ABSTRACT
Disparities in HPV vaccination coverage by metropolitan statistical area (MSA) status were observed in the 2016 and 2017 National Immunization Survey – Teen (NIS-Teen). In 2017, HPV vaccination initiation (≥1dose) coverage was 11 percentage points lower for adolescents living in non-MSAs (mostly rural areas) and 7 percentage points lower among those living in MSA, non-principal cities (suburban areas) compared to those living in MSA, principal cities (mostly urban areas). In order to understand how this disparity has changed over time, we examined trends in HPV vaccine initiation by MSA status from 2013 to 2017. Weighted linear regression by survey year was used to estimate annual percentage point changes in HPV vaccination initiation. The five-year average annual percentage point increases in HPV vaccination initiation coverage were 5.2 in mostly urban areas, 4.9 for suburban areas, and 5.2 for mostly rural areas. Despite increases in each MSA area, coverage in mostly rural areas was consistently and significantly lower than coverage in mostly urban areas. Coverage was significantly lower among teens living in mostly rural areas regardless of poverty status, sex, and race/ethnicity except among black, non-Hispanic adolescents. There was no significant change in the magnitude of the disparity between mostly urban areas and mostly rural areas over time (p = .98). A better understanding of the facilitators and barriers to HPV vaccination in mostly rural areas is needed to identify and implement targeted strategies to improve HPV vaccination coverage and reduce these disparities.
KEYWORDS: Human papillomavirus (HPV) vaccine, adolescents, disparity, urban, rural, trend
Introduction
Human papillomavirus (HPV) is the most common sexually transmitted infection in the United States. Each year, HPV infections result in the diagnosis of HPV-related cancers for more than 40,000 men and women – HPV is associated with 90% of all anal and cervical cancers; 70% or more of all oropharyngeal and vaginal cancers, and more than 60% of all penile and vulvar cancers.1,2 To prevent HPV-related infections and cancers, the Advisory Committee on Immunization Practices (ACIP) recommended a three-dose series of HPV vaccine for 11- to 12-year-old girls in 2006 and for boys in 2011.3,4 In December 2016, the ACIP revised the recommendation to a two-dose series for immunocompetent adolescents beginning the series prior to their 15th birthday, when the two doses are given at least 6 months apart.5 Persons aged 15–26 years and those with compromised immune systems are recommended to complete a three-dose vaccine series.5,6
Since ACIP recommended HPV vaccination for all adolescents, vaccination coverage has increased gradually among females and more rapidly among males. In 2017, coverage with ≥1-dose of HPV vaccine was 65.5% among adolescents aged 13 through 17 years; coverage was 68.6% among females and 62.6% among males.7 While vaccination coverage with ≥1-dose of HPV vaccine continues to increase, coverage has not reached the level seen for other vaccines recommended for preadolescents aged 11–12 years – tetanus, diphtheria and acellular pertussis vaccine (Tdap) and quadrivalent meningococcal conjugate vaccine (MenACWY). In 2017, coverage with ≥1-dose of HPV vaccine was 23.2 percentage points lower than coverage with ≥1-dose of Tdap and 19.6 percentage points lower than coverage with ≥1-dose of MenACWY.7 Reasons for the lower coverage with ≥1-dose of HPV vaccine in comparison to coverage with Tdap and MenACWY are not fully understood; however, state requirements of Tdap and MenACWY vaccination for school enrollment may be a factor.8 Additionally, lack of a strong provider recommendation for HPV vaccination at age 11–12, lack of awareness of the HPV vaccine, low perceived risk of infection, and safety concerns about the vaccine have been reported by parents as major barriers to HPV vaccine initiation.9–11
Based on analysis of the 2016 National Immunization Survey – Teen (NIS-Teen) data, urban-rural disparities (as defined by the MSA status variable) in HPV vaccination initiation (receipt of ≥1dose of HPV vaccine) were observed among adolescents,12 similar to other previously published studies.13–16 In 2017, the disparity in HPV vaccination initiation among adolescents living in MSA non-principal cities (suburban areas) compared to those living in MSA, principal cities (mostly urban areas) remained the same.7 However, the disparity in HPV vaccination initiation among adolescents living in non-MSAs (mostly rural areas) compared to those living in mostly urban areas decreased by 5 percentage points – from a difference of 16 to 11 percentage points.7,12
The decrease in the magnitude of the urban-rural disparity in HPV vaccination initiation observed during 2016–2017 is promising. However, determining whether the disparities in coverage is on the decline requires monitoring over time. The purpose of this analysis was: 1) to examine trends in HPV vaccination initiation coverage by MSA status and 2) to examine trends in disparities in HPV vaccination initiation coverage by MSA status during 2013–2017. The examination of trends in HPV coverage by MSA status will allow us to determine if targeted interventions toward rural populations are needed (e.g., if the disparity between urban and rural populations is increasing or remains the same over time) or if trends should continue to be monitored (e.g., if the disparity between areas is decreasing) without immediate action.
