Health Disparities in Human Papillomavirus Vaccine Coverage: Trends Analysis From the National Immunization Survey-Teen, 2008-2011

Article (PDF Available)inClinical Infectious Diseases 58(2) · October 2013with15 Reads
DOI: 10.1093/cid/cit707 · Source: PubMed
Abstract
Adolescent uptake of human papillomavirus (HPV) vaccine remains low. We evaluated HPV vaccine uptake patterns over 2008–2011 by race/ethnicity, poverty status, and the combination of race/ethnicity and poverty status, utilizing National Immunization Survey–Teen data. Minority and below-poverty adolescents consistently had higher series initiation than white and above-poverty adolescents.
BRIEF REPORT
Health Disparities in Human
Papillomavirus Vaccine Coverage:
Trends Analysis From the National
Immunization SurveyTeen, 2008
2011
Robert A. Bednarczyk,
1,2
Eileen A. Curran,
1
Walter A. Orenstein,
3,4
and Saad B. Omer
1,2,3,4
1
Rollins School of Public Health, Emory University;
2
Center for Health Research
Southeast, Kaiser Permanente Georgia;
3
Emory Vaccine Center and
4
School of
Medicine, Emory University, Atlanta, Georgia
Adolescent uptake of human papillomavirus (HPV) vaccine
remains low. We evaluated HPV vaccine uptake patterns
over 20082011 by race/ethnicity, poverty status, and the
combination of race/ethnicity and poverty status, utilizing
National Immunization SurveyTeen data. Minority and
below-poverty adolescents consistently had higher series ini-
tiation than white and above-poverty adolescents.
Keywords. HPV vaccines; adolescent; vaccination; health-
care disparities; poverty.
Since 2007, the US Centers for Disease Control and Prevention
(CDC) has annually estimated adolescent (ages 1317) immu-
nization coverage, through the National Immunization Survey
Teen (NIS-Teen). These reports have documented adolescent
immunization cove r age successes (eg, rapid increases in uptake of
new vaccines, such as tetanus and diphtheria toxoids, acellular
pertussis vaccine [Tdap], and quadrivalent meningococcal conju-
gate vaccine [MCV4]) as well as remaining challenges (eg, cover-
age levels below Healthy People 2020 goals). Compared to more
rapid increases in Tdap and MCV 4 co ver age since 2008, low er
HPVvaccineuptakehasbeenanintractableproblem[14].
In these reports, the CDC has highlighted atypical demo-
graphic patterns in HPV vaccine series initiation, with HPV
vaccine series initiation higher among Hispanic and black teens
compared to white teens, and among girls below the poverty
line, compared to those at or above the poverty line (hereafter
above poverty)[14]. However, examining vaccination pat-
terns among these characteristics independently may miss
more nuanced health disparities. It has been postulated that
racial disparities should not be analyzed without simultane-
ously considering the contribution of class disparities . . .
Moreover, this approach suggests that class-based health dis-
parities should never be analyzed without simultaneously con-
sidering the contribution of race [5]. We are not aware of
adolescent vaccine uptake analyses taking both of these factors
into account simultaneously over multiple years.
Understanding multiyear patterns in these national estimates
is important to mitigating barriers to greater HPV vaccine
uptake. We conducted this evaluation to (1) assess HPV vaccine
uptake by the combination of race/ethnicity and poverty status
and (2) conduct a multiyear analysis of HPV vaccine uptake,
using 4 years of data (2008 through 2011 NIS-Teen cohorts).
METHODS
Public use data les for the 2008 through 2011 NIS-Teen were
available from the CDC [6]. The NIS-Teen utilizes random
digit dialing to identify households with 13- to 17-year-old ad-
olescents, for whom routine vaccine coverage is measured and
veried wit h the adolescents healthcare provider [6, 7]. We
evaluated uptake of Tdap, MCV4, and HPV vaccine among
female adolesce nts, by race/ethnicity, poverty status, and the
combination of race/ethnicity and poverty status. Socio-
demographic categories were self-reported, and classied as
non-Hispanic white, non-Hispanic black, Hispanic, and other
non-Hispanic, with poverty status assessed by compar ing re-
ported household income to US Census poverty levels [7]. This
analysis was conducted only for female adolescents, for all vac-
cines, to provide the most consistent comparison.
