Background
Invasive meningococcal disease (IMD) is an uncommon and unpredictable infection that progresses rapidly and can have severe consequences, including death and disfigurement, despite appropriate medical treatment [
1‐
5]. In the United States, serogroup B (MenB) is now the leading cause of IMD among the 6 common meningococcal disease-causing serogroups globally (ie, A, B, C, W, X, and Y) [
6,
7]. In addition to infants, adolescents and young adults are particularly vulnerable because they are the primary asymptomatic carriers, with meningococcal carriage peaking at around 19 years of age [
8]. In institutional settings such as college dormitories, carriage rates can exceed 50% [
9,
10] and can lead to disease transmission due to age-typical social mixing behaviors [
7]. The Centers for Disease Control and Prevention (CDC) Enhanced Meningococcal Surveillance has shown that MenB accounts for approximately 69.6% of IMD cases in 16- to 23-year-olds in the United States and MenB has caused all 14 meningococcal outbreaks on US college campuses since 2011 [
6,
11‐
13]. MenB vaccines have been available in the United States since 2014, which currently include MenB-FHbp (Trumenba®, Pfizer Inc, Philadelphia, PA) and MenB-4C (Bexsero®, GlaxoSmithKline Vaccines, Srl, Sovicille, Italy) [
14,
15]. Quadrivalent conjugate MenACWY vaccines have been available in the United States since 2005 [
16].
The US Advisory Committee on Immunization Practices (ACIP) recommends that all individuals receive MenACWY vaccine at 11 to 12 years of age, followed by a booster dose at 16 years of age [
16,
17], which is a “Category A” or routine recommendation that applies to everyone in the indicated age group [
18]. For MenB vaccines, ACIP issued a “Category B” recommendation (shared clinical decision-making in consultation with a healthcare provider [HCP] [
19]) for vaccination of healthy individuals 16 to 23 years of age, with a preferred age of 16 to 18 years [
20,
21]; a Category A recommendation was made for individuals ≥10 years of age at increased risk of IMD, such as those with asplenia or complement deficiency, or due to laboratory or outbreak exposure [
20]. MenACWY vaccines were first recommended in 2005 followed by a booster dose recommendation in 2010 [
16]. In 2018, MenACWY vaccination rates among individuals 13 to 17 years of age were 86.6% for ≥1 dose and 50.8% for ≥2 doses [
22]. Since the initial recommendations for MenB vaccines in 2015 [
21], the MenB vaccine uptake reported in CDC’s 2018 National Immunization Survey–Teen (NIS-Teen) indicated that 17.2% of US 17-year-olds had received ≥1 dose of a MenB multi-dose vaccine series (and < 50% complete the full series) [
20,
22,
23].
Given that there is a structural difference in ACIP recommendations for the 2 classes of vaccines (MenACWY and MenB) needed for prevention of IMD among healthy adolescents [
14,
15,
20], and MenB vaccine uptake in adolescents is low nationally [
22], this study examined factors associated with parental/guardian awareness and utilization of MenB vaccines.
Methods
Recruitment and data collection
All data were collected via a survey conducted across the United States from December 9, 2016, through December 28, 2016. Survey participants were identified through the Ipsos KnowledgePanel® (formerly Growth from Knowledge; New York, NY), an online, probability-based, representative, random sample of US households. Because KnowledgePanel® includes households regardless of internet access, members are provided with laptops and/or internet access as needed for potential survey participation. This panel has been used for several previous national studies on immunization issues [
24‐
27].
Email invitations were sent to a random, nationally representative sample of KnowledgePanel® households without details of the research topic, so as to minimize bias in the responding sample. Eligible participants were adult parents or guardians of ≥1 dependent aged 16 to 19 years, spoke either English or Spanish, and agreed with the confidentiality statement. An English or Spanish version of the survey was available to participants. Recruitment was quota oriented rather than a convenience sample. To have sufficient numbers and a proper distribution of parents whose adolescents were vaccinated or not vaccinated, and based on the MenB vaccination rate in 2015, the study planned to recruit at least 525 participants. These included 75 parents/guardians of MenB-vaccinated adolescents and 150 participants in each of the 3 additional mutually exclusive groups of varying levels of MenB awareness and utilization (i.e., MenB vaccine-unaware, aware and intending to vaccinate, or aware but not intending to vaccinate).
