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Article

Effect of an HPV Vaccination Multi-Level, Multi-Component Program on HPV Vaccination Initiation and Completion in a Pediatric Clinic Network

by
Lara S. Savas
1,*,
Ross Shegog
1,
Erica L. Frost
1,
C. Mary Healy
2,
Dale S. Mantey
3,
Sharon P. Coan
1,
L. Aubree Shay
4,
Travis A. Teague
1,
Juan J. Ferreris
5,
Sharice M. Preston
1,† and
Sally W. Vernon
1
1
Center for Health Promotion and Prevention Research, UTHealth Houston School of Public Health, Houston, TX 77030, USA
2
Department of Pediatrics, Infectious Diseases Section, Baylor College of Medicine, Houston, TX 77030, USA
3
Michael & Susan Dell Center for Healthy Living, UTHealth Houston School of Public Health in Austin, Austin, TX 78701, USA
4
Center for Health Promotion and Prevention Research, UTHealth Houston School of Public Health in San Antonio, San Antonio, TX 78229, USA
5
Christus Health, Children’s General Pediatric Clinic, San Antonio, TX 78257, USA
*
Author to whom correspondence should be addressed.
†
Deceased author.
Vaccines 2024, 12(5), 510; https://doi.org/10.3390/vaccines12050510
Submission received: 26 February 2024 / Revised: 13 April 2024 / Accepted: 23 April 2024 / Published: 8 May 2024
(This article belongs to the Special Issue Recent Research on Human Papillomavirus (HPV) Infection and Vaccination)
Browse Figures
Versions Notes

Abstract

:
Despite clear evidence of the public health benefits of the human papillomavirus (HPV) vaccine in preventing HPV-related cancers and genital warts, underutilization of HPV vaccination in the United States persists. Interventions targeting multi-level determinants of vaccination behavior are crucial for improving HPV vaccination rates. The study’s purpose was to implement and evaluate the adapted Adolescent Vaccination Program (AVP), a clinic-based, multi-level, multi-component intervention aimed at increasing HPV vaccine initiation and completion rates in a five-clinic pediatric network in Bexar County, Texas. The adaptation process was guided by established frameworks and involved formative work with clinic stakeholders. The study utilized a quasi-experimental single group pre- and post- study design, with an external comparison data using the National Immunization Survey-Teen (NIS-Teen) datasets for the same time period to examine the AVP’s effect on HPV vaccination initiation and completion. A series of interrupted time series analyses (ITSA) compared the clinic system patient outcomes (HPV vaccination initiation and completion rates) in the post-intervention to the general adolescent population (NIS-Teen). Of the 6438 patients (11–17 years) with clinic visits during the 3-year study period, HPV vaccination initiation rates increased from 64.7% to 80.2% (p < 0.05) and completion rates increased from 43.2% to 60.2% (p < 0.05). The AVP was effective across various demographic and economic subgroups, demonstrating its generalizability. ITSA findings indicated the AVP improved HPV vaccination initiation and completion rates in clinic settings and that AVP strategies facilitated resilience during the pandemic. The minimal adaptation required for implementation in a new clinic system underscores its feasibility and potential for widespread adoption.

1. Introduction

The public health benefit of the human papillomavirus (HPV) 9-valent vaccine is clear in its opportunity to prevent infection of 9 HPV types, which cause an estimated 90% of cervical and anal cancers [1,2,3], 70% of oropharyngeal cancer [4], 75% vaginal cancer [2], 69% of vulvar cancers [2], 63% of penile cancers [2], and 90% of genital warts [2,5]. By preventing nine high-risk HPV infections, the HPV 9-valent vaccine has the potential to prevent approximately 34,400 new cases of HPV-associated cancers in the United States (U.S.) each year [6]. However, each year in the U.S., approximately 196,000 women are diagnosed with high-grade cervical dysplasia [7], 360,000 men and women are affected by genital warts [8], 1.4 million women are diagnosed with low-grade cervical dysplasia [9], and over three million abnormal cervical cancer Pap screenings [9,10]. While the Centers for Disease Control and Prevention (CDC) [11], American Cancer Society [12], and American Academy of Pediatrics [13] recommend completion of the HPV vaccination series by 13 years of age to prevent HPV-related cancers and related morbidity in males and females, HPV vaccine initiation rates fall far below other adolescent vaccines recommended at the same age (i.e., Tdap and meningococcal) [14]. Moreover, after 2018, HPV vaccine series completion, or HPV-up-to-date (HPV-UTD: >3 doses or >2 doses when the first dose was initiated before age 15 years) rates, have stagnated [14] with most states attaining below 50% HPV-UTD rates [15]. In 2022, the national HPV-UTD rate for males 13–17 years (60.6%) [16] and females 13–17 years (64.6%) [16] was far below the Healthy People 2030 goal of 80% [17].
HPV vaccination coverage (with >1 dose) and completion rates differ by ethnicity/race [18]. Minority Hispanic/Latino, Black, and American Indian/Alaskan Native youth have demonstrated greater coverage compared to non-Hispanic (NH) White and NH Asian youth [16,19]. While minority HPV-UTD rates have historically been reported as lower [20], most recent data suggest the NH White HPV-UTD rates now lag behind all minority groups, except for female Hispanics [21].
System-, provider-, and parent-level barriers to HPV vaccination include lack of consistent patient reminders of when vaccination is due, lack of clinician awareness of vaccine-eligible youth and associated missed opportunities, lower parental knowledge about vaccine dosing or scheduling, and inadequate patient-provider communication that alleviates vaccine hesitancy [14]. Evidence for system-, provider- and parent-targeted strategies to mitigate these barriers has been established. Strategies include system-level changes to electronic health records to routinize provider prompts to recommend HPV vaccination and audit and feedback strategies [22], provider-level interventions to promote effective provider communication (including presumptive, bundled, and/or unqualified provider recommendations) [23], and patient reminders [24] and parent education [25] aimed at parent determinants. There is also modest evidence for the implementation of parent- and patient-focused apps to promote HPV education and vaccination [26,27,28].
Emerging evidence suggests the strength of using multiple intervention strategies through multi-level and multi-component (MLMC) clinic-based intervention approaches to address the complex factors affecting vaccination at the clinic system (organization), provider, and parent levels [29,30,31,32]. Recent studies indicate that implementing these evidence-based interventions concurrently has a synergistic impact on HPV vaccination rates [33,34,35]. The Community Preventive Services Task Force (CPSTF), also known as the ‘Community Guide’, offers compelling evidence for the effectiveness of these intervention strategies in increasing vaccination rates [36]. Our team developed and evaluated the clinic-based MLMC intervention called the Adolescent Vaccination Program (AVP) to address the need for evidence-based MLMC HPV vaccination interventions designed for clinic organizations to implement to reach diverse patient populations. The AVP comprises six evidence-based strategies that target clinic systems, providers, and parents (Figure 1). AVP development was guided by the Intervention Mapping systematic approach [37], informed by behavioral theory (i.e., Social Cognitive Theory [38], Theory of Reasoned Action [39], Health Belief Model) [40], and guided by formative work with clinic leadership, providers (pediatricians and medical assistants) and parents [41], to increase provider delivery of consistent, bundled (when possible), presumptive and unqualified HPV vaccination recommendations [42].
We previously demonstrated that the AVP effectively increased HPV vaccination initiation in a 51-clinic pediatric network in Houston, Texas [43]. The patient population in the original study was primarily privately insured (80.3%), identified as English speakers (93.1%), and was demographically diverse (44.4% non-Hispanic White, 24.8% Hispanic and 13.8% Hispanic, and among 17% ethnicity was unknown). The purpose of this study was to adapt, implement, and evaluate the AVP’s effect on HPV vaccination initiation and completion in a five-clinic pediatric network. The new clinic setting comprised a primarily insured, English-speaking, and largely diverse patient population, with a slightly larger proportion of Hispanic/Latino patients, reflecting the local population in Bexar County, Texas. This study was designed to increase understanding regarding the generalizability of the AVP and to contribute new evidence regarding its effect on increasing the completion of the HPV vaccination series.

