Mandatory Vaccination in Europe · Vaccination in Europe. Pediatrics. 2020;145(2):e20190620...

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Mandatory Vaccination in Europe Olivia M. Vaz, MPH, a Mallory K. Ellingson, MPH, b Paul Weiss, MS, c Samuel M. Jenness, PhD, a Azucena Bardají, MD, PhD, d Robert A. Bednarczyk, PhD, a,b,e,f Saad B. Omer, MPH, MBBS, PhD a,b,g,e abstract BACKGROUND: Mandatory vaccination has been effective in maintaining high vaccination coverage in countries such as the United States. However, there are no peer-reviewed analyses of the association between mandates and both coverage and subsequent incidence of vaccine- preventable disease in Europe. METHODS: Using data from the European Centre for Disease Prevention and Control and the World Health Organization, we evaluated the relationship between country-level mandatory vaccination policies and (1) measles and pertussis vaccine coverage and (2) the annual incidence of these diseases in 29 European countries. Multivariate negative binomial and linear regression models were used to quantify these associations. RESULTS: Mandatory vaccination was associated with a 3.71 (95% condence interval [CI]: 1.68 to 5.74) percentage point higher prevalence of measles vaccination and a 2.14 (95% CI: 0.13 to 4.15) percentage point higher prevalence of pertussis vaccination when compared with countries that did not have mandatory vaccination. Mandatory vaccination was only associated with decreased measles incidence for countries without nonmedical exemptions (adjusted incidence rate ratio = 0.14; 95% CI: 0.05 to 0.36). We did not nd a signicant association between mandatory vaccination and pertussis incidence. CONCLUSIONS: Mandatory vaccination and the magnitude of nes were associated with higher vaccination coverage. Moreover, mandatory vaccination was associated with lower measles incidence for countries with mandatory vaccination without nonmedical exemptions. These ndings can inform legislative policies aimed at increasing vaccination coverage. WHATS KNOWN ON THIS SUBJECT: Outbreaks in Europe are in part due to decreased vaccine coverage. Vaccine mandates have been used successfully in countries such as the United States to establish and maintain high vaccine coverage; however, the impact of such laws in Europe is unknown. WHAT THIS STUDY ADDS: In evaluating current vaccine mandates in Europe, we found that mandatory vaccination and the magnitude of nes were associated with higher vaccination coverage in European countries. To cite: Vaz OM, Ellingson MK, Weiss P, et al. Mandatory Vaccination in Europe. Pediatrics. 2020;145(2):e20190620 a Departments of Epidemiology and c Biostatistics and Bioinformatics, b Hubert Department of Global Health, Rollins School of Public Health, g Department of Pediatrics, School of Medicine, e Emory Vaccine Center, and f Winship Cancer Institute, Emory University, Atlanta, Georgia; and d Hospital Clínic, Barcelona Institute for Global Health, Universitat de Barcelona, Barcelona, Spain Ms Vaz conducted the literature search, created the gures, conducted data collection, analysis, and interpretation and was primarily responsible for the writing of the manuscript; Ms Ellingson assisted in the literature search, data analysis and interpretation, and writing and editing of the manuscript; Prof Weiss and Dr Jenness contributed to data analysis and interpretation and the editing of the manuscript; Dr Bardají assisted in data interpretation and the editing of the nal manuscript; Dr Bednarczyk contributed to the data analysis and interpretation and the writing and editing of the manuscript; Dr Omer conceptualized and designed the study and contributed to data analysis and interpretation, writing, and editing; and all authors approved the nal manuscript as submitted and agree to be accountable for all aspects of the work. Ms Vazs current afliation is Department of Epidemiology, Gillings School of Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC. Ms Ellingsons current afliation is Department of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, CT. Dr Omers current afliations are Department of Epidemiology of Microbial Diseases, School of Public Health; Department of Infectious Disease, School of Medicine; and Yale Institute of Global Health, Yale University, New Haven, CT. PEDIATRICS Volume 145, number 2, February 2020:e20190620 ARTICLE by guest on March 19, 2020 www.aappublications.org/news Downloaded from

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Page 1: Mandatory Vaccination in Europe · Vaccination in Europe. Pediatrics. 2020;145(2):e20190620 aDepartments of Epidemiology and cBiostatistics and Bioinformatics, bHubert Department

