Impact of HPV Vaccine Availability on Uptake

Article Outline

• Abstract
• Methods
  • Study Design
  • Participants
  • Data Sources/Measurement
  • Statistical Methods
• Results
  • Participants
  • Study Population Characteristics
  • HPV Vaccine Uptake
• Discussion
  • Key Results
  • Limitations
  • Generalizability
• Implications
• Acknowledgment
• References
• Copyright

Abstract 

Purpose

To evaluate the impact of human papillomavirus (HPV) vaccine availability on uptake among 19- to 26-year-old female patients of Planned Parenthood of Mid and South Michigan before and after the vaccine became available at the health centers.

Results

Availability of the HPV vaccine increased vaccine uptake from 11% before clinic availability to 16% after availability. Accessibility, including cost and provider recommendation, may have influenced uptake.

Implications

Improving availability of the HPV vaccine, while helpful, is not sufficient for a substantial increase in uptake. Issues of accessibility, including cost and provider recommendation, must also be addressed.

Keywords:  HPV , human papillomavirus , uptake , vaccine

Despite widespread support for the human papillomavirus (HPV) vaccine and high acceptability rates,¹ HPV vaccine uptake has remained low since the Food and Drug Administration (FDA) approval of Gardasil® (Merck and Co, Inc, Whitehouse Station, New Jersey) in 2006. By the end of 2009, only 44% of females 13 to 17 years old had initiated the HPV vaccine series and 27% had received the full 3 doses.² Even fewer young adults 19 to 26 have initiated HPV vaccination, with some estimates at less than 10% for receipt of at least 1 dose.³

Gardasil and the more recently approved Cervarix® (GlaxoSmithKline, Research Triangle Park) have the potential to drastically reduce the prevalence of HPV, which infects 44.8% of 20- to 24-year-old females in the United States.⁴ In addition, vaccination against HPV, the most common sexually transmitted infection, could prevent a majority of the 12,200 cervical cancers, 3,900 vulvar cancers, and 2,300 vaginal cancers estimated to have developed in the United States in 2010.⁵ Widespread use of the HPV vaccine can result in significant savings in health care expenditures, but it is generally considered cost-effective only with high population level uptake.⁶ In addition, data suggest that achieving high vaccine coverage among females is more cost effective than adding male vaccination,⁷ supporting the examination of factors related to vaccine uptake in various female populations.

Several studies have attempted to identify factors influencing HPV vaccine uptake, with the ultimate goal of improving vaccination rates.⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰ One influence that has emerged is vaccination opportunity. Females presenting for a health care visit,⁸, ⁹, ¹² specifically a preventive maintenance visit,¹² where the vaccine is available are more likely to initiate HPV vaccination, indicating that increased availability of the vaccine should result in increased uptake. To test this hypothesis, we studied the impact of Gardasil availability on vaccine uptake at 2 Planned Parenthood Mid and South Michigan (PPMSM) health centers 4 years after the FDA approved the vaccine.

Consistent with Planned Parenthood—s mission to “provide comprehensive reproductive and complementary health care services,”²¹ PPMSM began carrying Gardasil for 19- to 26-year-old female patients starting May 1, 2010, in 2 of its largest sites. Before then, organizational protocols encouraged PPMSM clinicians to recommend the HPV vaccine to females but required that patients seek out primary care providers or the county health departments to receive the vaccine. After May 1, 2010, PPMSM clinicians were able to offer the vaccine.

The primary objective of this study was to evaluate the impact of HPV vaccine availability on uptake among 19- to 26-year-old female PPMSM patients. Specifically, the objective was to compare uptake before and after the vaccine became available at 2 health centers 4 years after the vaccine became publicly available elsewhere. The secondary objective was to explore clinic level variables other than availability that may have influenced uptake.

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Methods 

Study Design 

The study was an observational study reflecting the reality of introducing Gardasil in 2 reproductive health centers without the strict controls of a clinical trial. Data were collected from 2 large, urban, outpatient PPMSM health centers that serve a largely uninsured, low-income patient population. Each health center employs 1 main clinician (nurse practitioner [NP], nurse midwife, or physician—s assistant), with other clinicians providing patient services as needed.