2. Materials and Methods

2.1. The Evidence-Based AVP HPV Vaccination Intervention

The AVP is a pediatric clinic-based intervention that comprises six evidence-based strategies aimed at the clinic organization, providers and parents and designed to synergistically facilitate an increase in HPV vaccination initiation and completion, including (1) HPV immunization champions [44], (2) provider assessment and feedback (A&F) [22,45], (3) continuing medical/nursing education (CME/CNE) [46], (4) electronic health record (EHR)-based provider reminders [47], (5) patient (parent) HPV vaccination reminders [48], and (6) a self-tailored parent education app [49,50].
The champions facilitate the implementation of AVP strategies in their clinic (e.g., by distributing A&F reports, promoting continuing education activity to all clinic staff, training clinic staff on provider and parent reminders, and distributing HPV vaccination education materials for parents in clinic examination and waiting rooms). The provider A&F quarterly reports provide a comparison of each provider’s and clinic’s HPV vaccination initiation and completion statistics for the previous quarter and HPV vaccination goals for the coming quarter to raise provider awareness of personal and clinic HPV vaccination rates. The online 50 min ethics-accredited CME/CNE HPV vaccination communication education included provider and clinical staff training on HPV vaccine national guidelines, evidence-based strategies to increase HPV vaccination, and communication strategies for providers to deliver strong, presumptive [51], bundled (when concurrent with other vaccines) HPV vaccination recommendations, and to roll with patient resistance [52]. The CME/CNE engaged viewers with real-life case vignettes aimed at enhancing provider communication skills and confidence to deliver strong recommendations. Provider EHR-based real-time HPV vaccination reminders are designed to be delivered during the patient encounter to reduce missed vaccination opportunities. The AVP team worked with the clinic system staff to design reminder messages and coordinate delivery through the EHR system (i.e., Epic software).
The clinic-wide patient registry and HPV vaccination reminder system were developed to notify parents of their child’s vaccine initiation due date (triggered by birth date) and to remind parents of completion due dates for the 2nd (or 3rd) HPV vaccination dose. This system was designed for automated delivery through the Epic MyChart patient portal. The parent educational materials promoted positive messaging about the HPV vaccine, as well as provided a QR code for parents to download the AVP HPVcancerFree parent education app. Outcome analyses of the original AVP conducted in a 51-pediatric clinic network indicated the AVP MLMC intervention approach effectively increased HPV vaccination initiation 28% from baseline to 3-year follow-up compared with a 20% change for Houston reported by the NIS-Teen data for the same age group and period (2014 through 2018) [43].

2.2. The Adapted AVP Intervention

In the current study, our team, comprising UTHealth behavioral scientists and a Baylor College of Medicine pediatric infectious disease specialist, adapted, implemented, and evaluated the AVP intervention for a new five-clinic pediatric network. Adaptation was guided by the Intervention Mapping approach and CDC Replicating Effective Programs (REP) frameworks [37,53]. The REP framework includes four phases: (1) preconditions (to identify need, target population, and suitability of the intervention); (2) pre-implementation activities (e.g., adapting the program for the new practice setting and patient population with stakeholder input and planning implementation rollout with clinic leadership); (3) implementation (e.g., delivery of the AVP strategies); and (4) maintenance (e.g., preparing the AVP intervention for sustainability).
Focus groups and surveys were conducted with clinic staff and managers to identify psychosocial factors in patients and providers (e.g., social and cultural norms) and clinic structural factors (e.g., EHR capabilities) that affect the implementation of the clinic-based AVP strategies. We did not identify new cultural-related determinants of vaccination that required adaption to parent education. Adaptation included updates to CME and CNE content, including updated HPV vaccination guidelines, new information on HPV vaccine safety, and more evidence for vaccinating at the recommended age (11–12 years). Working with the clinic partners, we identified the need to tailor the A&F preparation strategy to fit with the clinic Athena EHR system capabilities. In addition, the delivery of A&F reports to each provider was designed to align with the clinic organization. Reports were compiled by the AVP team and delivered to champions via email. Champions at each clinic site printed the reports and distributed them to physicians and other clinic staff.
To adapt and integrate the provider reminder strategy into the new clinic system EHR platform, the AVP team worked with the medical director and EHR team. The result was the creation of provider HPV vaccination job aids that outline HPV vaccination best practices and instructions for providers that included the following steps to set up vaccination reminder prompts: (1) use the EHR’s (i.e., Athena) quality tab to check whether the patient is due for HPV, (2) subscribe to a customized order set that includes HPV, and (3) manually add HPV immunization alerts to patient’s records. These job aids were distributed to all physicians and managers. Champions and managers promoted the job aids and posted them in exam rooms for easy reference by physicians and clinical staff.
Parent reminder delivery methods were also adapted to align with the clinic patient communication infrastructure, changing the delivery method, which was developed with the previous clinic system [43], to sending reminders through an automated email reminder campaign to align with the clinic system’s current patient communication methods. The AVP HPVcancerFree parent education app adaptation was informed by the formative work with the new system adoptees. In addition, we reviewed the parent survey and app usage data from the original AVP evaluation to improve user engagement and improved relevance to parents. AVP HPVcancerFree parent education app adaptations included the addition of (1) an animated, infographic-based video on HPV and the HPV vaccine, and (2) biweekly push notifications containing factual information to serve as reminders to app users and as an additional source of information. The AVP intervention strategies are presented in Figure 1 below and may be viewed at the AVP URL https://avptexas.org (accessed on 29 April 2004).

2.3. Study Setting and Population

Eligible clinics were part of an urban pediatric clinic network in Bexar County, Texas, which serves approximately 7000 children and adolescents aged 11–17 years per year, and served approximately 26,000 11–17-year-olds from 2018 to 2022. No clinics in this system were excluded. At the time of AVP intervention implementation, the system had five clinic sites, 18 pediatricians, and 40 clinical staff (e.g., CMA, RN, LVN). Of those patients, most were privately insured (85%) and identified as Hispanic. (Table 1).

2.4. Study Design

We conducted a quasi-experimental single group, pre- and post-study design with an external comparison group to examine the effect of the adapted AVP intervention on HPV vaccination initiation and completion rates and compare the HPV vaccination initiation rates to the original AVP study. This research was approved by the Institutional Review Board at the University of Texas Health Sciences Center at Houston (HSC-SPH-18-0733).

2.5. Measures

The primary outcomes include HPV vaccination initiation among 11–12-year-olds and HPV vaccination completion, or up-to-date (UTD), by age 13. UTD status is defined as having ≥3 doses, or 2 doses when the first HPV vaccine dose was initiated before age 15 years of age and there were at least 5 months between the first and second dose. We also examined HPV vaccination among 13–17-year-olds to examine the effect of the intervention on the catch-up age groups. We ascertained HPV vaccination outcomes from EHR data at baseline and follow-up. Patient sociodemographic characteristics were also obtained through EHR data, including age (11–12 and 13–17), sex, race/ethnicity (NH Black, Hispanic/Latino, NH White), and health insurance status (public or private).

