key: cord-339638-yrxoj1hl
authors: Goldman, Ran D.; McGregor, Sophie; Marneni, Shashidhar R.; Katsuta, Tomohiro; Griffiths, Mark A.; Hall, Jeanine E.; Seiler, Michelle; Klein, Eileen J.; Cotanda, Cristina Parra; Gelernter, Renana; Hoeffe, Julia; Davis, Adrienne L.; Gualco, Gianluca; Mater, Ahmed; Manzano, Sergio; Thompson, Graham C.; Ahmed, Sara; Ali, Samina; Brown, Julie C.
title: Willingness to Vaccinate Children against Influenza after the COVID-19 Pandemic
date: 2020-08-07
journal: J Pediatr
DOI: 10.1016/j.jpeds.2020.08.005
sha: 
doc_id: 339638
cord_uid: yrxoj1hl

OBJECTIVES: To determine factors associated with parents who plan to vaccinate their children against influenza next year, especially those who did not vaccinate against influenza last year using a global survey. STUDY DESIGN: A survey of caregivers accompanying their children 1-19 years-old in 17 Pediatric Emergency Departments (ED) in six countries at the peak of the COVID-19 pandemic. Anonymous online survey included caregiver and child demographic information, vaccination history and future intentions, and concern about the child and caregiver having COVID-19 at the time of ED visit. RESULTS: Of 2422 surveys, 1314 (54.2%) caregivers stated they plan to vaccinate their child against influenza next year, an increase of 15.8% from the prior year. Of 1459 caregivers who did not vaccinate their children last year, 418 (28.6%) plan to do so next year. Factors predicting willingness to change and vaccinate included child’s up-to-date vaccination status (adjusted odds ratio (aOR)=2.03, 95% confidence interval (CI) 1.29 – 3.32 P = .003); caregivers’ influenza vaccine history (aOR=3.26, 95% CI 2.41 – 4.40 , p< 0.010), and level of concern their child had COVID-19 (aOR=1.09, 95% CI 1.01 – 1.17, p=0.022). CONCLUSIONS: Changes in risk perception due to COVID-19, and prior vaccination, may serve to influence decision-making among caregivers regarding influenza vaccination in the coming season. In order to promote influenza vaccination among children, public health programs can leverage this information.

To determine factors associated with parents who plan to vaccinate their children against influenza next year, especially those who did not vaccinate against influenza last year using a global survey.

Pediatric Emergency Departments (ED) in six countries at the peak of the COVID-19 pandemic.

Anonymous online survey included caregiver and child demographic information, vaccination history and future intentions, and concern about the child and caregiver having COVID-19 at the time of ED visit.

Of 2422 surveys, 1314 (54.2%) caregivers stated they plan to vaccinate their child against influenza next year, an increase of 15.8% from the prior year. Of 1459 caregivers who did not vaccinate their children last year, 418 (28.6%) plan to do so next year. Factors predicting willingness to change and vaccinate included child's up-to-date vaccination status (adjusted odds ratio (aOR)=2.03, 95% confidence interval (CI) 1.29 -3.32 P = .003); caregivers' influenza vaccine history (aOR=3.26, 95% CI 2.41 -4.40 , p< 0.010), and level of concern their child had COVID-19 (aOR=1.09, 95% CI 1.01 -1.17, p=0.022).

Changes in risk perception due to COVID-19, and prior vaccination, may serve to influence decision-making among caregivers regarding influenza vaccination in the coming season. In order to promote influenza vaccination among children, public health programs can leverage this information. year, including children (1) . Despite the wide availability of seasonal influenza vaccines and clear guidelines for who should be immunized, vaccine uptake remains low in most countries (2) .

With the unprecedented coronavirus SARS-CoV-2 illness, now called the coronavirus disease 2019 (COVID- 19) , which currently lacks a publicly available vaccine, public health authorities worldwide recommended numerous strategies to reduce spread, including reducing physical encounters and wearing masks. These measures have had variable success in curtailing the spread of the virus around the world. Vaccines are likely to provide the best protection from contracting the illness and there are currently more than 100 projects centered on the development of a vaccine and many have entered clinical trials (3).

There is a high likelihood that community transmission of COVID-19 will continue into the next influenza epidemic (4), complicating diagnoses and further increasing the burden on health care systems (5) . To mitigate these issues, vaccinating large parts of the population against influenza in late 2020 is a key goal of public health officials.

