Vaccine Mandates and Influenza Vaccination During the Pandemic

Abstract

Objective:

To determine whether a state influenza vaccine mandate and elevated community COVID severity affected a child’s probability of receiving an influenza vaccine during the 2020–2021 influenza season, given the child’s prior vaccination history.

Methods:

Longitudinal cohort study using enrollment and claims data of 71,333 children aged 6 months to 18 years living in Massachusetts, New Hampshire, and Maine, from a regional insurer. Schoolchildren in Massachusetts were exposed to a new influenza vaccine mandate in the 2020–2021 season. Community COVID severity was measured using county-level total cumulative confirmed case counts between March 2020 and August 2020 and linked by zip codes. The primary outcome of interest was a claim for any influenza vaccine in the 2020–2021 season.

Results:

Children living in a state with a vaccine mandate during the 2020–2021 influenza season had a higher predicted probability of receiving an influenza vaccine than those living in states without a mandate (47.7%, CI 46.4%−49.0%, vs. 21.2%, CI 18.8%−23.6%, respectively for prior non-vaccinators, and 78.2%, CI 77.4%−79.0%, vs. 58.2%, CI 54.7%−61.7%, for prior vaccinators); the difference was 6.5 percentage points greater among prior non-vaccinators (CI 1.3%−11.7%). Previously vaccinated children had a lower predicted probability of receiving an influenza vaccine if they lived in a county with the highest COVID severity compared to a county with low COVID severity (72.1%, CI 70.5%−73.7%, vs. 77.3%, CI 74.7%−79.9%).

Conclusion:

Strategies to improve uptake of influenza vaccination may have differential impact based on prior vaccination status and should account for community factors.

Article Summary

Using claims data, we assess the impact of a state influenza vaccine mandate and elevated community COVID severity on pediatric influenza vaccination.

Introduction

Despite the clearly defined risks to children from influenza^1–4 and benefits of vaccination,^5–9 pediatric influenza vaccination rates are suboptimal. Though rates have improved in the last decade, pediatric influenza vaccination coverage in the United States has recently been between 50% to 75%, depending on age group and varying from 42% to 83% across states.¹⁰ Rates may be lower in countries that prioritize other childhood vaccinations.¹¹ Pediatric immunization status can also greatly affect a family’s contribution to community influenza-related morbidity and health care use, as young children are often responsible for the spread of influenza to household contacts.^12,13 Vaccinating school age children against influenza is the most effective strategy to minimize influenza incidence and hospitalization, especially in years with low vaccine efficacy.⁹ As a result, increasing pediatric influenza vaccination rates in the United States is a priority¹⁴ and the majority of state health departments stress the importance of vaccinating children against influenza.

Influenza vaccination became an even higher priority during the early COVID-19 pandemic when there was concern that the upcoming influenza season could further strain an already overburdened healthcare system.^15–17 Some states were proactive in addressing what was anticipated to be a severe influenza season and implemented influenza vaccination mandates for school children during the 2020–2021 flu season. In August of 2020, Massachusetts mandated that all children age 6 months and older, attending daycare through college, virtually or in-person, receive an influenza vaccine by December 31, 2020, allowing for medical and religious exemptions.¹⁸ Enforcement was determined at the local level. Maine and New Hampshire did not adopt mandates in 2020, though both state health departments recommended that all children 6 months and older be fully vaccinated against influenza.

In addition to the enactment of an influenza vaccine mandate, the COVID pandemic may have changed family decision making about influenza vaccination in other ways. High prevalence of COVID-19 and witnessing its severe implications may have heightened fear of viral infections and hospitalization¹⁹ and prompted families to get influenza vaccination for their previously unvaccinated children.²⁰ Alternatively, in settings of high COVID severity, families who previously had vaccinated their children may not have done so if they avoided in-person clinic visits due to fear of COVID exposure,²¹ were unable to schedule appointments due to limited availability of in-person office visits, or no longer had options for vaccination through schools due to remote schooling.