2.6. Comparison Data

Comparison data are from the National Immunization Survey-Teen (NIS-Teen) datasets for the years 2017–2021, which provides vaccination surveillance data based on a representative sample of adolescents 13–17 years of age, collected among U.S. parents (mailed questionnaires) and providers (by telephone) [54]. The NIS-Teen dataset includes HPV vaccination uptake (≥1 dose) and vaccination UTD rates (≥3 doses, or 2 doses when the first HPV vaccine dose was initiated before age 15 years of age and there were at least 5 or more months minus 4 days, between the first and second dose). The age group reported by NIS-Teen was 13–17 years so we used that age group as our comparison to examine secular trends. The NIS-Teen database presents coverage rates (≥1 dose of HPV vaccine) based on a representative sample of males and females nationally (sample sizes in the years 2017–2021 range from 990–2256 in Texas and 296–336 in Bexar County, Texas.

2.7. Statistical Methods

Before testing the study hypotheses, we calculated patient-level mean and prevalence figures (i.e., descriptive statistics) for study variables among all patients presenting for care during the study period. To test the study hypotheses, we conducted a series of interrupted time series analyses (ITSA) [55,56]. First, we used an ITSA to compare trends in HPV vaccine initiation before delivery of the intervention (1 September 2017 to August 2018) and relative to after delivery of the intervention (1 September 2018 to 31 May 2022). Second, we conducted a similar ITSA to compare trends in HPV vaccine competition before delivery of the intervention, relative to after delivery of the intervention. This method is used to compare the outcome (HPV vaccination initiation) in the post-intervention among the clinic system patient population period to the counterfactual [57]. Each ITSA controlled for age, sex, race/ethnicity, and health insurance status. We also conducted an interaction between interruption and race/ethnicity to test for any possible differences in treatment effect. In addition, we conducted a comparison of clinic HPV initiation and completion (UTD) trends with trends in the general adolescent population provided by NIS-Teen data (2017–2021). All analyses were conducted in Stata 17.2 (College Station, TX, USA).

3. Results

During this three-year intervention study, an average of 6771 patients, aged 11 through 17 years, completed a clinical appointment (52.1% female and 47.9% male). Patients’ sociodemographic characteristics, as ascertained from EHRs, indicate that 43% of patients were identified as Hispanic, 33.8% NH White, and 4.3% NH Black. Patients were primarily covered by private insurance, with 10.4% covered by Medicaid, and the majority spoke English (Table 1).

AVP Intervention Effect on HPV Initiation and Completion Rates

We examined HPV vaccination initiation and completion trends from the baseline period (1 September 2017–31 August 2018) to year 1, before rolling out the AVP intervention strategies, and annually through year 3 (1 September 2020–31 August 2021), as well as at a 9-month post-intervention follow-up period. Results indicate a significant increase in initiation rates among 11–17-year-olds from baseline to 3-year follow-up (64.7% to 80.2%; p-value < 0.001) (Table 1). Similarly, initiation rates increased from baseline to the 3-year follow-up among both younger adolescents (11–12-year-olds: 52.1% to 70.9%) and older adolescents (13–17-year-olds: 72.3% to 84.3%) (Figure 2). Initiation rates also increased for patients across all races/ethnicities and insurance coverage types, including those with commercial insurance, Medicare/Medicaid, and those with no insurance (Table 1 and Figure 3 and Figure 4).
HPV vaccination completion rates also increased significantly among 11–17-year-olds from baseline to the 3-year follow-up (43.2% to 60.2%; p-value < 0.001) (Table 2). The increase was observed among both younger adolescents (11–12-year-olds: 20.9% to 28.6%) and older adolescents (13–17-year-olds: 56.7% to 74.2%) (Figure 5). In addition to age, the increase over time was observed across all race/ethnicity and insurance groups (Table 2 and Figure 6 and Figure 7).
Overall, a greater increase in initiation and completion rates occurred from year 1 to year 2, following the rollout of A&F, patient reminders, provider CME/CNE, and the parent education app (Figure 8).
Figure 9 and Figure 10 present HPV vaccination rates comparing the intervention clinic network patient population initiation and series completion rates to adolescents in the same age groups residing in Bexar County (where the clinic system is located) and Texas. The external comparison was based on NIS-Teen data provided for 13–17-year-olds in the same period (January 2017–February 2022) [58,59,60].
Figure 11 presents the ITSA of the network HPV vaccination initiation data results, which indicate that prior to the intervention, HPV vaccine initiation prevalence was significantly increasing at ~0.34% per month (p = 0.002), relative to ~0.18% after the intervention. These trends were not statistically different (p = 0.173); however, the onset of the intervention (i.e., the “interruption”) was associated with a significant increase in HPV vaccine initiation (+3.0%; p = 0.002). No statistical differences were observed between race/ethnicity categories with Hispanic as the referent group or NH White as the referent group.
Figure 12 presents HPV vaccination completion ITSA results, which indicate that prior to the intervention, HPV vaccination completion was unchanged (~0.04% per month; p = 0.812) and then increased to 0.43% per month following the intervention (p < 0.001). These trends were significantly different, indicating that HPV vaccine competition increased significantly following the intervention (p = 0.033). There was no immediate change in the prevalence of HPV vaccination completion (p = 0.077) at the onset of the intervention (i.e., interruption).
Because the COVID-19 pandemic lockdown was initiated on 15 March 2020 [61], we assessed the potential effect of the pandemic on HPV vaccination rates during the 3-year intervention period. We found no decrease in HPV vaccination when comparing HPV vaccination rates pre-COVID with post-COVID within the five-clinic network.