A pre-post observational study design following a single group of patients over a 2-year period was developed to study the impact of the newly available (at PPMSM) HPV vaccine. Participants— vaccination status was assessed at 2 annual exams. Before May 1, 2010, participants had the opportunity to discuss the HPV vaccine but had to receive it elsewhere. During the subsequent annual exam after May 1, 2010, unvaccinated participants had the opportunity to receive Gardasil at the clinic visit.

Data for the first 3 months of PPMSM Gardasil availability—May 1 to July 31, 2010—were collected by chart review of all qualifying participants between May and August 2010. The “Notice of Health Information Privacy Practices” provided to all participants at registration served as informed consent for the research. The study was approved by the University of Michigan Institutional Review Board, PPMSM, and Planned Parenthood Federation of America.

Participants 

Inclusion criteria for the participants reviewed included female sex, age between 19 and 26, and an annual exam between May and July 2010 and an annual exam within the previous 2 years at either of the 2 PPMSM health centers. The inclusion criteria was designed to reflect the FDA—s approval of Gardasil for 9- to 26-year-olds, the Advisory Committee on Immunization Practices— recommendation for routine HPV vaccination of all females, and PPMSM—s policy to offer Gardasil only to females between the age of 19 to 26.

Data Sources/Measurement 

All data were collected through review of the electronic medical records (EMR) at PPMSM. No personally identifiable information was collected, and no participants were contacted. The components of the electronic medical records were developed for clinical use by PPMSM and are updated periodically using input for improvement from all clinicians. Clinic information and self-reported demographic information was gathered from the EMR and measured as indicated in Table 1, Table 2.

Table 1. Demographic Characteristics of Participants (N = 171)

SD = standard deviation.

Table 2. Clinic Characteristics of Participants (N = 171)

The primary outcome for this analysis was HPV vaccine uptake, specifically self-reported or PPMSM clinician-administered series initiation. Uptake was defined as receipt of at least 1 dose of HPV vaccine, even though the regimen consists of a series of 3 doses. Series completion was not considered for the purposes of this study.

Some parts of the EMR were updated by PPMSM between the 2 annual exams as a result of periodic revision of the patient history form and therefore differ slightly in format. To measure HPV vaccine uptake among participants before vaccine availability at PPMSM, participants were asked in the patient history form, “Please indicate which vaccines you have received: …HPV/Gardasil_1_2_3_unsure” at the first annual exam. This was revised to, “Please indicate which vaccines you have received: …HPV/Gardasil × 3 shots_yes_no_unsure” by the second annual exam. Participants who marked yes or any of the numbered injections were considered to have initiated vaccination. Those who marked no or unsure were considered to be unvaccinated. To measure HPV vaccine uptake at PPMSM after it became available there, clinician documentation of the visit note was reviewed. If the visit included documentation of vaccine administration, the patient was considered vaccinated at PPMSM.

The provider was considered to have recommended the vaccine if she checked “__vaccine discussion and/or recommendations” on the patient history form to indicate her recommendation and was considered not to have recommended the vaccine if the prompt remained blank.

Statistical Methods 

Data were evaluated using PASWStatistics 18.0 (IBM Corp, Armonk, New York). Descriptive statistics for the sample were calculated. Following the sample statistics, subgroup descriptive statistics were calculated, including those who received vaccination at PPMSM and those who remained unvaccinated. Any data missing for an individual variable are indicated in the results. Fisher—s exact test was used to calculate statistical significance between those who received vaccination at PPMSM and those who remained unvaccinated.

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Results 

Participants 

Of the 344 women ages 19 to 26 years who received annual exams between May 1, 2010, and July 31, 2010, 171 (49.7%) also received an annual exam within the previous 2 years and were included in the analyses.

