ABSTRACT
Objective: Understanding whether interventions designed to improve antenatal vaccine uptake also change women's knowledge about vaccination is critical for improving vaccine coverage. This exploratory study evaluates the effectiveness of a multi-component influenza and tetanus, diphtheria, and acellular pertussis (Tdap) vaccine promotion package on improving women's knowledge, attitudes and beliefs toward antenatal vaccination. Study Design: In 2012/2013 a cluster-randomized trial was conducted to test the effectiveness of a vaccine promotion package on improving antenatal vaccine coverage. Participants included 325 unvaccinated pregnant women from 11 obstetric practices in Georgia. Eleven health beliefs measures were assessed at baseline and 2–3 months post-partum. Outcomes were differences in proportions of women citing favorable responses to each measure between study groups at follow-up. Results: Women enrolled in their third trimester had a higher probability of asking family members to vaccinate to protect the infant if they were in the intervention group versus the control group (36% vs. 22%; risk ratio [RR] = 1.65, 95% confidence interval [CI]: 1.21, 2.26). A similar association was not observed among women enrolled before their third trimester (39% vs. 44%; RR = 0.93, 95% CI: 0.50, 1.73). There were no other significant differences at follow-up between study groups. Conclusions: While exposure to the intervention package may have raised awareness that vaccinating close contacts can protect an infant, there is little evidence that the package changed women's attitudes and beliefs toward antenatal vaccination. Future research should ensure adequate exposure to the intervention and consider study design aspects including power to assess changes in secondary outcomes, discriminatory power of response options, and social desirability bias. This study is registered with clinicaltrials.gov, study ID NCT01761799.
Introduction
In the US, neither seasonal influenza nor pertussis vaccination rates during pregnancy consistently exceed 50%.Citation1-4 Considerable research has sought to understand why women do not get vaccinated despite antenatal vaccination recommendations by the Centers for Disease Control and Prevention (CDC).Citation5,6 Reasons women have cited for not receiving antenatal vaccines include inadequate knowledge of the need for vaccination, lack of a provider recommendation, low perceptions of susceptibility to the diseases, safety concerns, and logistical or financial barriers to obtaining a vaccine.Citation7-11 While some of these reasons arise from barriers beyond a pregnant woman's control, others emanate from her own understanding or perceptions of vaccination. With considerable amounts of evidence-based and non-evidence-based information on vaccination available to women, both legitimate and misguided concerns about vaccination have arisen.
In response to these reasons for not receiving antenatal vaccines, researchers are developing and evaluating interventions to increase vaccine uptake.Citation12,13 While improving vaccine coverage is the primary objective of these endeavors, a major upstream challenge to accomplishing this goal is changing women's knowledge, attitudes and beliefs about antenatal vaccines and the diseases against which they protect. This is especially true among women who may already be “vaccine hesitant,” or reluctant to make immediate immunization decisions. While there was no effect in vaccination endpoints on account of exposure to the multi-component intervention package developed for the MOMVAX study,Citation14 changes may have occurred in women's thoughts and attitudes toward vaccination. Using measures derived from the Health Beliefs Model and predictive of antenatal vaccination,Citation15 the aim of this study is to assess whether the intervention package evaluated in the MOMVAX study affected women's knowledge, attitudes and beliefs toward antenatal influenza and tetanus, diphtheria and acellular pertussis (Tdap) vaccination. Since the intervention package also included an introduction to the importance of childhood vaccination, we also explore whether the package had any effect on women's likelihood of vaccinating her infant.
Results
From December 2012–April 2013, 1,876 women were approached from the 11 participating practices and 1,436 (77%) were screened for eligibility.Citation16 Of the 1,436 women screened, 388 (27%) were eligible. Following declinations to enroll, incomplete enrollments and withdrawals, 325 (84%) of the eligible women were included in the study sample. Most participant characteristics were balanced across study groups; enrollment from a practice stocking Tdap vaccine was the only variable exhibiting a meaningful difference between intervention and control groups (40% vs. 60%; chi-square p–value = 0.0003).Citation14
Of the 325 women enrolled, 277 (85.2%) completed the follow-up questionnaire. Of these women, 271 (97.8%) completed the follow-up questionnaire by phone. Compared to the women who completed the follow-up questionnaire, women either refusing to take the questionnaire or lost to follow-up were younger (Mean age: 27.5 vs. 25.5, p = 0.02), less educated (Proportion having completed only high school or less: 42.9% vs. 70.8%, p < 0.0001) and more likely to be uninsured or on Medicaid (40.0% vs. 58.3%, p = 0.02). Of the 48 women who did not complete the follow-up questionnaire, equal proportions were from the intervention (n = 24) and control (n = 24) groups.