Methods
The survey
The National Immunization Survey – Teen (NIS-Teen) has been conducted annually since 2006.17 The survey collects data on vaccines received by adolescents aged 13–17 years in the 50 states, the District of Columbia, selected local areas, and selected territories. NIS-Teen is conducted among parents or guardians of age-eligible adolescents identified using a random-digit-dialed sample of landline and cellular telephone numbers. The survey occurs in two phases. In the first phase, parents and guardians of eligible teens are interviewed by telephone. During the telephone interview, information is obtained on the sociodemographic characteristics of the teen and household and contact information and consent to contact the teen’s vaccination providers are requested. In the second phase, vaccination providers are mailed a questionnaire requesting the vaccination history from the teen’s medical record. Vaccination coverage estimates are based on provider-reported vaccination histories. We used NIS-Teen data from 2013 to 2017 for our analysis.
Measures
We combined 5 years (2013–2017) of NIS-Teen data on adolescents aged 13–17 years in the 50 states and the District of Columbia. The outcome of interest was HPV vaccination initiation (receipt of ≥1-dose of HPV vaccine). We estimated coverage with ≥1-dose of HPV vaccine among adolescents aged 13–17 years for each survey year, by MSA status, and by select demographic subgroups (i.e. sex, race/ethnicity, and poverty level). Additionally, we assessed the trends and variations in initiation of HPV vaccine among adolescents aged 13–17 years by MSA status and survey year. Since ACIP recommends administration of HPV vaccine during the same pre-adolescent visit as Tdap and MenACWY, we also examined the trends in coverage and disparities by MSA status for Tdap and MenACWY to determine whether these variations in coverage by MSA status were unique to the HPV vaccine.
The three-level metropolitan statistical area (MSA) categorization is based on the legal statistical area designation (city, town, village, census-designated places, or townships), county of residence, and the principal city designation, as defined by the US Census Bureau.18 The U.S. Census Bureau defines an MSA as an area that consists of at least one urban area with a population of at least 50,000 inhabitants.18 The principal city is the largest city in each metropolitan statistical area. Each county is designated as being either an MSA county or a non-MSA county. When the statistical area was a principal city and in an MSA county, then it was categorized as an MSA principal city. When the statistical area was not a principal city but it was in an MSA county, then it was categorized as an MSA non-principal city. When the statistical area did not belong to an MSA county, the area was categorized as Non-MSA. MSA categories can be interpreted as approximating mostly urban areas (MSA principal city), suburban areas (MSA non-principal city), and mostly rural areas (non-MSA).
