initiative in North Carolina that achieved an 80% completion rate among middle school girls who started the vaccine series.27 In order to meaningfully measure the success of the program, it is essential to estimate vaccination rates for the entire school population. If the program vaccinated 100% of students who consented but only ten students Table 3. HPV Vaccination (Initiation and Completion) Rates According to Student Sex Initiation (1 dose)
Completion (3 doses)
Rate, % (95% CI)
Rate, % (95% CI)
11 (8, 15)
4 (2, 6)
Vaccinated
40 (36, 45)
33 (29, 37)
Finalc
47 (42, 52)
36 (32, 40)
39 (34, 45)
27 (22, 32)
Vaccinated
42 (36, 48)
33 (28, 38)
c
64 (59, 70)
50 (45, 56)
Time points Male Baselinea b
Female Baselinea b
Final a
Baseline, percentage of students vaccinated prior to the start of the intervention. b Vaccinated, percentage of eligible students vaccinated during the intervention period (i.e., those who were not already vaccinated). c Final, percentage of students vaccinated by the end of the intervention period. CI, credible interval; HPV, human papillomavirus.
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consented, then it hardly could be considered a success. Estimating initiation and completion rates for this entire “intent-to-treat” population involves making assumptions about non-responding students. Though difficult to verify empirically without labor-intensive follow-up of non-responders, our approach of assuming baseline vaccination rates for non-responders were similar to 2012 national estimates seems reasonable. A case could be made that this overestimates (or underestimates) the actual vaccination rates of our non-responders; to investigate, we carried out a sensitivity analysis (Appendix Tables 1–3). Although the baseline and final estimates are affected by this assumption, the percentage of eligible students vaccinated as part of the school-based program, particularly those completing the full series, remains fairly stable. Regardless of the vaccination rate among non-responders, the program was clearly successful in vaccinating a substantial proportion of the unvaccinated student population. Furthermore, our uncertainty about this assumption is reflected in the CIs presented in Tables 2 and 3.
Strengths and Limitations There are numerous strengths as well as recognized limitations to the current project that must be outlined, especially when considering generalizability, replicability, and adaptation by others. One of the primary strengths of the project was the coupling of evidenceand practice-based strategies into the design, implementation, and evaluation of an HPV vaccine–specific program that immunized more than 300 adolescents. Additionally, all students, regardless of their financial circumstance, were provided the opportunity to be vaccinated at no cost. In terms of logistics, parents did not have to be present during immunization delivery as has been required by other school districts.27 Although the study did not use an experimental control design, the project and its varying components represent a plausible model and partnership that may be replicated by local public health departments and area schools.27 Several project limitations must also be acknowledged. First, we did not have access to the vaccination status for those students who did not return a consent form; however, we observed no significant differences in grade or sex between students who returned the consent forms and those who did not (data not shown). Second, the 55% return rate for the HPV vaccination consent forms was significantly lower than expected; based on previous experiences with health-related consent forms (e.g., permission to administer medications) the staff expected the majority of forms to be returned. Challenges with consent form return has also been documented by
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others ; in our case, the fact that the HPV vaccination consent form was separate from the standard health-related consent form may have proved problematic. Relatedly, we did not directly assess parents’ perceptions of the school program, although its overall success may indicate high acceptability among this group of rural parents, specifically for high school–delivered HPV vaccination.41,42 Third, it would have been beneficial to conduct a cost-effectiveness analysis as well as parse exactly which program components contributed to its success. Fourth, the study was conducted in only two schools for 1 year, and the investigative team did not have a comparison group of schools/students that did not receive the vaccination program, which is a significant limitation to the current study, our interpretation of study findings, and broader applicability to other adolescent populations or school settings. We also were unable to enumerate how many students would have been vaccinated between baseline and final time points without the intervention because of maturation. Maturation may be especially true for adolescent boys given the notable increases in male HPV vaccination rates (both initiation and completion) at the national level between 2012 and 2013 (2012 Kentucky data are unavailable).3,39 However, it is interesting to note that HPV vaccination rates (both initiation and completion) among female adolescents in Kentucky decreased between 2012 and 2013.3,39 Lastly, there may be concern regarding the study’s generalizability, particularly as it relates to replicating a similar project without adequate funding and vaccine supply for non–VFC eligible youth. However, it is plausible that this project could be conducted with in-kind health department personnel and school nurse effort and with minimal (if any) incentives. There are intermediary vaccine vendors now available to assist public health departments with vaccine procurement and billing for privately insured patients in school-based settings.43
Conclusions The results of this project provide further evidence for the use of school-based immunization programs to improve HPV vaccination rates for Kentucky and U.S. adolescents. Promotion and facilitation of vaccination in venues outside the medical home are warranted to improve population-based HPV vaccination rates and prevent subsequent HPV-related disease among youth. Following this recommendation, implementation and rigorous evaluation of school-based HPV vaccination programs, including cost-effectiveness analyses and improved generalizability, deserve more research and attention.
