Abstract
Purpose:
In this study, we evaluated factors associated with receipt of meningococcal B (MenB) vaccine among adolescents in the United States.
Methods:
We used public-use data files from the National Immunization Survey–Teen from 2017–2018. Logistic regression was used to model associations between sociodemographic, healthcare, and vaccination variables of interest and MenB vaccine receipt (≥ 1 vs. 0 dose). To explore associations between state-level meningococcal vaccination requirements and MenB vaccine uptake, we performed a secondary analysis stratified by presence of a quadrivalent meningococcal (MenACWY) vaccination requirement for secondary school attendance in the adolescent’s state of residence (no requirement vs. a 1- or 2- dose requirement).
Results:
Among 7,288 adolescents, MenB vaccine receipt was significantly associated with up-to-date HPV (aOR 1.74, 95% CI: 1.29–2.35) and MenACWY (aOR 5.81, 95% CI: 4.14–8.13) vaccination status in multivariable analysis. Adolescents with private insurance were less likely to be vaccinated (aOR: 0.61, 95% CI: 0.46–0.79) compared to adolescents with other health insurance types. In secondary analyses, health insurance was no longer significantly associated with MenB vaccine uptake among adolescents in states with a MenACWY requirement.
Conclusions:
We found that MenB vaccination is associated with receipt of other vaccines recommended for use in adolescents. Adolescents with private health insurance were less likely to be vaccinated against MenB, though state MenACWY requirements appeared to modify the effect of insurance on MenB vaccine receipt. Further work to understand how these factors may influence delivery and acceptance of MenB vaccine can inform interventions and strategies to improve uptake.
Keywords: meningococcal vaccine, adolescent vaccination, vaccination recommendations, serogroup B meningococcal disease, NIS-Teen
Background
Neisseria meningiditis is a rare but potentially life-threatening cause of invasive disease, including bacteremia and meningitis, that disproportionately affects adolescents and young adults. Invasive meningococcal disease is associated with a case fatality rate of 15%, and up to 20% of survivors experience significant sequelae of infection such as limb amputations, neurologic complications, and hearing and vision loss [1, 2]. In the United States, disease caused by N. meningiditis serogroup B (MenB) is currently the most prevalent type of meningococcal infection [3]. Most (>80%) cases of MenB disease occur in adolescents and young adults and several recent outbreaks of MenB disease have been reported in university settings, highlighting the increased risk of MenB disease among college students [3, 4, 5].
In 2015, following the licensure of two serogroup B meningococcal vaccines, the Centers for Disease Control and Prevention’s (CDC) Advisory Committee on Immunization Practices (ACIP) recommended that on the basis of individual clinical decision making (formerly Category B recommendation, now referred to as shared clinical decision making), a MenB vaccine series may be administered to healthy individuals aged 16–23 years to protect against MenB disease, with 16–18 years the preferred ages for vaccination [3, 6]. Routine MenB vaccination is only recommended for individuals with underlying conditions that place them at high risk of invasive meningococcal disease, such as complement deficiencies and asplenia, and in outbreak settings [3]. Thus, in most situations, and in contrast to quadrivalent meningococcal conjugate (MenACWY) vaccine, which is recommended for a booster dose at the same target ages following a first dose at ages 11–12, clinicians together with parents and adolescents must decide whether MenB vaccination is in the adolescent’s best interest. The rationale for vaccination on the basis of shared clinical decision making was intended to balance the current low and decreasing prevalence of meningococcal B disease at the population level on the one hand, against the individual benefit from protective vaccines and the known seriousness of meningococcal disease on the other [3]. This recommendation is unique, in that no other vaccine for healthy adolescents, and few vaccines overall, carry this type of recommendation [6]. To date, uptake of MenB vaccine has been low but rising, with 17.2% and 21.8% of 17-year-olds initiating the vaccine series by 2018 and 2019, respectively [7, 8]. There has been limited attention to MenB vaccine in the literature compared to other adolescent vaccines. To better understand patterns of MenB vaccine uptake following implementation of the 2015 ACIP recommendation for shared clinical decision making, we sought to identify factors associated with MenB vaccine receipt in the initial years following its inclusion on the vaccine schedule, using data from the National Immunization Survey-Teen (NIS-Teen) in 2017–2018.