Statistical analysis
Data were analyzed using SAS®9.4 Survey Procedures to account for the complex survey design. To adjust for non-response and phoneless households, the data were weighted. Stratifying by MSA status, vaccination coverage estimates for ≥1-dose HPV vaccine, ≥1 MenACWY, and ≥1 Tdap were computed using weighted bivariate analysis. Additionally, for ≥1-dose HPV vaccine, weighted bivariate analysis was conducted to produce vaccination coverage estimates stratifying by MSA and select characteristics (i.e. poverty status, sex, and race/ethnicity). Weighted linear regression7,12,19 was used to estimate the average annual percentage point change in coverage with ≥1-dose of HPV vaccine, ≥1 MenACWY, and ≥1 Tdap among adolescents aged 13–17 years by MSA status from 2013 to 2017. The weighted linear regression analysis was also used to estimate the average annual percentage point changes in coverage with ≥1-dose of HPV vaccine among adolescents stratifying by MSA status and select characteristics. The reciprocal of the estimated variance of vaccination coverage estimates was used for weighting. We used the estimated slope from the linear regression to measure the change in value each year and tested whether the slope was significantly different from 0 (p < .05).19 T-tests were used for statistical comparison of differences in HPV vaccine initiation coverage by MSA status and survey year. The differences reported were statistically significant at p < .05.
Results
During 2013–2017, the NIS-Teen national sample included data regarding 103,074 adolescents aged 13–17 years from 50 states and the District of Columbia – 39.9% lived in mostly urban areas 39.2% lived in suburban areas, and 20.9% lived in mostly rural areas (Table 1). Overall, about half of the adolescents in the sample were male (51.1%), white non-Hispanic (53.6%), with private insurance (51.6%). The majority were living in households at/above poverty level (76.6%). A large percentage of mothers of adolescents in the survey were older than 44 years (47.0%) and were college graduates (38.2%). During 2013–2017, 23.3% of all adolescents did not have an 11–12-year preventive care visit. One-third (32.9%) of all parents reported not receiving a provider recommendation for vaccination with HPV vaccine for their adolescent (Table 1).
Table 1.
Characteristics of adolescents 13–17 years by Metropolitan Statistical Area (MSA) Status* and nationally, National Immunization Survey – Teen, United States, 2013–2017.
| United States |
MSA Principal City |
MSA Non-Principal City |
Non-MSA |
|||||
|---|---|---|---|---|---|---|---|---|
| (N = 103,074) |
(N = 41,110) |
(N = 40,389) |
(N = 21,575) |
|||||
| Sample (n) | Weighted % (95% CI) | Sample (n) | Weighted % (95% CI) | Sample (n) | Weighted % (95% CI) | Sample (n) | Weighted % (95% CI) | |
| Year of Birth | 92523 | 100.0 (– – –) | 36857 | 100.0 (– – –) | 36150 | 100.0 (– – –) | 19516 | 100.0 (– – –) |
| 1996 | 5360 | 6.3 (6.0–6.6) | 2023 | 6.2 (5.7–6.7) | 2100 | 6.1 (5.7–6.5) | 1237 | 7.0 (6.2–7.7) |