We compared vaccine uptake over the period between 2008
and 2011, and used regression analysis to compute the average
annual increase for a 1-year change in vaccine uptake by the so-
ciodemographic characteristics under study. Analyses were
conducted in SAS version 9.3 (SAS Institute, Cary, North Caro-
lina), using the survey methodspecic procedures PROC
SURVEYMEANS and PROC SURVEYREG, with weights as
provided in the NIS-Teen datasets. Sex- and sociodemo-
graphic-level specic values were computed using domain anal-
ysis in the survey procedures.
Received 29 May 2013; accepted 17 October 2013; electronically published 25 October 2013.
Correspondence: Robert A. Bednarczyk, PhD, Hubert Department of Global Health, Rollins
School of Public Health, CNR, 7020-F, Emory University, 1518 Clifton Rd NE, Atlanta, GA 30322
(rbednar@emory.edu).
Clinical Infectious Diseases 2014;58(2):23841
© The Author 2013. Published by Oxford University Press on behalf of the Infectious Diseases
Society of America. All rights reserved. For Permissions, please e-mail: journals.permissions@
oup.com.
DOI: 10.1093/cid/cit707
238
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Because this analysis utilized existing previously collected
and freely available public data, this was considered to be non
human subjects research and did not require institutional
review board approval.
RESULTS
Overall Coverage
HPV vaccine series initiation increased by approximately 16
percentage points between 2008 and 2011 (from 37.2% to
53%). Over the same period, MCV4 uptake increased by 26.5
percentage points (from 43.1% to 69.6%) and Tdap uptake in-
creased by 37.3 percentage points (from 41.0% to 78.3%).
Coverage by Poverty Status
Since 2008, HPV vaccine series initiation for below-poverty ad-
olescents has been consistently and stably higher than for
above-poverty adolescents (Supplementary Figure 1; Table 1).
The initial difference by poverty status (10.6% higher in below-
poverty adolescents in 2008) persisted over the study period
(12.0% higher in below-poverty adolescents in 2011) (Table 1).
HPV vaccine is the only routinely recommended adolescent
vaccine to exhibit this pattern (Supplementary Figure 1). Series
completion was initially low among below poverty adolescents
(15% in 2008, compared to 19% for above poverty), but
exceeded that of above-poverty adolescents by 2011 (39% vs
33%) (Supplementary Table 1).
Coverage by Race/Ethnicity
HPV vaccine series initiation was consistently highest for His-
panic adolescents, followed by black adolescents, with lowest
uptake among white adolescents (Supplementary Figure 1;
Table 1). Hispanics had both the highest initial coverage
(44.4%) and the greatest increase by 2011 (increase of 20.6 per-
centage points). The average rate of increase for Hispanics was
nearly double that for whites (7.0% vs 3.8% average annual in-
crease, respectively) over this period (Table 1). This pattern is
similar to that for MCV4 coverage (Supplementary Figure 1).
For T dap, white and Hispanic adolescents had nearly identical
vaccine coverage, and black adolescents had slightly, but consis-
tently, lower Tdap coverage (Supplementary Figure 1). More
than 40% of Hispanic females completed the 3-dose series by
2011, whereas all other race/ethnicity groups had completion
percentages ranging from 32% to 35% (Supplementary Table).