Study Population Characteristics 

Demographic characteristics of the study population are shown in Table 1. Overall, the mean age of participants was 23.0 (SD 5 2.0), and the average household income was $18,977.0 (SD 5 $13,938.30). Most of the 171 participants were single (89.5%) and white (62.6%). A majority of the participants were uninsured (71.3%), while 21.6% had private insurance and 7.0% had public insurance. Of the 37 participants with private insurance, 11 did not use their insurance at PPMSM, often because it was not accepted there or the insurance had high deductibles, but they were still considered to be privately insured for the purpose of this study. Most participants (73.1%) had no other sources of health care.

Descriptive clinic characteristics of the study population are shown in Table 2. Participants were divided between the 2 health centers, with 92 (53.8%) participants seen in health center “A” and 79 (46.2%) seen in health center “B.” Most participants (76%) were seen by 2 clinicians, while the remaining 6 clinicians saw 24% of the participants. Despite the PPMSM protocol indicating that clinicians should recommend or offer the HPV vaccine, fewer than half (38.9%) of all participants who were unvaccinated had a clinician-documented recommendation for HPV vaccination at the second annual exam. This differed almost entirely by individual clinician, with some clinicians consistently recommending the vaccine and others consistently not. Provider recommendation was statistically significant (Fisher—s exact test P value 5 0.006) between those who received the HPV vaccine at the annual exam and those who did not. A total of 15.2% (N 5 26) of participants received a report of an abnormal Papanicolaou (Pap) smear at the second annual exam.

HPV Vaccine Uptake 

Eleven percent (n 5 19) of the 171 participants indicated they were already vaccinated. Upon availability of Gardasil at PPMSM during the second annual exam, nine (5.9%) of the 152 participants who did not indicate they were already vaccinated received the HPV vaccine at PPMSM. Thus, the vaccination rate increased from 11% to 16% in the overall population.

Between the first and second annual exam, when Gardasil was not available at PPMSM, 3 individuals indicated they received the vaccine elsewhere and changed their response on the patient history form from unvaccinated at the first annual exam to vaccinated at the second annual exam. Interestingly, 4 others reversed their vaccination status, changing their response from vaccinated at the first annual exam to unvaccinated at the second annual exam, possibly because of the change in wording of the questionnaire.

Almost all of the 9 participants who received the vaccine at the second annual exam were single (88.9%, n 5 8), white (88.9%, n 5 8), and non-Hispanic (88.9%, n 58). Two thirds (n 5 6) who became vaccinated were uninsured, taking advantage of the Merck Vaccine Patient Assistance Program, and one third (n 5 3) had private insurance. One third (n 5 3) had an abnormal Pap smear result at the second visit. All of the vaccines were given by 2 of the 8 clinicians. One clinician, who saw 39.2% (n 5 67) of the participants, gave 55.6% (n 5 5) of the vaccinations, and the second clinician, who saw 9.9% of the participants, gave 44.4% (n 5 4) of the vaccinations.

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Discussion 

Key Results 

In this study of patients receiving annual exams at 2 PPMSM health centers, 5.9% became vaccinated upon availability of the HPV vaccine in the health center, a small number overall but an increase from the 11.1% who were already vaccinated. We hypothesized that increasing the availability of the HPV vaccine, so that participants could receive it when they were already at their annual exam rather than having to make a separate trip to another provider, would substantially improve HPV vaccine uptake. Any additional patient vaccinated can be considered an improvement, especially on an individual level. However, the additional 6% of participants who were vaccinated as a result of vaccine availability at the clinic visit does not provide the large-scale increase necessary for population-level changes that would result in significant reduction in disease.

Other influences are likely contributing to the low uptake. One of the most important influences on HPV vaccine uptake observed in other populations is provider recommendation.⁸, ¹⁰, ¹¹, ¹³, ¹⁴, ¹⁹, ²⁰ However, fewer than half of the participants at PPMSM reported receiving the clinician recommendation, which may have influenced the observed level of uptake.

Cost and insurance coverage has been found to significantly influence vaccine uptake in other populations³, ⁸, ¹⁰, ¹² and likely contributed to low vaccine uptake in this study. In our study—s largely uninsured, low-income population, two thirds of the participants who received HPV vaccination at the second visit used the Merck Vaccine Patient Assistance program for free Gardasil despite the additional $30 injection fee charged by PPMSM. Still, the additional $30 injection fee may make vaccination financially unfeasible for many people. Those participants with public health insurance had to seek vaccination outside of PPMSM as Medicaid does not reimburse PPMSM for the vaccine. Even those with private insurance may not have vaccine coverage and would have to pay the full cost of $160 per dose for the 3-dose series.