| 1997 | 9653 | 11.1 (10.7–11.4) | 3798 | 10.7 (10.1–11.4) | 3753 | 11.2 (10.7–11.9) | 2102 | 11.3 (10.5–12.2) |
| 1998 | 13846 | 15.4 (14.9–15.8) | 5462 | 14.7 (14.0–15.4) | 5361 | 15.7 (15.0–16.4) | 3023 | 16.1 (15.2–17.0) |
| 1999 | 18229 | 19.6 (19.2–20.1) | 7212 | 19.8 (19.0–20.6) | 7161 | 19.4 (18.7–20.1) | 3856 | 19.8 (18.9–20.8) |
| 2000 | 19254 | 20.5 (20.0–21.0) | 7780 | 21.0 (20.2–21.8) | 7491 | 20.5 (19.8–21.2) | 3983 | 19.3 (18.4–20.3) |
| 2001 | 15294 | 16.0 (15.6–16.4) | 6124 | 16.4 (15.6–17.2) | 6041 | 15.7 (15.0–16.3) | 3129 | 15.9 (15.0–16.9) |
| 2002 | 10887 | 11.2 (10.8–11.5) | 4458 | 11.1 (10.5–11.7) | 4243 | 11.4 (10.8–12.0) | 2186 | 10.5 (9.8–11.3) |
| Sex | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| Female | 49140 | 48.9 (48.3–49.5) | 19739 | 49.1 (48.2–50.1) | 19134 | 48.8 (47.9–49.7) | 10267 | 48.7 (47.5–49.9) |
| Male | 53934 | 51.1 (50.5–51.7) | 21371 | 50.9 (49.9–51.8) | 21255 | 51.2 (50.3–52.1) | 11308 | 51.3 (50.1–52.5) |
| Race/Ethnicity | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| White, non-Hispanic | 64670 | 53.6 (53.0–54.2) | 20421 | 41.9 (41.0–42.8) | 27989 | 59.1 (58.2–60.0) | 16260 | 69.7 (68.5–70.8) |
| Black, non-Hispanic | 9648 | 13.9 (13.5–14.3) | 5782 | 19.1 (18.4–19.8) | 2788 | 10.7 (10.2–11.3) | 1078 | 9.4 (8.7–10.2) |
| Hispanic | 17842 | 22.8 (22.3–23.4) | 10245 | 28.5 (27.5–29.4) | 5525 | 20.9 (20.0–21.8) | 2072 | 12.5 (11.7–13.4) |
| American Indian/Alaska -Native, non-Hispanic | 1439 | 0.9 (0.8–1.0) | 313 | 0.5 (0.4–0.6) | 355 | 0.7 (0.6–0.8) | 771 | 2.7 (2.4–3.1) |
| Asian, non-Hispanic | 3781 | 4.0 (3.7–4.2) | 1933 | 4.9 (4.5–5.4) | 1586 | 4.0 (3.7–4.4) | 262 | 0.9 (0.7–1.2) |
| Multiracial, non-Hispanic | 5242 | 4.6 (4.3–4.8) | 2251 | 4.9 (4.5–5.3) | 1955 | 4.3 (3.9–4.6) | 1036 | 4.6 (4.2–5.1) |
| Native Hawaiian, Pacific Islander, non-Hispanic | 452 | 0.3 (0.2–0.4) | 165 | 0.3 (0.2–0.4) | 191 | 0.3 (0.2–0.5) | 96 | 0.2 (0.2–0.3) |
| Mother’s Age | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| ≤ 34 years | 8389 | 9.1 (8.8–9.5) | 3674 | 10.3 (9.8–10.9) | 2675 | 7.7 (7.2–8.2) | 2040 | 10.7 (10.0–11.4) |
| 35–44 years | 42382 | 43.9 (43.3–44.5) | 16604 | 43.7 (42.7–44.6) | 15820 | 42.3 (41.5–43.2) | 9958 | 50.3 (49.1–51.5) |
| > 44 years | 52303 | 47.0 (46.4–47.5) | 20832 | 46.0 (45.0–46.9) | 21894 | 50.0 (49.1–50.8) | 9577 | 39.0 (37.9–40.2) |
| Mother’s Education | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| < High school | 12093 | 13.5 (13.1–13.9) | 6110 | 16.7 (15.9–17.5) | 3555 | 10.9 (10.3–11.6) | 2428 | 13.0 (12.2–13.9) |
| High School | 16916 | 23.0 (22.5–23.6) | 6566 | 22.3 (21.5–23.2) | 5878 | 21.7 (20.9–22.5) | 4472 | 30.0 (28.9–31.2) |
| > High school, some college | 27218 | 25.3 (24.8–25.8) | 9798 | 23.7 (22.8–24.5) | 10623 | 25.5 (24.7–26.2) | 6797 | 29.6 (28.6–30.6) |
| College graduate | 46847 | 38.2 (37.7–38.7) | 18636 | 37.4 (36.5–38.2) | 20333 | 41.9 (41.1–42.8) | 7878 | 27.4 (26.3–28.4) |
| Income to Poverty Ratio† | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| < 133% of federal poverty | 19373 | 23.8 (23.3–24.3) | 9598 | 29.0 (28.1–29.9) | 5478 | 18.0 (17.3–18.8) | 4297 | 28.8 (27.6–29.9) |