Mandatory Vaccination in EuropeOlivia M. Vaz, MPH,a Mallory K. Ellingson, MPH,b Paul Weiss, MS,c Samuel M. Jenness, PhD,a Azucena Bardají, MD, PhD,d

Robert A. Bednarczyk, PhD,a,b,e,f Saad B. Omer, MPH, MBBS, PhDa,b,g,e

abstractBACKGROUND:Mandatory vaccination has been effective in maintaining high vaccination coveragein countries such as the United States. However, there are no peer-reviewed analyses of theassociation between mandates and both coverage and subsequent incidence of vaccine-preventable disease in Europe.

METHODS: Using data from the European Centre for Disease Prevention and Control and theWorld Health Organization, we evaluated the relationship between country-level mandatoryvaccination policies and (1) measles and pertussis vaccine coverage and (2) the annualincidence of these diseases in 29 European countries. Multivariate negative binomial andlinear regression models were used to quantify these associations.

RESULTS:Mandatory vaccination was associated with a 3.71 (95% confidence interval [CI]: 1.68to 5.74) percentage point higher prevalence of measles vaccination and a 2.14 (95% CI: 0.13to 4.15) percentage point higher prevalence of pertussis vaccination when compared withcountries that did not have mandatory vaccination. Mandatory vaccination was onlyassociated with decreased measles incidence for countries without nonmedical exemptions(adjusted incidence rate ratio = 0.14; 95% CI: 0.05 to 0.36). We did not find a significantassociation between mandatory vaccination and pertussis incidence.

CONCLUSIONS: Mandatory vaccination and the magnitude of fines were associated with highervaccination coverage. Moreover, mandatory vaccination was associated with lower measlesincidence for countries with mandatory vaccination without nonmedical exemptions. Thesefindings can inform legislative policies aimed at increasing vaccination coverage.

WHAT’S KNOWN ON THIS SUBJECT: Outbreaks inEurope are in part due to decreased vaccine coverage.Vaccine mandates have been used successfully incountries such as the United States to establish andmaintain high vaccine coverage; however, the impactof such laws in Europe is unknown.

WHAT THIS STUDY ADDS: In evaluating current vaccinemandates in Europe, we found that mandatoryvaccination and the magnitude of fines wereassociated with higher vaccination coverage inEuropean countries.

To cite: Vaz OM, Ellingson MK, Weiss P, et al. MandatoryVaccination in Europe. Pediatrics. 2020;145(2):e20190620

aDepartments of Epidemiology and cBiostatistics and Bioinformatics, bHubert Department of Global Health,Rollins School of Public Health, gDepartment of Pediatrics, School of Medicine, eEmory Vaccine Center, andfWinship Cancer Institute, Emory University, Atlanta, Georgia; and dHospital Clínic, Barcelona Institute for GlobalHealth, Universitat de Barcelona, Barcelona, Spain

Ms Vaz conducted the literature search, created the figures, conducted data collection, analysis, andinterpretation and was primarily responsible for the writing of the manuscript; Ms Ellingsonassisted in the literature search, data analysis and interpretation, and writing and editing of themanuscript; Prof Weiss and Dr Jenness contributed to data analysis and interpretation and theediting of the manuscript; Dr Bardají assisted in data interpretation and the editing of the finalmanuscript; Dr Bednarczyk contributed to the data analysis and interpretation and the writing andediting of the manuscript; Dr Omer conceptualized and designed the study and contributed to dataanalysis and interpretation, writing, and editing; and all authors approved the final manuscript assubmitted and agree to be accountable for all aspects of the work.

Ms Vaz’s current affiliation is Department of Epidemiology, Gillings School of Public Health,University of North Carolina at Chapel Hill, Chapel Hill, NC.

Ms Ellingson’s current affiliation is Department of Epidemiology of Microbial Diseases, School ofPublic Health, Yale University, New Haven, CT.

Dr Omer’s current affiliations are Department of Epidemiology of Microbial Diseases, School ofPublic Health; Department of Infectious Disease, School of Medicine; and Yale Institute of GlobalHealth, Yale University, New Haven, CT.

