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. Author manuscript; available in PMC: 2021 Sep 3.
Published in final edited form as: Vaccine. 2020 Jul 24;38(39):6112–6119. doi: 10.1016/j.vaccine.2020.07.026

An Innovative Housing-Related Measure for Individual Socioeconomic Status and Human Papillomavirus Vaccination Coverage: A Population-Based Cross-Sectional Study

Kathy L MacLaughlin 1, Robert M Jacobson 1, Jennifer L St Sauver 1, Debra J Jacobson 1, Chun Fan 1, Chung-Il Wi 1, Lila J Finney Rutten 1
PMCID: PMC7484398  NIHMSID: NIHMS1612507  PMID: 32713679

Abstract

Background:

Human papillomavirus (HPV) is a known cause of anogenital (eg, cervical) and oropharyngeal cancers. Despite availability of effective HPV vaccines, US vaccination-completion rates remain low. Evidence is conflicting regarding the association of socioeconomic status (SES) and HPV vaccination rates. We assessed the association between SES, defined by an individual validated Housing-based Socioeconomic Status index (HOUSES), and HPV vaccination status.

Methods:

We conducted a cross-sectional study of children/adolescents 9–17 years as of December 31, 2016, living in southeastern Minnesota by using a health-record linkage system to identify study-eligible children/adolescents, vaccination dates, and home addresses matched to HOUSES data. We analyzed the relationship between HPV vaccination status and HOUSES using multivariable Poisson regression models stratifying by age, sex, race, ethnicity, and county.

Results:

Of 20,087 study-eligible children/adolescents, 19,363 (96.4%) were geocoded and HOUSES measures determined. In this cohort, 57.9% did not receive HPV vaccination, 15.8% initiated (only), and 26.3% completed the series. HPV vaccination-initiation and completion rates increased over higher SES HOUSES quartiles (P<.001). Rates of HPV vaccination initiation versus unvaccinated increased across HOUSES quartiles in multivariable analysis adjusted for age, sex, race, ethnicity, and county (1st quartile referent; 2nd quartile, 0.97 [0.87–1.09]; 3rd quartile, 1.05 [0.94–1.17]; 4th quartile, 1.15 [1.03–1.28]; test for trend, P=.002). HOUSES was a stronger predictor of HPV vaccination completion versus unvaccinated (1st quartile referent; 2nd quartile, 1.06 [0.96–1.16]; 3rd quartile, 1.12 [1.03–1.23]; 4th quartile, 1.32 [1.21–1.44]; test for trend, P<.001). Significant interactions were shown for HPV vaccination initiation by HOUSES for sex (P=.009) and age (P=.006).

Conclusion:

The study showed disparities in HPV vaccination by SES, with the highest HOUSES quartiles associated with increased rates of initiating and even greater likelihood of completing the series. HOUSES data may be used to target and tailor HPV vaccination interventions to undervaccinated populations.

Keywords: ethnic groups, papillomavirus vaccines, social class, vaccination

Introduction

In the United States, approximately 34,800 cancers are diagnosed each year in women and men that are attributable to high-risk human papillomavirus (HPV) infection [1]. HPV is a common sexually transmitted infection that most often clears without major clinical consequence, but persistent high-risk HPV infection may cause cervical, other anogenital, or oropharyngeal cancer [2]. Despite the availability of effective HPV vaccine in the United States since 2006 for girls and 2011 for boys, only 53.7% of adolescent girls and 48.7% of adolescent boys (aged 13–17 years) have completed the vaccination series as recommended by national authorities [3]. HPV vaccination-completion rates are well below the Healthy People 2020 goal of 80% for 13- to 15-year-old adolescents [4]. Commonly reported barriers to HPV vaccination include parental concerns about vaccination safety, lack of knowledge about the vaccine or a belief the vaccine is not necessary, and absence of a clinician recommendation for the vaccine [5–7]. Additional factors associated with lower HPV vaccination rates include male sex [8], non-Hispanic ethnicity [3, 8], and rural residence [9].

Research has yielded inconsistent findings regarding the association between socioeconomic status (SES) and HPV vaccination rates. An analysis of 2008–2010 data from the Behavioral Risk Factor Surveillance System (BRFSS) showed higher SES, defined by self-reported maternal education, household income, and health insurance status, was associated with higher HPV vaccination-initiation rates for girls aged 12–17 years living in metropolitan but not nonmetropolitan areas [10]. We [11] have previously reported that higher SES scores were associated with higher rates of HPV vaccination initiation and completion in girls and boys aged 9–14 years, by using a composite SES measure derived from census-block, group-level data.