| 133% to < 322% of federal poverty level | 36246 | 37.3 (36.8–37.9) | 13574 | 36.3 (35.4–37.2) | 13121 | 36.0 (35.2–36.9) | 9551 | 45.1 (44.0–46.3) |
| 322% to < 503% of federal poverty level | 21748 | 18.1 (17.7–18.6) | 7705 | 15.4 (14.8–16.1) | 9706 | 21.2 (20.5–21.8) | 4337 | 15.5 (14.7–16.4) |
| ≥ 503% of federal poverty level | 25707 | 20.7 (20.3–21.2) | 10233 | 19.3 (18.6–20.0) | 12084 | 24.8 (24.1–25.5) | 3390 | 10.6 (9.9–11.2) |
| Poverty Level (2 level) | 99648 | 100.0 (– – –) | 39616 | 100.0 (– – –) | 39106 | 100.0 (– – –) | 20926 | 100.0 (– – –) |
| Below poverty level | 18486 | 23.4 (22.9–23.9) | 9133 | 28.5 (27.5–29.4) | 5199 | 17.5 (16.8–18.3) | 4154 | 29.0 (27.9–30.2) |
| At/Above poverty level | 81162 | 76.6 (76.1–77.1) | 30483 | 71.5 (70.6–72.5) | 33907 | 82.5 (81.7–83.2) | 16772 | 71.0 (69.8–72.1) |
| Insurance Status | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| Private Insurance | 59798 | 51.6 (51.1–52.2) | 22273 | 46.4 (45.5–47.4) | 26352 | 58.7 (57.9–59.6) | 11173 | 42.0 (40.8–43.2) |
| Any Medicaid | 30411 | 35.5 (34.9–36.1) | 13428 | 40.2 (39.2–41.1) | 9483 | 29.2 (28.4–30.1) | 7500 | 44.0 (42.8–45.2) |
| Other Insurance | 8599 | 7.9 (7.6–8.2) | 3433 | 7.7 (7.2–8.2) | 3214 | 7.8 (7.4–8.3) | 1952 | 8.6 (7.9–9.2) |
| No Insurance | 4266 | 5.0 (4.7–5.2) | 1976 | 5.7 (5.3–6.2) | 1340 | 4.2 (3.8–4.6) | 950 | 5.5 (4.9–6.2) |
| Had 11- to 12-year preventive care visit | 103074 | 100.0 (– – –) | 41110 | 100.0 (– – –) | 40389 | 100.0 (– – –) | 21575 | 100.0 (– – –) |
| Yes | 48095 | 44.9 (44.3–45.5) | 19193 | 43.7 (42.7–44.6) | 21044 | 48.8 (47.9–49.7) | 7858 | 34.8 (33.7–36.0) |
| No | 25271 | 23.3 (22.8–23.7) | 8715 | 21.9 (21.1–22.7) | 8173 | 20.2 (19.5–20.9) | 8383 | 38.3 (37.2–39.5) |
| Don’t know | 29708 | 31.8 (31.3–32.4) | 13202 | 34.4 (33.5–35.4) | 11172 | 31.0 (30.2–31.8) | 5334 | 26.8 (25.8–27.9) |
| Received provider recommendation for HPV vaccine | 94406 | 100.0 (– – –) | 37514 | 100.0 (– – –) | 37224 | 100.0 (– – –) | 19668 | 100.0 (– – –) |
| Yes | 65718 | 67.1 (66.6–67.7) | 26718 | 68.2 (67.3–69.2) | 26573 | 68.1 (67.2–68.9) | 12427 | 60.4 (59.2–61.6) |
| No | 28688 | 32.9 (32.3–33.4) | 10796 | 31.8 (30.8–32.7) | 10651 | 31.9 (31.1–32.8) | 7241 | 39.6 (38.4–40.8) |
| Provider Facility Type | 102445 | 100.0 (– – –) | 40858 | 100.0 (– – –) | 40181 | 100.0 (– – –) | 21406 | 100.0 (– – –) |
| All Public Facilities | 15013 | 15.1 (14.7–15.6) | 5041 | 15.2 (14.4–15.9) | 3748 | 11.0 (10.4–11.7) | 6224 | 29.6 (28.5–30.8) |
| All Hospital Facilities | 11493 | 9.6 (9.3–10.0) | 5154 | 10.8 (10.3–11.4) | 3931 | 8.7 (8.2–9.2) | 2408 | 9.3 (8.6–10.0) |
| All Private Facilities | 50041 | 52.4 (51.8–53.0) | 21138 | 52.3 (51.3–53.3) | 23504 | 59.4 (58.5–60.3) | 5399 | 27.4 (26.3–28.4) |
| All School/Other | 1680 | 1.8 (1.7–2.0) | 745 | 2.0 (1.7–2.3) | 593 | 1.8 (1.5–2.1) | 342 | 1.6 (1.4–2.0) |
| Mixed | 22732 | 19.7 (19.3–20.2) | 8094 | 18.5 (17.8–19.2) | 7764 | 17.6 (16.9–18.2) | 6874 | 31.3 (30.2–32.4) |