Between-group comparisons of outcome measures at baseline
At baseline, there were no significant differences in the proportions of women citing favorable responses for any of the 11 measures between study groups. Across both study groups, greater than 90% of women perceived pertussis as serious or very serious for an infant within the first 6 months of life. Compared to perceptions of pertussis severity during infancy, perceptions of influenza severity during infancy were only slightly lower (Intervention group: 93.2% perceiving pertussis as serious vs. 88.8% perceiving influenza as serious; Control group: 92.0% perceiving pertussis as serious vs. 86.4% perceiving influenza as serious). Women also perceived pertussis as more severe during pregnancy than influenza, yet only about one-quarter of women perceived antenatal influenza vaccination as safe (26.4% in intervention group and 24.1% in control group). Similarly, only 36.9% of women in the intervention group and 34.6% of women in the control group reported not being hesitant about getting recommended antenatal vaccinations.
Table 3. Questions on MOMVAX study questionnaires assessing knowledge, attitudes and beliefs about influenza and pertussis infection and associated vaccinations.
Table 1. Differences in proportions of women citing favorable responses to measures of knowledge, attitudes and beliefs about antenatal and childhood vaccination at baseline and follow-up, Emory MOMVAX Study.
In terms of willingness to receive vaccines during pregnancy, women across both groups were reticent with only 16.3% and 11.6% indicating a strong willingness to receive a Tdap vaccine in the intervention and control groups respectively, and 10.6% and 6.7% indicating a strong willingness to receive an influenza vaccine. In contrast, 80% across both study groups indicated a strong willingness to get their infant vaccinated with all recommended childhood vaccines.
Primary analyses – log binomial regression
No significant differences were observed for any of the 11 measures at follow-up. While not reaching statistical significance, the imbalance between study groups at baseline for the measures of willingness to receive antenatal influenza or Tdap vaccines may be meaningful; however, adjustment for the baseline values of these measures did not attenuate the effect estimates by more than 10% (adjusted risk ratio [aRR] for likelihood of influenza vaccine receipt: 1.14, 95% confidence interval [CI]: 0.81, 1.61; aRR for likelihood of Tdap vaccine receipt: 1.15, 95% CI: 0.86, 1.54). Similarly, adjustment for enrollment from practices stocking Tdap did not change the risk ratios for the pertussis, Tdap or general vaccination-related measures by more than 10% (data available upon request).
Secondary analyses – ordinal logistic regression
Results from analyzing each of the 11-point Likert scales using ordinal logistic regression also demonstrated no significant associations between study group and likelihood of increasingly favorable attitudes toward antenatal vaccination or childhood vaccination. As observed in the dichotomized results for the measures assessing likelihood of antenatal vaccine receipt, the unadjusted ORs comparing proportions of women citing a strong likelihood of receipt demonstrate slight imbalance favoring the intervention group at baseline; adjusting for the baseline values of these measures in each model again attenuated the effect estimates (antenatal influenza vaccination: unadjusted OR = 1.35, 95% CI: 0.76, 2.39 vs. baseline-adjusted OR = 1.27, 95% CI: 0.75, 2.15; antenatal Tdap vaccination: unadjusted OR = 1.17, 95% CI: 0.55, 2.49 vs. baseline-adjusted OR = 1.13, 95% CI: 1.13, 95% CI: 0.55, 2.33).
Table 2. Intervention effects (odds ratios and 95% confidence intervals) on knowledge, attitudes and beliefs about antenatal vaccination among pregnant women in Georgia, estimated by ordinal regression.
Interaction analyses
Of the 277 women completing the follow-up questionnaire, 250 (90.3%) and 205 (74.0%) had heard of pertussis and Tdap, respectively before participating in this study. Neither prior awareness of pertussis nor of the Tdap vaccination to protect against pertussis had significant impacts on associations between study group and any of the 6 measures related to pertussis, Tdap vaccination or general vaccination (data available upon request).
For analyses exploring interactions between study group and trimester of gestation at enrollment for each of the 11 measures at follow-up, only the interaction between study group and trimester at enrollment was significant for asking close family members to vaccinate. Women enrolled in their third trimester were significantly more likely to ask their family members to get vaccinated if they were in the intervention group vs. the control group (36% vs. 22%; RR = 1.65, 95% CI: 1.21, 2.26), whereas no between-group difference was observed among women enrolled before their third trimester (39% vs. 44%; RR = 0.93, 95% CI: 0.50, 1.73).
