Professional Documents
Culture Documents
Kathleen Conroy, M.D.,1 Susan L. Rosenthal, Ph.D.,2 Gregory D. Zimet, Ph.D.,3 Yan Jin, M.S.,4
David I. Bernstein, M.D., M.A.,5 Susan Glynn, B.A.,6 and Jessica A. Kahn, M.D., M.P.H.6
Abstract
Objective: To describe human papillomavirus (HPV) vaccine uptake, predictors of vaccination, and barriers to
vaccination in young women.
Methods: Participants were 1326-year-old girls and women recruited from an urban, hospital-based clinic.
Between June and December 2007, 6 months after they had completed a baseline survey, they were recontacted
to assess receipt of at least one HPV vaccine dose and barriers to receiving the vaccine. We assessed whether
demographic factors, gynecological history, and attitudes measured at baseline were associated with vaccination
at follow-up using logistic regression.
Results: Of the 262 women who completed the baseline study, 189 (72%) participated in this follow-up study. At
follow-up, 68 of 189 (36%) had received 1 HPV vaccine dose. Factors measured at baseline that predicted
vaccination 6 months later included insurance coverage for HPV vaccination (odds ratio [OR] 5.31, 95% confi-
dence interval [CI] 1.61-17.49) and the belief that ones parents, partners, and clinicians endorsed HPV vacci-
nation (OR 2.21, 95% CI 1.29-3.79); those with a history of an abnormal Pap test were less likely to have received
the vaccine (OR 0.30, CI 0.10-0.92). Of the 121 who were unvaccinated, 54 (45%) had not returned to the clinic
since the baseline study, 51 (42%) had returned but were not offered vaccine, and 15 (12%) had declined
vaccination.
Conclusions: Interventions to increase HPV vaccination rates in women in the catch-up age group for vacci-
nation should ensure that vaccine costs are covered, promote HPV vaccination as normative, and establish clinic-
based systems to prevent missed opportunities for vaccination.
Introduction HPV-18 among women who are not infected with those types
at the time of vaccination.3,4 Given that both high-risk HPV
1
Department of General Pediatrics, Boston Medical Center, Boston, Massachusetts.
2
Division of Adolescent and Behavioral Health, University of Texas Medical Branch at Galveston, Texas.
3
Division of Adolescent Medicine, Indiana University, Indianapolis, Indiana.
4
Department of Biostatistics, University of Cincinnati, Ohio.
5
Division of Infectious Diseases and 6Division of Adolescent Medicine, Cincinnati Childrens Hospital Medical Center, Cincinnati, Ohio.
1679
1680 CONROY ET AL.
of vaccination, and self-reported barriers to vaccination dur- survey conducted in this follow-up study assessed whether or
ing the first 2 years after vaccine licensing. It is especially not the participant had received any doses of HPV vaccine
important to explore these factors among low-income, mi- and, if so, dates of vaccination. All immunization dates were
nority women because they are at relatively high risk for confirmed by reviewing the state immunization registry, and
HPV infection and for developing cervical cancer later in life. any discrepancies were resolved by chart review. Participants
In addition, special attention should be paid to predictors were considered late for the second or third dose of the vac-
of vaccination and barriers to vaccination in the age group cine if the interval between the first and second doses was >4
eligible for catch-up vaccination, as they may experience months or if the interval between the second and third doses
specific barriers to vaccination, including lack of insurance was >6 months. Self-reported barriers to receiving the HPV
coverage. vaccine were assessed only among participants who had yet
Thus, we designed a longitudinal study of predominantly to receive any doses of the HPV vaccine at the time of the
low-income, minority, 1326-year-old girls and women with follow-up interview. These participants were asked whether
the following aims: (1) to describe rates of HPV vaccination in they had not returned to see the physician since enrollment,
this sample approximately 1218 months after the quadriva- had returned but not been offered the vaccine, or had been
lent HPV vaccine was licensed, (2) to identify which demo- offered the vaccine but did not receive it. Participants indi-
graphic, attitudinal, behavioral, and health systems-related cating that they did not receive the vaccine when offered were
factors measured at baseline predicted actual vaccine receipt then asked why they did not. They were prompted from a list
at follow-up, and (3) to identify self-reported barriers to HPV of 10 possible reasons, including an open-ended response
vaccination among those who had not received the vaccine at category, and were allowed to select multiple reasons. Parti-
follow-up. cipants who had received at least one dose of vaccine but were
late for their second or third vaccine doses (or both) were also
asked to report one or more reasons why they were unable to
Materials and Methods
get the vaccination on time; they were prompted from a list
The study sample comprised 1326-year-old girls and of 8 possible reasons, including an open-ended response
women recruited from an urban, hospital-based teen health category.
