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Vaccine. Author manuscript; available in PMC 2021 October 07.
Published in final edited form as:
Vaccine. 2020 October 07; 38(43): 6730–6734. doi:10.1016/j.vaccine.2020.08.048.
County-level correlates of missed opportunities for HPV
vaccination in Indiana: An environmental scan
Sharon C. Enujiokea, Rivienne Shedd-Steeleb, Joanne Daggyc, Heather Burneyd, Lisa
Robertsone, Katharine Headf, Gregory Zimetg,*
a.Indiana
100th
University School of Medicine, Department of Pediatrics-Adolescent Medicine. 410 W.
Street. Ste 100. Indianapolis, IN 46202, USA.
Author Manuscript
b.Indiana
University Simon Cancer Center. 535 Barnhill Dr. Indianapolis, IN 46202, USA.
University School of Medicine, Department of Biostatistics. 410 W. 10th St. Indianapolis,
IN 46202, USA.
c.Indiana
University School of Medicine, Department of Biostatistics. 410 W. 10th St. Indianapolis,
IN 46202, USA.
d.Indiana
e.Indiana
Immunization Coalition. 6239 S East St. Indianapolis, IN 46227 USA.
f.Indiana
University-Purdue University Indianapolis, Department of Communication Studies, 425
University Boulevard, Indianapolis, IN 46202, USA.
g.Indiana
Author Manuscript
100th
University School of Medicine, Department of Pediatrics-Adolescent Medicine. 410 W.
Street. Ste 100. Indianapolis, IN 46202, USA.
Abstract
Background: The goal of this study was to examine variability across the 92 Indiana counties in
missed opportunities for HPV vaccination and to assess county-level correlates of missed
opportunities.
Methods: The Indiana immunization registry provided county level data on 2017 missed
opportunity rates for adolescents ages 11-18. A missed opportunity was an encounter when a
patient eligible for HPV vaccination received one or more other recommended vaccines, but not
HPV. Potential county-level correlates of missed opportunities included race, income, insurance
Author Manuscript
*
Corresponding author. gzimet@iu.edu.
Declaration of Competing Interest
Sharon Enujioke has no interest to disclose.
Rivienne Shedd-Steele has no interest to disclose.
Joanne Daggy has no interest to disclose.
Heather Burney has no interest to disclose.
Lisa Robertson has no interest to disclose.
Katharine J. Head has no interest to disclose.
Gregory Zimet received travel funding from Merck to present research at a scientific conference and received honoraria from Sanofi
Pasteur and Merck for consultations related to adolescent vaccination.
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our
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Enujioke et al.
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status, population density, education, primary care providers per capita, smoking rates,
mammography screening, diabetes monitoring, and Pap testing.
Results: The missed opportunity rate ranged from 31% to 85% across Indiana counties. Higher
population density, mammography screening, income inequality, and diabetes monitoring were
associated with fewer missed opportunities.
Conclusions: We found wide variability in missed opportunities across counties, which were
associated with population density and county-level participation in other health-related behaviors
Keywords
Vaccination; HPV Vaccination; Health Status; Adolescence; Immunization Surveillance
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Human papillomavirus (HPV) is the most common sexually transmitted infection in the
United States. An estimated 14 million persons are newly infected every year. HPV is also
the primary cause of genital warts and is a major contributing factor in at least six cancers:
cervical, vulvar, vaginal, penile, anal, and oropharyngeal. [1]
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Currently only one HPV vaccine, the 9-valent vaccine (9vHPV) is available in the U.S. and
is licensed by the Food and Drug Administration (FDA) for use in males and females 9
through 45 years of age [2]. The Center for Disease Control’s (CDC) Advisory Committee
on Immunization Practices (ACIP) recently issued an updated set of recommendations for
HPV vaccination.[3] The guidelines continue to indicate that HPV vaccine should be
routinely administered to females and males ages 11 and 12 years and that vaccination can
start as early as age 9 years. They also recommend routine catch-up vaccination for all
females and males from ages 13 through 26 years, with a shared clinical decision-making
approach recommended for individuals 27 through 45 years of age.[3] The ACIP currently
recommends two doses of vaccine 6-12 months apart if the first dose is administered before
age 15 years, with a three-dose recommendation for those who get the first dose at age 15
years or older. [4] The Healthy people 2020 goal is for 80% of adolescents to have
completed their HPV vaccination series. In the United States, the HPV vaccination
completion rate in 13-17 year olds is 51.1%, lagging behind the Healthy People 2020 goal.