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Vaccination is 1 of the most usefultools for preventing infectious diseaseand reducing morbidity andmortality.1 Availability of vaccines hashad a substantial impact on rates ofvaccine-preventable diseases acrossthe world.1 However, achieving highvaccination rates is challenged byless-than-optimal acceptance. Incountries such as the United Statesand Australia, vaccine mandates, suchas those requiring vaccination forentry into school, have been used toincrease and sustain vaccinationrates.2,3

In Europe, mandatory vaccinationpolicies are heterogeneous acrosscountries. Countries vary not only inthe presence or absence of a mandatebut also in the implementation andenforcement of the mandates as wellas in the consequences faced byindividuals who fail to comply withtheir country’s policy.4,5 Multiplecountries in Europe, including Franceand Italy, have recently facedoutbreaks of vaccine-preventablediseases, such as measles, and inresponse have changed their policies,whereas other countries areconsidering introducingimmunization mandates.6–8 Theeffectiveness of these legal andadministrative policies and theirpossible consequences has not beenassessed in a peer-reviewed analysis.In the face of these changes, anevaluation of existing vaccinemandates in Europe could informpolicy choices in Europe and beyond.

In this study, we aimed to determineif (1) the vaccination rates forpertussis-antigen vaccines andmeasles, mumps, and rubella vaccineswere associated with mandatoryvaccination and the availability ofnonmedical exemptions to thesemandates; (2) the incidence ofpertussis and measles was associatedwith mandatory vaccination and theavailability of nonmedicalexemptions; and (3) if the magnitudeof the financial penalties faced bynoncompliant parents was associated

with the rates of vaccination againstpertussis and measles.

METHODS

Data Collection Methods

Analyses were conducted usingpublicly available data on vaccinemandate policies and vaccine rates bythe first author. We focused ouranalysis on the 29 countries that wereanalyzed in the Vaccine EuropeanNew Integrated Collaboration Effort(VENICE).9 This included the memberstates of the European Union (at thetime of the study) as well as Icelandand Norway.9

Vaccination Rates

Vaccination rates were collected for2006 to 2015 for measles and 2006to 2016 for pertussis for thesecountries from the Global HealthObservatory, a World HealthOrganization (WHO) collection ofhealth-related statistics for its 194member states.10 These were themost recent available data at the timethe analysis was conducted. Weelected to focus on measles andpertussis for multiple reasons. First,recent measles outbreaks have been 1of the main drivers of policy changesin Europe. Both measles and pertussishave relatively high infectivity,meaning that even small changes invaccine coverage can impact diseaseincidence. Lastly, both are diseasesfor which there is good surveillanceof vaccine coverage and diseaseincidence. This country-specificinformation was compiled fromreports by the health ministries ordepartments of WHO member statesand was reported by the WHO ona global level. Immunization rates arecollected as 1 of the Core HealthIndicators used by the WHO.Although immunization rates are self-reported by the individual countries,the WHO does provide guidance andtraining to health systems on whatand how to report.10

Measles and Pertussis Case Counts

Both measles and pertussis casecounts were acquired from the WHO’scentralized information system forinfectious diseases. This systemcollects, analyzes, and presents dataon infectious diseases in the WHOEuropean Region, compiled fromreports submitted by memberstates.11 The population estimatesused were from Eurostat, thestatistical office of the EuropeanUnion. These population statistics areprovided annually by member statesfrom the country’s statisticalauthorities and are consolidated byEurostat, which also ensures that themethodology is harmonized acrosscountries to ensure comparabledata.12

Vaccine Mandates

Information on whether vaccinationwas mandatory was obtained froma combination of sources. First, weused the VENICE 2010 survey, whichindicated the 2010 status ofvaccination requirements. TheVENICE 2010 project surveyedexperts working within immunizationprograms in participating countries.These experts were asked about therequirements for their country andwere given a definition of“mandatory” and “recommended” toavoid misinterpretation.9 We thenevaluated any changes in country-level vaccine mandate policiesbetween 2010 and 2015 using theVaccine Scheduler, a tool maintainedby the European Centre for DiseasePrevention and Control that presentsthe vaccine schedules of all countriesin the European Union, includinginformation on recommended versusmandated vaccinations.13

For those countries with vaccinemandates, we obtained additionalinformation on the mandates and anyavailable exemptions by conductinga review of country-specific vaccinepolicy on health ministry Websites.We collected information on thepresence of nonmedical exemptions