After completing screening questions, qualified participants completed a 25-min, self-administered online questionnaire, which included questions on demographics, vaccine awareness, status and intention, perceptions related to diseases and vaccines, HCP interaction related to vaccines, their decision-making process for vaccination, and general knowledge of the subject area (questionnaire available upon request). Respondents who indicated that their dependent(s) had been vaccinated with ≥1 dose of a MenB vaccine were then directed to a verification section requesting confirmation of the vaccine used and the date received (acquired via electronic medical records [EMRs], if available, or by contacting the HCP office). Additional demographic (age, race), social (education, housing), and economic data (insurance coverage) were extracted from KnowledgePanel® member profiles. All KnowledgePanel® members who participated in this study provided explicit consent prior to collection of any health/sensitive information.
Groups and assessments
In the survey, respondents were first asked if they were aware of any available vaccines for meningococcal disease (meningitis). If they responded “yes,” they were prompted to indicate their awareness level for each vaccine type (i.e., MenB, MenACWY, and MenCY, the latter of which is recently no longer available in the United States) as “not at all aware,” “slightly aware,” “somewhat aware,” “moderately aware,” or “extremely aware.” “Aware” was defined as respondents who were at least slightly aware of MenB vaccines; otherwise, they were classified as “unaware.” Of those classified as “aware,” respondents were further designated as “vaccinated” if at least 1 of their children between 16 and 19 years of age had received ≥1 dose of a MenB vaccine, and as “intend to vaccinate” or “not intend to vaccinate” if they did or did not anticipate vaccinating their eligible children with MenB in the next 6 to 12 months, respectively. Respondents classified as “unaware” were asked to indicate their interest level for obtaining more information or speaking with an HCP about MenB vaccination, and vaccinating their child against MenB upon physician recommendation; the scale of interest level ranged from 1 to 7, where 1 indicated “not at all interested” and 7 indicated “extremely interested.” “Unaware but interested in vaccination” included respondents who were not aware of any MenB vaccine but responded that they were very interested (rated “6” or “7”).
Data analysis
Data were analyzed using a population-based weighting method by adjusting sample weights to known population distributions among individuals ≥35 years of age and based on information retrieved from the US Census Bureau’s Current Population Survey (CPS; March 2016 Supplement). Specifically, computation was conducted on the design or base weights to reflect selection probabilities. Sample weights for all respondents (eligible and not eligible) were then adjusted to known population distributions obtained from the CPS. Prespecified dimensions used for weighting were sex, race/ethnicity, geographic region, educational attainment, household income, and language proficiency, consistent with prior studies [
25‐
27].
Univariate and multivariate analyses were conducted to identify factors associated with MenB awareness, utilization, and interest. Specifically, 4 sets of comparisons were conducted: 1) aware versus unaware of the MenB vaccines, 2) aware and vaccinated or with intention to vaccinate versus aware with no intention to vaccinate, 3) aware and vaccinated versus aware with intention to vaccinate, and 4) unaware but interested in vaccination versus unaware and not interested in vaccination. Variables examined included age, sex, race (White, non-Hispanic; Hispanic; Black and Others, Non-Hispanic), education (high school or below, some college or above), property ownership (own, rent), annual income, insurance status (employer-based, Medicaid, no insurance, others), awareness of MenACWY vaccine, awareness of MenB outbreaks, seeing the same HCP, feeling the HCP knows their child well, HCP recommended MenB vaccine, and first made aware of MenB vaccine by HCP. For the univariate analyses, binary variables (e.g., yes, no) were presented by weighted proportion of each group. Continuous variables (e.g., number of children aged 16–19 years, household income) were presented by weighted means. For the multivariate analyses, logistic regression models based on weighted study samples were applied for each of the comparison groups. To ensure that results were consistent and robust, a classification and regression tree (CART) analysis was then used to identify key predictors and their estimated relative importance. CART is a robust procedure, particularly in the presence of multi-collinearity among a long list of predictor variables [
28].
The analyses of how respondents became aware of MenB vaccines, if they received recommendation from their HCP, and the type of HCP who recommended MenB vaccines, were further compared across the 4 comparison groups. P values of the comparisons between 2 groups were calculated using a Chi-squared test of the weighted sample.
Univariate and multivariate analyses were conducted using the Statistical Analysis System statistical software package (version 9.4) and CART analysis was performed using Salford Predictive Modeler 8.2.