center who had previously participated in a multisite baseline We used insurance information collected during the base-
study that assessed cervicovaginal HPV infection as well as line study to create a new variable indicating whether each
attitudes toward HPV vaccination.9 Inclusion criteria for the participant was likely to have coverage for the HPV vaccine
baseline study included a history of sexual contact with a man through either private insurance, Medicaid, or the Vaccines
or a woman and ability to complete a survey in English or for Children Program. Insurance plan information collected
Spanish. The participants provided written consent to par- at baseline was highly correlated with insurance informa-
ticipate in the baseline study (a requirement for parental tion collected at the time of the follow-up survey (r 0.71,
consent was waived) and were asked if they were willing to be p < 0.0001).
contacted by phone at a later date to ask if they would be The primary outcome variable was receipt of at least one
interested in participating in a follow-up study. When par- HPV vaccination, and the secondary outcome variables were
ticipants were recontacted for the follow-up study, verbal self-reported barriers to receiving at least one HPV vaccina-
consent was requested, and those who consented completed a tion. Exploratory outcomes included reasons why those who
phone survey. The baseline cohort was enrolled between had been offered the vaccine between the baseline and follow-
November 2006 and May 2007. The follow-up study was up study visits had not received it and reasons why partici-
performed approximately 6 months after each participant was pants had received a second or third dose late.
enrolled in the original study, between June and December We first examined if demographic, attitudinal, and be-
2007. At the beginning of the follow-up study, the HPV vac- havioral variables measured at baseline were associated with
cine had been available in the clinic for approximately receipt of at least one HPV vaccine dose at follow-up, using
6 months (Fig. 1). This study was approved by the Cincinnati chi-square analysis for dichotomous predictor variables and a
Childrens Hospital Medical Center Institutional Review Wilcoxon rank-sum test for ordinal variables. Those variables
Board. associated with vaccination at p < 0.05 were entered into a
The survey completed by participants at baseline assessed multivariable logistic regression model to identify baseline
demographic factors, gynecological history, risk behaviors, variables independently associated with receipt of the HPV
HPV knowledge, beliefs about HPV and HPV vaccines, HPV vaccine; a stepwise procedure was used for variable selection.
vaccination history, and both intention and self-confidence to We found evidence for collinearity between age and the var-
receive the HPV vaccine.9 Participants received written in- iable measuring coverage for the HPV vaccine and, therefore,
formation about HPV infection and HPV vaccines. The phone did not include age in the multivariable model.
6/06 7/06 8/06 9/06 10/06 11/06 12/06 1/07 2/07 3/07 4/07 5/07 6/07 7/07 8/07 9/07 10/07 11/07 12/07
FIG. 1. Timeline: HPV vaccine licensing, vaccine availability, recruitment for baseline study, recruitment for follow-up
study.