The objective of this timely survey study was to determine, during the COVID-19 peak pandemic, caregiver intentions towards influenza vaccination of their children, as well as themselves. In order to better understand how COVID-19 has influenced attitudes towards J o u r n a l P r e -p r o o f influenza vaccination, we specifically aimed to describe characteristics of caregivers who intend to immunize their children in 2020-2021 despite the child not receiving influenza immunization in the prior year. Understanding caregivers' attitudes can help public health officials plan targeted messaging to parents in order to promote influenza vaccination in the upcoming season.

This study is part of a larger COVID-19 Parental Attitude Study (COVIPAS) study, surveying caregivers of children presenting for emergency care, in the era of COVID-19. Caregivers who arrived to 17 pediatric emergency departments (ED) in the USA (Seattle, Tacoma, Los Angeles, Dallas, Atlanta), Canada (Vancouver, Toronto, Saskatoon, Edmonton, Calgary), Israel (Shamir), Japan (Tokyo), Spain (Barcelona), and Switzerland (Zurich, Bern, Geneva, Bellinzona) were asked to participate, using posters in waiting areas and patient rooms. For infectious control purposes, respondents used their own smartphones to complete the survey by logging into a secured online platform based on REDCap metadata-driven software (Vanderbilt University).

Several IRBs (in Switzerland and Spain) provided a waiver of consent such that responding to the survey was considered consent to participate.

Languages available to complete the study were English, French, German, Italian, Spanish, Hebrew, and Japanese. Although sites joined recruitment in a staggered fashion, surveys were obtained between March 27 and June 30, 2020. Only one caregiver per family was asked to complete the survey. Vaccination against influenza is available for children over 6 months in all countries that this survey took place.

The study-specific questionnaire was developed to include questions regarding demographic characteristics, information about the ED visit, and attitudes around COVID-19. Respondents were also asked about their child's vaccination history excluding influenza. Children were presented in this report, were evaluated a priori by 10 individuals representing the target group and 10 healthcare providers working in the ED environment. The final version of the survey is based on the feedback and test clarity generated from these 2 groups.

Basic descriptive statistics and frequencies were used to describe all variables. We compared survey data from caregivers who stated whether they plan to immunize or not immunize their children against influenza in the coming year. We then compared caregivers that did not immunize for influenza their children last year and compared those that said they do or do not plan to immunize their children for influenza next year. To determine which factors were significantly associated with caregiver decision-making to vaccinate next year despite not doing so last year, we used bivariate analyses: Mann-Whitney test was used for comparing nonnormal continuous variables, independent t-tests were used for comparing normallydistributed continuous variables, and Chi-squared or Fisher exact tests were used for categorical variables. Multivariable logistic regression was used to estimate the adjusted odds ratio of agreeing to immunize against influenza in the coming year using all the variables that showed a level of p<0.100 in the bivariate analyses. All analyses were conducted with R version 3.5.1. A p-value less than 0.05 in the multivariate analysis was considered statistically significant.

Results A total of 2785 surveys were completed online. Seven (0.3%) were excluded because the surveys were incomplete, seven (0.3%) were completed by the patient, 343 (12.3%) were for a patient less than one year of age, three (0.1%) for patients over 19 years old, and three (0.1%) with an unspecified patient age ( Figure 1 ). Some participants abstained from answering certain questions, accounting for a small number of unknown responses to each question. The final study sample included 2422 respondents: 2350 parents (97.0%), 67 other caregivers, and 5 respondents who did not specify their relationship to the child. Median age of caregivers was 40.0 (Standard Deviation (SD) = 7.6) years and median age of the child was 8.3 (SD = 4.6) years.

A total of 1314 (54.3%) respondents stated they intend to vaccinate their children against influenza in the coming 12 months, an increase of 15.9% compared with those that reported an influenza vaccine for their child in the past 12 months ( Figure 1 ). As many as 42/2422 (1.7%) respondents did not specify their intention to vaccinate their child and 1394/2393 (58.3%) respondents stated they planned to obtain the vaccine for themselves next influenza season, compared with 974 (40.6%) in the past year (Table I) . Table 1 provides demographic information including a comparison between caregivers who plan to vaccinate for influenza in the coming season and those who do not. The highest likelihood of planning to vaccinate the child next year was if the caregiver planned to vaccinate themselves in the upcoming year (1213/2422; 50.1% of children). Caregivers were more likely to suggest they will immunize next year if they had education beyond high school, if the child had a chronic illness or took medications regularly, if the child was up-to-date on their vaccines J o u r n a l P r e -p r o o f other than influenza according to their country-specific vaccination schedule, or if the child or caregiver received influenza vaccine the prior year.