[5]
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Although Indiana HPV vaccination rates have shown steady progress over the years,
initiation of vaccination continues to lag in comparison to the national average. In 2017,
when data for the current study were collected, Indiana had a 59.3% initiation rate among
adolescents ages 13-17 years, ranking 40th in the United Stated.[6] In comparison, Indiana
ranks in the top ten for administration of the tetanus, diphtheria, pertussis (Tdap; 93.1%) and
meningococcal ACWY (MenACWY; 95%) vaccines. The discrepancies in vaccination rates
between HPV and Tdap/MenACWY are significant, as Tdap and MenACWY are usually
administered at 11-12 years of age, the same age that the ACIP recommends initiating HPV
vaccination.[6] There could be several reasons for the discrepancies. For instance, Indiana
code IC 20-34-4-2 mandates Hepatitis A, Tdap, and MenACWY for middle school entry
(ISDH), but not HPV vaccine.[7] Another reason could be a weak recommendation (or no
recommendation) for HPV vaccination from a health care provider (HCP).[8] A missed
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opportunity is classified as a health care encounter when a patient eligible for HPV
vaccination received one or more other recommended vaccinations, but not the HPV
vaccine.[9]
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Indiana is made up of 92 counties that vary greatly with respect to population density, access
to healthcare, and other sociodemographic factors. A study of HPV vaccination rates across
the state of Utah showed that there was substantial variability in missed opportunities,
suggesting this may be the case for other states.[10] The purpose of the present study was to
similarly document county level variability in missed opportunities for adolescent HPV
vaccination in Indiana and to examine county level factors that may be associated with
missed opportunities across the 92 counties. The findings from this study can provide
important insight into different county characteristics associated with vaccination rates,
which could be useful when developing geographically-targeted interventions to improve
adolescent HPV vaccination rates.
MATERIALS AND METHODS
This study examined missed opportunities across Indiana’s 92 counties for initiating HPV
vaccination amongst adolescents 11-18 years of age during the 2017 calendar year. We
included age 18 as the upper limit, because the Vaccines for Children (VFC) program covers
vaccination through age 18 years. The data were extracted from the Indiana State
Department of Health (ISDH) Indiana Immunization Information System (IIS), also known
as CHIRP (Children and Hoosier Immunization Registry Program). The Indiana University
Institution Review Board made the determination that this study was exempt from review.
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MEASURES
The outcome variable of interest, a missed opportunity for HPV vaccination during the 2017
calendar year, was defined as a clinical visit during which an HPV-vaccine-eligible
adolescent between the ages of 11-18 received one or more vaccines (i.e., Tdap, MenACWY,
Hepatitis A), but not the first dose of HPV vaccine. Since the influenza vaccine is seasonal,
receipt of the influenza vaccine was not counted as a missed opportunity. We retrieved
county-level adolescent immunization data from CHIRP, which is a secure web-based
immunization registry program that permanently stores immunizations records. It is
administered by the ISDH, which mandates that all immunization providers enter vaccine
administration information for all individuals under the age of 19. No patient-level
information (other than age group) or information on race/ethnicity was available through
the CHIRP database.
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We derived county-specific socio-demographic and health data from two sources: the 2010
U.S Census (https://www.census.gov/programs-surveys/decennial-census/decade.2010.html)
and the 2018 County Health Rankings report (https://www.countyhealthrankings.org/), a
program supported by the Robert Wood Johnson Foundation. From the measures available,
we selected measures that focused on sociodemographic characteristics and health-related
factors, including population density per square mile, percentage rural, primary care
providers and mental health providers per capita, dental providers per capita, race, rates of
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mammography screening (i.e., percentage of female Medicare enrollees ages 67-69 that
receive mammography screening), median household income, income inequality, diabetes
monitoring (i.e., percentage of Medicare enrollees with diabetes ages 65-75 that receive
HbA1c monitoring), rates of smoking, and parental education. See Table one for a complete
list of measures and the source of each measure. Although the mammography screening and
diabetes monitoring measures involve older populations, we included them as variables that
might indirectly reflect county-level access to care and utilization of health resources.
STATISTICAL METHODS
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Descriptive statistics were reported for all covariates and outcomes at the county level.