HPV VACCINE UPTAKE, PREDICTORS, AND BARRIERS 1681
1682
HPV VACCINE UPTAKE, PREDICTORS, AND BARRIERS 1683
Vaccine recall and reminder systemsin which clinics contact and barriers to vaccination will be helpful in designing in-
patients by mail or phone to remind them to make or keep terventions to improve HPV vaccination recommendations.
vaccine appointmentsare known to be effective in increas- Of the 121 subjects reporting barriers to vaccination, <5%
ing vaccination rates in both children and adults18 and might reported concerns about safety and efficacy, echoing pre-
be effective in increasing rates of HPV vaccination. Proactive licensing studies that reported high acceptability of an HPV
outreach to girls in the target age group for catch-up immu- vaccine among young adults.29,30 Of the 10 subjects who re-
nization may be particularly important for HPV vaccination ported concerns about insurance as a reason for refusing
efforts because the vast majority of young women initiate vaccine, 5 did in fact have insurance coverage for vaccination,
sexual activity and are at high risk for acquiring HPV infection consistent with prior research demonstrating that recipients
during the years when they are eligible for catch-up vacci- of both private and public insurance plans may underestimate
nation.19,20 In our sample, for example, 43% of girls reported their benefits.31 In addition to recall and reminder systems for
having a new sexual partner in the past 3 months. As vacci- patients and providers, healthcare personnel should help
nation appears to have no therapeutic benefit in women al- patients to understand their insurance benefits for vaccination
ready infected with vaccine-type HPV at the time of if concerns arise.
vaccination,4 the individual and public health benefits of Contrary to our expectations, intention to receive the HPV
vaccination in the catch-up age group will depend on vaccine was not associated with having received the vaccine
timely vaccination. Recall and reminder systems for vacci- at the time of follow-up. The previously published baseline
nation were not in place at the state, local, or clinic level at the study in this same cohort examined the correlations among
time of this study. Establishing such systems for young demographic, behavioral, and attitudinal factors and inten-
women in this age group may help maximize both vaccina- tion to vaccinate at baseline.9 With the exception of history of
tion rates and the health benefits of vaccination. an abnormal Pap test, all the predictors found to be signifi-
The second most commonly cited reason for not getting cantly associated with intention to be vaccinated in the
vaccinated was not being offered the vaccine despite return- baseline study were also predictive of actual vaccination in
ing to the physicians office during the study period. A clini- this study. Given the short follow-up period and the fact that
cian may not have recommended HPV vaccination during an 90% of those not vaccinated had either not returned to the
office visit if a participant was moderately or severely ill, in physician or had not been offered the vaccine, it is likely that
which case vaccination is not recommended. In other cases, many of those intending to receive the HPV vaccine simply
however, a clinician may have missed an opportunity to did not have the opportunity to do so during the follow-up
vaccinate a young woman seeking treatment for a mild illness period. Studies with longer follow-up periods will likely be
or another reason. Given the importance of timely vaccination necessary to definitively assess whether intention to receive
in this age group, office-based interventions may be helpful in the vaccine predicts actual receipt of the vaccine.
maximizing vaccination rates, for example, office-based pro- Our study has several limitations. Participants were re-
cedures that identify patients eligible for vaccination.21,22 cruited from a hospital-based adolescent primary care clinic
Other reasons clinicians do not recommend HPV vaccination serving a racially and ethnically diverse, predominantly low-
may have to do with their attitudes about the vaccine or income population. Generalization from this population is
specific barriers to recommending the vaccine. In prelicensing limited both by the demographic composition of our sample
studies, providers reported largely positive attitudes about and their connection to clinical care. However, initial re-
recommending HPV vaccines.2326 However, little informa- cruitment took place during both ill visits and health main-
tion is available concerning actual clinician recommendations tenance visits, and the follow-up study did not require a
for HPV vaccines. As clinician recommendation is one of the repeat clinical visit; thus, there was at least some variation in
most important predictors of vaccination,17,27,28 further in- terms of connectedness to care. Those who participated in the
formation about clinicians attitudes, prescribing practices, follow-up study may differ from those who did not partici-
HPV VACCINE UPTAKE, PREDICTORS, AND BARRIERS 1685
pate; however, there were no baseline characteristics that Rockville, MD: National Cancer Institute, Center to Reduce
differed in the two groups. The study sample consisted of Cancer Health Disparities. Report No. NIH Pub. No. 05-
those previously enrolled in a study of attitudes about HPV 5282, 2005.