Inverse associations between SES and HPV vaccination rates have also been reported. The National Immunization Survey-Teen (NIS-Teen) data showed an inverse relationship between SES and HPV vaccination rates, with higher SES associated with lower HPV vaccination-initiation and completion rates [3, 12]. In the 2017 NIS-Teen survey analysis, those from households with parent-reported incomes at or above the federal poverty level had an HPV vaccination-initiation rate of 62.8% and a completion rate of 46.7% compared with an initiation rate of 73.3% and a completion rate of 53.7% for those living below the federal poverty level [12]. The 2018 NIS-Teen data were similar; adolescents from higher-income households had an HPV vaccination-initiation rate of 65.8% and a completion rate of 49.6% compared with an initiation rate of 76.2% and a completion rate of 57.1% for adolescents for those living below the federal poverty level [3].

Mixed results have also been reported from single studies. Moss et al [13] used US census data for median income by state and showed higher rates of HPV vaccination-initiation rates among adolescent girls from higher median household-income states but no association between median income by state and rates of HPV vaccination-initiation rates for adolescent boys or for HPV vaccination-completion rates for adolescent girls. Higher self-reported household income and lower county-level poverty based on US census data were both associated with lower HPV vaccination rates among adolescent girls in 6 states, although the opposite association was seen by state-level poverty status in an analysis of BRFSS data, with adolescent girls from wealthier states more likely to be vaccinated [14].

Observed inconsistencies in prior research may, in part, be attributed to variability in how SES is defined and measured. Addressing this methodologic heterogeneity by using an individual-level SES measure is crucial for targeted interventions for improving HPV vaccination-initiation and completion rates. Individual-level factors such as family income or parental education may be used as a marker for SES, but that information is often not available in health records or datasets [15, 16] and is instead dependent on self-report, which may be subject to social desirability and recall biases [17]. Area-level estimates of SES at the neighborhood, county, and state levels are generally derived using self-reported US census data and have been used as an estimate of individual-level measures of SES. However, a low level of agreement between individual-level and area-level SES measures within populations has been reported, suggesting potential for misclassification bias [18, 19]. Within-group heterogeneity of aggregated data (eg, variability of earning for each educational category) could be a reason for inconsistent results in the literature as well. Accurately adjusting for individual-level SES in epidemiologic studies of HPV vaccination is necessary to evaluate the independent effect of SES on HPV vaccination status.

Given these observed limitations and noted inconsistencies, we aimed to study the association between a novel, objective, housing-based SES measure, the Housing-based Index of Socioeconomic Status (HOUSES), and HPV vaccination rates. The HOUSES index provides an alternative, validated individual-level SES measurement based on 4 publicly available housing variables: home value, square footage, number of bedrooms, and number of bathrooms [15]. HOUSES has been used to study pertussis vaccination in the pediatric population but has not been used in prior studies of HPV vaccination coverage [16]. Secondarily, we aimed to assess HPV vaccination rates overall and by age, sex, race, and ethnicity.

Methods

Study Design and Population

A cross-sectional, population-based study was done to assess the association between SES as measured by the HOUSES index and HPV vaccination status. The Rochester Epidemiology Project (REP) research infrastructure was used to identify female and male children and adolescents, ages 9 to 17 years, living in 1 of 3 southeastern Minnesota counties (Olmsted, Dodge, and Wabasha) on December 31, 2016, and to obtain their HPV vaccination data as of that date [20, 21]. The REP links health-record data at the patient level across health care providers in a 27-county region of southeastern Minnesota [22]. HOUSES data, at the time of the study index date, were available for 3 of the REP counties, and that data determined the counties included in this study. The institutional review boards at Mayo Clinic and Olmsted Medical Center approved this study, waiving parental permission and child assent, limiting the study to children whose parents and guardians already authorized the use of their children’s health records for research purposes as required by state law.

Individual SES by HOUSES Index

The HOUSES index is a robust individual measure of SES represented by a single factor made up of 4 items (estimated building value of the unit, square footage, number of bedrooms, and number of bathrooms) ascertained by the county assessor’s office and publicly available from online property records database websites searched by county. The number of household members is not accounted for in the HOUSES index because the real property data source from the county assessor’s office does not include this information. However, the HOUSES index is available for multiple settings including single-family homes, multiplex housing (eg, duplex), condominiums, mobile home parks, and apartment complexes. Development of the HOUSES index has been previously described [15]. To calculate the index, the 4 housing variables are determined for the entire county population and are converted into z-scores and combined to create the standardized HOUSES index. The HOUSES measure may be reported as a continuous variable (z-score) and also as a categorical variable by placing the raw z-scores into quartiles, which we did for this study. A higher HOUSES score indicates higher SES (Q1 = lowest SES quartile, Q4 = highest SES quartile) [15]. The home address of each child on the index date of December 31, 2016, was identified through the REP, which collects and maintains all historical individual addresses [20, 23, 24], and matched to the publicly available county government property data. Subsequently, an individual HOUSES index z-score was generated along with a HOUSES quartile for each child and adolescent in the study. The study cohort was a subset of the entire county population, so one would not expect an even 25% distribution per SES quartile among the study cohort.