Understanding how COVID response and mandate policies affect changes in decision making about influenza vaccination, particularly for previously unvaccinated children, may aid in the development of future strategies to increase pediatric vaccination rates for influenza and other infectious diseases like COVID-19. While prior research has examined the effect of vaccination mandates on influenza vaccination rates in young children,^22,23 we lack within-child longitudinal studies of the impact of an influenza vaccination mandate given prior vaccination status, or the relationship between community COVID severity and influenza vaccination. The objective of this study was to use longitudinal child-level data to determine whether a state influenza vaccine mandate and elevated community COVID severity affected a child’s probability of receiving an influenza vaccine during the 2020–2021 pandemic influenza season and if there were differential impacts based on influenza vaccination in the prior year.

Methods

Design and setting:

We conducted a longitudinal cohort study using enrollment and claims data from a regional non-profit insurer in the Northeast with 13% to 30% of market share in the region.²⁴ State variation in influenza vaccine mandates provided a natural experiment to evaluate the effect of the mandate.

Study population:

We included children aged 6 months to 18 years living in Massachusetts, New Hampshire, and Maine, with continuous commercial insurance coverage from March 2019 through May 2021. Individuals under the age of 6 months by September 1, 2019 or 19 years or older by April 1, 2021 were excluded. Children with a claim documenting a history of an allergic reaction to any vaccine (ICD-10 Z88.7) were also excluded.

Measures:

The primary outcome of interest was receipt of any influenza vaccine in the 2020–2021 season, based on having one or more influenza vaccine CPT/HCPCS codes (see appendix) in claims from September 1, 2020 through March 1, 2021.

The main predictors in this study were living in a state that adopted an influenza vaccine mandate in 2020, county level COVID severity, and receipt of any influenza vaccine in the preceding influenza season (2019–2020). Children living in Massachusetts were exposed to a vaccine mandate in the 2020–2021 season, while those living in New Hampshire and Maine were never exposed to a mandate. Community COVID severity was measured using county-level total cumulative confirmed case counts between the start of the pandemic (March 2020) and August 2020 (start of the 2020–2021 flu season) compiled by Johns Hopkins University²⁵ and connected to member data through zip codes. Case counts per 100,000 in the child’s zip code were converted to categorical variables (less than 500, 500–999, 1000–1499, 1500–1999, >2000) based on prior studies.²⁶ Children with one or more influenza vaccine CPT/HCPCS codes in claims from September 1, 2019 through March 1, 2020 were categorized as receiving an influenza vaccine in the 2019–2020 season (i.e., “prior vaccination”). We truncated the 2019–2020 and 2020–2021 flu seasons at the beginning of March due to overlap of the 2019–2020 season with the start of the COVID-19 pandemic in March 2020.

Covariates included member sex, age, race and ethnicity, overall Social Vulnerability Index (SVI)²⁷ score for child’s census tract of residence, presence of a chronic condition in 2019 based on the Pediatric Medical Complexity Algorithm (PMCA),²⁸ child’s diagnosis of influenza in the 2019–2020 season, family member diagnosis of influenza in the 2019–2020 season, and family member diagnosis of COVID between January 1, 2020 and September 1, 2020. The social constructs of race and ethnicity were included as a potential confounder in our analyses as they have been shown to be associated with both influenza vaccination rates and community COVID severity.^29–31 To measure race and ethnicity, the health plan uses a hierarchical combination of 1) self-reported data, 2) data from hospitals and health systems, and 3) predicted race and ethnicity based on the RAND Bayesian Improved Surname Geocoding.³² Information on member census tract was used to link to the Center for Disease Control (CDC) SVI scores, representing a ranking of each census tract on 15 social factors meant to identify communities with decreased capacity to anticipate and recover from natural disasters and disease outbreaks.²⁷ SVI scores have been used as a measure of social risk and to characterize factors that may contribute to health disparities.^33,34 As in these studies, scores were categorized by quartile, labeled as low, low-moderate, moderate-high, and high. Race/ethnicity, SVI, and community COVID severity did not exhibit multicollinearity based on variance inflation factors <10. Prior diagnosis of influenza or COVID infection in children and family members on the same insurance plan were identified using ICD 10 codes (see appendix).