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and the potential penalties faced fornoncompliance, including the amountof any financial penalties, from eachcountry’s health ministry Web sitesand vaccine policy.9,13–20 For accuratecomparison among countries, wetransformed these financial penaltiesusing Purchasing Power Parities(PPPs) on the actual individualconsumption scale, calculated andprovided by Eurostat.21 PPPs area measure of how the units ofnational currency of a countrycompare in value to a standardizedunit of currency and market, whichEurostat set as 1 euro in the EU.These PPPs were calculated andaggregated by using a set of annualprices for certain products and thebreakdown of expenditure on grossdomestic product (GDP) provided byparticipating countries.21

Data Analysis

All analyses were conducted by usingSAS version 9.4 (SAS Institute, Inc,Cary, NC) and R version 3.3.3. Weused multivariate models to conducta longitudinal analysis of theassociation between different vaccinepolicies, vaccination rates, anddisease incidence over time in thecountries of interest.

Vaccination Rates and Associations WithVaccine Policy

A linear mixed-effects model was fitto estimate the association betweenthe vaccination rates (outcome) andmandatory vaccination policies(primary exposure) in our countriesof interest. We used anautoregressive correlation structureto account for within-countrycorrelation over time. Usingpropensity score methods forcovariate adjustment,22,23 weadjusted for the following covariates:percentage of the population living inurban areas, proportion of adultsaged 24 to 65 with at least a lower-secondary education, GINI coefficient,universal health care service index,percentage of the population,14 years of age, and median age of

the country’s residents. Covariateselection was informed by theexisting literature on vaccine uptakeand disease incidence as well asprevious evaluations of therelationship between vaccine policyand disease incidence.24–28 The GINIcoefficient represents the wealthdistribution of the citizens ofa country and is a commonly usedmeasure of inequality.29 Theuniversal health care index combines16 health service coverage indicatorsfor reproductive health, maternal andchild health, infectious diseases,noncommunicable diseases, andservice capacity and access intoa single metric.30 The resultingregression coefficients comparing thepresence of a mandatory vaccinationpolicy, a nonmedical vaccinationexemption, and a financial penaltywere interpreted as the percentagepoint difference associated with eachof these binary conditions.

Disease Incidence and AssociationsWith Policy

We analyzed disease incidence forboth measles and pertussis and theassociation between diseaseincidence and vaccine mandate policyfor the years 2006 to 2015 (formeasles) and 2006 to 2016 (forpertussis) for the countries ofinterest. To estimate the rates ofpertussis and measles infections andassociations with country mandates,a negative binomial model was fitwith the assumption that the numberof cases for each year was distributedas a Poisson random variable withmean m and an offset for thepopulation of the country. A negativebinomial model was used to accountfor overdispersion. We used anautoregressive correlation structureto account for within-countrycorrelation of the incidence of thedisease over time. We usedpropensity score methods forcovariate adjustment to account fordemographic variables that have beenpreviously shown to be associatedwith vaccine uptake.22,23 Incidence

rate ratios were derived from themodels as a measure of associationbetween incidence and thevaccination requirements of thecountry. Incidence rate ratios areinterpreted as a relative difference inthe incidence of the diseaseassociated with the presence ofvaccine mandates in a country.

RESULTS

Of the 29 European countriesincluded in this study, 7 mandatedvaccination (Fig 1 A and B).14–20

Among these countries, only theCzech Republic and Latvia offeredprocesses to acquire a nonmedicalvaccination exemption.14,16 Theseprocesses required parents to eitherreceive information (either online orthrough their health care provider)about vaccination or providea written refusal of the vaccination aswell as discuss the decision with theirchild’s health care provider.14,16 In 6of the 7 countries that had mandatoryvaccination policies in place, ifparents failed to meet therequirements of their country’sregulations and requirements, theyfaced a financial penalty. Of these 7countries, Latvia was the only onethat did not have a financial penaltyfor refusing to vaccinate withoutobtaining a nonmedical exemption.16

In Latvia, health care providers arecompelled to collect the signature ofindividuals who refuse vaccinationand are required to inform theindividual of the health consequencesof failing to vaccinate.31