The HOUSES index has shown strong psychometric properties and demonstrated criterion validity such that there were moderate to good correlations with education, income, Hollingshead Index, and Nakao-Treas Index in Olmsted County, Minnesota (r=0.29–0.54, P<.001) and in Jackson County, Missouri (r=0.39–0.59, P<.001), respectively [15]. In addition, because Jackson County, Missouri—an urban setting encompassing Kansas City—is much more socioeconomically and racially diverse than Olmsted County, the HOUSES index demonstrated its applicability to both urban and mixed urban-rural settings [15]. Construct validity was also found such that the HOUSES index predicted a broad range of health behavior (eg, household smoking exposure, pertussis vaccination) and outcomes (eg, overweight, hospitalizations, multiple chronic conditions, and falls) that are conceptually and empirically known to be associated with SES [15, 16, 25, 26]. External validity (generalizability) of the HOUSES index was independently assessed by showing that HOUSES predicted poorly controlled childhood asthma as determined by the Asthma Control Test in a random sample of children with asthma in Sioux Falls, South Dakota [27].

HPV Vaccination Data

HPV vaccination history, including initiation or completion of the HPV vaccination series, was obtained from the REP through current procedure terminology codes for HPV vaccination. Consistent with Advisory Committee on Immunization Practices (ACIP) recommendations, which were in effect at our index date, HPV vaccination completion was defined as 2 HPV vaccine doses at least 5 months apart with the first dose given at or after age 9 and before age 15 years. For adolescents who had their first HPV vaccine dose at age 15 or later, HPV vaccination completion was defined as 3 doses of vaccine appropriately spaced (at least 4 weeks between the first and second dose, with the third dose given at least 5 months after dose 1 and 12 weeks after dose 2) [28]. As per ACIP recommendations, we allowed a 4-day grace period in defining a valid dose that counted toward vaccination-series completion [29]. We defined HPV vaccination-initiation only as receipt of at least 1 HPV vaccine dose, but criteria were not met for HPV vaccination-series completion. The HPV vaccination-initiation only group did not include those who went on to complete the vaccination series. HPV vaccination-series completion rates represented a percentage of the total eligible population, not a percentage of those who initiated the HPV vaccination series.

Statistical Analyses

Demographic characteristics of the study population were reported overall and by HOUSES quartiles and HPV vaccination status (no HPV vaccination, HPV vaccination-initiation only, or HPV vaccination completion) using descriptive statistics. χ2 Tests were used to assess differences in descriptive characteristics by HOUSES quartiles and by HPV vaccination status and to assess differences in HPV vaccination status by HOUSES quartiles overall and by age groups. Separate multivariable Poisson regression models were used to assess HPV vaccination-initiation only versus unvaccinated status and HPV vaccination completion versus unvaccinated status as predicted by the HOUSES index, adjusted for age, sex, race, ethnicity, and county. Poisson regression models were also used to assess a linear trend across levels of the HOUSES quartiles. Interactions between race, ethnicity, age, sex, and HOUSES status were also assessed. Significant interactions were presented graphically with stratified adjusted model results displayed in a forest plot.

Results

Sociodemographic Characteristics of the Study Population

Descriptive characteristics of the study population overall and by HOUSES quartile and HPV vaccination status are summarized in Table 1. Of the identified 20,087 study-eligible children and adolescents, 19,363 (96.4%) were geocoded and HOUSES measures determined. Age at index date was fairly equally distributed across age groups (34.6%, aged 9–11; 34.4%, aged 12–14; and 31.1%, aged 15–17 years). The majority of children and adolescents (9–17 years) in our 3-county study population were white (76.2%), non-Hispanic (90.9%), living in an urban geographic area (98.2%), and residing in Olmsted County (80.5%).

Table 1.

Descriptive Characteristics of the Study Population Overall and by HOUSES Quartiles and HPV Vaccination Status