4. Discussion

To improve vaccination efforts, we developed the AVP, comprised of evidence-based strategies [48,62,63,64] to address clinic system-, provider- and patient-related factors influencing HPV vaccination in clinic settings (Figure 1). In our first evaluation of the MLMC intervention (2015–2017), in a 51-clinic network with 44.4% NH White, 24.8% Hispanics, and 13.8% NH Black patients, and predominately English speakers (93.1%), we found the AVP effectively increased HPV initiation rates among 11–17-year-olds by 36% from baseline to 3-year follow-up across all clinic sites [43]. In this current study (2018–2022), in the five-clinic network with fewer NH White (33.8%) and NH Black patients (4.3%), a larger proportion of Hispanic patients (43%), and a slightly higher proportion of English speakers (95.8%), we found the adapted AVP again effectively increased HPV vaccination initiation rates by 24% from baseline to 3-year follow-up, to an overall 80% initiation among 11–17-year-olds. However, we observed the rates began to plateau once clinic site initiation rates approached 80%, indicating there could be a threshold effect. Additionally, this current study establishes the effectiveness of the AVP on increasing HPV vaccination completion rates from 43.2% at baseline to 60.2% at 3-year follow-up (while varying, an increase was observed across each subgroup) (Table 2). Comparing clinic initiation and completion ITSA rates with those among adolescents in the same age groups residing in Bexar County during the same period, we observed that the onset of the intervention was associated with a significant increase in initiation prevalence (+3.0%; p = 0.002). In addition, we observed a 0.43% per month increase in completion rates following the intervention (p < 0.001). No differences in treatment effect were found by race/ethnic subgroups, indicating that the positive effect of the AVP intervention was observed across race/ethnicity groups. This replicates the findings of our original AVP effectiveness study focused on increasing HPV vaccination initiation [43] and adds new findings regarding effectively increasing completion rates.
The success of the AVP also indicates that minimal adaptation of the MLMC AVP program for the new clinic system was needed to retain its effectiveness on initiation, as well as to positively affect HPV vaccination completion rates. This study thus provides strong evidence of feasibility regarding the minimal burden on AVP program clinic adopters to adapt the AVP strategies for new clinic settings and implement them with fidelity. Thus, the results from this study indicate promise regarding the generalizability of the strategies and scalability of the AVP approach. Moreover, this study adds to the evidence in the literature regarding using MLMC clinic-based intervention strategies [65], including training HPV vaccination champions to implement provider reminder job aids and assessment and feedback (A&F), encouraging providers to complete the CME/CNE to obtain HPV vaccination-specific communication training focused on increasing providers’ consistent and effective HPV vaccination recommendation style with adolescent patients/parents and delivering parent education via an HPV vaccination self-tailored app [66].
Importantly, during this study, the COVID-19 pandemic shutdown in the U.S. began in mid-March 2020. During the early pandemic period that coincided with this study, the vaccination initiation and completion rates in the AVP clinic sites continued to rise, albeit with slightly depressed increases (Figure 2, Figure 5, Figure 8 and Figure 9). This increase occurred despite a marked decline in pediatric vaccine administration during the COVID-19 pandemic [67,68]. Moreover, while the NIS-Teen data indicate a significant decrease in HPV vaccination initiation rates among Medicaid and uninsured adolescents during the pandemic period [16], in the present study, these groups continued to experience a slight increase in both initiation and completion rates, suggesting the AVP strategies mitigated the COVID-19-related decline in HPV vaccination rates. Findings of AVP effectiveness during the pandemic were supported by a smaller HPV vaccination quality improvement project conducted in two clinics during the pandemic, which also found the HPV vaccination strategies helped to sustain both HPV initiation and completion rates during the pandemic [69].
This study also has several limitations, particularly related to study design. We used a one-group pre- and post-study design, and the analysis methods did not control for time-varying confounders [57]. We also cannot control for secular trends; however, during the pandemic, secular vaccination trends would not have supported an increase in vaccination rates, and rather, our examination of the vulnerable subgroups most affected by the pandemic (uninsured and Medicaid-covered adolescents) suggests the AVP mitigated negative effects on these vulnerable patient groups receiving care at the AVP clinics. Finally, implementation of the AVP was partially supported by the UTHealth research team, particularly in facilitating the adaptation of the AVP strategies to fit with the capacity and EHR infrastructure of the adopting clinic system. This study also has several strengths. First, this study replicates the original AVP’s effect on increasing HPV vaccination initiation, as well as provides new evidence that the AVP had a significant effect on increasing HPV completion rates during the COVID-19 pandemic. By replicating the AVP in a smaller clinic network in a different city, with different patient population demographic profiles, EHR systems, and organizational factors, the results provide insight into the generalizability of the AVP approach across clinic systems. The HPV vaccination outcome data were also ascertained using EHR data.
Findings from this intervention study further establish the AVP as an EBI that supports an increase in HPV vaccination initiation and completion in a pediatric clinic network. This study also serves as an example of the minimal adaptation required to prepare the AVP for new clinic systems. Finally, our findings suggest that the AVP vaccination strategies facilitated resilience during the pandemic, helping to support best practices to promote HPV vaccination initiation and completion. To promote scale-up and sustainment of the evidence-based AVP, research is underway to design implementation support strategies to guide clinic leaders and staff in safety-net clinic systems in the adoption, implementation planning, and delivery of the AVP [70].

Author Contributions

The authors contributing to the study and manuscript development were as follows: Conceptualization, L.S.S., S.W.V., E.L.F., R.S. and C.M.H.; methodology, L.S.S., S.P.C., E.L.F., R.S., S.W.V. and D.S.M.; software, D.S.M.; validation, L.S.S., D.S.M. and E.L.F.; formal analysis, S.P.C. and D.S.M.; investigation L.S.S., E.L.F., R.S., S.W.V., J.J.F. and S.M.P.; resources, L.S.S., R.S., S.W.V., C.M.H., J.J.F., L.A.S., S.M.P. and E.L.F.; data curation, S.P.C. and D.S.M.; writing—original draft preparation, L.S.S. and E.L.F.; writing—review and editing, L.S.S., E.L.F., T.A.T., R.S., L.A.S. and C.M.H.; visualization, E.L.F., D.S.M. and S.P.C.; supervision, L.S.S.; project administration, E.L.F.; funding acquisition, L.S.S., S.W.V., R.S. and E.L.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by The Cancer Prevention and Research Institute of Texas (CPRIT), grant number PP180089.

Institutional Review Board Statement

This study was approved by the University of Texas Health Science Center at Houston Institutional Review Board (HSC-SPH-18-0733).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to security restrictions.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

AVPAdolescent Vaccination Program
A&FAssessment and feedback
CDCCenters for Disease Control and Prevention
CME/CNEContinuing medical/nursing education
HERElectronic health record
HCPHealth Care Provider
HPVHuman papillomavirus
ITInformation Technology
ITSAInterrupted time series analyses
MLMCMulti-level and multi-component
NIS-TeenNational Immunization Survey-Teen
REPReplicating Effective Programs
U.S.United States
UTDUp-to-date