This study was supported in part by a research grant from the Investigator-Initiated Studies Program of Merck Sharp & Dohme Corporation to the Lake Cumberland District Health Department (IISP 40305). Merck had no involvement in the study design; collection, analysis, and interpretation of data; the writing of the manuscript; or the decision to submit the manuscript for publication. No financial disclosures were reported by the authors of this paper.
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30. Daley MF, Curtis CR, Pyrzanowski J, et al. Adolescent immunization delivery in school-based health centers: a national survey. J Adolesc Health. 2009;45(5):445–452. http://dx.doi.org/10.1016/j.jadohealth. 2009.04.002. 31. Brown DS, Arnold SE, Asay G, et al. Parent attitudes about schoollocated influenza vaccination clinics. Vaccine. 2014;32(9): 1043–1048. http://dx.doi.org/10.1016/j.vaccine.2014.01.003. 32. Reiter PL, Stubbs B, Panozzo CA, Whitesell D, Brewer NT. HPV and HPV vaccine education intervention: effects on parents, healthcare staff, and school staff. Cancer Epidemiol Biomarkers Prev. 2011;20(11): 2354–2361. http://dx.doi.org/10.1158/1055-9965.EPI-11-0562. 33. Lindley MC, Boyer-Chu L, Fishbein DB, et al. The role of schools in strengthening delivery of new adolescent vaccinations. Pediatrics. 2008;121(suppl 1):S46–S54. http://dx.doi.org/10.1542/peds.2007-1115F. 34. Nodulman JA, Starling R, Kong AS, et al. Investigating stakeholder attitudes and opinions on school-based human papillomavirus vaccination programs. J Sch Health. 2015;85(5):289–298. 35. Moss JL, Feld AL, O’Malley B, et al. Opportunities for increasing human papillomavirus vaccine provision in school health centers. J Sch Health. 2014;84(6):370–378. http://dx.doi.org/10.1111/josh.12158. 36. Kids Count Data Center. Children Eligible for Free or Reduced-Price Meals, Kentucky. Annie E. Casey Foundation. 2011. http://datacenter. kidscount.org/data/tables/3805-children-eligible-for-free-or-reducedprice-meals#detailed/2/any/false/867,133,38,35,18/any/10845,10846. Accessed January 9, 2014. 37. Gold R, Naleway AL, Jenkins LL, et al. Completion and timing of the three-dose human papillomavirus vaccine series among adolescents attending school-based health centers in Oregon. Prev Med. 2011;52 (6):456–458. http://dx.doi.org/10.1016/j.ypmed.2011.04.010. 38. Rubin DB. Bayesianly justifiable and relevant frequency calculations for the applied statistician. Ann Stat. 1984;12(4):1151–1172. http://dx.doi.org/10. 1214/aos/1176346785. 39. CDC. National and state vaccination coverage among adolescents aged 13-17 years—United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62(34):685–693. 40. Middleman AB, Short MB, Doak JS. Focusing on flu: Parent perspectives on school-located immunization programs for influenza vaccine. Hum Vaccin Immunother. 2012;8(10):1395–1400. http://dx.doi.org/10. 4161/hv.21575. 41. Gargano LM, Weiss P, Underwood NL, et al. School-located vaccination clinics for adolescents: correlates of acceptance among parents. J Community Health. 2014. http://dx.doi.org/10.1007/s10900-014-9982z Epub ahead of print. 42. McRee AL, Reiter PL, Pepper JK, Brewer NT. Correlates of comfort with alternative settings for HPV vaccine delivery. Hum Vaccin Immunother. 2013;9(2):306–313. http://dx.doi.org/10.4161/hv.22614. 43. VaxCare Corporation. Public health departments. www.vaxcare.com/ health-departments.html. Accessed April 3, 2015.