When adjusted to the euro, thecountry with the highest possiblefinancial penalty was Hungary, whereparents could face a financial penaltyof up to 500 000 forints (∼€1600 or∼$1800) in 2016 if they failed tofollow vaccination requirements.17

The country with the lowest financialpenalty was Bulgaria, where parentscould be fined a maximum of 300 lev(∼€150 or ∼$170) in 2016 if they

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failed to comply with vaccinationrequirements (Fig 1A).17

Vaccination Rates and AssociationsWith Vaccine Policy

Mandatory vaccination wasassociated with a difference of 3.71percentage points for measlesvaccination and 2.14 percentagepoints for pertussis vaccination whencompared with countries that did nothave mandatory vaccination(measles: 3.71 [95% confidenceinterval (CI): 1.68 to 5.74]; pertussis:2.14 [95% CI: 0.13 to 4.15]; Table 1,Fig 2). Mandatory vaccinationwithout exemption was associatedwith a difference of 3.80 percentagepoints for measles and 2.07percentage points for pertussisvaccination (measles: 3.80 [95% CI:1.23 to 6.37]; pertussis: 2.07 [95% CI:21.74 to 5.89]).

Among countries that impose a finefor noncompliance by parents, every€500 increase in the maximumpossible penalty was associated withan increase of 0.8 points for measlesvaccination coverage (95% CI: 0.50 to1.15; P #.0001) and an increase of1.1 percentage points for pertussisvaccination coverage (95% CI: 0.95 to1.30; P #.0001).

Disease Incidence and AssociationsWith Policy

For measles, Bulgaria had the highestincidence at 32.9 cases per 100 000individuals per year (Fig 1B).Countries with mandatoryvaccination experienced lowerincidence rates of measles comparedwith countries without mandatoryvaccination, although the 95% CIcrossed the null (adjusted incidencerate ratio [aIRR] = 0.38; 95% CI: 0.13to 1.16). Countries that hadmandatory vaccination without thepossibility of nonmedical exemptionsdid have 86% lower disease incidencethan countries without mandatoryvaccination (aIRR = 0.14; 95% CI:0.05 to 0.36). The presence ofa financial penalty was associated

FIGURE 1A, Annual reported incidence per 100 000. The mean annual reported pertussis incidence by country(2006–2016) among the entire population is shown. B, Annual reported incidence per 100 000. Themean annual reported measles incidence by country (2006–2016) among the entire population isshown. a Slovakia penalizes per parent, so if it is a 2-parent household, the total financial penaltywould be €662. €, euro; Ft, forint; лв, lev; K�c, koruna; zł, złoty.

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with lower incidence rates of measles(aIRR = 0.14; 95% CI: 0.05 to 0.39).

Norway had the highest incidence ofpertussis at 73.6 cases per 100 000individuals per year (Fig 1A).Pertussis incidence in countries thathad mandatory vaccination was 70%lower than in countries that did nothave mandatory vaccination, althoughthe 95% CI crossed the null (aIRR =0.30; 95% CI: 0.07 to 1.30). Countrieswith mandatory vaccinations withoutthe possibility of nonmedicalexemption had incidence rates similarto countries without mandatoryvaccination policies (aIRR = 1.04;95% CI: 0.18 to 6.32) (Table 2). Thepresence of a financial penalty wasassociated with lower incidence ratesof pertussis (aIRR = 0.42; 95% CI:0.18 to 0.98).

DISCUSSION

Mandatory vaccination policies inEurope were associated with higherrates of vaccination for both measlesand pertussis. Although mandatoryvaccination overall was notassociated with a lower incidence ofeither measles or pertussis, whenthere was no option of a nonmedicalvaccination exemption, the incidenceof measles was significantly lower.Moreover, the presence of a financialpenalty for nonvaccination wasassociated with a lower incidence ofboth pertussis and measles. Countrieswith a fine for noncomplianceexperienced incidence rates of less

than half that of countries withoutmandatory vaccination for bothmeasles and pertussis. Among thesecountries with a financial penalty,a €500 increase in the maximumpenalty parents could face for failingto comply with their country’svaccination regulations wasassociated with a 1.1% highervaccination rate for pertussis anda 0.8% higher vaccination rate formeasles.