Coverage by Race/Ethnicity and Poverty Status
By 2011, above-poverty non-Hispanic white females had the
lowest HPV vaccine series initiation (46.7%), an increase of
only 11% from 2008. Below-poverty Hispanics had the highest
coverage in 2011 (69.2%), following their high initial coverage
Table 1. Uptake of at Least 1 Dose of Human Papillomavirus Vaccine Among Adolescent (Aged 1317) Females, in Aggregate, and by
Poverty Status, Race/Ethnicity, and the Combination of Race/Ethnicity and Poverty Status, United States, NIS-Teen, 2008 2011
Poverty Status
2008 2011
Increase, %, Average Annual
Increase, %
a
% 95% CI % 95% CI 20082011
Overall 37.2 35.139.3 53.0 51.454.7 15.8 5.2
Poverty
Above poverty level 35.8 33.737.9 50.1 48.252.0 14.3 4.8
Below poverty level 46.4 39.753.1 62.1 58.465.9 15.7 4.9
Race/ethnicity
NH white 35.0 32.937.1 47.5 45.649.4 12.5 3.8
NH black 35.7 29.342.2 56.0 51.360.7 20.3 6.4
Hispanic 44.4 37.950.8 65.0 60.969.1 20.6 7.0
NH other 41.8 33.150.6 54.7 48.460.9 12.9 5.0
Race/ethnicity/poverty
NH white, above poverty 35.7 33.438.0 46.7 44.748.7 11.0 3.7
NH white, below poverty 33.6 26.640.5 53.6 47.160.1 20.0 4.6
NH black, above poverty 31.2 24.937.5 52.5 46.158.8 21.3 6.8
NH black, below poverty 45.9 31.360.5 60.2 52.867.6 14.3 4.7
Hispanic, above poverty 39.3 31.447.2 61.9 56.267.6 22.6 8.1
Hispanic, below poverty 53.0 41.864.2 69.2 63.175.4 16.2 5.5
NH other, above poverty 39.5 29.349.7 50.3 43.357.2 10.8 4.4
NH other, below poverty 49.5 32.666.3 65.1 52.477.8 15.6 5.7
Abbreviations: CI, confidence interval; NH, non-Hispanic; NIS-Teen, National Immunization SurveyTeen.
a
As estimated through PROC SURVEYREG.
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in 2008 (53%). For every race/ethnicity group, coverage was
higher among below-poverty adolescents by 2011 (Table 1).
There was less variabilit y in series completion by the combi-
nation of race/ethnicity and poverty status; below-poverty His-
panics again had the highest overall coverage (45%). HPV
vaccine series completion was higher for below-poverty adoles-
cents in the non-Hispanic black, non-Hispanic other, and His-
panic groups compared to their above-poverty peers. Series
completion was the same (33%) for both above- and below-
poverty white adolescents (Supplementary Table 1 ), following a
larger increase in series completion among below-poverty
whites (from 12% to 33%) compared to above-poverty whites
(from 20% to 33%) (Supplementary Table 1).
DISCUSSION
We found that national estimates of HPV vaccine series initia-
tion by adolescent girls demonstrate a consistent pattern of
higher HPV vaccine uptake among adolescents below the
federal poverty level, compared to those above the poverty level.
This nding is unique to the HPV vaccine, and persisted across
racial and ethnic categories.
The nding of lowest HPV vaccination among above-
poverty white adolescents needs further evaluation. This may
be related to ndings of greater active refusal of all childhood
vaccines among mothers who were white, were college educat-
ed, and had higher incomes [8]. It is possible that HPV vaccine
is more often refused by above-poverty whites because of
greater access to routine cervical screening, leading to a lowered
perceived need for the HPV vaccine.
Medically underserved populations with less access to
routine care, especially racial and ethnic minorities, have higher
rates of cervical cancer [9, 10]. Maternal experiences with HPV-
related disease have been associated with greater willingness to
vaccinate daughters against HPV [11]. A recent study identied
increasing safety concerns about the HPV vaccine, relative to
those of Tdap and MCV4, as a contributor to lower HPV
vaccine uptake [12 ]; it is possible that greater awareness of
HPV-related diseases in some populations may overcome
vaccine safety concerns. Continued research is needed on soci-
ocultural impacts of disease awareness within the context of
sociodemographic information, includ ing more in-depth quali-
tative assessment s on the interactions of these factors.
Given the high cost of the HPV vaccine, it has been hypothe-
sized that the Vaccines for Children program may have a
greater impact on HPV vaccine uptake among traditionally un-
derserved populations [14]. However, health insurance plans
provide rst-dollar coverage and/or have no annual deductible
requirements for HPV vaccine at levels consistent with other
routinely recommended adolescent vaccines [13], indicating
little difference in cost-sharing for adolescent vaccines among
privately insured adolescents.