Discussion
MenB causes the majority of meningococcal disease cases among adolescents in the United States (greater than the number of serogroup A, C, W, and Y cases combined) [
6], and meningococcal carriage rates are highest in this age group [
8]. Ensuring equitable access to ACIP-recommended MenB vaccines is essential to help protect this vulnerable population, particularly in light of the ACIP’s non-routine, shared clinical decision-making (previously called “Category B” [
19]) recommendation for MenB vaccines [
21], the first recommendation to apply to an entire age group [
29]. This study investigated parental and guardian awareness and utilization of MenB vaccines, revealing that the majority of parents/guardians were unaware of MenB vaccines and highlighting important racial and socioeconomic disparities in awareness and vaccination status; additionally, vaccination status or intention to vaccinate were strongly predicted by HCP-related factors.
Lack of awareness among parents/guardians regarding MenB vaccines
The majority of parents and guardians (57%) in this study were unaware of MenB vaccination. These results are corroborated by a growing body of evidence on the impact of the shared clinical decision-making (Category B) recommendation on MenB vaccine awareness and utilization. In a 2017 survey of parents of high school students in Minnesota, 75.5% of parents were generally aware of the availability of meningococcal vaccines, but 31% were aware specifically of the MenACWY vaccine and only 18 to 20% were specifically aware of either licensed MenB vaccine [
30]. Even fewer parents (7%) understood that the MenB vaccine helps protect against MenB disease, which is not covered by MenACWY vaccination. However, most parents were at least somewhat willing to vaccinate their adolescent children with MenB vaccines (90%), and intended to seek information from their providers about MenB vaccines (81%). The 2018 CDC NIS-Teen survey report indicated that nationwide only 17.2% of 17-year-olds in the United States had received 1 or more doses of the multidose MenB vaccine series [
22], and only approximately half go on to complete the series [
23]. By comparison, coverage rates for other adolescent vaccines administered in this age group were 86.6% (≥1 dose) and 50.8% (≥2 doses) for MenACWY, 51.1% (up-to-date doses) for the human papilloma virus (HPV) vaccine series, and 88.9% (≥1 dose) for the tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis (Tdap) vaccine, among those aged 11 to 17 years [
22].
Socioeconomic and racial differences in MenB vaccine awareness and uptake
Our findings indicated that females and non-Hispanic, White individuals were significantly associated with increased MenB awareness among parents or guardians. Among parents or guardians unaware of MenB vaccines, there was significantly higher interest in the vaccine among parents of Hispanic ethnicity. Additionally, a marginally higher percentage of unaware respondents had insurance through Medicaid. Although insurance-related factors were not associated with awareness in our study, there is substantial precedent of insurance type-based disparities in healthcare and vaccine access among the US population, including among those patients insured through Medicaid [
31‐
35].
These disparities in awareness are consistent with other studies examining factors associated with MenB vaccination among adolescents and young adults. In a cross-sectional study of 85,789 adolescents (aged 16–18 years) in the Philadelphia immunization registry between 2015 and 2017, only 16% had received ≥1 dose of a multidose MenB vaccine series, and 5% had completed the series [
36,
37]. Multivariate analysis revealed that female sex, unknown or other reported race (compared with Black/African American race), and residing in a neighborhood with a median household income of greater than $100,000 were significantly associated with MenB vaccination, whereas Asian ethnicity was negatively associated with MenB vaccination. Additionally, in a retrospective cohort study using EHRs of 45,428 patients (aged 16–23 years) from 31 pediatric primary care practices in the Philadelphia region between 2015 and 2017, only 21% had received ≥1 dose of a multidose MenB vaccine [
31]. Multivariate analyses revealed that MenB vaccine series completion was significantly associated with White race, having private insurance, and MenACWY vaccine receipt. As this study cohort comprised patients who had access to pediatric primary care, these results suggest that sociodemographic disparities likely persist regardless of access to healthcare.
Healthcare provider impact on MenB vaccine awareness and uptake
Both the likelihood of having been vaccinated (compared with intention to vaccinate) and of being vaccinated/intending to vaccinate (compared with no intention to vaccinate) were most strongly predicted by factors directly related to the HCP. The importance of HCP recommendation was further supported by the CART results. More than a quarter of parents/guardians intending to vaccinate their adolescent were awaiting the recommendation from their HCP, and those who had first learned about MenB vaccines through their provider were significantly more likely to have vaccinated or have the intention of vaccinating their dependents.