| All Military/All WIC Clinic Facilities, All Pharmacies | 1486 | 1.3 (1.2–1.5) | 686 | 1.3 (1.1–1.5) | 641 | 1.5 (1.3–1.7) | 159 | 0.8 (0.6–1.0) |
* MSA categories can be interpreted as approximating mostly urban areas (MSA principal city), suburban areas (MSA non-principal city), and mostly rural areas (non-MSA).
† Imputed Poverty-to-Income ratio variable.
HPV vaccination initiation increased both nationally and by MSA status area; the slopes were significantly different from 0 (p < .05). Nationally, coverage with ≥1-dose of HPV vaccine increased from 44.9% to 65.5% from 2013 to 2017; the average annual increase was 5.1 percentage points. In mostly urban areas, coverage with ≥1-dose of HPV vaccine ranged from 49.0% to 70.1% over the five-year period for an average annual increase of 5.2 percentage points. In suburban areas, coverage with ≥1-dose of HPV vaccine ranged from 43.8% to 63.1% for an average annual increase of 4.9 percentage points. HPV vaccination initiation among adolescents living in mostly rural areas ranged from 36.5% to 59.3% over the five-year period for an average annual increase of 5.2 percentage points (Figure 1).
Figure 1.
Coverage with ≥1 HPV vaccine among adolescents aged 13–17 years by MSA status and nationally, NIS-teen, 2013–2017.
Footnotes:AAPPC = Average annual percentage point change. *Statistically significant (p < .05) percent point increase compared to the previous year.† Statistically significant average annual increase/decrease
HPV vaccination coverage increased each year in all MSA areas. However, disparities in vaccination coverage between MSA areas were observed; these differences did not significantly change over time – the slopes of the differences did not significantly differ from zero (Figure 2(a-c)). HPV vaccination initiation was 11–16 percentage points lower for adolescents living in mostly rural areas compared to those living in mostly urban areas (Figure 2(a)), 5–9 percentage points lower for adolescents living in suburban areas compared to those living in mostly urban areas (Figure 2(b)), and 4–8 percentage points lower for adolescents living in mostly rural areas compared to those living in suburban areas (Figure 2(c)).
Figure 2.
(a). Disparities in HPV vaccination initiation among adolescents aged 13–17 years living in mostly urban vs. mostly rural areas, NIS-teen 2013–2017. Between 2013 and 2017, the estimated average annual percentage point change in the difference in coverage between mostly urban and mostly rural areas: 0.0, p = .98. (b). Disparities in HPV vaccination initiation among adolescents aged 13–17 years living in mostly urban vs. suburban areas, NIS-teen 2013–2017. Between 2013 and 2017, the estimated average annual percentage point change in the difference in coverage between mostly urban and suburban areas: 0.3, p = .50. (c). Disparities in HPV vaccination initiation among adolescents aged 13–17 years living in suburban vs. mostly rural areas, NIS-teen 2013–2017. Between 2013 and 2017, the estimated average annual percentage point change in the difference in coverage between suburban and mostly rural areas: −0.3, p = .59.