HOUSES Measure of SES, No (%)a HPV Vaccination Group, No. (%)b
HOUSES HOUSES HPV
Characteristic Total, No. (%) Q1 (Lowest SES) HOUSES Q2 HOUSES Q3 Q4 (Highest SES) No HPV Vaccine Vaccination Initiated Onlyc HPV Vaccination Completiond
Total population 19,363 4,001 (20.7) 4,253 (22.0) 4,855 (25.1) 6,254 (32.3) 11,218 (57.9) 3,054 (15.8) 5,091 (26.3)
Age at index date, y
 9–11 6,689 (34.6) 1,570 (23.5) 1,495 (22.4) 1,677 (25.1) 1,947 (29.1) 5,676 (84.9) 713 (10.7) 300 (4.5)
 12–14 6,655 (34.4) 1,352 (20.3) 1,458 (21.9) 1,647(24.8) 2,198 (33.0) 3,214 (48.3) 1,430 (21.5) 2,011 (30.2)
 15–17 6,019 (31.1) 1,079(17.9) 1,300 (21.6) 1,531 (25.4) 2,109 (35.0) 2,328 (38.7) 911 (15.1) 2,780 (46.2)
Sex
 Male 9,782 (50.5) 2,046 (20.9) 2,120 (21.7) 2,441 (25.0) 3,175 (32.5) 6,025 (62.0) 1,589 (16.2) 2,168 (22.2)
 Female 9,581(49.5) 1,955 (20.4) 2,133 (22.3) 2,414 (25.2) 3,079 (32.1) 5,193 (54.2) 1,465 (15.3) 2,923 (30.5)
Race
 White 14,762 (76.2) 2,047 (13.9) 3,283 (22.2) 3,932 (26.6) 5,500 (37.3) 8,440 (57.2) 2,317 (15.7) 4,005 (27.1)
 Black 1,747 (9.0) 1,023 (58.6) 298 (17.1) 311 (17.8) 115 (6.6) 1,087 (62.2) 285 (16.3) 375 (21.5)
 Asian 1,140(5.9) 247 (21.7) 236 (20.7) 289 (25.4) 368 (32.3) 663 (58.2) 173 (15.2) 304 (26.7)
 Other 1,714 (8.9) 684 (39.9) 436 (25.4) 323 (18.8) 271 (15.8) 1,028 (60.0) 279 (16.3) 407 (23.8)
Ethnicity
 Hispanic 1,767 (9.1) 679 (38.4) 437 (24.7) 357 (20.2) 294 (16.6) 1,028 (58.2) 284 (16.1) 455 (25.7)
 Not Hispanic 17,596 (90.9) 3,322 (18.9) 3,816 (21.7) 4,498 (25.6) 5,960 (33.9) 10,190 (57.9) 2,770 (15.7) 4,636 (26.3)
Geographice areas 40 (12.1)
 Rural 332 (1.7) 98 (29.5) 93 (28.0) 101 (30.4) 234 (70.5) 47 (14.2) 51 (15.4)
 Urban 18,230 (98.2) 3,829 (21.0) 3,992 (21.9) 4,571 (25.1) 5,838 (32.0) 10,513 (57.7) 2,894 (15.9) 4,823 (26.5)
County
 Olmsted 15,590 (80.5) 3,424 (22.0) 3,411 (21.9) 3,868 (24.8) 4,887 (31.3) 8,895 (57.1) 2,476 (15.9) 4,219 (27.1)
 Dodge 2,260 (11.7) 464 (20.5) 505 (22.3) 560 (24.8) 731 (32.3) 1,382 (61.2) 344 (15.2) 534 (23.6)
 Wabasha 1,513 (7.8) 113 (7.5) 337 (22.3) 427 (28.2) 636 (42.0) 941 (62.2) 234 (15.5) 338 (22.3)
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Abbreviations: HOUSES, Housing-based Index of Socioeconomic Status; HPV, human papillomavirus; SES, socioeconomic status.

a

χ2 Test for a significant difference of descriptive characteristic by HOUSES quartile: P<.001 for all characteristics except sex, which was P=.65.

b

χ2 Test for a significant difference of descriptive characteristic by HPV vaccination status: P<.001 for all characteristics except ethnicity, which was P=.76.

c

Defined as receipt of at least 1 HPV vaccine dose, but the vaccination series was not completed.

d

Defined as 2 HPV vaccine doses if series started before age 15 years and 3 HPV vaccine doses if series started at or after age 15 years (with appropriate spacing).

e

A rural-urban commuting area code was not assigned if the matching score was <35, accounting for missing data (approximately 4%) for geographic area.

Association of HOUSES Index With Sociodemographic Characteristics

The population distribution of age, race, ethnicity, rural/urban status, and county differed significantly by HOUSES quartile (P<.001), although no significant differences in HOUSES quartile by sex were observed (Table 1). Overall, older adolescents (aged 15–17 years) were from higher SES homes, as measured by HOUSES quartiles, than younger children (aged 9–11 years). More white and Asian children and adolescents had higher SES, as defined by HOUSES, than black children. More non-Hispanic children and adolescents were in higher HOUSES SES quartiles than Hispanic children and adolescents. Similar rates were observed between rural and urban children and adolescents in the highest HOUSES quartile, although a higher percentage of urban residents were in the lowest SES category relative to rural residents. The county of residence differed significantly by HOUSES quartile, with Wabasha County having the lowest percentage of their population in the lowest HOUSES quartile and the highest percentage in the highest HOUSES quartile.