Limitations 

One limitation of the study is the use of self-reported measures, especially vaccination status. Young adults may have difficulty remembering if they received the HPV vaccine, or even what the HPV vaccine is, and we had no means of confirming self-reported vaccination status. The patient history form referred to the vaccine in 2 forms, using both the name of the vaccine (Gardasil) and the virus (HPV), intended to help improve the likelihood of an accurate response. Self-reported demographic information, especially annual household income, may also be vulnerable to bias as the health centers— visit fees for uninsured participants are determined by patient household income, thereby providing an incentive for participants to underreport income.

Additional limitations include history and maturation as a result of time between annual exams. Also, participants had 1 to 2 years after their first annual exam to receive the vaccine elsewhere, while participants had only 1 visit to receive the vaccine at the second annual exam before they were measured. Participants may have chosen to return to the health centers for vaccination after the second annual exam, but this time period was not included in measurement.

Another limitation of the study is that 11.1% of participants had already been vaccinated before the vaccine became available at PPMSM. The remaining participants may have been inherently less likely to become vaccinated, as they had not done so in the previous 4 years. Additional vaccine uptake in this age group 4 years after Gardasil—s FDA approval may be limited.

Finally, the primary investigator of this study was employed as a per diem nurse practitioner at the 2 PPMSM health centers, and her visits are included in the analysis to provide a complete and accurate reflection of the data. Her visits represented a small percentage of the total participant population but may be considered by some to be a limitation to the study.

Generalizability 

The ability to generalize results of the study to other reproductive health centers, specifically non-Planned Parenthood centers, may be limited. The study took place at 2 PPMSM health centers, using regularly updated protocols approved by a national organization with resources that may not be available to other centers. As part of a network of 880 Planned Parenthood health centers serving 3 million patients each year, however, the settings may be generalizable across a large portion of the population. Furthermore, 2 clinics were chosen instead of a single site to decrease the chance that the results are specific to a single location.

Selection bias within PPMSM was avoided by using all participants who received annual exams during the defined study time period rather than a sample of the population. However, only participants who received regular annual exams at PPMSM were used and not participants who presented for other types of visits or even participants using PPMSM for a single annual exam. Therefore, this cohort may represent a population more active in preventive health care and perhaps less able to access care at other non-Planned Parenthood sites.

Wide disparities in HPV vaccine uptake have surfaced among states, likely resulting from differences in approaches to cost coverage and accessibility. Massachusetts, for example, achieved 69% vaccination coverage in 2009, while Mississippi lagged behind at 23%.² Michigan—s HPV vaccination rates are below the national average, with 39% of adolescent females initiating the series.² State policy influences were controlled in the study by using only clinic data from Michigan, thus results must be interpreted within this context.

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Implications 

In this study of participants accessing annual exams at 2 PPMSM health centers, we found that improving availability of the HPV vaccine, while helpful, is not sufficient to substantially improve uptake of the vaccine. NPs must also address issues of accessibility, including cost and provider recommendation. Future research that focuses on evaluating interventions for improving cost and provider recommendation in organizations that provide HPV vaccination on site may be helpful to improve HPV prevention for patients.

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Acknowledgment 

This research was conducted with investigator support from the University of Michigan Horace H. Rackham School of Graduate Studies 2010 Spring/Summer Research Grants Program and the Health Promotion/Risk Reduction Interventions with Vulnerable Populations Training Grant (5 T32 NR007073-18).