References

  1. Senkomago, V.; Henley, S.J.; Thomas, C.C.; Mix, J.M.; Markowitz, L.E.; Saraiya, M. Human Papillomavirus-Attributable Cancers—United States, 2012–2016. MMWR Morb. Mortal Wkly. Rep. 2019, 68, 724–728. [Google Scholar] [CrossRef] [PubMed]
  2. Saraiya, M.; Unger, E.R.; Thompson, T.D.; Lynch, C.F.; Hernandez, B.Y.; Lyu, C.W.; Steinau, M.; Watson, M.; Wilkinson, E.J.; Hopenhayn, C.; et al. US assessment of HPV types in cancers: Implications for current and 9-valent HPV vaccines. J. Natl. Cancer Inst. 2015, 107, djv086. [Google Scholar] [CrossRef] [PubMed]
  3. de Martel, C.; Georges, D.; Bray, F.; Ferlay, J.; Clifford, G.M. Global burden of cancer attributable to infections in 2018: A worldwide incidence analysis. Lancet Glob. Health 2020, 8, e180–e190. [Google Scholar] [CrossRef] [PubMed]
  4. Mahal, B.A.; Catalano, P.J.; Haddad, R.I.; Hanna, G.J.; Kass, J.I.; Schoenfeld, J.D.; Tishler, R.B.; Margalit, D.N. Incidence and Demographic Burden of HPV-Associated Oropharyngeal Head and Neck Cancers in the United States. Cancer Epidemiol. Biomark. Prev. 2019, 28, 1660–1667. [Google Scholar] [CrossRef] [PubMed]
  5. Garland, S.M.; Steben, M.; Sings, H.L.; James, M.; Lu, S.; Railkar, R.; Barr, E.; Haupt, R.M.; Joura, E.A. Natural history of genital warts: Analysis of the placebo arm of 2 randomized phase III trials of a quadrivalent human papillomavirus (types 6, 11, 16, and 18) vaccine. J. Infect. Dis. 2009, 199, 805–814. [Google Scholar] [CrossRef]
  6. Centers for Disease Control and Prevention. Cancers Associated with Human Papillomavirus, United States—2015–2019; Centers for Disease Control and Prevention, US Department of Health and Human Services: Atlanta, GA, USA, October 2022. Available online: https://www.cdc.gov/cancer/uscs/about/data-briefs/no31-hpv-assoc-cancers-unitedstates-2015-2019.htm (accessed on 2 April 2024).
  7. McClung, N.M.; Gargano, J.W.; Park, I.U.; Whitney, E.; Abdullah, N.; Ehlers, S.; Bennett, N.M.; Scahill, M.; Niccolai, L.M.; Brackney, M.; et al. Estimated Number of Cases of High-Grade Cervical Lesions Diagnosed Among Women—United States, 2008 and 2016. MMWR Morb. Mortal Wkly. Rep. 2019, 68, 337–343. [Google Scholar] [CrossRef]
  8. Centers for Disease Control and Prevention. Genital HPV Infection—Basic Fact Sheet; Centers for Disease Control and Prevention, US Department of Health and Human Services: Atlanta, GA, USA, 2023. Available online: https://www.cdc.gov/std/hpv/hpv-Fs-July-2017.pdf (accessed on 2 April 2024).
  9. Centers for Disease Control and Prevention. Priority: Cervical Cancer Statistics; Centers for Disease Control and Prevention, US Department of Health and Human Services: Atlanta, GA, USA, 2023. Available online: https://www.cdc.gov/cancer/cervical/statistics/index.htm (accessed on 4 April 2024).
  10. Sirovich, B.E.; Welch, H.G. The frequency of Pap smear screening in the United States. J. Gen. Intern. Med. 2004, 19, 243–250. [Google Scholar] [CrossRef]
  11. Centers for Disease Control and Prevention. HPV Vaccination Recommendations. 2021. Available online: https://www.cdc.gov/vaccines/vpd/hpv/hcp/recommendations.html (accessed on 2 April 2024).
  12. American Cancer Society. Guideline for Human Papillomavirus (HPV) Vaccine Use. 2023. Available online: https://www.cancer.org/health-care-professionals/american-cancer-society-prevention-early-detection-guidelines/hpv-guidelines.html (accessed on 2 April 2024).
  13. O’Leary, S.C.; Frost, H.M. Does HPV vaccination initiation at age 9, improve HPV initiation and vaccine series completion rates by age 13? Hum. Vaccin. Immunother. 2023, 19, 2180971. [Google Scholar] [CrossRef]
  14. Chido-Amajuoyi, O.G.; Talluri, R.; Wonodi, C.; Shete, S. Trends in HPV Vaccination Initiation and Completion Within Ages 9-12 Years: 2008–2018. Pediatrics 2021, 147, e2020012765. [Google Scholar] [CrossRef]
  15. Centers for Disease Control and Prevention. Vaccination Coverage among Adolescents (13–17 Years); Centers for Disease Control and Prevention, US Department of Health and Human Services: Atlanta, GA, USA, 2021. Available online: https://www.cdc.gov/mmwr/volumes/71/wr/mm7135a1.htm (accessed on 2 April 2024).
  16. Pingali, C.; Yankey, D.; Elam-Evans, L.D.; Markowitz, L.E.; Valier, M.R.; Fredua, B.; Crowe, S.J.; DeSisto, C.L.; Stokley, S.; Singleton, J.A. Vaccination Coverage Among Adolescents Aged 13–17 Years—National Immunization Survey-Teen, United States, 2022. MMWR Morb. Mortal Wkly. Rep. 2023, 72, 912–919. [Google Scholar] [CrossRef]
  17. Department of Health and Human Services: Office of Disease Prevention and Health Promotion. Increase the Proportion of Adolescents Who Get Recommended Doses of the HPV Vaccine—IID-08 Healthy People 2030. Available online: https://health.gov/healthypeople/objectives-and-data/browse-objectives/vaccination/increase-proportion-adolescents-who-get-recommended-doses-hpv-vaccine-iid-08 (accessed on 2 April 2024).
  18. Chao, C.R.; Xu, L.; Cannizzaro, N.; Bronstein, D.; Choi, Y.; Riewerts, R.; Mittman, B.; Zimmerman, R.K.; Gilkey, M.; Glenn, B.; et al. Trends in HPV vaccine administration and HPV vaccine coverage in children by race/ethnicity and socioeconomic status during the COVID-19 pandemic in an integrated health care system in California. Vaccine 2022, 40, 6575–6580. [Google Scholar] [CrossRef] [PubMed]
  19. National Center for Immunization and Respiratory Diseases Supplemental Table 1: Estimated vaccination coverage with selected vaccines and doses among adolescents aged 13–17* years, by Race and Ethnicity—National Immunization Survey–Teen (NIS-Teen), United States. 2021. Available online: https://www.cdc.gov/ncird/surveillance/hpvimpact/overview.html (accessed on 5 February 2024).
  20. Spencer, J.C.; Calo, W.A.; Brewer, N.T. Disparities and reverse disparities in HPV vaccination: A systematic review and meta-analysis. Prev. Med. 2019, 123, 197–203. [Google Scholar] [CrossRef] [PubMed]
  21. National Center for Immunization and Respiratory Diseases. Supplemental Table 1. Estimated Vaccination Coverage with Selected Vaccines and Doses among Adolescents Aged 13–17* Years, by Race and Ethnicity—National Immunization Survey–Teen (NIS-Teen), United States, 2021; Centers for Disease Control and Prevention. National Center for Immunization and Respiratory Diseases. 24 August 2022. Available online: https://www.cdc.gov/vaccines/imz-managers/coverage/teenvaxview/pubs-presentations/NIS-teen-vac-coverage-estimates-2021-tables.html (accessed on 5 February 2024).
  22. Groom, H.C.; Irving, S.A.; Caldwell, J.; Larsen, R.; Beaudrault, S.; Luther, L.M.; Naleway, A.L. Implementing a Multipartner HPV Vaccination Assessment and Feedback Intervention in an Integrated Health System. J. Public Health Manag. Pract. 2017, 23, 589–592. [Google Scholar] [CrossRef] [PubMed]
  23. Bright, T.J.; Wong, A.; Dhurjati, R.; Bristow, E.; Bastian, L.; Coeytaux, R.R.; Samsa, G.; Hasselblad, V.; Williams, J.W.; Musty, M.D.; et al. Effect of clinical decision-support systems: A systematic review. Ann. Intern. Med. 2012, 157, 29–43. [Google Scholar] [CrossRef]
  24. Hanley, K.; Chung, T.H.; Nguyen, L.K.; Amadi, T.; Stansberry, S.; Yetman, R.J.; Foxhall, L.E.; Bello, R.; Diallo, T.; Le, Y.L. Using Electronic Reminders to Improve Human Papillomavirus (HPV) Vaccinations among Primary Care Patients. Vaccines 2023, 11, 872. [Google Scholar] [CrossRef] [PubMed]
  25. Potts, J.; Southard, E. Teaching It Forward: Educating Parents About HPV/HPV Vaccine. J. Dr. Nurs. Pract. 2019, 12, 46–58. [Google Scholar] [CrossRef] [PubMed]
  26. Gockley, A.A.; Pena, N.; Vitonis, A.; Welch, K.; Duffey-Lind, E.C.; Feldman, S. Tablet-Based Patient Education Regarding Human Papillomavirus Vaccination in Colposcopy Clinic. J. Low. Genit. Tract Dis. 2019, 23, 188–192. [Google Scholar] [CrossRef] [PubMed]
  27. Ruiz-Lopez, T.; Sen, S.; Jakobsen, E.; Trope, A.; Castle, P.E.; Hansen, B.T.; Nygard, M. FightHPV: Design and Evaluation of a Mobile Game to Raise Awareness About Human Papillomavirus and Nudge People to Take Action Against Cervical Cancer. JMIR Serious Games 2019, 7, e8540. [Google Scholar] [CrossRef] [PubMed]
  28. Savas, L.S.; Loomba, P.; Shegog, R.; Alaniz, A.; Costa, C.; Adlparvar, E.; Allicock, M.A.; Chenier, R.; Goetz, M.; Markham, C.M.; et al. Using Implementation Mapping to Increase the Implementation of Salud en Mis Manos: A Breast and Cervical Cancer Screening and HPV Vaccination Intervention for Latinas. Front. Public Health 2022, 11, 966553. [Google Scholar] [CrossRef]