To determine whether these disparities by MSA status were unique to the HPV vaccine, we examined trends in coverage and disparities by MSA status for Tdap and MenACWY – other vaccines routinely recommended for preadolescents aged 11–12 years. Compared with adolescents living in mostly urban and suburban areas, those living in mostly rural areas had significantly lower coverage with ≥1-dose MenACWY (Figure 3(a)). Over the five-year period, coverage with meningococcal vaccine was similar between suburban and mostly urban areas whereas the difference in coverage with ≥1-dose MenACWY between mostly urban and mostly rural areas ranged from 7.4 to 16.9 percentage points (Figure 3(b)). During 2013–2017, there was a significant decrease (p < .01) in the disparity in coverage between mostly urban and mostly rural areas for MenACWY vaccine (Figure 3(b)). Coverage with ≥1-dose of Tdap vaccine was significantly lower among adolescents living in mostly rural areas compared with those living in mostly urban and suburban areas from 2013 to 2015. However, in 2016 and 2017, there were no disparities in ≥1-dose of Tdap vaccination coverage by MSA area (Figure 4).
Figure 3.
(a). Disparities in ≥1 MenACWY vaccination coverage among adolescents aged 13–17 Years by MSA, NIS-teen, 2013–2017. Footnotes: * Statistically different from adolescents living in both mostly urban and suburban areas (p < .05). (b). Disparities in ≥1 MenACWY vaccination coverage among adolescents aged 13–17 years living in mostly urban vs. mostly rural areas, NIS-teen 2013–2017. Between 2013 and 2017, the estimated average annual percentage point change in the difference in coverage between mostly urban and mostly rural areas: −2.2, p < .01.
Figure 4.
Disparities in ≥1 Tdap vaccination coverage among adolescents aged 13–17 Years by MSA, NIS-teen, 2013–2017.
Footnotes:* Statistically different from adolescents living in both mostly urban and suburban areas (p < .05).
Additional analyses were conducted to examine the trends in coverage with ≥-1dose of HPV vaccine among subgroups of adolescents by MSA status and whether similar trends in urban-rural disparities exist among these subgroups. From 2013 to 2017, significant increases in coverage with ≥1-dose of HPV vaccine were observed among adolescents in each MSA regardless of sex, race/ethnicity, and poverty level (Supplementary Figure 1a – 3b). Despite significant increases in HPV vaccination initiation observed over the five-year period, urban-rural disparities among subgroups of adolescents persisted over time. The five-year average annual percentage point change in the difference in HPV vaccine initiation between mostly urban and mostly rural areas did not change significantly among females (p = .19) (Supplementary Figure 1a.) or among males (p = .38) (Supplementary Figure 1b.). Additionally, the average annual percentage point change in the difference in HPV vaccination initiation between mostly urban and mostly rural areas did not change among white, non-Hispanic (p = .65) (Supplementary Figure 2a.) or Hispanic adolescents (p = .92) (Supplementary Figure 2c). While there was no change in the difference in HPV vaccination initiation between black non-Hispanic adolescents by geographic area (p = .55), there was also no disparity in coverage with ≥1-dose of HPV vaccine as seen in other racial/ethnic groups (Supplementary Figure 2b). During the five-year period, there was no significant change in the difference in coverage with ≥1-dose of HPV vaccine among adolescents living below the poverty level (p = .91) (Supplementary Figure 3a) or at/above the poverty level (p = .96) (Supplementary Figure 3b).
Discussion
This study examined the trends in HPV vaccination initiation and disparities in ≥1-dose HPV vaccine coverage by MSA status over a five-year period. From 2013 to 2017, we observed that coverage with ≥1-dose of HPV vaccine increased an average of about 5 percentage points each year among adolescents living in urban, suburban, and rural areas. We also observed that HPV vaccination initiation in mostly rural and suburban areas were significantly lower than coverage in mostly urban areas, and these differences persisted over time. These findings were consistent with previous studies that examined differences by urbanicity7,12–16.