Appendix Supplementary data Supplementary data associated with this article can be found at, http://dx.doi.org/10.1016/j.amepre.2015.05.001.
Introduction
T
o aid in the prevention of human papillomavirus (HPV)-related diseases, including genital warts and cervical cancer, the Advisory Committee on Immunization Practices (ACIP) currently recommends the threedose HPV vaccine for male and female 11- and 12-year-olds and catch-up vaccination for unvaccinated female youth From the 1Department of Health Behavior, College of Public Health, University of Kentucky, Lexington, Kentucky; 2Department of Biostatistics, College of Public Health, University of Iowa, Iowa City, Iowa; and 3Lake Cumberland District Health Department, Somerset, Kentucky Address correspondence to: Robin C. Vanderpool, DrPH, Department of Health Behavior, University of Kentucky College of Public Health, 2365 Harrodsburg Road, Suite A230, Lexington KY 40504. E-mail: robin@ kcr.uky.edu. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2015.05.001
& 2015 American Journal of Preventive Medicine
aged 13–26 years and unvaccinated male youth aged 13–21 years.1,2 However, HPV vaccination rates remain marginal across the country. Nationally, in 2013, 57% of adolescent girls had received Dose 1, and only 38% completed the three-dose series.3 Only 35% of adolescent boys received Dose 1 in 2013, and only 14% completed the full series.3 Kentucky, a state recognized for increased HPV-related cancer burden,4–6 remains below national estimates in terms of HPV vaccination. In 2013, 48% of female adolescents received Dose 1 and 27% completed the full series. Only 19% and 11% of male adolescents received Dose 1 and 2, respectively, representing some of the lowest male HPV vaccination rates in the country.3 Initiation and completion of the HPV vaccine remains an obvious public health challenge,7,8 requiring innovative strategies and partnerships. An evidence-based strategy for increasing adolescent immunization rates is the offering of vaccines in school
Published by Elsevier Inc.
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settings. Other countries have achieved impressive increases in adolescent HPV vaccination rates by using schools as the primary delivery method for vaccination.14,17–25 In the U.S., however, HPV vaccination policies vary, and school-based vaccination initiatives often require partnerships among public health departments, school officials, and academic researchers.13,26–28 Notably, school-based services can immunize significant numbers of adolescents by removing barriers related to access to health care, cost, separate medical appointments, parental time away from work, student absenteeism, transportation, and parental presence.8,9,12,13,26,29–31 Moreover, school programs can provide students, parents, and school administration with vaccine education.8,10,32–34 However, school immunization programs are not without challenges. For example, obtaining school leadership support and parental consent may prove difficult; education of school personnel is required; billing for services when children are ineligible for the Vaccines for Children (VFC) program is problematic; developing and maintaining vaccination tracking systems is necessary for medical record keeping and project evaluation purposes; and sustainability is challenging.15,26,29,32,33,35 Similar to most states, Kentucky currently lacks a statewide mandate requiring HPV vaccination for school entry. However, health agencies may proactively provide HPV vaccination in school settings with the support of school leadership. One such agency is the Lake Cumberland District Health Department (LCDHD), a regional public health department covering ten medically underserved counties in rural south-central Kentucky. Although population-based HPV vaccination rates are not available in Kentucky owing to limitations of the Kentucky Immunization Registry (i.e., voluntary data contributions from local health departments and VFC providers, and non-mandatory reporting of HPV vaccination), internal health department records suggested adolescent HPV vaccination rates in the region were lower than state and national estimates. From a socioeconomic perspective, in 2011, the percentage of children eligible for free or reduced-price meals in each county ranged from 61% to 76% across the district,36 serving as a proxy measure for the number of VFC-eligible students. Given these factors and the fact that the health department is one of the few HPV vaccination providers in the district, LCDHD partnered with faculty from the University of Kentucky (UK) to design, implement, and evaluate the impact of a school-based HPV vaccination program on vaccine initiation and completion among students in two high schools during the 2012–2013 school year. The purpose of this article is to describe the program’s systematic approach and methods, present findings, and discuss the strengths and limitations of the project.