Discussion
Aside from evidence suggesting exposure to the intervention package may have persuaded more women in their third trimester to request their family members get vaccinated to protect the infant, results suggest that the MOMVAX study intervention package had no other significant effects on women's knowledge, attitudes and beliefs about influenza, pertussis and associated vaccinations during pregnancy. It also had no apparent impact on women's attitudes toward childhood vaccination. Observational findings, however, emphasize substantial hesitancy on behalf of these women regarding antenatal vaccination, and specifically of the safety of antenatal influenza vaccination.Citation16 While the vast majority of women seemed to understand the severity of influenza and pertussis to themselves and their infants, more than 60% were hesitant about antenatal vaccination and 70% either perceived the influenza vaccine as risky during pregnancy or were unsure of its safety. Congruent with other studies reporting similar uncertainties,Citation1,9,17,18 these results underscore the importance of finding why this disconnect persists and closing this knowledge gap especially as increasing numbers of studies are finding no increased risk for severe adverse events following antenatal vaccination.Citation19-22
There are multiple factors to consider when deciphering these primarily null findings. First, no findings presented here suggest the intervention package had a detrimental effect on knowledge, attitudes and beliefs toward vaccination. This is important in light of recent research by Nyhan, et al. that found provision of pro-vaccine messages can reduce intent to vaccinate, especially among individuals with unfavorable attitudes toward vaccination.Citation23 Despite the fact that participants in our study were likely more vaccine reticent than typical pregnant women (since women remaining unvaccinated by initiation of study recruitment in December likely had some reason for not wanting an influenza vaccine), we did not observe any increases in negative attitudes toward vaccination on account of exposure to our intervention package. Since our formative research on messaging about vaccination suggested that positive, or “gain-framed” messaging resonates better with pregnant women,Citation24 we incorporated messages primarily emphasizing the positive benefits of vaccinating as opposed to the risks or dangers of not vaccinating. This difference in message framing may have prevented the negative reaction that was observed after exposure to the loss-framed messages included in Nyhan's intervention.
Secondly, women may not have been exposed to the intervention messages and materials in repeated doses over an extended period of time. Research examining changes in knowledge, attitudes and beliefs about health-related behaviors suggest routine, extended exposure to an intervention is more effective than brief or single exposures.Citation25 If a woman was enrolled late in her pregnancy, she may have only been exposed to certain elements of the intervention package (e.g., the poster, brochure) a few times. Working under the assumption that women enrolled in their first trimester of gestation would have theoretically been exposed to the intervention materials more times, we attempted to assess the effect of repeated exposure on the impact of the intervention package. While we found no associations between presumably more exposures to the package and its effectiveness, this analysis could not take other factors into account like the impact of early refusal. If a woman declined vaccination at one visit early in her pregnancy, subsequent discussion of antenatal vaccination and exposure to intervention components like the educational brochure or iPad-tutorial may not have been reinitiated. Since the only significant interaction between trimester at enrollment and study group was among women in their third trimester for requesting family members to vaccinate, this finding alternatively suggests that targeted exposure at the appropriate time in gestation may be as impactful as repeated or continuous exposures throughout pregnancy.
Another factor to consider when deciphering these findings is the high proportion of women providing favorable responses to many of the measures, even at baseline. Based on the low antenatal vaccination rates against both influenza and pertussis among these women, the high proportions of women perceiving influenza and pertussis as serious seem counterintuitive. However, 2 possible explanations for these high proportions include: 1) poor discriminatory power of the questions' response options to uncover meaningful variability in vaccine-related attitudes, and 2) perceived pressure to provide socially desirable or responsible answers. While the Likert-scaled questions used in this study to correlate women's beliefs with specific psychosocial domains of the Health Beliefs Model were based on similar questions used to evaluate attitudes toward vaccination in other studies, those studies have primarily been about childhood vaccination, not maternal vaccination.Citation26 The possibility remains that these types of questions may need further refinement for their utility among expectant mothers. Moreover, in regards to perceived pressure to respond favorably on matters related to protecting their health or their child's health, women may not have wanted to answer honestly if providing unfavorable responses could make them appear negligent or ignorant about their health or their infant's health. This issue of social desirability bias may have impacted the follow-up questionnaire more than the baseline questionnaire since participants were responding directly to a study team member over the phone; compared to the analogous proportions at baseline, favorable response proportions were higher at follow-up across both study groups for 8 of the 11 measures.