County-level variables considered as potential covariates in this analysis include population
density per square quarter mile, percentage of individuals with certain educational
attainment levels (i.e., less than a high school diploma, only a high school diploma, some
college, or Bachelor’s degree or higher), percentage of smokers, percentage of women with
mammography screening, median household income, percentage of racial groups (i.e.,
African Americans, Hispanics, Non-Hispanic Whites), percentage of the county that is rural,
income inequality ratio, dentists per capita, mental health providers per capita, percentage of
individuals who engage in diabetes monitoring, and total number of primary care providers
per 100,000.
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Generalized linear mixed models (GLMM) with a binomial distribution and logit link were
used to determine county-level covariates that were independently associated with the
proportion of missed opportunities for HPV vaccination, while adjusting for the patient-level
covariate of age group (11-12 years old vs 13-18 years old). [11] A random intercept for
county was included to account for correlation of outcomes from patients in the same
county.
For model-building univariable GLMMs were fit, which included age group and each
candidate covariate. Odds ratios and associated 95% confidence intervals are reported.
Covariates significant at the 0.05 level in univariable models were then included in a
multivariable model. The intraclass correlation (ICC) of the outcome was estimated from a
model which included only the county-level random intercept and from the full model. From
the estimates of the ICC the percent of variability in the county-level proportions of missed
opportunities explained by the patient age group and county-level covariates was estimated.
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To determine if the effect of the important county-level covariates differed by age group, all
two-way interactions between age group and the county-level covariates were then included
in the model. The logistic regression model with the final selected county-level covariates
was then fit separately by age-group. Odds ratios and the associated 95% profile-likelihood
confidence intervals are reported. All analysis was conducted with SAS V9.4 (Cary, NC).
RESULTS
Descriptive statistics of the 92 counties in Indiana is outlined in Table 1. Table 2 provides
summary statistics for the proportion of missed opportunities for HPV vaccination for the
state of Indiana. There were significant missed opportunities, with 33% of counties having
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greater than 66% missed opportunities for receiving HPV vaccination. The mean proportion
of missed opportunities for adolescents’ ages 11-18 years was 60%, with 57% missed
opportunities in the 11-12 age group and 61% missed opportunities in the 13-18 age group
(Table 2). The proportion of missed opportunity was significantly higher in children 13-18
years of age vs 11-12 years of age, OR = 1.12, 95% CI = [1.10, 1.14], p-value < 0.0001.
From the logistic regression models adjusting for only age group (Table 3), increases in
population density (p=.02), mammography screening (p<.0001), income inequality (p=.03),
and diabetes monitoring (p=.0006) are significantly associated with less missed
opportunities.
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Based on the intracluster correlation (ICC) of the intercept-only model (ICC = .07), 7% of
the variability in missed opportunities was due to variability between counties. From the full
model including interaction terms (ICC = 0.052), only 5.2% of the total variability was due
to variability between counties, thus patient age group and county-level factors explained
25.7% of the county-level variability in missed opportunities. The addition of the interaction
terms provided an improved model fit compared to the model including only main effects
based on the likelihood ratio test (p < 0.0001), thus the effect of these county-level factors on
missed opportunities varied by age group.
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From the final logistic regression model (Table 4), the two-way interaction terms between
each of the four factors and age group were all statistically significant (all p < 0.01). Thus, a
separate logistic regression model was fit to each age group including the main effects of
population density, mammography screening, income inequality, and diabetes monitoring.
For both age groups, lower population density, lower income inequality ratio, and lower
percentage of individuals who engage in diabetes monitoring were associated with higher
risk of missed opportunities. The odds ratio for population density was smaller for the 13-18
year-old age group indicating a more pronounced association for this age group, whereas the
association of income inequality ratio and diabetes monitoring was less pronounced in the
13-18-year-old age group (see Table 5).
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For the 13-18 year-old age group, a higher percentage of women with mammography
screening was associated with lower risk of a missed opportunity (OR = 0.90, 95% CI
=[0.89, 0.92]) which is what we would expect. However, for the 11-12 year-old group, the
association was reversed (OR = 1.04, 95% CI =[1.01, 1.07]). In univariable results for the
11-12 year old group, we found that mammography screening was in the direction we would
expect (OR = 0.95, 95% CI = [0.92,0.98]) but not when including the three variables of
population density, income inequality ratio, and diabetes monitoring. Thus, we ran
additional logistic regression models for this age group by examining the inclusion of each
of these variables one at a time with mammography screening. We found that if diabetes
monitoring only is included, mammography screening is no longer statistically significant
(OR = 1.00, 95% CI =[0.96, 1.03], p-value = 0.766). Thus, mammography screening and
diabetes monitoring are highly related in this age group.