Analysis:

We used means and frequencies to describe the characteristics of children who did and did not receive influenza vaccination in the 2020–2021 season. We assessed whether living in a state with an influenza vaccine mandate or community COVID severity predicted influenza vaccine uptake in the 2020–2021 influenza season using an individual-level logistic regression model controlling for prior vaccination in the 2019–2020 season, child age, sex, race/ethnicity, presence of chronic conditions based on PMCA, overall SVI category, child influenza diagnosis in the 2019–2020 season, family member with an influenza diagnosis in the 2019–2020 season, and family member with a COVID diagnosis in 2020.

To assess whether living in a state with an influenza vaccine mandate or a county with elevated COVID severity had a differential impact for prior vaccinators vs. non-vaccinators (i.e., effect modification by prior vaccination status), we included two interaction terms in the model. The first was between living in a state with an influenza vaccine mandate and receipt of influenza vaccine in the 2019–2020 influenza season. The second was between county COVID severity category and receipt of influenza vaccine in the 2019–2020 influenza season. Using marginal effects methods,³⁵ we compared the difference in predicted probability of influenza vaccination in 2020–2021 between those living in mandate and non-mandate states for prior vaccinators and non-vaccinators respectively, and then calculated the difference between prior vaccinators and non-vaccinators. We did the same to compare predicted probabilities of vaccination between those living in the counties with the highest COVID severity (>2,000 cases per 100,000) and the lowest COVID severity (<500 cases per 100,000) by prior vaccination status, and then the differences between prior vaccinators and non-vaccinators. As prior studies have demonstrated a differential impact by race/ethnicity, we separately added another interaction term for mandate and White vs. non-White race.³⁶ All analyses accounted for clustering between children within the same family sharing the same insurance plan.

As influenza vaccines given at sites other than physicians’ offices may not be fully captured in claims data, a sensitivity analysis was conducted among children under age 3 years as of September 1, 2019. This age group is more likely to be vaccinated in a physician’s office than a school setting and most pharmacies will not vaccinate children under age 3.^37,38

Results

Of the 71,333 children in this study, the mean age was 9.7 years. The majority of the population was White and two-thirds of participants lived in Massachusetts (Table 1). More than half lived in a county where between 1500 and 2000 COVID cases per 100,000 had been identified through August 2020.

Table 1:

Characteristics of the study population

Total Population (N= 71,333)	Received influenza vaccine in the 2020–2021 season (n = 42,845)	Did not receive influenza vaccine in 2020–2021 season (n = 28,488)
Received influenza vaccine in 2019–2020 season	32,284 (75%)	10,276 (36%)
Age
1–4 years old	10,238 (24%)	3,540 (12%)
5–8 years old	10,441 (24%)	5,076 (18%)
9–12 years old	10,172 (24%)	6,997 (25%)
13–17 years old	11,994 (28%)	12,875 (45%)
Gender
Female	21,079 (49%)	13,797 (48%)
Male	21,766 (51%)	14,691 (52%)
Race and ethnicity a
White	38,155 (89%)	25,258 (89%)
Black	1,188 (3%)	1,112 (4%)
Hispanic	1,644 (4%)	1,156 (4%)
Asian/Pacific Islander	1,758 (4%)	869 (3%)
Alaskan Native/American Indian/Multiracial	100 (<1%)	93 (<1%)
State
MA	35,749 (83%)	18,812 (66%)
ME	2,917 (7%)	4,246 (15%)
NH	4,179 (10%)	5,430 (19%)
Presence of chronic conditions by PMCA b
None	23,227 (54%)	15,898 (57%)
Non-complex	12,102 (28%)	7,752 (28%)
Complex	7,516 (18%)	4,430 (16%)
SVI Overall c
Low	24,494 (57%)	15,374 (54%)
Low moderate	11,963 (28%)	7,650 (27%)
High moderate	4,264 (10%)	3,504 (12%)
High	2,124 (5%)	1,960 (7%)
County COVID (cases per 100,000)
<500	3,125 (7%)	4,818 (17%)
500–999	5,384 (13%)	5,550 (19%)
1000–1499	0	0
1500–1999	25,637 (60%)	13,167 (46%)
>2000	8,699 (20%)	4,953 (17%)
Child with COVID in 2020	172 (<1%)	144 (<1%)
Family member with COVID in 2020	1,342 (3%)	967 (3%)
Child with influenza in 2019–2020 season	3,735 (9%)	1,887 (7%)
Family member with influenza in 2019–2020 season	3,881 (9%)	2,012 (7%)