In line with these results, previous research has indicated that parents expect providers to guide them on adolescent vaccines and cite the provider’s office as the most common information source for knowing when their adolescents’ vaccines are due [
24]. The ACIP recommended that MenB vaccination be available to adolescents and young adults through provider-patient discussion and shared clinical decision-making (i.e., a Category B recommendation) [
21], yet studies have shown that providers have a poor understanding of MenB vaccines and this ACIP recommendation [
29,
36,
38‐
40]; Category B designation has paradoxically been shown to be the factor that hinders MenB vaccination [
29,
38,
39]. In a nationally representative sample of US providers surveyed in 2016 by Kempe and colleagues, only 38% of family physicians and 56% of pediatricians were able to correctly define a Category B recommendation [
29]. Many providers were also unsure about insurance coverage for a Category B vaccine, despite the fact that under the Affordable Care Act in the United States, all ACIP-recommended vaccines are covered by both private insurance plans and the CDC’s Vaccines for Children (VFC) program for all individuals 18 years and younger [
41]. Ultimately, shared clinical decision-making requires discussion between provider and patients, which is impeded by providers’ lack of understanding of the ACIP recommendations.
Previous work also suggests a link between socioeconomic inequities and provider prescribing behavior. In a nationally representative survey, HCPs who prescribed MenB vaccines (compared with those who prescribed MenACWY only) were most likely to be seeing patients with private or commercial healthcare plans (i.e., not Medicaid) [
40]. Additional findings from the aforementioned study from the Philadelphia region of 45,428 patients (aged 16–23 years) revealed lower MenB vaccine uptake among those seen in urban practice locations (vs suburban practice locations) [
31]. This disparity may reflect different provider practices for MenB vaccine recommendations for different patient populations, and clinical-level purchasing decisions that impact rates of vaccine receipt.
Taken together, these data suggest a need to clarify the existing ACIP recommendation for MenB vaccines and to support providers and parents in the United States by developing consistent guidelines and concrete metrics that define a well-informed discussion for shared clinical decision-making. These efforts will help increase parental awareness of MenB vaccines and avoid reinforcing disparities in vaccine access and utilization that our study has uncovered, and ultimately ensure adolescents are comprehensively protected against meningococcal disease.
Strengths and limitations
This survey had several strengths, including the use of the KnowledgePanel® as a data source, which is one of the most representative online panels in the United States, and has been successfully used in previous studies [
25‐
27]. In addition, this study is one of the first national studies that corroborated findings from previously published regional studies evaluating MenB awareness [
30]. Moreover, the use of address-based sampling and population-weighting methodology ensured data broadly represented the diverse US population. The panel also collected a wide range of demographic, social, and economic data that can be applied to survey analysis.
There were limitations of this study design relative to other studies involving online data collection, which included that the reported behaviors may not estimate actual behavior; for instance, the intention to vaccinate may not equate with vaccination. Vaccination statuses of approximately a third of participants were verified by EMR or HCP, as described in the Methods, to substantiate study results. Given that the survey was self-administered, some parents/guardians may have sought more information on the topic before completing the survey, leading to potential over reporting of MenB vaccine awareness. Finally, the study population may not be entirely representative of the US population as the sample size for some analyses was relatively small and KnowledgePanel® members may have been more inclined towards study participation, which could influence responses. However, as explained in the Methods, our study used population weighting to reduce biases from non-responders. Future analyses could further inform variables related to MenB vaccine uptake by including a stepwise regression to minimize the influence of HCP recommendation and to determine the remaining influential factors.
Conclusion
A high percentage of parents and guardians of vaccine-eligible adolescents in the United States are unaware of MenB vaccines, with awareness influenced by racial and socioeconomic factors. Vaccination decisions by parents and guardians are highly reliant on the provider’s recommendation. Nevertheless, recently published studies demonstrate substantial gaps in provider understanding of MenB vaccine ACIP recommendations and raise concerns. Thus, to improve awareness among parents and guardians, provider understanding of the ACIP shared clinical decision-making (Category B) recommendation must be supported to aid consistent implementation of this recommendation for MenB vaccines. Overall, our data underscore the need for efforts to improve knowledge and awareness of MenB vaccines among parents and guardians.
Acknowledgments
Editorial/medical writing support was provided by Anna Stern, PhD, Tricia Newell, PhD, and Kim Kridsada, PhD, of ICON plc (North Wales, PA).
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