Whereas there are few states with HPV vaccine middle
school entry requirements, 30 states have middle school Tdap
requirements and 22 states have MCV4 requirements [14].
However, even with more states having middle school entry
vaccination requirements for Tdap than for MCV4, Tdap cov-
erage exceeded that of MCV4 by only 8% by 2011.
This evaluation is subject to some limitations. First, because
of relatively small samples of some racial groups (eg, American
Indian/Alaska Native and Asian), we used a 4-level race/ethnic-
ity classication (non-Hispanic white, non-Hispanic black,
Hispanic, non-Hispanic other), which may overlook differences
in other racial groups by poverty status. Future studies speci-
cally addressing poverty-level disparities among these groups
are needed. This study was focused on the effects of race/eth-
nicity and poverty on adolescent vaccination, and did not
address other factors that can affect HPV vaccination, including
provider recommendation [15, 16]. Additional studies are needed
to address the relationship between provider recommendation
and sociodemographic factors. The lack of a SAS procedure for
generalized linear models for complex survey data necessitated
the use of the SURVEYREG procedure to evaluate the average
per-year increase in vaccine coverage, using linear regression.
Although not optimal, this approach will not provide estimates
biased in the same way as logistic regression estimates. Finally,
the available data only spanned 4 years; the 2012 NIS-Teen
publi
c use les were not available at the time of this analysis.
Generally high coverage of Tdap and MCV4 indicates the
potential for high HPV vaccine uptake. Expanded use of de-
tailed surveillance efforts to reach more granular subpopula-
tions of adolescents and greater utilization of multiple years of
data to evaluate consistent disparity patterns are needed to
develop and implement interventions to address disparities in
adolescent immunization coverage.
Supplementary Data
Supplementary materials are available at Clinical Infectious Diseases online
(http://cid.oxfordjournals.org/). Supplementary materials consist of data
provided by the author that are published to benet the reader. The posted
materials are not copyedited. The contents of all supplementary data are the
sole responsibility of the authors. Questions or messages regarding errors
should be addressed to the author.
Notes
Disclaimer. All analyses, interpretations, or conclusions reached are at-
tributed to the authors and not to the National Center for Health Statistics,
which is responsible only for the initial data.
Potential conicts of interest. All authors: No potential conicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conicts of Interest. Conicts that the editors consider relevant to the
content of the manuscript have been disclosed.
240
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    • "This coupled with our observation that later meningococcal/Tdap initiation is strongly associated with later HPV vaccine initiation suggests that there are some females delaying initiation of multiple vaccines while others may just be delaying initiation of the HPV vaccine. This study also found that the age of HPV vaccine initiation is comparable across race/ethnicity, which mirrors the finding that HPV vaccine uptake is fairly similar by race/ethnicity [7], although uptake may be modestly higher among Hispanic females [7,9]. There were some differences between factors for HPV vaccine uptake and age of vaccine initiation. "
    [Show abstract] [Hide abstract] ABSTRACT: Background: Since 2006, routine HPV vaccination has been recommended for females aged 11-12 in the US. However not much is known about the extent of and factors associated with HPV vaccination after the ages of 11-12. Methods: Provider-verified data on 8,710 females aged 13-17 were analyzed from the 2013 NIS-Teen survey. 2013 data was utilized since it was the first year one can fully evaluate the age at vaccination through age 17 for females who could receive the HPV vaccine at age 11. Results: Among HPV vaccinated females who were 17 in 2013, 47% (95%CI=43%-50%) received their first dose after age 12, and 24% (95%CI=21%-26%) received their first dose after age 14. The HPV vaccine was more likely to be initiated later than the meningococcal and Tdap vaccines (p<0.05), and later HPV vaccine initiation was more common among those having a more highly educated mother and those not receiving a check-up/well visit between the ages of 11 and 12 in adjusted analyses (p-values<0.05). Females initiating the HPV vaccine late were more likely to not receive three doses (RR=1.90, 95%CI=1.76-2.04). Conclusions: HPV vaccination is commonly initiated after the age of 12 in the US, which could limit the vaccine's population-level effectiveness.