^aRace and ethnicity imputed from a modified RAND Bayesian Improved Surname Geocoding algorithm

^bPediatric Medical Complexity Algorithm

^cSocial Vulnerability Index overall score

Within the study population, 45% of individuals received influenza vaccines in both the 2019–2020 and 2020–2021 influenza seasons, 26% did not receive an influenza vaccine in either season, and 29% were vaccinated in one season but not the other (14.4% in the 2019 season only, 14.8% in the 2020 season only).

Overall, receipt of an influenza vaccine in the 2019–2020 season was a statistically significant predictor of vaccination in the 2020–2021 season (Table 2). Living in a state with a vaccine mandate was a significant predictor of vaccination in the 2020–2021 season whereas the county COVID severity was not. Young age (1–4 years), having a chronic medical condition, and having a family member who was diagnosed with influenza in the 2019–2020 season were also significant predictors of influenza vaccination in the 2020–2021 season. Black race was significantly associated with not receiving influenza vaccination in the 2020–2021 season.

Table 2:

Adjusted analyses of characteristics associated with receiving an influenza vaccine in the 2020–2021 season

Variable	OR	95% CI
Influenza vaccine in prior season (i.e., 2019–2020)	6.22	5.49–7.05
Age
1–4 years old	[Reference]
5–8 years old	0.82	0.77–0.86
9–12 years old	0.62	0.59–0.66
13–17 years old	0.43	0.41–0.46
Gender
Male	0.96	0.93–1.00
Race and Ethnicity a
White	[Reference]
Black	0.83	0.73–0.95
Hispanic	1.01	0.90–1.13
Asian/Pacific Islander	1.04	0.93–1.17
Alaskan Native/American Indian/Multiracial	0.77	0.54–1.08
Presence of chronic conditions by PMCA b
None	[Reference]
Non-complex	1.10	1.06–1.15
Complex	1.18	1.11–1.23
State mandate 2020	3.50	2.91–4.21
County COVID (cases per 100,000)
<500	[Reference]
500–999	0.96	0.84–1.10
1500–1999	0.93	0.76–1.15
>2000	0.85	0.68–1.05
SVI overall c
Low	[Reference]
Low moderate	1.03	0.98–1.08
High moderate	0.88	0.81–0.94
High	0.77	0.69–0.86
Family member with COVID in 2020	0.96	0.85–1.08
Child with influenza in 2019–2020 season	1.06	0.99–1.14
Family member with influenza in 2019–2020 season	1.11	01.02–1.20

Results presented were adjusted for all variables included in the table as well as interaction terms for influenza vaccination in prior season (2019–2020) and state mandate influenza vaccination in prior season (2019–2020) and county level COVID severity.

^aRace and ethnicity imputed from a modified RAND Bayesian Improved Surname Geocoding algorithm

^bPediatric Medical Complexity Algorithm

^cSocial Vulnerability Index overall score

The association between influenza vaccination in 2020–2021 and the main predictors of interest (vaccine mandate and COVID severity) varied based on whether the child had been vaccinated in the prior season (Table 3). While both prior vaccinators and non-vaccinators had significantly higher probability of vaccination in mandate vs. non-mandate states in the 2020–2021 season (47.7% vs. 21.2%, respectively for prior non-vaccinators, p<0.001, and 78.2% vs. 58.2% for prior vaccinators, p<0.001), the mandate was associated with a 6.5 percentage point higher increase in vaccination rate among prior non-vaccinators than prior vaccinators (p=0.014). There was no differential impact of mandate by race (interaction term p=0.682). Among prior vaccinators, high (vs. low) community COVID severity was associated with significantly lower rates of influenza vaccination in 2020–2021 (72.1% vs. 77.3%, p=0.005). The impact of county level COVID severity on vaccination rates for prior non-vaccinators was not statistically significant (39.4% vs. 43.2%, p=0.125 in high vs. low COVID severity communities, respectively). The differential impact of COVID severity on vaccination rates for prior non-vaccinators relative to prior vaccinators was not significant (interaction term p=0.6).