Methods
We utilized the public use data files from NIS-Teen, a cross-sectional, nationally representative survey conducted annually by CDC to monitor vaccination coverage among adolescents ages 13–17 years. Methodology of NIS-Teen has been described in detail previously [9, 10]. Briefly, the survey is conducted in two phases: in the first phase, parents of 13–17-year-olds are contacted by telephone to complete a household survey, which is then followed by verification of the teen’s immunization records after parents grant permission to contact the adolescent’s healthcare providers. For this analysis, we combined data from the 2017 and 2018 surveys, the first two years for which NIS-Teen data on MenB vaccine is available, following recommended methods [9, 10]. Based on the preferred age range for MenB vaccine administration of 16–18 years, and to ensure that all adolescents had equal opportunity to receive MenB vaccine, we chose to restrict the present analysis to adolescents 17 years of age with adequate provider data, which resulted in a final sample of 7,288 adolescents.
The primary outcome of interest was provider-verified receipt of ≥1 dose of MenB vaccine, compared to no doses of MenB vaccine. We considered several covariates that could potentially account for differences in adolescents’ MenB vaccination status to control for confounding. Sociodemographic characteristics included sex, race/ethnicity, and census region of the adolescent’s state of residence, as defined by the US Census Bureau. Healthcare characteristics included health insurance status, presence of an underlying chronic medical condition, and whether the adolescent attended a healthcare visit in the past year. Based on previous literature suggesting an association between receipt of other adolescent vaccines and vaccines newly added to the ACIP schedule (e.g. human papillomavirus (HPV) vaccine), we included provider-verified receipt of HPV vaccine (up-to-date vs. not up-to-date with vaccine series), meningococcal conjugate (MenACWY) vaccine (2 doses vs. 0–1 dose), and tetanus-diphtheria-pertussis (Tdap) vaccine as covariates to examine associations between MenB uptake and up-to-date status for other adolescent vaccines [11–13].
Descriptive statistics including frequencies and survey-weighted percentages were calculated. Logistic regression was then used to model the unadjusted associations between variables of interest and MenB vaccine receipt. All covariates were initially entered into a full multivariate model, with manual backward selection used to remove covariates starting with the largest p value until all covariates retained in the model were significantly associated at p<0.05.
A secondary analysis stratified by whether a MenACWY vaccination requirement was in effect in the adolescent’s state of residence by the 2016–2017 school year, was also performed. We hypothesized that school entry requirements for MenACWY vaccine could be associated with MenB vaccine uptake based on our prior work suggesting that state-level school entry requirements for MenACWY vaccine were associated with up-to-date MenACWY coverage, and because vaccination requirements have been observed to lead to spillover increases in coverage for nontargeted vaccines [14, 15]. MenACWY school entry requirements for each state were obtained from the Immunization Action Coalition [16]. Because only 8 states had a requirement for 2 MenACWY doses in place by the 2016–2017 school year, we classified each state and the District of Columbia as either having no requirements for MenACWY (n=27) or a 1- or 2-dose requirement (n=24) [16]. For this analysis, all covariates from the primary analysis were initially entered into full multivariate models stratified by MenACWY vaccination requirements. Manual backward selection was used to remove covariates starting with the largest p value until all covariates retained in the model were significantly associated at p<0.05.
All analyses were conducted in SAS (version 9.4, The SAS Institute, Cary, NC) using procedures for complex survey data and appropriate sampling weights for the analysis of provider-reported data, as per the NIS-Teen Data User’s Guides [9, 10]. This study was deemed to be exempt from review by the Yale University IRB because NIS-Teen datasets are de-identified and publicly available online [17].
Results
When compared with adolescents who had not received MenB vaccine, adolescents who received at least 1 dose of MenB vaccine were more likely to be Hispanic, have received other recommended adolescent vaccines (Tdap, MenACWY, and HPV), and less likely to be privately insured (Table 1). Vaccinated and unvaccinated adolescents did not differ significantly with respect to sex, census region, presence of a chronic health care condition, or whether they had a health care visit in the past year.
Table 1.