vaccines; thus, participants could have had inherently higher 7. Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that
interest in HPV vaccination or be more likely to get the vac- are associated with parental acceptance of human papillo-
cine. In addition, the barriers to vaccination in this study are mavirus vaccines: A randomized intervention study of writ-
self-reported, and although they provide information about ten information about HPV. Pediatrics 2006;117:14861493.
the young womens perceived barriers, they are subject to 8. Zimet GD, Liddon N, Rosenthal SL, Lazcano-Ponce E, Allen
recall error. Finally, our study followed this population for B. Psychosocial aspects of vaccine acceptability. Vaccine
2006;24(Suppl 3):S201209.
only 6 months after initial recruitment and, therefore, reports
9. Kahn JA, Rosenthal SL, Jin Y, Huang B, Namakydoust A,
relatively short-term predictors of vaccination. However,
Zimet GD. Rates of human papillomavirus vaccination, atti-
conducting such a study soon after the HPV vaccine was li-
tudes about vaccination, and human papillomavirus preva-
censed should provide useful preliminary information for the lence in young women. Obstet Gynecol 2008;111:11031110.
timely design of interventions that address barriers and aim to 10. Bartlett D, Williams L, Curtis R. Uptake of HPV vaccine:
improve vaccination rates. Immunization Information Systems Sentinel Sites. In: 2008
National STD Prevention Conference: Chicago, IL, March 11,
Conclusions 2008.
Our data suggest that strategies to ensure that those who 11. Vaccination coverage among adolescents aged 1317
are eligible for catch-up immunization are vaccinated should yearsUnited States, 2007. MMWR 2008;57:11001103.
12. Rosenthal SL, Rupp R, Zimet GD, et al. Uptake of HPV vac-
include attention to young womens attitudes about vacci-
cine: Demographics, sexual history and values, parenting
nation and to the implementation of office-based procedures
style, and vaccine attitudes. J Adolesc Health 2008;43:239
to ensure that clinicians do not miss opportunities for vacci-
245.
nation. Ensuring that all young women in this age group are 13. Brabin L, Roberts SA, Stretch R, et al. Uptake of first two
able to afford vaccination will help to avoid an increase in doses of human papillomavirus vaccine by adolescent
existing racial and economic disparities in cervical cancer schoolgirls in Manchester: Prospective cohort study. BMJ
mortality. 2008;336:10561058.
14. Adams SH, Newacheck PW, Park MJ, Brindis CD, Irwin CE
Disclosure Statements Jr. Health insurance across vulnerable ages: Patterns and
disparities from adolescence to the early 30s. Pediatrics
K.C., Y.J., and S.G. have no conflicts of interest to report. 2007;119:e10331039.
S.L.R. is a co-principal investigator with G.D.Z. on an 15. Sturm LA, Mays RM, Zimet GD. Parental beliefs and deci-
investigator-initiated grant from Merck and is a research con- sion making about child and adolescent immunization:
sultant for Merck. G.D.Z. is a research consultant for Merck From polio to sexually transmitted infections. J Dev Behav
and a co-principal investigator on an investigator-initiated Pediatr 2005;26:441452.
grant from Merck. D.I.B. has received honoraria from Glaxo- 16. Mok E, Yeung SH, Chan MF. Prevalence of influenza vac-
SmithKline, Alpha Vax, Vical, Medimmune, and Novartis, for cination and correlates of intention to be vaccinated among
whom he has served as an advisor. He has received a royalty Hong Kong Chinese. Public Health Nurs 2006;23:506515.
from Glaxo-SmithKline for work on the rotavirus vaccine. 17. Daley MF, Crane LA, Chandramouli V, et al. Influenza
J.A.K. is a co-principal investigator on an NIH-funded study among healthy young children: Changes in parental atti-
of HPV vaccination of HIV-infected adolescents, for which tudes and predictors of immunization during the 2003 to
Merck is providing vaccine and immunogenicity testing. 2004 influenza season. Pediatrics 2006;117:e268277.
18. Jacobson VJ, Szilagyi P. Patient reminder and patient recall
systems to improve immunization rates. Cochrane Database
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