    Full-text · Article · Dec 2016
    • "A trend analysis of NIS-Teen data for 2008 through 2011 reported that minority and below-poverty adolescents had consistently higher HPV vaccine series initiation than white and above-poverty adolescents. In this analysis, all race/ethnicity groups had completion percentages ranging from 32% to 40% [6]. Overall, these current HPV vaccination rates are well below the Healthy People 2020 goal of an 80% coverage level of 3 doses of HPV vaccine by age 13–15 years [7]. "
    [Show abstract] [Hide abstract] ABSTRACT: Objective: Minority populations in the United States are disproportionally affected by human papillomavirus (HPV) infection and HPV-related cancer. We sought to understand physician practices, knowledge and beliefs that affect utilization of the HPV vaccine in primary care settings serving large minority populations in areas with increased rates of HPV-related cancer. Study design: Cross-sectional survey of randomly selected primary care providers, including pediatricians, family practice physicians and internists, serving large minority populations in Brooklyn, N.Y. and in areas with higher than average cervical cancer rates. Results: Of 156 physicians randomly selected, 121 eligible providers responded to the survey; 64% were pediatricians, 19% were internists and 17% were family practitioners. Thirty-four percent of respondents reported that they routinely offered HPV vaccine to their eligible patients. Seventy percent of physicians reported that the lack of preventive care visits for patients in the eligible age group limited their ability to recommend the HPV vaccine and 70% of those who reported this barrier do not routinely recommend HPV vaccine. The lack of time to educate parents about the HPV vaccine and cost of the vaccine to their patients were two commonly reported barriers that affected whether providers offered the vaccine. Conclusions: Our study found that the majority of providers serving the highest risk populations for HPV infection and HPV-related cancers are not routinely recommending the HPV vaccine to their patients. Reasons for providers' failure to recommend the HPV vaccine routinely are identified and possible areas for targeted interventions to increase HPV vaccination rates are discussed.
    Full-text · Article · May 2014
  • [Show abstract] [Hide abstract] ABSTRACT: Introduction: Human papillomavirus (HPV) infection remains one of the most commonly sexually transmitted infections in both females and males. HPV viruses are associated with several manifestations including genital warts, but more importantly for urology practitioners, cervical and penile carcinomas and recurrent genital condylomata in both sexes. The incidence of HPV-related carcinomas has increased in cervical, oropharyngeal, vulvar, penile, and anal cancers. Effective vaccines have been available for almost a decade, but widespread adoption of vaccine administration has been problematic for multiple reasons. Many countries (over 100) have adopted vaccine programs for females and an increasing number of countries are extending the indications to include males between the ages of 9-26. There still seems to be controversy surrounding these universal vaccination programs as well as some ethical and practical concerns regarding the administration of a vaccine for diseases that are associated with sexual contact in both sexes, especially during the early adolescent years. Objective: The objective was to provide a review of the available literature so pediatric and adult urologists may be more aware of the issues related to HPV vaccination in order to more effectively counsel patients and parents regarding the risks, benefits, and public health issues regarding HPV vaccination. This topic is especially relevant to pediatric urologists who see patients in the target age group for the HPV vaccine. There has been an explosion of literature regarding HPV vaccination programs and the relative difficulty in adopting the vaccine series with a completion rate of under 50% of patients in the recommended age ranges for vaccination. Methods: Articles were obtained from an extensive Medline literature search (1998-present) to evaluate the current HPV vaccination regimens for teenagers with special emphasis on the urologically focused disease burden. Results: The adoption of universal HPV vaccination has been difficult, but appears to be increasing over time as public education improves and governmentally- mandated vaccine programs increase. Despite the ethical concerns raised, the benefits of vaccination with regard to cancer prevention outweigh the risks and potential side effects related to the quadrivalent vaccine administration. Clearly, more follow-up over time is required to document these improvements in public health. Urologists need to remain aware of the prevention strategies for HPV infection and should help with counseling parents and patients in the appropriate age groups for HPV vaccination. Urology providers need to help engage and educate the parents and teenage patients to help promote broader adoption of the HPV vaccine regimen.
    Article · Dec 2014
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