Bivariate and multivariable associations between study variables and MenB vaccinated vs. unvaccinated status among US adolescents aged 17 years, overall and stratified by state MenACWY school entry requirements (n=7288)a
| Characteristic | n | n (%) with ≥ 1 dose MenB vaccine | Unadjusted OR (95% CI) | Adjusted OR (95% CI) | School Requirementsd Adjusted OR (95% CI) | No School Requirementse Adjusted OR (95% CI) |
|---|---|---|---|---|---|---|
| Sex | ||||||
| Male | 3900 | 551 (15.1) | 0.89 (0.68 – 1.15) | --f | -- | -- |
| Female | 3388 | 547 (16.8) | 1.00 (Ref) | -- | -- | -- |
| Race/Ethnicity | ||||||
| Non-Hispanic White | 4548 | 626 (13.5) | 1.00 (Ref) | -- | -- | -- |
| Hispanic | 1341 | 258 (20.8) | 1.68 (1.21 – 2.32) | -- | -- | -- |
| Non-Hispanic Black | 615 | 92 (16.1) | 1.22 (0.82 – 1.83) | -- | -- | -- |
| Other | 784 | 122 (17.4) | 1.34 (0.84 – 2.15) | -- | -- | -- |
| Census Region | ||||||
| Northeast | 1440 | 261 (18.3) | 1.00 (Ref) | -- | -- | 1.00 (Ref) |
| Midwest | 1603 | 291 (15.2) | 0.80 (0.61 – 1.06) | -- | -- | 2.58 (1.47 – 4.54) |
| South | 2695 | 376 (14.6) | 0.76 (0.58 – 1.00) | -- | -- | 1.87 (1.04 – 3.37) |
| West | 1550 | 170 (17.0) | 0.91 (0.59 – 1.43) | -- | -- | 1.80 (0.93 – 3.49) |
| ≥ 1 Healthcare visit in past year | ||||||
| Yes | 6326 | 1002 (16.3) | 1.35 (0.87 – 2.08) | -- | -- | -- |
| No | 887 | 80 (12.6) | 1.00 (Ref) | -- | -- | -- |
| Health Insurance | ||||||
| Private | 4257 | 620 (13.3) | 0.65 (0.51 – 0.84) | 0.61 (0.46 – 0.79) | -- | 0.40 (0.24 – 0.66) |
| Medicaid/other/uninsured | 3031 | 478 (19.1) | 1.00 (Ref) | 1.00 (Ref) | -- | 1.00 (Ref) |
| Chronic health condition | ||||||
| Yes | 385 | 55 (20.6) | 1.40 (0.76 – 2.56) | -- | -- | -- |
| No | 6878 | 1039 (15.6) | 1.00 (Ref) | -- | -- | -- |
| HPV Vaccinationb | ||||||
| Yes | 4049 | 861 (21.7) | 3.10 (2.31 – 4.15) | 1.74 (1.29– 2.35) | 1.67 (1.25 – 2.21) | 1.97 (1.06 – 3.65) |
| No | 3239 | 237 (8.2) | 1.00 (Ref) | 1.00 (Ref) | 1.00 (Ref) | 1.00 (Ref) |
| MenACWY Doses | ||||||
| 0–1 | 3884 | 167 (5.2) | 1.00 (Ref) | 1.00 (Ref) | 1.00 (Ref) | 1.00 (Ref) |
| 2 | 3404 | 931 (27.2) | 6.77 (4.79 – 9.55) | 5.81 (4.14 – 8.13) | 6.26 (4.50 – 8.70) | 5.41 (3.01 – 9.72) |
| Tdap Vaccinationc | ||||||
| Yes | 6524 | 1039 (16.7) | 1.90 (1.01 – 3.56) | -- | -- | -- |
| No | 764 | 59 (2.7) | 1.00 (Ref) | -- | -- | -- |
Table values are n (weighted %). Numbers may not sum to total due to missing data, and percentages may not sum to 100% due to rounding.
Received 3+ HPV shots, or 2+ shots with first shot received before age 15
Received Tdap after age 10
Analysis restricted to adolescents who resided in a state with a MenACWY vaccine mandate in place during the 2016–2017 school year (n=3977).
Analysis restricted to adolescents who resided in a state with no MenACWY vaccine mandate in place during the 2016–2017 school year (n=3311).
Dashes (--) indicate covariates that were initially included in the model but removed due to lack of significance at the p<0.05 level.
OR = odds ratio; CI = confidence interval
In bivariate analyses, factors associated with MenB vaccine uptake included race/ethnicity, receipt of other recommended adolescent vaccines (Tdap, MenACWY, and HPV), census region, and insurance status. In the multivariable analysis, MenB vaccine receipt remained significantly associated with up-to-date HPV vaccination status (aOR 1.74, 95% CI: 1.29–2.35) and receipt of 2 MenACWY vaccine doses compared to 0–1 doses (aOR 5.81, 95% CI: 4.14 – 8.13). In addition, adolescents with private insurance were less likely to be vaccinated against MenB (aOR: 0.61, 95% CI: 0.46–0.79) compared to adolescents with other health insurance types.