Of 1459 caregivers who did not vaccinate their children against influenza in the last year, 418 (28.6%) indicated they plan to vaccinate next season, 1025 (70.3%) did not vaccinate last year and will not vaccinate this year, and 16 (1.1%) abstained from answering. Only 38/2422 (1.6%) vaccinated their child last year but do not plan to do so next year.

Most caregivers were not concerned about their child having COVID-19 when coming to the EDs in the six countries where this survey took place, and we found a significant correlation between level of concern and plan to vaccinate against influenza (p-value= 0.037; Figure 2 [available at www.jpeds.com]). Table 2 describes characteristics of caregivers who did not vaccinate the child last year, but plan to vaccinate their child against influenza in the coming year. Caregivers were more likely to change from non-vaccination last year to vaccination in the coming year when they had education more than high-school, they took the vaccine themselves or planning to get vaccinated themselves next year, had a child with an up-to-date vaccination schedule excluding influenza vaccines or were worried their child may have COVID-19 or influenza during the visit in the ED.

In the multivariate logistic regression analysis (Table 3) Behavioral changes related to COVID-19, including social distancing, hand washing, and wearing a mask, will impact influenza spread in the coming year (3) and it is unclear how relaxation of social distancing measures will influence the spread of influenza. Co-infection of COVID-19 and other respiratory pathogens, including influenza, occurred in a significant subset of COVID-19 patients (8, 9) and a case report from China describing co-infection with COVID-19 and Influenza A virus represent the difficulty in differentiating other causes of respiratory illness from COVID-19 (10) . The Director of the US Center for Disease Control predicted that "we're going to have a flu epidemic and coronavirus epidemic at the same time" and that the combination of the two will be "more difficult and potentially complicated" (4). Combined influenza and COVID-19 pandemics could result in considerable morbidity and mortality, stressing the health system J o u r n a l P r e -p r o o f (3, 7) and a global interest (as seen through Google trends) in pneumococcal and influenza vaccines during February-March, 2020 of the COVID-19 pandemic ( has been reported (11) .

In our global survey of primarily parents attending pediatric EDs, a significant shift in parents' plan to vaccinate against influenza in the season following COVID-19 pandemic was noted. A total of 54.3% survey respondents plan to vaccinate for influenza and 29.0% (418/1443) of caregivers that did not vaccinate last year report a change in plan to do so next year, adding to the protection of their children and reducing the chance of transmission to others. We report that caregivers who plan to vaccinate themselves are very likely to vaccinate their children and predictors for caregivers to plan to vaccinate after not doing so last year include children that have up-to-date vaccinations other than influenza, if the caregiver received influenza vaccine last year, and if they were worried their child had COVID-19.

Seasonal influenza epidemics result in tens of millions of cases, and we have recently reported that caregivers in 14 EDs are likely to provide their children with a COVID-19 vaccine if it becomes available (12) . Ensuring influenza vaccine acceptance and uptake in children may also serve public health in promoting COVID-19 vaccines, when those become available (7).

More than 70 independent barriers are associated with vaccine hesitancy and include psychological barriers (such as perceived risk, utility, and social benefit); contextual barriers (such as access to health care services); and lifestyle barriers (such as smoking, drinking, and physical activity) (13) . Trust in healthcare providers' advice and mainstream medicine, influence of social network and social norms, knowledge sources about vaccines, and general views toward health are key factors in parental vaccine decision-making (14) . Vaccine risk-perception J o u r n a l P r e -p r o o f of parents is often complicated by cognitive bias and personal experience (15) and in our cohort, caregivers were most likely to report plans to vaccinate their children against influenza next year if they plan to vaccinate themselves, meaning they trust the medical system and more specifically put faith in vaccines. Of interest, caregivers put more value and enhance the perceived risks associated with taking action, such as a child having a severe reaction to a vaccine, than the risk of an omitted action, like the chance of contracting a disease (16) . It is important for primary care providers to highlight the safety and efficacy of the flu vaccines to parents.