Association of HPV Vaccination Rates With Sociodemographic Characteristics

Among the total study population, 57.9% did not receive HPV vaccination, 15.8% had only initiated the HPV vaccination series, and 26.3% had completed the HPV vaccination series. The population distribution by age, sex, race, rural/urban status, and county differed significantly across HPV vaccination status groups of unvaccinated, initiated vaccination-series only, or completed (P<.001), although no significant differences in HPV vaccination status by ethnicity were shown (Table 1). HPV vaccination is recommended across all ages in our study (9–17 years); therefore, it was expected that a higher proportion of younger children would be unvaccinated (84.9%, 9–11 years) than older adolescents (38.7%, 15–17 years) and that completion rates would be greater for the older group (4.5%, 9–11 years vs 46.2%, 15–17 years). Although initiation rates were similar, more girls than boys completed the HPV vaccination series. HPV vaccination-initiation only rates were similar by race, but vaccination-series completion was higher in the white and Asian groups than in the black population. Initiation-only rates were also similar between rural and urban populations, although the urban population had a higher completion rate for the HPV vaccination series.

Association Between HOUSES and HPV Vaccination Status

Figure 1 summarizes the vaccination status of HPV series-initiation only or completion by HOUSES quartiles for the overall population and by age group. In the overall population and within each age group, both HPV vaccination-initiation only and completion rates increased significantly across progressively higher HOUSES quartiles (test for trend, P<.001 for all categories except HPV vaccination-initiation only for 15–17 year olds [test for trend, P=.002]).

Figure 1.

Figure 1.

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HPV Vaccination Series Percentage for the Initiation Only and Completion Groups by HOUSES Quartile,* Overall, and Age Group. A, Total population. B, Age, 9–11 years. C, Age, 12–14 years. D, Age, 15–17 years. “Initiation only” was defined as receipt of at least 1 HPV vaccine dose, but the vaccination series was not completed. The P values for an increasing trend were all <.001, except for initiation at 15–17 years, which was .002. Q indicates quartile. *Q1 (lowest SES) to Q4 (highest SES). HOUSES indicates Housing-based Index of Socioeconomic Status.

Multivariable Poisson regression models were used to determine associations between the HOUSES index and odds of HPV vaccination-series initiation only versus unvaccinated and odds of HPV vaccination-series completion versus unvaccinated after adjusting for age, sex, race, ethnicity, and county (Tables 2 and 3). Rates of HPV vaccination-initiation only versus unvaccinated increased across HOUSES quartiles in multivariable analysis adjusted for age, sex, race, ethnicity, and county (1st quartile = referent; 2nd quartile, 0.97 [0.87–1.09]; 3rd quartile, 1.05 [0.94–1.17]; 4th quartile, 1.15 [1.03–1.28]; test for trend, P=.002) (Table 2). A similar analysis of HPV vaccination completion versus unvaccinated showed HOUSES was an even stronger predictor of completion than initiation (1st quartile = referent; 2nd quartile, 1.06 [0.96–1.16]; 3rd quartile, 1.12 [1.03–1.23]; 4th quartile, 1.32 [1.21–1.44]; test for trend, P<.001) (Table 3).

Table 2.

HPV Vaccination-Initiation Onlya vs Unvaccinated Predicted by HOUSES Index

Unadjusted Adjusted for Age, Sex, Race, Ethnicity, and County
HOUSES Index RR (95% CI) P Value RR (95% CI) P Value
HOUSES quartile <.001b .002b
 First (lowest SES) Referent Referent
 Second 0.99 (0.88–1.10) 0.97 (0.87–1.09)
 Third 1.06 (0.96–1.18) 1.05 (0.94–1.17)
 Fourth (highest SES) 1.17 (1.06–1.29) 1.15 (1.03–1.28)
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Abbreviations: HOUSES, Housing-based Index of Socioeconomic Status; HPV, human papillomavirus; OR, odds ratio; SES, socioeconomic status.

a

Defined as receipt of at least 1 HPV vaccine dose, but the vaccination series was not completed.

b

Test for trend.

Table 3.

HPV Vaccination Completeda vs Unvaccinated Predicted by HOUSES

HOUSES Unadjusted Adjusted for Age, Sex, Race, Ethnicity, and County
RR (95% CI) P Value RR (95% CI) P Value
HOUSES quartile <.001b <.001b
 First (lowest SES) Referent Referent
 Second 1.17 (1.06–1.28) 1.06 (0.96–1.16)
 Third 1.26 (1.15–1.38) 1.12 (1.03–1.23)
 Fourth (highest SES) 1.57 (1.45–1.70) 1.32 (1.21–1.44)
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Abbreviations: HOUSES, Housing-based Index of Socioeconomic Status; HPV, human papillomavirus; OR, odds ratio; SES, socioeconomic status.

a

Defined as 2 HPV vaccine doses if series started before age 15 years and 3 HPV vaccine doses if series started at or after age 15 years (with appropriate spacing).

b

Test for trend.