In the secondary analysis stratified by presence of a MenACWY vaccination requirement in the adolescent’s state of residence (Table 1), up-to-date HPV vaccination status and receipt of 2 doses of MenACWY vaccine remained significantly associated with MenB vaccine receipt regardless of whether a MenACWY vaccination requirement for school entry was in effect [aOR HPV: 1.67, 95% CI: 1.25–2.21, aOR MenACWY 6.26, 95% CI: 4.50–8.70 (states with school requirements) vs. aOR HPV 1.97, 95% CI: 1.06–3.65, aOR MenACWY 5.41, 95% CI: 3.01–9.72 (states with no school requirements)]. However, differences were observed in the association of health insurance status with MenB vaccine uptake. Health insurance was no longer significantly associated with MenB vaccine uptake among adolescents who resided in a state with a meningococcal vaccine school requirement. Among adolescents who resided in a state with no meningococcal vaccine requirement, those with private health insurance remained less likely to be vaccinated, compared to adolescents who were uninsured or had other types of health insurance (aOR 0.40, 95% CI: 0.24 – 0.66).
Discussion
In this analysis, we examined patterns of MenB vaccine uptake in a national sample of US adolescents in the first few years after the ACIP recommendation. Uptake of MenB vaccine varied by receipt of other adolescent vaccines and health insurance status. These findings add to the knowledge on MenB vaccine uptake in the US and are consistent with prior studies which found that adolescents who received MenB vaccine were more likely to have received HPV vaccine and studies that have found receipt of other adolescent vaccines to be strong predictors of HPV vaccine initiation and completion [18, 11].
It is less clear why adolescents with private insurance were 39% less likely to receive MenB vaccine to as compared to uninsured adolescents and adolescents with other types of insurance, including Medicaid, though similar patterns of uptake have also been observed with HPV vaccine [19, 8]. Drawing from the HPV vaccine implementation experience, one possibility could be that private insurance coverage, as a marker of higher socioeconomic status, may be an indicator of greater vaccine hesitancy, with parents of privately insured adolescents more likely to delay or refuse MenB vaccine [20]. In addition, if clinicians perceive greater MenB vaccine hesitancy among privately insured populations, they may in turn be more likely to defer recommending vaccination, as prior studies have suggested that clinicians tend to overestimate parents’ vaccine concerns [21].
In secondary analyses, we explored the association of school entry requirements for MenACWY vaccine with MenB vaccine uptake, and found that the presence of state-level school entry requirements for meningococcal vaccination appeared to mitigate the association of health insurance with MenB vaccine uptake, while in states that lacked a meningococcal vaccine mandate, the association of MenB unvaccinated status and private insurance coverage became more pronounced. It is notable that differences by state vaccine policy were observed. Given that in a recent nationally representative survey of parents, a majority (57%) were unaware of MenB vaccine, it is possible that school entry requirements for MenACWY could improve MenB coverage indirectly, by raising awareness of the importance of meningococcal vaccines more broadly [22]. State-level school entry vaccination requirements have previously been shown to be a powerful tool to promote equity and reduce disparities in coverage levels of other vaccines in adolescent populations [14, 23]. They have also been shown to lead to spillover increases in coverage in non-targeted vaccines [15, 24]. Our findings suggest that the influence of school requirements on increasing coverage more broadly and reducing health disparities may also extend to vaccines with a recommendation for shared clinical decision making. As additional states have enacted requirements for meningococcal vaccination since the time period analyzed in the current study, and colleges have begun to either require or recommend MenB vaccination prior to matriculation, the influence of state- and university-level requirements on MenB vaccine coverage is an area that warrants future study [16, 25, 26].
In contrast to prior studies that identified contact with the medical system as a factor associated with HPV vaccine series uptake and up-to-date MenACWY coverage, we did not find that having a healthcare visit in the past year was associated with MenB vaccine receipt [12, 14]. It should be noted that the NIS-Teen dataset broadly defines healthcare visits, so we were unable to examine association of MenB uptake with different visit types; this should be a focus of future work. Specifically, it will be important to understand whether there are missed opportunities for MenB vaccination at well child visits because vaccination is one of the main purposes of these visits. In addition, it has been recommended that any adolescent healthcare encounter should be used as vaccination opportunities to boost coverage, should circumstances permit [27]. Another potential reason why a healthcare visit was not significantly associated with MenB vaccination could be due to the unique nature of the MenB vaccine recommendation, which does not call for universal administration of this vaccine to all adolescents. Previous research has identified clinicians’ poor understanding of the MenB vaccine recommendation for shared clinical decision-making as a contributing factor to its low uptake, highlighting a need for greater guidance for clinicians on how to implement of this type of recommendation [18, 28, 29].