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DISCUSSION
The findings from this study indicate wide variability in missed opportunities for HPV
vaccination across the 92 counties in Indiana, results similar to those reported by Kepka et
al., who found extensive missed opportunities across Utah. [10] Although Indiana does not
require HPV vaccine for entry into middle school (6th grade), it does require students to
receive Tdap, MenACWY, and Hepatitis A vaccines. Therefore, there should be ample
opportunities to improve HPV vaccine delivery at the appropriate target age of 11-12 years
old.
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Keeping in mind that we were only looking at county-level factors, the association between
increased mammography screening and diabetes monitoring with less missed opportunities,
particularly in the older age group, may reflect county-level issues related to engagement
with, and orientation to, health. Even though health care providers per capita was not related
to missed opportunities, in sparsely populated counties, it may nonetheless be challenging to
access health care. In support of this idea is the finding that counties with lower population
density had higher missed opportunities, a result also reflected in NIS-Teen data [5], which
show lower vaccine coverage in rural vs. urban areas.
Although 2018 National Immunization Survey-Teen data have shown racial/ethnic
disparities in HPV vaccinations (NIS-Teen Supplementary Table 1) [5], this study did not
find variability in missed opportunities related to race/ethnicity, which may simply be a
reflection of the fact that our analyses could only consider race as a county-level variable
(e.g., percentage of African Americans). A lower missed opportunity rate was associated
with greater income inequality, which might be attributed to income inequality being higher
in urban areas.[12]
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The findings from this study are consistent with the framework of Bronfenbrenner’s SocialEcological Model, which considers how factors at the community and societal level can
influence relationship-level factors and individual behaviors.[13] We found, for instance,
that county-level measures (e.g., population density and engagement in mammography
screening) were associated with missed opportunities for HPV vaccination. Although
parental beliefs and health care provider recommendation are strong proximal determinants
of HPV vaccination, findings from this study suggest that it may be important to consider
the ways in which these proximal factors influence, and are influenced by, larger community
characteristics.
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A strength of this study was the availability of comprehensive vaccination data from the
Indiana IIS, which mandates that all vaccine providers submit vaccination records for all
persons under 19 years of age. These data enabled us to accurately assess missed
opportunities for HPV vaccination at the county level. A limitation of this study was the
focus on a single state in the U.S., which limits generalizability of the results to other states.
Also, we were constrained by the availability of only county level data, which necessarily
limited our ability to identify a full range of potential correlates of missed opportunities.
Furthermore, we were not able to obtain a county-level breakdown of missed opportunities
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by race or gender. Finally, we could not track follow-up data for individual adolescents to
determine if they had received HPV vaccine at a separate clinical visit.
CONCLUSION
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This study evaluated missed opportunities for adolescent HPV vaccination across the 92
counties in Indiana. We found wide variability in missed opportunities from county to
county, which were associated with population density and county-level participation in
other health related behaviors. Findings suggest that interventions designed to improve HPV
vaccine coverage may need to consider and target smaller geographic areas. The use of the
IIS data set can help identify counties that have high missed opportunities for HPV
vaccination, therefore indicating a need for a deeper understanding of the barriers present in
each of those counties. This study also reinforces the need to address rural-urban disparities
and suggests there is a need to better understand the difference across counties in orientation
towards health and access to healthcare.
Acknowledgments
Funding/Support
This study was supported by the National Cancer Institute under Award number P30CA08270918S4.
References
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title-20-education/in-code-sect-20-34-4-2.html [accessed January 13, 2020].
8. Sturm L, Donahue K, Kasting M, Kulkarni A, Brewer NT, Zimet GD. Pediatrician-Parent
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9. Oliveira CR, Rock RM, Shapiro ED, et al. Missed opportunities for HPV immunization among
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10. Kepka D, Spigarelli MG, Warner EL, Yoneoka Y, McConnell N, Balch A. Statewide analysis of
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11. Brown HP, Prescott R. Applied Mixed Models in Medicine. New York, NY: John Wiley and Sons,
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12. Bishaw A, Posey KG. A comparison of rural and urban America: Household income and poverty.
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Table 1
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Descriptive statistics for county-level variables (N = 92).