This study has some important limitations. First, this was a relatively small pilot study including only 11 obstetric care practices. While we attempted to balance key predictors of our outcomes across study conditions by pair-matching practices on practice-level confounders prior to randomization, there still may have been variability in package implementation across intervention group practices. Moreover, since the study was designed to detect differences in antenatal vaccine receipt, we likely lacked the sample size necessary to detect significant changes in measures of knowledge, attitudes and beliefs. Given the high prevalence of favorable responses to many of the measures at baseline, studies with larger sample sizes would likely be necessary to detect meaningful improvements. To the extent this small study can serve as a pilot for future research, however, these results can serve as useful signals for larger studies.
Secondly, considerable numbers of intervention group women did not recall seeing some of the educational components of the intervention package. For example, of the 137 intervention group women who completed the follow-up questionnaire, only 60 (43.8%) recalled seeing the educational brochure and 10 (7.3%) recalled seeing the iPad-based educational app.Citation14 Since components like the brochure and the interactive iPad-based tutorial were highly educational, lack of exposure to these items likely diluted the package's overall effectiveness on improving knowledge or changing attitudes. Additionally, because the brochure and the iPad-app do not inherently involve provider-patient interaction, coupling the presentation of these items to patients with more explanation from the provider about their utility could increase their influence. Future studies evaluating interventions in a clinical setting should ensure exposure to all components of the intervention and leverage provider-patient interactions as much as possible. Researchers should also assess patient exposure to the intervention components in ways that mitigate recall bias, such as routinely collecting data from clinical personnel on their experiences administering intervention materials.
As the first known study to scientifically evaluate a multi-component antenatal vaccine promotion package in the obstetric setting, it serves as an important foundation for future research examining the ability of clinical interventions to change knowledge, attitudes and beliefs about antenatal vaccination. While the primary endpoint of promoting antenatal vaccination is actual vaccine receipt before delivery, understanding the degree to which any intervention also improves women's underlying knowledge of the importance of vaccination is useful. As evidenced by the considerable proportions of women expressing hesitancy about antenatal vaccination – despite perceptions of high disease severity and after exposure to an education-based intervention package addressing vaccine safety and efficacy - future research should explicitly explore reasons for this disconnect. Quantifying interventions' abilities to affect knowledge will help guide development of more robust, sustainable tools that can result in more informed vaccine-related decision making for women even beyond their current pregnancy.
Materials and methods
Data for these analyses were from the Emory MOMVAX Study. Detailed methods of the MOMVAX study design, recruitment strategy, intervention package components, and primary results have been described elsewhere.Citation14,16 In summary, the MOMVAX study was a cluster-randomized trial conducted among 11 obstetric practices in Georgia from 2012 – 2013. Through this pilot study, we sought to evaluate the effectiveness of a comprehensive multi-component vaccine promotion package on improving influenza and Tdap vaccine receipt among pregnant women. The primary study outcomes were differences in likelihood of antenatal influenza and Tdap vaccination between study groups; secondary outcomes (presented here) included changes in knowledge, attitudes and beliefs toward antenatal vaccination between study groups. This study was approved by the institutional review boards of Emory University and the Medical Center of Central Georgia, and signed informed consent was obtained from all eligible women interested in participating.
Prior to randomization and patient recruitment, practices were pair-matched on 3 factors predictive of receipt: provision of influenza vaccination in-house, percent patient population on Medicaid, and estimated influenza vaccine coverage among pregnant patients during the 2011/2012 influenza season. After randomization, intervention group practices were supplied the intervention package which consisted of practice-based components (promotional posters, educational brochures, lapel pins, and identification of an in-house vaccine champion), provider-based components (1-hour peer-to-peer educational training session and provider-to-patient talking points on influenza vaccination and Tdap vaccination), and a patient-level component (interactive iPad-based educational app). Maps to nearby pharmacies and health departments stocking influenza and/or Tdap vaccines were also provided to practices not offering one or both vaccines in-house as a resource to distribute to patients. Control group practices maintained their standards of care regarding antenatal vaccine promotion for the duration of follow-up.
Following practice randomization and provision of intervention package materials to intervention group practices, pregnant women were screened and enrolled from each practice.Citation14 To assess changes in women's knowledge, attitudes and beliefs toward antenatal vaccination, 11 questions addressing 3 domains (perceived susceptibility, perceived severity, and perceived safety) of the Health Beliefs Model (HBM) were included on the study's baseline questionnaire and repeated on the study's follow-up questionnaire. Developed in 1966, the HBM model is one of the most widely used psychological constructs to predict and explain individuals' health-related behaviors, including intention to vaccinate.Citation27-30 Additional questions assessing likelihood of receiving antenatal influenza and Tdap vaccines, likelihood of vaccinating their child, intention to ask family members and friends to get vaccinated, and degree of vaccine hesitancy were also included. The paper-based baseline questionnaire was administered upon enrollment following written informed consent; the follow-up questionnaire was administered over the phone or electronically 2 – 3 months postpartum.