While this study did not directly evaluate how clinicians communicate about MenB vaccine, the recommendation for shared clinical decision-making makes the topic of when and how clinicians discuss MenB vaccine an important one that warrants further examination. Experts and professional societies have advocated that a discussion about MenB vaccine should take place with all patients and their parents; for example, the American Academy of Pediatrics’ Committee on Infectious Diseases encourages pediatricians to discuss the availability of MenB vaccines with families, to allow a decision that is in the patient’s best interest [30]. However, prior studies geared at understanding clinicians’ interpretation of MenB vaccine recommendations suggest that this is not yet occurring uniformly: a nationally representative survey found that only 51% of pediatricians and 31% of family practitioners reported always or often discussing MenB vaccine [28]. Another aspect of the shared clinical decision-making dynamic that warrants attention in view of the target age range for MenB vaccination is adolescents’ desired role in the decision-making process. While adolescents are generally not the primary decision-makers regarding vaccination (due to state laws that require parental consent for vaccination of adolescents under 18 years of age in most cases), given the older ages targeted for MenB vaccine, it is conceivable that adolescents play a role in decision-making for this vaccine, but this has not yet been studied. Although we cannot directly measure the frequency or content of discussions of MenB vaccine that are occurring based on the data at hand, our findings of factors associated with uptake can provide an indication of the patterns of acceptance of the vaccine following a discussion during the first few years of the recommendation’s existence.
There are a few limitations in this analysis worth noting. First, NIS-Teen does not include 18-year-olds, who are also within the preferred age range for MenB vaccination, and MenB vaccine may be considered for administration up to age 23. Therefore, any vaccination occurring among 18-year-olds or young adults would not be captured in the present analysis. With heightened attention on the risk of MenB disease among college students, it is possible that MenB vaccination is being deferred by clinicians, parents, and/or adolescents until closer to starting college, or until young adults can decide about vaccination for themselves. One study of MenB vaccination within a single health care system found older age (19–23 years) to be significantly associated with MenB vaccine uptake and series completion; further research should investigate patterns of MenB vaccine uptake among young adults [31]. Another limitation of this study is that it focused on MenB vaccination among adolescents in 2017 and 2018, and so describes factors associated with early adopters of vaccination. As these are the only years for which public use NIS-Teen data are currently available, we were unable to include subsequent years of data in this analysis, but as MenB vaccination coverage has shown a steady upward trend each year, future work will be needed to establish whether the patterns described here hold over time. Lastly, our analysis was restricted to adolescents who had adequate provider data, because the outcome variable of interest –MenB vaccine uptake – was only measured among adolescents for whom provider-verified vaccine histories could be reviewed. NIS-Teen uses sampling weights to adjust for parent and health care provider non-response, but it is possible that by only including adolescents with adequate provider data, bias towards inclusion of adolescents with higher vaccine coverage remains.
Conclusions
Prevention of invasive meningococcal disease is an important public health goal, and the availability of MenB vaccines represents a key tool towards reducing the impact of meningococcal disease in adolescents and young adults, who disproportionately experience its burden. We found that MenB vaccination is associated with receipt of other vaccines recommended for use in adolescents. Adolescents with private health insurance were less likely to be vaccinated against MenB, though state MenACWY requirements appeared to modify the effect of insurance on MenB vaccine receipt. Future research will be needed to bridge gaps in understanding how these factors influence clinicians’ practice patterns in recommending MenB vaccines, and drive demand for MenB vaccine at the parent/patient level, as well as how variable state and university-level entry requirements as well as vaccine hesitancy may influence MenB coverage. Given this study’s focus on vaccination in older adolescence, our findings may also have implications for other new vaccines that are recommended for use in this age group. Lastly, with limited studies examining vaccines that carry a recommendation for shared clinical decision making from ACIP, our findings may also contribute to a greater understanding of factors associated with uptake for this category of vaccines.
Implications & Contributions.
MenB vaccine uptake varied by receipt of other adolescent vaccines and health insurance status. Findings provide insight on how MenB vaccines, the only adolescent vaccines that are recommended for administration on the basis of shared clinical decision-making, are being used in clinical practice.
Acknowledgments
Funding: This work was supported by the National Institutes of Health grant number K23 HD098710–02 awarded to Dr. Hansen. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Abbreviations:
- MenB
meningococcal serogroup B
- NIS-Teen
National Immunization Survey-Teen
- MenACWY
quadrivalent meningococcal; serogroups A, C, W, Y
- CDC
Centers for Disease Control and Prevention
- ACIP
Advisory Committee on Immunization Practice
Footnotes
Declaration of interests: Dr. Niccolai has served as Scientific Advisor for Merck.
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