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References 

1. Brewer NT , Fazekas KI . Predictors of HPV vaccine acceptability: A theory-informed, systematic review . Prev Med . 2007;45(2–3):107–114
   • View In Article
   • CrossRef
2. National, state, and local area vaccination coverage among adolescents aged 13-17 years – United States, 2009 . Morb Mortal Weekly Rep . 2010;59(32):1018–1023
   • View In Article
3. Jain N , Euler GL , Shefer A , et al.   Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States, national immunization survey-adult 2007 . Prev Med . 2009;48(5):426–431
   • View In Article
   • CrossRef
4. Dunne EF , Unger ER , Sternberg M , et al.   Prevalence of HPV infection among females in the United States . JAMA . 2007;297(8):813–819
   • View In Article
   • CrossRef
5. Jemal A , Siegel R , Xu J , et al.   Cancer statistics, 2010 . CA Cancer J Clin . 2010;60(5):277–300
   • View In Article
   • CrossRef
6. Brisson M , Van de Velde N , Boily MC . Economic evaluation of human papillomavirus vaccination in developed countries . Public Health Genomics . 2009;12(5–6):343–351
   • View In Article
   • CrossRef
7. Kim JJ , Goldie SJ . Cost effectiveness analysis of including boys in a human papillomavirus vaccination programme in the United States . Br Med J . 2009;339(b3884):909
   • View In Article
8. Caskey R , Lindau ST , Alexander GC . Knowledge and early adoption of the HPV vaccine among girls and young women: Results of a national survey . J Adolesc Health . 2009;45(5):453–462
   • View In Article
   • CrossRef
9. Chao C , Velicer C , Slezak J , et al.   Correlates for human papillomavirus vaccination of adolescent girls and young women in a managed care organization . Am J Epidemiol . 2010;171(3):357–367
   • View In Article
   • CrossRef
10. Conroy K , Rosenthal SL , Zimet GD , et al.   Human papillomavirus vaccine uptake, predictors of vaccination, and self-reported barriers to vaccination . J Women Health . 2009;18(10):1679–1686
    • View In Article
11. Dempsey AF , Abraham LM , Dalton V , et al.   Understanding the reasons why mothers do or do not have their adolescent daughters vaccinated against human papillomavirus . Ann Epidemiol . 2009;19(8):531–538
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (113 KB)
    • CrossRef
12. Dempsey A , Cohn L , Dalton V , et al.   Patient and clinic factors associated with adolescent human papillomavirus vaccine utilization within a university-based health system . Vaccine . 2010;28(4):989–995
    • View In Article
    • CrossRef
13. Gerend MA , Weibley E , Bland H . Parental response to human papillomavirus vaccine availability: Uptake and intentions . J Adolesc Health . 2009;45(5):528–531
    • View In Article
    • CrossRef
14. Gottlieb SL , Brewer NT , Sternberg MR , et al.   Human papillomavirus vaccine initiation in an area with elevated rates of cervical cancer . J Adolesc Health . 2009;45(5):430–437
    • View In Article
    • CrossRef
15. Jain N , Euler GL , Shefer A , et al.   Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States, national immunization survey-adult 2007 . Prev Med . 2009;48(5):426–431
    • View In Article
    • CrossRef
16. Licht AS , Murphy JM , Hyland AJ , et al.   Is use of the HPV vaccine among female college students related to HPV knowledge and risk perception? . Sex Transm Infect . 2010;86(1):74–78
    • View In Article
    • CrossRef
17. Mathur M , Mathur V , Reichling D . Participation in the decision to become vaccinated against human papillomavirus by California high school girls and the predictors of vaccine status . J Pediatr Health Care . 2010;24(1):14–24
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (238 KB)
    • CrossRef
18. Reiter P , Cates J , McRee A , et al.   Statewide HPV vaccine initiation among adolescent females in North Carolina . Sex Transm Dis . 2010;37(9):549–556
    • View In Article
    • CrossRef
19. Rosenthal SL , Weiss TW , Zimet GD , et al.   Predictors of HPV vaccine uptake among women aged 19-26: Importance of a physician's recommendation . Vaccine . 2011;29(5):890–895
    • View In Article
    • CrossRef
20. Daley E , Vamos C , Buhi E , et al.   Influences on human papillomavirus vaccination status among female college students . J Women Health . 2010;19(10):1885–1891
    • View In Article
21. Planned Parenthood Mission [Internet] . www.plannedparenthood.org Accessed March 30, 2011.
    • View In Article