Outcome measure analysis
For each of the 6 measures assessed on a 5-point Likert scale, responses were dichotomized into “favorable responses” and “unfavorable responses.” Cut-points for these dichotomizations were based on the meaning of the scales' categories; for measures assessing perceived susceptibility and self-efficacy, responses of “Strongly agree (1)” and “Agree (2)” were combined and compared to responses of “Neutral/No opinion/Don't know (3),” “Disagree (4),” and “Strongly disagree (5).” For measures of perceived severity, responses of “Serious (4)” and “Very serious (5)” were combined and compared to responses of “Neutral/Don't know (3),” “Somewhat serious (2),” and “Not serious at all (1).”
The 4 measures assessed on 11-point Likert scales were analyzed in 2 ways. First, for the primary analyses, these questions were also dichotomized. Cut-points for these dichotomizations were scale-based; for the cues-to-action measures assessing intention to vaccinate, responses with scores of 9 or 10 were combined to indicate “strong willingness” and compared against responses with scores of 0 – 8. Similarly, responses with scores of 0 and 1 on the self-efficacy measure assessing general hesitancy toward antenatal vaccination were combined into a “not hesitant” category and combined against responses with scores of 2 – 10.
In addition to dichotomization, the four 11-point measures were analyzed using ordinal logistic regression. This secondary analysis was conducted to determine whether exposure to the intervention package impacted knowledge, attitudes and beliefs across the spectrum of response options. For these analyses, 3 categories of responses were created for each measure, grouping scores in the following manner: scores of 0 and 1, scores of 2 – 8, and scores of 9 and 10.
For all measures, the primary outcome was the risk ratio (RR) comparing proportions of favorable responses between study groups at follow-up. Additional practice or participant level covariates were added if imbalance across study groups was apparent at baseline. They were retained in the model if they changed the measure of effect by more than 10%. For the secondary analyses using ordinal logistic regression, the outcome for a given measure was the odds ratio (OR) comparing the odds of citing increasingly favorable responses between study groups.
Exploration of interactions
Anticipating that certain factors like prior awareness of Tdap vaccination or trimester of gestation at enrollment could modify the effectiveness of the intervention package on knowledge, attitudes and beliefs, we explored interactions between study group and 1) reported knowledge of pertussis before engagement in this study, 2) awareness of Tdap vaccination before engagement in this study, and 3) trimester of gestation at enrollment for each measure. Due to the small sample size, each interaction was determined separately in the dichotomized models generated for the primary outcome analyses.
Statistical analyses
Risk ratios were calculated using log binomial regression employing generalized estimating equations (GEE) using PROC GENMOD in SAS version 9.3 (Cary, NC). For the interaction analyses, only interaction terms resulting in Wald test p-values < 0.05 were considered statistically significant. Ordinal logistic regression was also conducted using generalized estimating equations (GEE) in PROC GENMOD using a cumulative logit link function. The proportional odds assumption was tested using a score test followed by graphical verification of parallel slopes.Citation31 All models accounted for correlation among women recruited from the same practice by adjusting for practice of enrollment with a REPEATED statement and an independent working correlation structure.
Disclosure of potential conflicts of interest
Allison Chamberlain, Katherine Seib, Eli Rosenberg, Paula Frew, Marielysse Cortés, Ellen Whitney, Ruth Berkelman, Walter Orenstein and Saad Omer have no conflicts of interest to report. Kevin Ault has acted as a consultant on maternal immunization with the Centers for Disease Control and Prevention (CDC), the National Institute of Allergy and Infectious Diseases (NIAID), and the American College of Obstetricians and Gynecologists (ACOG). Dr. Ault serves on a data safety and monitoring committee with Novartis and is the site principal investigator for a clinical trial sponsored by Novavax.
Acknowledgments
We would like to thank the 11 obstetric practices who participated in this study as well as all the study participants. We also thank the Emory graduate research assistants who assisted with this study.
Funding
This study was supported by a grant from the Centers for Disease Control and Prevention (CDC), grant # 5P01TP000300, to the Emory Preparedness and Emergency Response Research Center, Emory University, Atlanta, GA. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the CDC. The CDC had no involvement in the study design; in the collection, analysis and interpretation of the data; in writing this manuscript, and in the decision to submit this manuscript for publication.
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