Financial penalties could be aneffective measure in a comprehensivemandatory vaccination program,although they need to accompanyother measures, including a stablevaccine supply and vaccine education,to reach those who refuse tovaccinate. Financial penalties havebeen used in non-European countries,with some success. For example, inAustralia, 6 months after theimplementation of “No Jab No Pay” (ano vaccination, no family tax benefitsprogram) in the beginning of 2016,“fully immunized coverage” ofchildren at 1 year of age and 5 yearsof age had both reached recordhighs.2 However, individuals whoobjected to vaccination wereapproximately twice as likely toreside in areas of highersocioeconomic resources. In thisscenario, financial disincentives maynot be adequate because those morelikely to refuse vaccination may alsohave the ability to bear theconsequences of the financialdisincentives.32

Some European countries areconsidering making vaccinationsmandatory, including implementingfinancial penalties for noncompliance,even if they do not have a history ofsuch policies. Italy and France haveboth made childhood vaccinationsmandatory since the beginning of2017 in response to decreasingvaccination rates and outbreaks ofmultiple vaccine-preventableinfectious diseases, includingmeasles, although the Italian mandatewas later repealed.6,7 For countrieswith mandatory vaccination, therecan still be outbreaks of disease dueto the vaccination rate still notreaching the herd immunity thresholdor geographic clusters ofunvaccinated individuals.24 The WHORegional Office for Europe recentlyreleased a Guide to TailoringImmunization Programs, offeringa process through which to identifyobstacles and motivators toimmunization in areas of lowvaccination rates and for how todesign interventions tailored to meetthose factors.33

Previous examination of vaccinemandates in Europe via a nonpeer-reviewed analysis by the Action Planon Science in Society Related Issuesin Epidemics and Total Pandemics(ASSET) did not report a relationshipbetween national policies onmandatory vaccination andvaccination coverage in Europe.Although the ASSET study examinedmost of the countries that were

TABLE 1 Association of Mandatory Vaccination, the Availability of a Nonmedical Exemption Option, and the Penalty of Noncompliance With Rates ofVaccination Against Measles (2006–2015) and Pertussis (2006–2016)

No. Country-Years

Difference in Vaccination Rate, % (95% CI) P

MeaslesMandatory vaccination, yes or no 287 3.71 (1.68 to 5.74) .0003Mandatory vaccination without nonmedical exemption, yes or no 267 3.80 (1.23 to 6.37) .0037Financial penalty for noncompliance per €500 59 0.80 (0.5 to 1.15) ,.0001

PertussisMandatory vaccination, yes or no 316 2.14 (0.13 to 4.15) .04Mandatory vaccination without nonmedical exemption, yes or no 294 2.07 (21.74 to 5.89) .28Financial penalty for noncompliance per €500 65 1.1 (0.95 to 1.30) ,.0001

All models are adjusted for GDP per capita, GINI, urban population, universal health care coverage, median age, percentage of the population ,14 years of age, and education level.

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included in our study, there areseveral differences between theASSET analysis and our study. Forexample, whereas our studyaccounted for confounders in theregression models, the ASSETanalysis ostensibly did not useadjusted models (because there wereno adjusted analyses reported).Specifically, our study accounted forvarious factors that are associated

with vaccine uptake, includingeducation level, distribution of wealthin the country, and health careaccessibility. Moreover, our study alsoexamined a longer period of time(2006–2016) than did the ASSETstudy (2007–2013), providinga higher statistical power for variousanalyses. Whereas the ASSET studyonly examined the presence ofa mandate in a country as a binary

variable, we also examined the effectsof allowing for nonmedical exemptionon vaccine-preventable diseaseincidence and of the magnitude ofa fine for noncompliance.

There are a few limitations to ourstudy that should be considered. First,this study is ecological in nature;therefore, we cannot draw a direct linkbetween individual vaccine refusalsand vaccine policies. However, giventhat policy is implemented at thepopulation level, a country-levelanalysis is an appropriate way toevaluate the potential impact ofa policy. Second, although the WHO’sGlobal Health Observatory and thecentralized information system forinfectious diseases are the bestavailable sources for immunizationrates and disease incidence, both arereliant on reporting by physicians andofficials in each country. For diseaseincidence, case counts rely onindividuals seeking medical care in thecase of disease, their physicianreporting the case to the local healthauthority, and these local healthauthorities properly reporting thesecases to the national health ministryor other entities who would eventuallyreport to the WHO or the EuropeanCenters for Disease Control. However,this is true for countries withmandates and without; therefore, theassociations in our analysis are likelyto be an underestimate due tonondifferential misclassification.Similarly, although we conducteda review to identify the best availablesources of information on country-level vaccine policies, it is possible thatwe either did not or were unable tofind all details on a given policy.Therefore, we were unable to accountfor a lag in effect that a change inpolicy may have. Additionally, there isalso the possibility that the availabilityof nonmedical vaccination exemptionsas well as the magnitude of thefinancial penalties faced by those whofail to comply were measured by usinginformation that might not havereflected the entire period studied.