Methods School Participation The LCDHD invited four area high schools to participate in the project; area middle schools were not considered for the program because of limited community and parental support for HPV vaccination among preadolescents in the region, despite this age group being ideal candidates for vaccination. Two high schools—located in the same rural-designated county—agreed to participate in the program. One of the high schools serves the county seat (i.e., city school district) and had a student enrollment of 222, including 29 minority students, whereas the other high school serves the broader county (i.e., county school district) and had a student enrollment of 713, with 26 minority students. Although the two schools differed in total enrollment, the schools were comparable in the number of minority students and the percentage of students eligible for free or reduced-price meals (65% and 70%, respectively), and their school nurses were LCDHD employees.
Intervention Components and Logistics Guided by evidence- and practice-based strategies, the program involved multiple components to impact vaccination rates and reduce known immunization barriers.11 First, the nurses recommended including HPV educational materials and parental consent forms in students’ back-to-school packets. Nurses also used the high schools’ “One Call” telephone reminder system to contact all parents/guardians listed in the schools’ student records database during the first month of school to inform them about the program and encourage return of consent forms; the phone system also was used to remind parents about their child’s subsequent receipt of Doses 2 and 3. Additionally, nurses delivered HPV information to students and parents through an informational booth at school orientation, classroom settings, newspaper articles, school website postings, and special events (e.g., football games). Grant-funded incentives were used to increase student participation, including T-shirts, pizza and sub sandwich parties, and prize drawings. Students helped to design small media materials; for example, students designed posters and banners emblazoned with the student-coined slogan “Spread the Word, Not the Disease: Get Your Vaccine.” Lastly, a community advocate who had lost her daughter to cervical cancer at age 22 years was invited to speak to the students at a special event. In terms of programmatic logistics, staff developed a protocol that outlined a project timeline; recruitment procedures; processes for consent form tracking; eligibility criteria for vaccination (e.g., parental consent, no clinical contraindications) and VFC status; vaccination tracking procedures; a scheduling algorithm for delivering the three-dose series (at 0, 2, and 6 months); student retention strategies; procedures for documenting adverse vaccine reactions and other student/parental concerns; and plans to send home an updated vaccination record at the end of the school year. Related to the study timeline, the majority of students could be vaccinated with all three doses of HPV4 (Gardasil) during the school year (versus summer months, when students are more transient).37 Dose 1 would be available through December 1, 2012, allowing for 4 months of vaccine initiation (August–November); the majority of students were subsequently vaccinated with Doses 1 and 2 in the fall of 2012 and Dose 3 in the winter of 2013. Nurses facilitated grade-specific immunization clinics during the school day, providing advanced notice to school administration. Finally, similar to other school immunization programs,26 staff determined that all students would www.ajpmonline.org
Vanderpool et al / Am J Prev Med 2015;49(2):317–323 be able to participate in the program and secured extra vaccine stock for students who were ineligible for VFC (e.g., private insurance). This inclusion criterion was an important component of the project given the fact that during the project period, school nurses in Kentucky were not allowed to bill private insurance companies. If the vaccine had only been given to VFC-eligible children, staff were concerned that (C Weyman, LCDHD, personal communication, 2014) (1) the project could have increased the stigma of low-SES adolescents as candidates for a sexually transmitted disease (prevention) vaccine; and (2) school leadership would not have approved project participation if all students were not offered the opportunity to be vaccinated.