  29. Walling, E.B.; Dodd, S.; Bobenhouse, N.; Reis, E.C.; Sterkel, R.; Garbutt, J. Implementation of Strategies to Improve Human Papillomavirus Vaccine Coverage: A Provider Survey. Am. J. Prev. Med. 2019, 56, 74–83. [Google Scholar] [CrossRef]
  30. Rodriguez, A.M.; Do, T.Q.N.; Goodman, M.; Schmeler, K.M.; Kaul, S.; Kuo, Y.F. Human Papillomavirus Vaccine Interventions in the U.S.: A Systematic Review and Meta-analysis. Am. J. Prev. Med. 2019, 56, 591–602. [Google Scholar] [CrossRef] [PubMed]
  31. Khalid, K.; Lee, K.Y.; Mukhtar, N.F.; Warijo, O. Recommended Interventions to Improve Human Papillomavirus Vaccination Uptake among Adolescents: A Review of Quality Improvement Methodologies. Vaccines 2023, 11, 1390. [Google Scholar] [CrossRef] [PubMed]
  32. Kelly, M.K.; Katzenellenbogen, R.A.; Fiks, A.G. What Health Systems Can Do Now to Improve Human Papillomavirus Vaccination. JAMA Pediatr. 2024, 178, 13–14. [Google Scholar] [CrossRef] [PubMed]
  33. Siddiqui, F.A.; Padhani, Z.A.; Salam, R.A.; Aliani, R.; Lassi, Z.S.; Das, J.K.; Bhutta, Z.A. Interventions to Improve Immunization Coverage Among Children and Adolescents: A Meta-analysis. Pediatrics 2022, 149, e2021053852D. [Google Scholar] [CrossRef] [PubMed]
  34. Finney Rutten, L.J.; Griffin, J.M.; St Sauver, J.L.; MacLaughlin, K.; Austin, J.D.; Jenkins, G.; Herrin, J.; Jacobson, R.M. Multilevel Implementation Strategies for Adolescent Human Papillomavirus Vaccine Uptake: A Cluster Randomized Clinical Trial. JAMA Pediatr. 2024, 178, 29–36. [Google Scholar] [CrossRef] [PubMed]
  35. Fiks, A.G.; Grundmeier, R.W.; Mayne, S.; Song, L.; Feemster, K.; Karavite, D.; Hughes, C.C.; Massey, J.; Keren, R.; Bell, L.M.; et al. Effectiveness of decision support for families, clinicians, or both on HPV vaccine receipt. Pediatrics 2013, 131, 1114–1124. [Google Scholar] [CrossRef] [PubMed]
  36. Guide to Community Preventive Services. CPSTF Findings for Increasing Vaccination. 16 April 2019. Available online: https://www.thecommunityguide.org/pages/task-force-findings-increasing-vaccination.html (accessed on 10 January 2022).
  37. Bartholomew, L.K.; Parcel, G.S.; Kok, G.; Gottlieb, N.; Fernandez, M.E. Planning Health Promotion Programs: An Intervention Mapping Approach, 3rd ed.; Jossey-Bass: San Francisco, CA, USA, 2011. [Google Scholar]
  38. Bandura, A. Human agency in social cognitive theory. Am. Psychol. 1989, 44, 1175–1184. [Google Scholar] [CrossRef]
  39. Fishbein, M. A reasoned action approach to health promotion. Med. Decis. Mak. 2008, 28, 834–844. [Google Scholar] [CrossRef] [PubMed]
  40. Glanz, K.; Rimer, B.K.; Viswanath, K. Health Behavior and Health Education: Theory, Research, and Practice; Jossey-Bass: San Franciso, CA, USA, 2008; Volume 4. [Google Scholar]
  41. Becker, E.R.; Shegog, R.; Savas, L.S.; Frost, E.L.; Healy, C.M.; Spinner, S.W.; Vernon, S.W. Informing Content and Feature Design of a Parent-Focused Human Papillomavirus Vaccination Digital Behavior Change Intervention: Synchronous Text-Based Focus Group Study. JMIR Form. Res. 2021, 5, e28846. [Google Scholar] [CrossRef]
  42. Crawford, C.A.; Shegog, R.; Savas, L.S.; Frost, E.L.; Healy, C.M.; Coan, S.P.; Gabay, E.K.; Spinner, S.W.; Vernon, S.W. Using Intervention Mapping to Develop an Efficacious Multicomponent Systems-Based Intervention to Increase Human Papillomavirus (HPV) Vaccination in a Large Urban Pediatric Clinic Network. J. Appl. Res. Child. 2019, 10, 9. [Google Scholar] [CrossRef]
  43. Vernon, S.W.; Savas, L.S.; Shegog, R.; Healy, C.M.; Frost, E.L.; Coan, S.P.; Gabay, E.K.; Preston, S.M.; Crawford, C.A.; Spinner, S.W.; et al. Increasing HPV Vaccination in a Network of Pediatric Clinics using a Multi-component Approach. J. Appl. Res. Child. 2019, 10, 11. Available online: https://www.ncbi.nlm.nih.gov/pubmed/34231977 (accessed on 5 February 2024). [CrossRef] [PubMed]
  44. Santos, W.J.; Graham, I.D.; Lalonde, M.; Demery Varin, M.; Squires, J.E. The effectiveness of champions in implementing innovations in health care: A systematic review. Implement. Sci. Commun. 2022, 3, 80. [Google Scholar] [CrossRef] [PubMed]
  45. Centers for Disease Control and Prevention. Vaccination Programs: Provider Assessment and Feedback. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-provider-assessment-and-feedback (accessed on 10 January 2022).
  46. Perkins, R.B.; Zisblatt, L.; Legler, A.; Trucks, E.; Hanchate, A.; Gorin, S.S. Effectiveness of a provider-focused intervention to improve HPV vaccination rates in boys and girls. Vaccine 2015, 33, 1223–1229. [Google Scholar] [CrossRef]
  47. Centers for Disease Control and Prevention. Vaccination Programs: Provider Reminders. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-provider-reminders (accessed on 10 January 2022).
  48. Centers for Disease Control and Prevention. Vaccination Programs: Client Reminder and Recall Systems. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-client-reminder-and-recall-systems (accessed on 10 January 2022).
  49. The Community Preventive Services Task Force. Vaccination Programs: Community-Wide Education When Used Alone. 2020. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-community-wide-education-when-used-alone.html (accessed on 10 January 2022).
  50. Henrikson, N.B.; Zhu, W.; Baba, L.; Nguyen, M.; Berthoud, H.; Gundersen, G.; Hofstetter, A.M. Outreach and Reminders to Improve Human Papillomavirus Vaccination in an Integrated Primary Care System. Clin. Pediatr. 2018, 57, 1523–1531. [Google Scholar] [CrossRef] [PubMed]
  51. Constable, C.; Ferguson, K.; Nicholson, J.; Quinn, G.P. Clinician communication strategies associated with increased uptake of the human papillomavirus (HPV) vaccine: A systematic review. CA Cancer J. Clin. 2022, 72, 561–569. [Google Scholar] [CrossRef] [PubMed]
  52. Gilkey, M.B.; McRee, A.L. Provider communication about HPV vaccination: A systematic review. Hum. Vaccin. Immunother. 2016, 12, 1454–1468. [Google Scholar] [CrossRef] [PubMed]
  53. Kilbourne, A.M.; Neumann, M.S.; Pincus, H.A.; Bauer, M.S.; Stall, R. Implementing evidence-based interventions in health care: Application of the replicating effective programs framework. Implement. Sci. 2007, 2, 42. [Google Scholar] [CrossRef] [PubMed]
  54. Centers for Disease Control and Prevention. About the National Immunization Surveys (NIS). 2018. Available online: https://www.cdc.gov/nchs/hus/sources-definitions/nis.htm (accessed on 2 April 2024).
  55. Linden, A. Conducting interrupted time-series analysis for single-and multiple-group comparisons. Stata J. 2015, 15, 480–500. [Google Scholar] [CrossRef]
  56. Linden, A. A comprehensive set of postestimation measures to enrich interrupted time-series analysis. Stata J. 2017, 17, 73–88. [Google Scholar] [CrossRef]
  57. Bernal, J.L.; Cummins, S.; Gasparrini, A. Interrupted time series regression for the evaluation of public health interventions: A tutorial. Int. J. Epidemiol. 2017, 46, 348–355. [Google Scholar] [CrossRef]
  58. Centers for Disease Control and Prevention. NIS-Teen Data and Documentation for 2015 to Present; CDC: Atlanta, GA, USA, 2023. Available online: https://www.cdc.gov/vaccines/imz-managers/nis/datasets-teen.html (accessed on 5 February 2024).
  59. Bavley, R.; Skalland, B.; Tao, X.; Wolter, K.; Elam-Evans, L.D.; Singleton, J.A.; Walker, T.Y. A User’s Guide for the 2017 Public-Use Data File; Centers for Disease Control and Prevention: Atlanta, GA, USA, October 2018. Available online: https://www.cdc.gov/vaccines/imz-managers/nis/downloads/NIS-TEEN-PUF17-DUG.pdf (accessed on 10 January 2022).
  60. Elam-Evans, L.D.; Mu, Y.; Pingali, C.; Singleton, J.A.; Francis, R.; Skalland, B.; Wolter, K.; Yarbrough, M. A User’s Guide for the 2021 Public-Use Data File; Centers for Disease Control and Prevention: Atlanta, GA, USA, November 2022. Available online: https://www.cdc.gov/vaccines/imz-managers/nis/downloads/nis-teen-puf21-dug.pdf (accessed on 5 February 2024).
  61. Ochani, R.; Asad, A.; Yasmin, F.; Shaikh, S.; Khalid, H.; Batra, S.; Sohail, M.R.; Mahmood, S.F.; Ochani, R.; Hussham Arshad, M.; et al. COVID-19 pandemic: From origins to outcomes. A comprehensive review of viral pathogenesis, clinical manifestations, diagnostic evaluation, and management. Infez. Med. 2021, 29, 20–36. [Google Scholar] [PubMed]
  62. The Community Preventive Services Task Force. Increasing Appropriate Vaccination: Provider Assessment and Feedback; 1/4/2016. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-provider-assessment-and-feedback.html (accessed on 5 February 2024).
  63. The Community Preventive Services Task Force. Increasing Appropriate Vaccination: Provider Reminders; 1/4/2016. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-provider-reminders.html (accessed on 10 January 2022).