Past behavior is a strong factor in vaccinating children and those having been vaccinated in the past against seasonal influenza being more likely to be vaccinated against pandemic influenza (17) . In our study, the influenza vaccination status of a child last year was strongly associated with a caregiver's plan to vaccinate next year (p <0.001). Similarly, in a study from England, among 1001 parents with half their children vaccinated to influenza, vaccine uptake was associated with the child having previously vaccinated against influenza (18) .

Understanding factors that influence a change in influenza vaccine behaviour from year-to-year may guide public health efforts to increase uptake. Fogel and Hicks recently coined the term "flu-floppers," describing patients who received the influenza vaccine in some years but not others. They suggested that many appear to randomly alternate vaccination status from year to year (19) . In a year of COVID-19 pandemic it is likely that public health worries influence parents to plan on vaccinating their children and only 4% of children vaccinated last year are likely not to be vaccinated next year (38/930 families) compared w 28.6% (417/1460) "flipping" towards vaccinating. Those who stop yearly influenza vaccinations for their children most commonly cited a perceived lack of effectiveness of the vaccine (29%, n=41) (19) . Public Health officials will need to ensure clear messaging on the safety of influenza vaccines next year, especially in face of COVID-19, to influence parental decision making to convert into vaccinating children.

In a web-based survey of 500 parents from an online panel representative of the US population, the main drivers of parents' decision to vaccinate their child against influenza were prevention of influenza, reduction of influenza symptoms, and doctor recommendation; barriers to vaccination included the risk of adverse effects and the perceived low risk of influenza (20) .

Similarly, a review of 64 studies reported an association between vaccination uptake and perceived vaccine safety, general positive attitudes towards vaccination, positive vaccine recommendations, social influences and trust in the healthcare profession, and perceiving fewer practical difficulties with vaccination (21) . We similarly found that caregivers vaccinating their children according to the schedule, and thus likely have trust in the idea of vaccination, are likely to accept the influenza vaccination for their child next year.

Level of caregiver concern that the child had COVID-19 was associated with the change in action towards planning to vaccinate children against influenza. In a systematic review of 37 studies involving the 2009 H1N1 pandemic influenza outbreak, the degree of threat experienced and perceptions of vaccination as an effective coping strategy was associated with stronger intentions and higher uptake of vaccination and concern about the disease as well as believing oneself to be at risk to H1N1 influenza were important factors (17) . Fear of the child J o u r n a l P r e -p r o o f being sick with COVID-19 is a significant predictor of caregivers changing their mind to start vaccinating next year, which is supported by the fact that correlations were found between online searches for influenza vaccines and COVID-19, especially in "hotspots" of COVID-19, and increased interest in influenza vaccine compared with similar time periods in non-pandemic years (11) .

Although caregivers with higher than high school education are more likely to vaccinate their children against influenza (79% vs 71.4%, p<0.01), including those not vaccinating last year (78.5% vs 71.4%, p=0.005), when other factors were assessed in the multivariate analysis, higher education was associated with lower likelihood of families changing their mind to start vaccinating (OR 0.71, 95% CI 0.52-0.96), p=0.028). Level of parental education is associated with both high and low uptake of vaccines (22) , likely due to education serving as a surrogate marker for other factors impacting adherence.

Our study has a number of limitations. First, the population of caregivers responding to the survey does not represent all parents in the sites where the study was conducted, as we administered the survey in a pediatric ED setting and only a subset of families (likely <5% of visitors to 17 the pediatric EDs) filled out the survey. We also relied on caregiver possession of a smartphone/tablet/computer to complete the survey online, which may have limited a small percentage of caregivers from responding. Secondly, we relied on the accuracy of caregiver responses to the status of both influenza and non-influenza vaccinations, because no patient records were checked for confirmation. Finally, as in any survey, caregivers may share their J o u r n a l P r e -p r o o f opinions about vaccinations, but act differently once cities are back to a more normal activity, which highlights the importance of public health measures to encourage and ensure adequate vaccination uptake.

In summary, we report propensity of caregivers to vaccinate their children against influenza at a higher rate in the next influenza season, with 29% of those that did not vaccinate last year reporting a plan to do so next year. Caregivers who plan to vaccinate themselves, who received influenza vaccine last year, who were worried their child had COVID-19, and whose children J o u r n a l P r e -p r o o f 

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