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All procedures were approved by the Kentucky Cabinet for Health and Family Services’ IRB.
Data Collection All 935 students at the two intervention schools were given a parental consent form in August 2012. Of those, 511 (54.7%) returned the form (Figure 1). Sex and grade for nearly all of the 935 students were known (Table 1). For students who returned forms, the nurses were able to document each student’s vaccination consent status, reason for declination (if available), VFC status, insurance type, and HPV vaccination status (Table 1). For students receiving consent to be vaccinated, the date of HPV vaccine administration for each dose was recorded as well as any vaccination side effects (e.g., syncope) or reasons for incomplete vaccination during the project period (e.g., pregnancy).
Statistical Analysis
Figure 1. Study design, sample sizes, and outcomes. August 2015
The primary analysis focused on the 447 students who returned the consent form and had not received any doses of the vaccine (i.e., HPV vaccine naïve). Of these 447 unvaccinated students, 329 (74%) received consent to be vaccinated (Figure 1). We considered rates of initiation (students who received at least one dose of the vaccine) and completion (students who received all three doses of the vaccine). A Bayesian approach to inference was taken, with uniform priors for initiation and completion rates, and 95% Credible Intervals (roughly speaking, the Bayesian equivalent of a Confidence Interval) were calculated from the posterior distribution for all vaccination rates of interest. The analysis of initiation and completion rates among consenting students was straightforward based on the conjugate relationship between the binomial data and uniform prior. Measures of significance (p) comparing rates between various groups are based on posterior predictive p-values for the null model.38 Estimation of schoolwide initiation and completion rates was less straightforward, as the number of vaccinated students in the entire student population was unknown. Corresponding to the study time frame, we estimated this number based on 2012 national adolescent
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Table 1. Characteristics of Students From Participating High Schools According to Consent Response Rate (N¼935) Non-responders
Responders
n¼424 (%)
n¼511 (%)
Female
210 (50)
240 (47)
Male
211 (50)
271 (53)
Characteristic Sex
Missing
3
Grade 9
109 (26)
142 (28)
10
123 (29)
128 (25)
11
113 (27)
116 (23)
12
79 (19)
124 (24)
Missing
1
Insurance status Insured
114 (22)
Medicaid/KCHIP
182 (36)
No insurance
22 (4)
Underinsured
28 (5)
Unknown Prior doses (baseline)
165 (32) a
0
447 (87)
1
9 (2)
2
5 (1)
3
50 (10)
a
Number of doses of the HPV vaccine that the student received prior to the start of the intervention. HPV, human papillomavirus; KCHIP, Kentucky Children’s Health Insurance Program.
HPV vaccination rates reported by CDC.39 Uncertainty about this number was carried through to all subsequent calculations and is reflected in the width of the 95% CIs. We also conducted separate analyses of male and female students based on the historic rollout of the vaccine (i.e., ACIP issued initial HPV vaccination guidance for female patients in 2007 and for male patients in 2010) and the marked differences in HPV vaccination rates between male and female Kentucky adolescents. All analyses were carried out in 2013– 2014 using R, version 3.2.0, and the UK Office of Research Integrity approved all de-identified secondary data analyses.
observed between the two schools in terms of initiation, completion, or consent. We first documented the vaccine status of the 511 students who returned consent forms: Fifty (10%) had already completed the HPV vaccine series; 14 (3%) had initiated the series (i.e., Doses 1, 2, or both); and 447 (87%) were considered HPV vaccine naïve (Figure 1). Of the vaccine-naïve students, 315 (70%) initiated the series (i.e., received at least one dose), with 276 (62%) completing all three doses (Figure 1). Stated differently, 88% of students initiating the series as part of the school-based program successfully completed all three doses. Furthermore, of the 14 students who had previously initiated the vaccine series, 12 (86%) completed it (Figure 1).