  64. Centers for Disease Control and Prevention. Vaccination Programs: Health Care System-Based Interventions Implemented in Combination. Available online: https://www.thecommunityguide.org/findings/vaccination-programs-health-care-system-based-interventions-implemented-combination (accessed on 10 January 2022).
  65. Smulian, E.A.; Mitchell, K.R.; Stokley, S. Interventions to increase HPV vaccination coverage: A systematic review. Hum. Vaccin. Immunother. 2016, 12, 1566–1588. [Google Scholar] [CrossRef] [PubMed]
  66. Escoffery, C.; Petagna, C.; Agnone, C.; Perez, S.; Saber, L.B.; Ryan, G.; Dhir, M.; Sekar, S.; Yeager, K.A.; Biddell, C.B.; et al. A systematic review of interventions to promote HPV vaccination globally. BMC Public Health 2023, 23, 1262. [Google Scholar] [CrossRef] [PubMed]
  67. Patel Murthy, B.; Zell, E.; Kirtland, K.; Jones-Jack, N.; Harris, L.; Sprague, C.; Schultz, J.; Le, Q.; Bramer, C.A.; Kuramoto, S.; et al. Impact of the COVID-19 Pandemic on Administration of Selected Routine Childhood and Adolescent Vaccinations—10 U.S. Jurisdictions, March-September 2020. MMWR Morb. Mortal Wkly. Rep. 2021, 70, 840–845. [Google Scholar] [CrossRef] [PubMed]
  68. Ryan, G.; Gilbert, P.A.; Ashida, S.; Charlton, M.E.; Scherer, A.; Askelson, N.M. Challenges to Adolescent HPV Vaccination and Implementation of Evidence-Based Interventions to Promote Vaccine Uptake During the COVID-19 Pandemic: “HPV Is Probably Not at the Top of Our List”. Prev. Chronic Dis. 2022, 19, E15. [Google Scholar] [CrossRef] [PubMed]
  69. Zorn, S.; Darville-Sanders, G.; Vu, T.; Carter, A.; Treend, K.; Raunio, C.; Vasavada, A. Multi-level quality improvement strategies to optimize HPV vaccination starting at the 9-year well child visit: Success stories from two private pediatric clinics. Hum. Vaccin. Immunother. 2023, 19, 2163807. [Google Scholar] [CrossRef] [PubMed]
  70. Shegog, R.; Savas, L.S.; Frost, E.L.; Thormaehlen, L.C.; Teague, T.; Steffy, J.; Healy, C.M.; Shay, L.A.; Preston, S.; Vernon, S.W. Adaptation and Formative Evaluation of Online Decision Support to Implement Evidence-Based Strategies to Increase HPV Vaccination Rates in Pediatric Clinics. Vaccines 2023, 11, 1270. [Google Scholar] [CrossRef]
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Figure 1. The Adolescent Vaccination Project (AVP) Clinic-Based Multi-level, Multi-Component Evidence-Based Strategies. Note Abbreviations: Information Technology (IT); Health Care Provider (HCP).
Figure 1. The Adolescent Vaccination Project (AVP) Clinic-Based Multi-level, Multi-Component Evidence-Based Strategies. Note Abbreviations: Information Technology (IT); Health Care Provider (HCP).
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Figure 2. HPV Vaccine Initiation for Clinic System Patients by Age Group, 2017–2022.
Figure 2. HPV Vaccine Initiation for Clinic System Patients by Age Group, 2017–2022.
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Figure 3. HPV Vaccine Initiation by Race/Ethnicity for Clinic System Patients Aged 11–17.
Figure 3. HPV Vaccine Initiation by Race/Ethnicity for Clinic System Patients Aged 11–17.
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Figure 4. HPV Vaccine Initiation by Patients’ Insurance Type Aged 11–17.
Figure 4. HPV Vaccine Initiation by Patients’ Insurance Type Aged 11–17.
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Figure 5. HPV Vaccine Completion for Clinic System Patients by Age Group, 2017–2022.
Figure 5. HPV Vaccine Completion for Clinic System Patients by Age Group, 2017–2022.
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Figure 6. HPV Vaccine Completion by Race/Ethnicity for Clinic System Patients Aged 11–17.
Figure 6. HPV Vaccine Completion by Race/Ethnicity for Clinic System Patients Aged 11–17.
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Figure 7. HPV Vaccine Completion by Patients’ Insurance Type Aged 11–17.
Figure 7. HPV Vaccine Completion by Patients’ Insurance Type Aged 11–17.
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Figure 8. Increase HPV Initiation and Completion Among Patients Aged 11–17 Years, by Year and Adolescent Vaccination Project (AVP) Intervention Strategy Roll-Out.
Figure 8. Increase HPV Initiation and Completion Among Patients Aged 11–17 Years, by Year and Adolescent Vaccination Project (AVP) Intervention Strategy Roll-Out.
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Figure 9. HPV Vaccine Initiation Comparing Intervention Clinics, Texas, and Bexar County Rates, Ages 13–17 *.
Figure 9. HPV Vaccine Initiation Comparing Intervention Clinics, Texas, and Bexar County Rates, Ages 13–17 *.
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Figure 10. HPV Vaccine Series Completion Comparing Intervention Clinics, Texas, and Bexar County Rates, Ages 13–17 *.
Figure 10. HPV Vaccine Series Completion Comparing Intervention Clinics, Texas, and Bexar County Rates, Ages 13–17 *.
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Figure 11. Interrupted Time Series for the Five-Clinic Network, 2017–2022.
Figure 11. Interrupted Time Series for the Five-Clinic Network, 2017–2022.
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Figure 12. Interrupted Time Series for the Five-Clinic Network, 2017–2022.
Figure 12. Interrupted Time Series for the Five-Clinic Network, 2017–2022.
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Table 1. Demographics and HPV Vaccine Initiation by Year, Patients Aged 11–17 Years.
Table 1. Demographics and HPV Vaccine Initiation by Year, Patients Aged 11–17 Years.
CharacteristicsMean Number of Patients per Year% of
Patient Pop.		BaselineYear 1Year 2Year 3End of Study
N%N%N%N%N%
Total6771 643864.7670370.5671579.1722980.2546981.6
Ages 11–12225333.3243052.1204857.9230470.5222870.9155170.5
Ages 13–17451966.7400872.3465576.0441083.7500184.3391886.0
Female352652.1338766.6349872.1348279.7373781.6275683.5
Male324547.9305162.6320568.7323278.6349278.6271379.7
Non-Hispanic White229033.8154062.3369270.8160677.6232279.4144579.3
Non-Hispanic Black2924.323162.831969.326777.935080.625684.4
Hispanic291443.0373967.882378.7384681.0324982.5286083.5
Other86012.760259.8133968.262077.487878.458979.0
Missing or Unknown4156.132650.353062.637570.143070.531977.4
Commercial Insurance577485.3557165.0572371.5573479.9606980.6448681.7
Medicare/Medicaid70710.461368.868270.270878.882481.773383.8
Other Insurance1201.88845.59656.312359.417272.115475.3
None1702.516649.420251.014966.416465.99671.9
English Language648895.8626565.1651471.0650479.4666980.7526481.7
Spanish Language1412.111659.513759.115076.015978.615781.5
Other Language30.01100.00-714.34100.01100.0
Unknown Language1402.15632.15244.25360.439772.04774.5
Baseline = 1 September 2017–31 August 2018; Year 1 = 1 September 2018–31 August 2019; Year 2 = 1 September 2019–31 August 2020; Year 3 = 1 September 2020–31 August 2021; End = 1 September 2021–31 May 2022.
Table 2. Sample Demographics and HPV Vaccine Series Completion * by Year, Patients Aged 11–17 Years.
Table 2. Sample Demographics and HPV Vaccine Series Completion * by Year, Patients Aged 11–17 Years.
CharacteristicsMean Number of Patients per Year% of
Patient Pop.		BaselineYear 1Year 2Year 3End of Study
N%N%N%N%N%
Total6771 643843.2670345.7671553.9722960.2546961.3
Ages 11–12225333.3243020.9204817.5230424.8222828.6155127.0
Ages 13–17451966.7400856.7465558.1441069.1500174.2391874.9
Female352652.1338745.7349847.7348255.2373761.6275662.9
Male324547.9305140.4320543.5323252.5349258.6271359.7
Non-Hispanic White229033.8154040.1369246.6160651.7232260.6144560.4
Non-Hispanic Black2924.323138.131943.326750.635061.125662.9
Hispanic291443.0373946.582353.3384656.8324962.9286063.4
Other86012.760238.7133941.762051.187855.058957.7
Missing or Unknown4156.132631.053039.437541.143046.731952.0
Commercial Insurance577485.3557143.2572346.6573455.0606961.0448662.1
Medicare/Medicaid70710.461348.668244.070850.782460.273361.3
Other Insurance1201.88830.79634.412339.017248.815450.7
None1702.516630.120232.714941.616442.19641.7
English Language648895.8626543.4651446.1650454.5666960.7526461.5
Spanish Language1412.111638.813738.015041.315954.715758.0
Other Language30.01100.00-70.0425.01100.0
Unknown Language1402.15623.25223.15328.339752.94751.1
* Completion was defined as completing 2 doses by age 15 and 3 doses from 15–17 years of age. Baseline = 1 September 2017–31 August 2018; Year 1 = 1 September 2018–31 August 2019; Year 2 = 1 September 2019–31 August 2020; Year 3 = 1 September 2020–31 August 2021; End = 1 September 2021–31 May 2022.
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MDPI and ACS Style