Table 3:

Predicted probability^a of the receipt of influenza vaccine in the 2020–2021 influenza season by prior vaccination status

	Prior non-vaccinatorsb n=10,297		Prior vaccinatorsc n=32,335		Difference for prior non-vaccinators relative to prior vaccinatorsd
	Pred. prob. (95% CI)	Difference	Pred. prob.(95% CI)	Difference
State influenza vaccine mandate					+6.5% (1.3–11.7%)
Yes	47.7% (46.4–49.0%)	+26.5% (23.2–29.9%)	78.2% (77.4–79.0%)	+20.0% (15.9–24.1%)
No	21.2% (18.8–23.6%)		58.2% (54.7–61.7%)
County COVID Severity					+1.5% (−4.4 – 7.4%)
Low (<500)	43.2% (39.3–47.1%)	−3.7% (−8.5 – 1.0%)	77.3% (74.8–79.9%)	−5.2% (−8.9 – 1.6%)
High (>2000)	39.4% (37.6–41.2%)		72.1% (70.5–73.7%)

^aAdjusted for member sex, age, race and ethnicity, overall SVI, PMCA, diagnosis of influenza in 2019–2020 season, family member diagnoses of influenza in the 2019–2020 season, and family member diagnosis of COVID between January 1, 2020 and September 1, 2020.

^bIndividuals who did not receive an influenza vaccine in 2019–2020 season

^cIndividuals who received an influenza vaccine in the 2019–2020 season

^dThis represents the percentage point difference within each row for prior non- vaccinators vs. prior vaccinators

The effect of living in a mandate state was similar in sensitivity analyses among children under 3 years of age, with significantly higher vaccination rates in a mandate state, more so among non-vaccinators (see Appendix). Among younger children, high county COVID severity was not associated with lower rates of influenza vaccination among prior vaccinators.

Discussion

This longitudinal child-level study found that, controlling for prior influenza vaccination, living in a state that adopted an influenza vaccine mandate was associated with higher probability of receiving an influenza vaccine during the 2020–2021 season compared to those living in states without a mandate. This impact was significantly greater among children who were not vaccinated against influenza in the prior season. Among previously vaccinated children, living in a county with high COVID severity was associated with lower influenza vaccination rates in 2020–2021 compared to living in low COVID severity counties.

An influenza vaccine mandate appears to be an effective but not sufficient strategy to achieve optimal vaccine coverage rates. Our findings are consistent with studies on influenza vaccine mandates in other states.^22,23 In New York City, cross-sectional vaccination rates for prekindergartners subject to a mandate increased by 6.3 percentage points relative to children not subject to the mandate. For Connecticut children aged 6–59 months, vaccination rates increased from 67.8% to 84% after an influenza vaccine mandate was implemented, a rate similar to ours among this age group. Among parents who have been willing to vaccinate, a vaccination mandate may be an additional stimulus to overcome barriers of convenience³⁹ to complete vaccination. For those not vaccinating previously, school-related mandates may be a strong lever. However, even in a state with a vaccine mandate, the predicted probability of influenza vaccination among prior non-vaccinators remained below 50%. Caregiver vaccine hesitancy, specifically as it relates to influenza vaccination,^40,41 may limit the effect of vaccine mandates and other approaches may be needed. Due to an ultimately mild influenza season, the Massachusetts influenza vaccination mandate was dropped in January of 2021.⁴² However, as the original mandate deadline for vaccination was December 31, 2020,¹⁸ the bulk of the response should have occurred prior to it being rescinded and the low severity of the 2020–2021 influenza season is unlikely to have affected vaccination rates.⁴³

Overall, we found that prior vaccinators had lower rates of subsequent vaccination in communities with high vs. low COVID severity. Parents in communities with high levels of COVID may have been wary of making an additional trip to a clinic or pharmacy for vaccination or may have faced limited availability of in-person visits. In the setting of more severe disease outbreaks, parents may need targeted messaging and strategies to encourage safe and convenient venues to access influenza vaccines.