Initiation and Completion The primary purpose of this study was to measure the initiation and completion rates among students participating in the school-based program. The percentages reported in the previous section (70% initiation, 62% completion) overstate the success of the program because they do not account for the 424 students who did not return a consent form (and thus were not vaccinated by the school program). Although the number of nonresponding vaccine-naïve students is unknown, we estimate it as described in the Methods section and properly account for the uncertainty in this estimate when presenting CIs for initiation and completion. Table 2 presents estimates and 95% CIs for the number of students who completed at least one (“initiation”) and all three (“completion”) HPV vaccine doses. We estimate that at the beginning of the academic year, only 14% of students had received all three doses of the HPV vaccine. As part of the school program, 36% of eligible students (i.e., those who were not already vaccinated) were vaccinated; as a result, 45% of students had received all Table 2. Overall HPV Vaccination (Initiation and Completion) Rates
Time points Baselinea Vaccinated Final
Results Summary Statistics Data from the two high schools were combined to present overall vaccination initiation and completion rates for the project; no significant differences were
c
b
Initiation (1 dose)
Completion (3 doses)
Rate, % (95% CI)
Rate, % (95% CI)
24 (20, 27)
14 (12, 17)
44 (40, 48)
36 (33, 39)
57 (53, 61)
45 (42, 49)
a
Baseline, percentage of students vaccinated prior to the start of the intervention. b Vaccinated, percentage of eligible students vaccinated during the intervention period (i.e., those who were not already vaccinated). c Final, percentage of students vaccinated by the end of the intervention period. CI, credible interval; HPV, human papillomavirus.
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three doses by the end of the project. We did not observe any significant differences between grades in terms of either initiation or completion. Stratifying the analysis by sex revealed that female students were far more likely than male students to have already received the vaccine at the outset of the program, although the percentage of eligible students initiating vaccination and completing all three doses during the study was similar for both sexes (Table 3).
Discussion Findings suggest that the program was successful in improving HPV vaccination initiation and completion rates among adolescents in two rural Kentucky high schools. Specifically, of the HPV vaccine–naïve students receiving consent to be vaccinated, 96% initiated the series and 84% completed the full regimen. Moreover, almost 90% of students who started the vaccine series completed it, demonstrating the feasibility of using school-based vaccination programs to successfully navigate adolescents from initiation through series completion during an academic year.9 These findings are comparable to a school-based HPV vaccine initiative in North Carolina that achieved an 80% completion rate among middle school girls who started the vaccine series.27 In order to meaningfully measure the success of the program, it is essential to estimate vaccination rates for the entire school population. If the program vaccinated 100% of students who consented but only ten students Table 3. HPV Vaccination (Initiation and Completion) Rates According to Student Sex Initiation (1 dose)
Completion (3 doses)
Rate, % (95% CI)
Rate, % (95% CI)
11 (8, 15)
4 (2, 6)
Vaccinated
40 (36, 45)
33 (29, 37)
Finalc
47 (42, 52)
36 (32, 40)
39 (34, 45)
27 (22, 32)
Vaccinated
42 (36, 48)
33 (28, 38)
c
64 (59, 70)
50 (45, 56)
Time points Male Baselinea b
Female Baselinea b
Final a
Baseline, percentage of students vaccinated prior to the start of the intervention. b Vaccinated, percentage of eligible students vaccinated during the intervention period (i.e., those who were not already vaccinated). c Final, percentage of students vaccinated by the end of the intervention period. CI, credible interval; HPV, human papillomavirus.