The disparity in coverage with ≥1-dose of HPV vaccine observed between adolescents living within urban areas and outside of urban areas is not well understood. Previous studies have identified several reasons likely responsible for the disparity in coverage observed between geographical areas. Among these reasons are lack of awareness of the HPV vaccine and knowledge on its role in protecting against certain cancers among residents of rural areas.20,21 Also, there may be a lack of knowledge of HPV vaccination recommendations among rural health-care providers who are likely family and/or general practitioners serving entire rural communities.20–22 Vaccination providers in rural areas are not likely to strongly recommend the HPV vaccine for reducing the risk of cancer if they are not themselves educated on the importance of vaccination of children ages 11–12 and prior to exposure to HPV virus. Parents and guardians from a study in rural Alabama stated that a strong provider recommendation would be most influential in initiation of the HPV vaccine series.20 This is consistent with other findings that the quality of the recommendation from the health-care provider continues to be a major predictor of HPV vaccination.23–27 Provider recommendation for HPV vaccination, at each age-eligible visit, even if parents choose initially not to have their children vaccinated, has been shown to improve vaccine acceptance.27
The differences in coverage with ≥1-dose of HPV vaccine by MSA status have remained over time. When MSA status was stratified by select characteristics (e.g. sex, race/ethnicity, and poverty level), the urban-rural disparity persisted over time for all groups except among black, non-Hispanic adolescents. In comparing the trends in coverage and disparities by MSA status for Tdap and MenACWY vaccines, we found similar trends of urban-rural disparities for coverage with ≥1 MenACWY. Urban-Rural disparities for coverage with ≥1 MenACWY are still present but appear to be diminishing. During 2013–2017, an increasing number of states required MenACWY vaccination for school enrollment (pre-2013: 19 states vs. post-2013: 30 states) which likely contributed to increased coverage with MenACWY in rural areas.28 Over the five-year period, the disparity in coverage with ≥1Tdap disappeared; however, it should be noted that the urban-rural disparities were observed for coverage with Tdap vaccine from 2013 to 2015. The Tdap vaccine is required for enrollment in secondary schools in the District of Columbia and all states except Hawaii and may partially explain the vanishing urban-rural disparity observed for coverage with the Tdap vaccine.29 Other factors associated with the decrease in the urban-rural disparity for MenACWY and Tdap vaccination should be investigated to determine if similar interventions could be targeted toward rural populations to improve vaccination coverage and reduce differences in HPV vaccination coverage by geographical area.
There are at least four limitations in this study. First, biases in estimates may remain after adjustments to minimize nonresponse bias and incomplete representation of the sampling frame due to phoneless households. Second, trends in coverage by survey year could be biased if residual bias remaining after weighting adjustments varied by survey year.17 Third, the three-level MSA status categorization lacks granularity to detect differences that might exist within MSA areas. For example, are there differences in vaccination coverage among adolescents living in larger versus smaller urban areas or more or less remote rural areas as suggested in other studies.14,15 Finally, an assumption of linearity was applied in estimating the average annual percentage point increase by year; if the trend is non-linear, this average may not reflect variations in the rate of increase from year to year.
A better understanding of the underlying factors behind lower HPV vaccine coverage in more rural areas when compared with more urban areas is needed in order to develop targeted interventions appropriate for rural populations. However, one place to start is for health-care providers to incorporate recommendation for and administration of HPV and MenACWY vaccines during the same visit they administer Tdap vaccine.
Acknowledgments
We gratefully acknowledge James A. Singleton, PhD for his contribution in conceptualizing this study and his critical review of the manuscript.
Disclosure of potential conflicts of interest
No conflicts of interest were reported by any of the authors. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
Source of work and financing
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Supplementary materials
Supplemental data for this article can be accessed on the publisher’s website.
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