We conducted additional analyses to determine if age, sex, race, or ethnicity modified the associations we observed between HOUSES and HPV vaccination status. There was evidence of an interaction between age and HOUSES with HPV vaccination-initiation only (P=.009) (Figure 2). HPV vaccination-initiation only increased with higher HOUSES quartiles for those aged 9 to 11 (P for trend <.001) and aged 12 to 14 (P for trend = .008) but not for those aged 15 to 17 years (P for trend = .32). In addition, an interaction was shown between sex and HOUSES index with HPV vaccination-initiation only (P=.006) (Figure 3). The HPV vaccination-initiation only rates progressively increased with higher HOUSES quartiles for girls (P for trend <.001) but not for boys (P for trend = .31) (Figure 3). There was also a marginal interaction (P=.10) for HPV vaccination-series completion with HOUSES and race. The HPV vaccination-completion rate progressively increased with higher HOUSES quartiles in white (P for trend <.001) and Asian (P for trend = .004) populations but not in black (P for trend = .16) or other race (P for trend = .65) populations. There were no significant interactions between race or ethnicity and HOUSES with HPV vaccination-initiation only and no significant interactions between age, sex, or ethnicity and HOUSES with HPV vaccination completion.

Figure 2.

Figure 2.

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Association of HPV Vaccination-Initiation Only Compared With Unvaccinated for Quartiles of the HOUSES Index by Age (Risk Ratio [95% CI]). HOUSES quartile 1 served as the referent. HOUSES indicates Housing-based Index of Socioeconomic Status; HPV, human papillomavirus; Q, quartile.

Figure 3.

Figure 3.

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Association of HPV Vaccination-Initiation Only Compared With Unvaccinated for Quartiles of the HOUSES Index by Sex (Risk Ratio [95% CI]). HOUSES quartile 1 served as the referent. HOUSES indicates Housing-based Index of Socioeconomic Status; HPV, human papillomavirus; Q, quartile.

Discussion

In this study, our primary aim was to assess the association between a novel individual-level SES measure (HOUSES) and HPV vaccination rates. Our intent was to address inconsistent results in prior studies of the association between SES and HPV vaccination status and to address a gap in the type of SES measures previously used, which include self-reported individual-level SES measures, such as parental income or education or aggregated area-level SES measures most often based on self-reported census data. We are not aware of other studies that have used a validated objective individual-level housing-based SES measure such as HOUSES to study HPV vaccination status in children and adolescents.

We observed that progressively higher SES, as measured by increasing HOUSES quartiles, was positively associated with the prevalence of HPV vaccination-series initiation, and an even stronger association was observed with HPV vaccination-series completion. Our findings align with the reported positive association between high SES and high HPV vaccination rates in girls in a Danish cohort study that used individual-level SES markers (eg, maternal education, marital status, employment status, and disposable income) from a population database [30] as well as with a Midwestern population-based study of boys and girls using census-block, group-level data to create an area-level SES measure [11]. Higher HPV vaccination-initiation rates but no association with vaccination-series completion rates have been reported for girls from higher SES metropolitan homes but not from homes in nonmetropolitan areas in a study using self-reported individual-level SES measures collected through the BRFSS survey [10] and for girls from higher SES median household-income states in a nationwide study using US census data to define area-level SES [13]. In marked contrast to our study observations, 2016–2018 NIS-Teen reports showed an inverse association of higher individual-level SES adolescents (as measured by parental-reported income) having lower HPV vaccination-initiation and completion rates than the lower SES group of male and female adolescents [3, 12, 31]. Given these discrepancies, our study using HOUSES, an objective and individual-level SES measure to reduce methodologic heterogeneity, may need to be replicated in different study settings.

HPV vaccination-series completion rates may be more strongly associated with HOUSES than HPV vaccination-initiation rates in our study because, regardless of SES, most children entering 7th grade in Minnesota have a health care visit to receive the state-mandated tetanus/diphtheria/acellular pertussis and meningococcal vaccines, as evidenced by those vaccination rates exceeding 90% statewide and exceeding 95% in the 3 counties we studied [32]. This visit should include a strong recommendation and equal opportunity to start the HPV vaccination series regardless of SES. So although uptake is significantly lower for the HPV vaccine than the other adolescent vaccines recommended at age 11 to 12 years in Minnesota [33] and nationwide [3], it is not unexpected to find less disparity in HPV vaccination initiation by SES as compared with completion. Niccolai et al [34] point out that completing the HPV vaccination series takes parental commitment to coordinate scheduling the extra appointments, the flexibility and financial resources to miss work, and access to adequate transportation. These potential barriers may be less of a challenge for the higher SES groups in our study population, leading to the stronger association with higher HPV vaccination-completion rates we observed. Given the potential barriers to HPV vaccine completion in the clinical setting, it is critical to explore alternative venues such as schools, pharmacies, emergency departments, and dental offices to address disparities [35] in vaccine access.