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consented, then it hardly could be considered a success. Estimating initiation and completion rates for this entire “intent-to-treat” population involves making assumptions about non-responding students. Though difficult to verify empirically without labor-intensive follow-up of non-responders, our approach of assuming baseline vaccination rates for non-responders were similar to 2012 national estimates seems reasonable. A case could be made that this overestimates (or underestimates) the actual vaccination rates of our non-responders; to investigate, we carried out a sensitivity analysis (Appendix Tables 1–3). Although the baseline and final estimates are affected by this assumption, the percentage of eligible students vaccinated as part of the school-based program, particularly those completing the full series, remains fairly stable. Regardless of the vaccination rate among non-responders, the program was clearly successful in vaccinating a substantial proportion of the unvaccinated student population. Furthermore, our uncertainty about this assumption is reflected in the CIs presented in Tables 2 and 3.
Strengths and Limitations There are numerous strengths as well as recognized limitations to the current project that must be outlined, especially when considering generalizability, replicability, and adaptation by others. One of the primary strengths of the project was the coupling of evidenceand practice-based strategies into the design, implementation, and evaluation of an HPV vaccine–specific program that immunized more than 300 adolescents. Additionally, all students, regardless of their financial circumstance, were provided the opportunity to be vaccinated at no cost. In terms of logistics, parents did not have to be present during immunization delivery as has been required by other school districts.27 Although the study did not use an experimental control design, the project and its varying components represent a plausible model and partnership that may be replicated by local public health departments and area schools.27 Several project limitations must also be acknowledged. First, we did not have access to the vaccination status for those students who did not return a consent form; however, we observed no significant differences in grade or sex between students who returned the consent forms and those who did not (data not shown). Second, the 55% return rate for the HPV vaccination consent forms was significantly lower than expected; based on previous experiences with health-related consent forms (e.g., permission to administer medications) the staff expected the majority of forms to be returned. Challenges with consent form return has also been documented by
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others ; in our case, the fact that the HPV vaccination consent form was separate from the standard health-related consent form may have proved problematic. Relatedly, we did not directly assess parents’ perceptions of the school program, although its overall success may indicate high acceptability among this group of rural parents, specifically for high school–delivered HPV vaccination.41,42 Third, it would have been beneficial to conduct a cost-effectiveness analysis as well as parse exactly which program components contributed to its success. Fourth, the study was conducted in only two schools for 1 year, and the investigative team did not have a comparison group of schools/students that did not receive the vaccination program, which is a significant limitation to the current study, our interpretation of study findings, and broader applicability to other adolescent populations or school settings. We also were unable to enumerate how many students would have been vaccinated between baseline and final time points without the intervention because of maturation. Maturation may be especially true for adolescent boys given the notable increases in male HPV vaccination rates (both initiation and completion) at the national level between 2012 and 2013 (2012 Kentucky data are unavailable).3,39 However, it is interesting to note that HPV vaccination rates (both initiation and completion) among female adolescents in Kentucky decreased between 2012 and 2013.3,39 Lastly, there may be concern regarding the study’s generalizability, particularly as it relates to replicating a similar project without adequate funding and vaccine supply for non–VFC eligible youth. However, it is plausible that this project could be conducted with in-kind health department personnel and school nurse effort and with minimal (if any) incentives. There are intermediary vaccine vendors now available to assist public health departments with vaccine procurement and billing for privately insured patients in school-based settings.43
Conclusions The results of this project provide further evidence for the use of school-based immunization programs to improve HPV vaccination rates for Kentucky and U.S. adolescents. Promotion and facilitation of vaccination in venues outside the medical home are warranted to improve population-based HPV vaccination rates and prevent subsequent HPV-related disease among youth. Following this recommendation, implementation and rigorous evaluation of school-based HPV vaccination programs, including cost-effectiveness analyses and improved generalizability, deserve more research and attention.
This study was supported in part by a research grant from the Investigator-Initiated Studies Program of Merck Sharp & Dohme Corporation to the Lake Cumberland District Health Department (IISP 40305). Merck had no involvement in the study design; collection, analysis, and interpretation of data; the writing of the manuscript; or the decision to submit the manuscript for publication. No financial disclosures were reported by the authors of this paper.
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Appendix Supplementary data Supplementary data associated with this article can be found at, http://dx.doi.org/10.1016/j.amepre.2015.05.001.