We found no difference by community COVID severity in the probability of vaccination in the 2020–2021 season for children under the age of 3 years in sensitivity analysis, regardless of prior vaccination status. In contrast to the dampening effect of high community COVID severity on vaccination rates for prior vaccinators that we saw among the full population, a lack of differential effect of COVID severity for younger children may be attributable to greater influenza vaccination access for younger children compared to older children.^44,45 During the first year of the pandemic when access to in-person care was limited, infants and young children were prioritized over older children for in-person visits at many clinics given the need for routine vaccination and developmental surveillance.⁴⁶

It is well established that COVID disproportionately affected minority and lower socioeconomic status communities.^30,31 Our findings highlight another way in which COVID may have worsened preexisting health disparities through lower rates of influenza vaccination access. We found that Black children and those living in communities with higher overall SVI scores were less likely to be vaccinated against influenza. These groups were also more likely to live in counties with elevated COVID severity,⁴⁷ where we found influenza vaccination rates among prior vaccinators to be significantly lower than in low COVID severity areas. Unlike prior studies,³⁶ this study found no differential impact of a mandate by race. Additional efforts should be made to improve messaging and increase accessibility of influenza vaccines within these communities to address the disproportionate morbidity and mortality caused by seasonal influenza.

Future studies are needed to assess the downstream effects of the COVID pandemic on family decisions about influenza vaccination. Preliminary studies suggest that concerns about the COVID vaccine may have already negatively influenced influenza vaccination rates nationally.⁴⁸ While mandates may encourage caregivers receptive to vaccines to vaccinate against influenza, they likely will not work as well among families with staunch anti-vaccine views.⁴⁹ Further work is needed to enhance communication and policy strategies incentivizing potentially hesitant caregivers to vaccinate children against influenza.

There were several limitations to this study. Results from a population with continuous private insurance in the Northeast may not generalize to publicly or intermittently-insured children in the rest of the country. To account for population differences between study states, we controlled for numerous sociodemographic characteristics, and used a continuously enrolled population to enable a within-child pre-post design. Only about 30% of enrollees were excluded for not having continuous coverage. Response to the mandate may have depended on whether children attended public or private school or attended remotely, as done by 67% of students nationally in the fall of 2020,⁵⁰ but school data were not available for our study. Children who were vaccinated at sites that do not bill insurance (i.e., schools or health departments) may have been miscategorized as not having received a vaccination. However, rates of vaccination in these alternate sites are low, particularly among younger children, and claims data have been used in other studies to measure influenza vaccination, including from pharmacies.^38,51

Conclusions

In this longitudinal cohort study, children living in a state with a vaccine mandate during the 2020–2021 influenza season had a higher predicted probability of receiving an influenza vaccine than those living in states without a mandate. The impact of the mandate was greater among prior non-vaccinators. Previously vaccinated children had a lower predicted probability of receiving an influenza vaccine if they lived in a county with high COVID severity. Strategies to improve uptake of influenza vaccination may have differential impacts based on prior vaccination acceptance and must account for community factors such as the COVID-19 pandemic.

What’s Known on This Subject

Influenza vaccination uptake among children is suboptimal despite the clearly defined benefits of annual vaccination. The COVID-19 pandemic may have changed vaccination behaviors due to concerns about COVID exposure and new mandates for influenza vaccination for children.

What This Study Adds

We assessed influenza vaccination uptake using insurance claims data. We found that during the pandemic, an influenza vaccination mandate for children in school was associated with higher vaccination rates, particularly for prior non-vaccinators.