Our secondary study aim was to assess HPV vaccination rates overall and in context of sociodemographic factors including age, sex, race, ethnicity, and geographic area. HPV vaccination-initiation rates of less than 20% were observed across all races, in girls and boys, and in both rural and urban populations in our study. HPV vaccination-series completion was 26.3% for our overall study population, but this low rate partially reflects our inclusion of 9- and 10-year-old children in our study. The ACIP provides a routine recommendation for HPV vaccination at age 11 or 12, but supports starting the HPV vaccination as early as age 9 years [36]. The HPV vaccination-completion rate of 46.2% for those aged 15 to 17 years in our study provides a more useful comparison to national data such as the NIS-Teen survey, which reported 51.1% HPV vaccination-completion rates for 13- to 17-year-olds in 2018 [3]. However, both our rates and NIS-Teen rates are well below the Healthy People 2020 goal for 13- to 15-year-olds of 80% HPV vaccination completion [4].

The higher prevalence of HPV vaccination-series completion was noted in our study with older age, female sex, urban residence, and white or Asian race. Many of these results are consistent with national data on sociodemographic characteristics and HPV vaccination coverage. Results from verified vaccination records of the 18,700 adolescents aged 13 to 17 years participating in the 2018 NIS-Teen survey showed higher HPV vaccination-completion rates with older age and higher HPV vaccination-completion rates in female (53.7%) versus male (48.7%) adolescents. An association with geographic residence was observed in the NIS-Teen survey, with a significant increase (P<.05) in HPV vaccination-series completion in teenagers living in metropolitan statistical areas (MSAs), particularly principal cities (56.1%), compared with those living in nonprincipal-city MSAs (49.1%) and especially compared with those living in non-MSAs (40.7%) [3]. Our urban population had a higher rate of HPV vaccination completion than the rural population, which is consistent with other observations [9] and congruent with reported lower levels of knowledge and awareness about HPV vaccination in rural versus urban populations [37]. However, given that a majority of our study cohort lived in an urban area, this may need to be confirmed in future studies by including more children and adolescents living in rural areas. Rural populations may face unique challenges to completion of the HPV vaccine series. Identifying and addressing multilevel barriers to vaccination among rural populations and pursuing alternative venues for vaccination, such as pharmacies, is critical to reducing this geographic disparity [38].

Although similarities exist between our results and the most recent NIS-Teen data for HPV vaccination completion by age, sex, and geographic residence, HPV vaccination coverage by race and ethnicity were different. Our results showed no difference in HPV vaccination-initiation rates by race, but the highest HPV vaccination-completion rates were in the white and Asian populations, with completion rates lowest in the black population. There was no difference in HPV vaccination-series initiation or completion in our study between children of Hispanic and non-Hispanic ethnicity. In contrast, the 3 most recent NIS-Teen surveys from 2016–2018 reported that black adolescents had higher HPV vaccination-initiation and completion rates than white adolescents and that Hispanic adolescents had higher initiation and completion rates than white, non-Hispanic adolescents [3, 12, 31].

Our study showed an interaction between both age and sex with HOUSES with HPV vaccination initiation. There was an increasing likelihood of HPV vaccination initiation associated with higher HOUSES quartiles for those in younger age groups (9–14 years) than the older age group (15–17 years). An interaction was also noted between sex and HOUSES index, with HPV vaccination-initiation rates increasing with higher HOUSES quartiles for girls but not for boys. If families with children of both sexes were making similar vaccination decisions for each child, regardless of sex, we would expect to see a similar pattern in HPV vaccination initiation by HOUSES quartile. Our findings might be explained by what Daley et al [39] have described as the “feminization” of the HPV vaccination, with initial testing, approval, marketing, and implementation targeted to girls, leading to an inequity in HPV vaccination rates by sex. Theoretically, this could include disparity in HPV vaccination occurring within the same family, which would help explain the lack of association of SES with HPV vaccination initiation in boys observed in our study.

White and Asian populations with higher SES HOUSES quartiles had increased likelihood of HPV vaccination completion, but a moderating effect of higher SES on HPV vaccination was not shown for the black population. However, we note that the interaction term was not statistically significant. Minnesota has the largest Somali population in the United States, and the city of Rochester in Olmsted County has one of the 4 largest populations within the state [40]. We speculate that the absence of interaction between HOUSES and race may reflect that the black population in the area studied includes large proportions of Somali American families who often live with extended family [40]. HOUSES does not take into consideration that the monetary value of the home, as determined by the housing variables, may not reflect the SES of just 1 family, but instead may be supported by more than 1 or 2 adult incomes and thus may less accurately reflect SES at the individual level. However, as there are relatively fewer minorities in our study setting, especially in Wabasha and Dodge counties, this finding may need to be confirmed in other settings with higher rates of minority populations.