Savas, L.S.; Shegog, R.; Frost, E.L.; Healy, C.M.; Mantey, D.S.; Coan, S.P.; Shay, L.A.; Teague, T.A.; Ferreris, J.J.; Preston, S.M.; et al. Effect of an HPV Vaccination Multi-Level, Multi-Component Program on HPV Vaccination Initiation and Completion in a Pediatric Clinic Network. Vaccines 2024, 12, 510. https://doi.org/10.3390/vaccines12050510

AMA Style

Savas LS, Shegog R, Frost EL, Healy CM, Mantey DS, Coan SP, Shay LA, Teague TA, Ferreris JJ, Preston SM, et al. Effect of an HPV Vaccination Multi-Level, Multi-Component Program on HPV Vaccination Initiation and Completion in a Pediatric Clinic Network. Vaccines. 2024; 12(5):510. https://doi.org/10.3390/vaccines12050510

Chicago/Turabian Style

Savas, Lara S., Ross Shegog, Erica L. Frost, C. Mary Healy, Dale S. Mantey, Sharon P. Coan, L. Aubree Shay, Travis A. Teague, Juan J. Ferreris, Sharice M. Preston, and et al. 2024. "Effect of an HPV Vaccination Multi-Level, Multi-Component Program on HPV Vaccination Initiation and Completion in a Pediatric Clinic Network" Vaccines 12, no. 5: 510. https://doi.org/10.3390/vaccines12050510

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