Variable
Mean ± Standard Deviation
Population 2010 Census
70.476 ± 116.748
Density Per Square Mile 2010 Census
11.1 ± 17.60
Percentage with Less than HS Diploma
12.7 ± 4.03
Percentage with HS Diploma
39.8 ± 6.21
Percentage with Some College
28.9 ± 2.81
Percentage with Bachelors or More
18.7 ± 8.02
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Percentage of Smokers
19.7 ± 1.95
Percentage with Mammography Screening
60.2 ± 5.92
Median Household Income ($)
52,606 ± 8,525.2
Percentage of African Americans
2.8 ± 4.46
Percentage of Hispanics
4.0 ± 3.51
Percentage of Non-Hispanic Whites
90.6 ± 7.72
Percentage of Rural
54.5 ± 26.91
Income Inequality Ratio
4.0 ± 0.47
Dentists Per Capita
39 ± 17.2
Mental Health Providers Per Capita
87 ± 71.7
Diabetes Monitoring
85 ± 6.7
Tout PCP Kate per 100,000
102 ± 46.3
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Table 2
Mean ± Standard Deviation (N = 92)
Median (25th–75th Percentile)
Minimum
Maximum
Missed Opportunities 11–12 Years
0.56 ± 0.13
0.55 (0.46–0.65)
27%
94%
Missed Opportunities 13–18 Years
0.61 ± 0.11
0.61 (0.51–0.68)
31%
84%
Missed Opportunities 11–18 Years
0.60 ± 0.11
0.60 (0.51–0.67)
31%
85%
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The proportion of missed opportunities summarized across counties by age group.
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Table 3
Effect
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*
Unit Increase
Odds Ratio, 95% CI
p-value
Density Per Square Mile 2010 Census
100
0.51 [0.29, 0.91]
0.023
Percentage with HS Diploma
10
0.91 [0.77, 1.08]
0.275
Percentage with Some College
10
1.42 [0.99, 2.04]
0.057
Percentage with Mammography Screening
10
0.72 [0.61, 0.84]
<0.0001
Median Household Income (thousands)
10
1.03 [0.91, 1.16]
0.638
Percentage of African Americans
10
0.84 [0.67, 1.06]
0.142
Percentage of Hispamcs
10
1.01 [0.75, 1.36]
0.926
Percentage of Non-Hispanic Whites
10
1.10 [0.96, 1.26]
0.161
Percentage of Rural
10
1.04 [1.00, 1.08]
0.063
Income Inequality Ratio
1
0.79 [0.64, 0.98]
0.034
Dentists Per Capita
10
0.95 [0.90, 1.01]
0.112
Mental Health Providers Per Capita
10
0.99 [0.98, 1.01]
0.210
Diabetes Monitoring
10
0.77 [0.66, 0.89]
0.001
Total PCP Rate per 100,000
10
0.98 [0.96, 1.00]
0.093
p < 0.05
*
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Logistic regression with each effect and age group only.
*
*
*
Indicates a statistically significant effect.
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Table 4
Effect
Intercept
Estimate
SE
Num DF
Den DF
F Value
p-value
4.221
0.805
-
-
-
-
Age Group (13–18)
−0.344
0.209
1
85
2.72
0.103
Density Per Square Mile
−0.001
0.003
1
85
0.58
0.450
Percent Mammography Screening
−0.010
0.008
1
85
4.20
0.043
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Income Inequality Ratio
−0.334
0.105
1
85
5.17
0.026
Diabetes Monitoring
−0.024
0.007
1
85
8.48
0.005
Density Pet Square Mile * Age Croup (13–18)
−0.003
0.0002
1
85
158.92
<0.0001
Percent Mammography * Age Croup (13–18)
−0.013
0.002
1
85
53.68
<0.0001
Income Inequality Ratio * Age Croup (13–18)
0.198
0.019
1
85
109.37
<0.0001
Diabetes Monitoring * Age Croup (13–18)
0.007
0.002
1
85
9.53
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Final multivariable logistic regression model with age interaction terms.
0.003
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Table 5
Age Group (11–12)
Effect
Unit Increase
Age Group (13–18)
Odds Ratio, 95% CI
p-value
Odds Ratio, 95% CI
p-value
Density Per Square Mile
100
0.79 [0.76 ,0.82]
<0.0001
0.60 [0.59 ,0.61]
0.023
Percent Mammography Screening
10
1.04 [1.01 ,1.07]
0.021
0.90 [0.89 ,0.92]
<0.0001
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Income Inequality Ratio
1
0.71 [0.69, 0.74]
<0.0001
0.88 [0.87, 0.89]
<0.0001
Diabetes Monitoring
10
0.72 [0.69, 0.75]
<0.0001
0.77 [0.76, 0.78]
<0.0001
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Multivariable logistic regression separately by age group (N = 92).
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