The associations we observed between SES, as measured by HOUSES and HPV vaccination rates, have important implications for both medical practice and public health. Among populations at highest risk of not completing the HPV vaccination series, specific barriers to vaccination completion must be identified to develop and test targeted interventions. As described above, HOUSES may be useful for further identifying a subgroup of high-risk populations for HPV vaccination (eg, lower SES in boys and younger age) at a population level. In addition, HOUSES could be deployed to augment risk-adjustment models often incorporated in value-based payment systems. For example, the National Academies of Sciences, Engineering, and Medicine [41] as well as the National Quality Forum [42] recommend adjusting for social factors of patient populations when the performance of health care organizations is determined, but acknowledge the lack of suitable individual-level measures for SES as a key challenge [41, 42]. When SES is not accounted for, unintended negative consequences result that can be detrimental to health care organizations, especially those serving disadvantaged populations, including implications for accountability applications (eg, payment) under the federal and state pay-for-performance programs. HOUSES is an individual-level SES measure based on readily available public data that could be used to facilitate equitable vaccine delivery through improved funding for health care systems serving those populations identified by HOUSES as being at increased risk of incomplete vaccination. Previous literature has supported the feasibility of incorporating social determinants of health into payment formulas for government-funded programs, such as MassHealth (Massachusetts Medicaid), to overcome underpayment limitations (eg, failure to account for social risk) of a diagnosis-based model [43].

A key strength of our study is the use of the HOUSES index, which provides an objective, individual-level assessment of SES based on publicly available housing factors, in contrast to individual and area-level SES measures that are dependent upon survey collection of self-reported data. The use of public property data enables implementation of HOUSES on a larger scale than is possible with the limitations frequently associated with conventional individual-level SES measures. HOUSES can also capture changes of individual SES over time as property data collected by a county assessor’s office is updated annually, and relocation or change of address often reflect changes in a person’s SES. An additional strength of the study is the utilization of confirmed HPV vaccination data obtained through the REP, which adds to the validity of our results, as parental report of HPV vaccination status can be susceptible to inaccuracies [44]. In addition, this is the first study, to our knowledge, to apply the HOUSES index as a measure of individual-level SES to assess the association with HPV vaccination prevalence.

Limitations of the study include lack of diversity in the study population, which was primarily white, non-Hispanic, and urban. Although results may not be applicable in settings with other sociodemographic characteristics, prior research indicates that the REP population is representative of populations in the Upper Midwest [23]. A limitation of the HOUSES index is that it does not take into account the number of people living in the home or the number of incomes supporting the household, which may result in an overestimate of individual-level SES. In addition, the usual limitations of a cross-sectional study design apply, including that data collected represent a point-in-time prevalence estimate and cannot be interpreted to explain cause and effect.

Conclusion

The importance and urgency of improving HPV vaccination-completion rates for children and adolescents was made clear by a 2019 Centers for Disease Control and Prevention report that receipt of the current 9-valent HPV vaccine series before HPV exposure may prevent up to 92% of HPV-attributable cancers [1]. The HOUSES index provides a validated, individual housing-level SES measure based on publicly available data that may be used to target HPV vaccination interventions in youth populations at highest risk of neither initiating nor completing the HPV vaccination series.

Highlights.

  • Prior study results are inconsistent for association between socioeconomic status (SES) and HPV vaccination.

  • A novel, individual-level housing-based SES marker was used for this study.

  • Increased rates of HPV vaccine coverage were observed with higher housing-based SES levels.

  • The moderating effect of higher SES on HPV vaccination differed by age, sex, and race.

Funding

This study was made possible using the resources of the Rochester Epidemiology Project, which is supported by the National Institute on Aging of the National Institutes of Health under Award Number R01AG034676, by the National Cancer Institute under Award Number 1R01CA217889-01A1 (Dr MacLaughlin, Dr Jacobson, and Dr Finney Rutten), and by the Department of Family Medicine and the Mayo Clinic Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery in Rochester, Minnesota. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the National Cancer Institute.

Abbreviations

ACIP

Advisory Committee on Immunization Practices

BRFSS

Behavioral Risk Factor Surveillance System

HOUSES

Housing-based Index of Socioeconomic Status

HPV

human papillomavirus

MSAs

metropolitan statistical areas

NIS

Teen, National Immunization Survey-Teen

REP

Rochester Epidemiology Project

SES

socioeconomic status

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Presented at the 47th North American Primary Care Research Group Annual Meeting, Toronto, Ontario, Canada, November 16–20, 2019.

Declarations of Interest

R.M.J. serves as a member of a safety review committee for a postlicensure safety study of Gardasil (4vHPV) and for a postlicensure safety study of Gardasil 9 (9vHPV). He also serves on a data-monitoring committee for a series of prelicensure trials of a 15-valent pneumococcal vaccine. All of these studies are funded by Merck & Co, Inc. All other authors have declared no competing interests.

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