FIGURE 2Median percentage and interquartile ranges of vaccination rates for countries with and withoutmandatory vaccination. a The horizontal line indicates the average vaccination rate across allcountries and years included in the study.

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Using resources from 2006 to2018, we were not able to find anyindications that any countriessubstantively changed theirmandatory vaccinations from 2006to 2016.7,9 Lastly, both vaccinecoverage and disease incidence arecomplicated outcomes dependent ona number of factors. We either didnot or could not account for allpossible factors that may influencethis relationship, such as thegeographic proximity of the selectedcountries or overall population size,instead choosing to prioritize thosefactors that had been previouslyassociated with these relationships inthe literature.

CONCLUSIONS

Although our findings support theuse of mandatory vaccination andfinancial penalties to ensure themaintenance of the necessary highvaccination rates, our analysisinvolved existing mandates. Theintroduction of new mandates shouldbe accompanied by carefulsurveillance of the impact on bothvaccine acceptance and diseaseoutcomes. Vaccine mandates shift thebalance of convenience in favor ofvaccination and, when accompaniedby robust vaccine safety assuranceand vaccine communicationsprograms, have the potential to playa substantial role in decreasing the

negative impacts of vaccine-preventable diseases.

ABBREVIATIONS

aIRR: adjusted incidence rate ratioASSET: Action Plan on Science in

Society Related Issues inEpidemics and TotalPandemics

CI: confidence intervalGDP: gross domestic productPPP: purchasing power parityVENICE: Vaccine European New

Integrated CollaborationEffort

WHO: World Health Organization

DOI: https://doi.org/10.1542/peds.2019-0620

Accepted for publication Sep 6, 2019

Address correspondence to Mallory K. Ellingson, MPH, Yale Institute for Global Health, 1 Church St, Suite 340, New Haven, CT 06510. E-mail: mallory.ellingson@

yale.edu

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2020 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

COMPANION PAPER: A companion to this article can be found online at www.pediatrics.org/cgi/doi/10.1542/2019-2436.

REFERENCES

1. Centers for Disease Controland Prevention. Ten greatpublic health achievements–worldwide, 2001-2010. MMWR MorbMortal Wkly Rep. 2011;60(24):814–818

2. Hull A, Dey A, Beard F, Brotherton J,McIntyre P. Annual ImmunisationCoverage Report 2016. Westmead,Australia: National Centre forImmunisation Research & Surveillanceof Vaccine Presentable Diseases; 2016

3. Orenstein WA, Hinman AR.The immunization system inthe United States - the roleof school immunization laws.Vaccine. 1999;17(suppl 3):S19–S24

TABLE 2 Association of Mandatory Vaccination, the Availability of a Nonmedical Exemption Option, and the Penalty of Noncompliance With the Incidence ofMeasles (2006–2015) and Pertussis (2006–2016)

Mandatory Vaccination No.Countries

Pertussisa Incidence Rate Ratio(95% CI)

Measles Incidence Rate Ratio (95% CI)

No mandatory vaccination 22 Reference ReferenceMandatory vaccination 7 0.30 (0.07 to 1.30) 0.38 (0.13 to 1.16)Mandatory vaccination without nonmedical exemptions 5 1.04 (0.18 to 6.32) 0.14 (0.05 to 0.36)Monetary fineNo mandatory vaccination 22 Reference ReferenceMandatory vaccination and monetary penalty for noncompliance 6 0.42 (0.18 to 0.98) 0.14 (0.05 to 0.39)

a Models are adjusted for GDP per capita, GINI, urban population, universal health care coverage, median age, percentage of the population ,14 years of age, and education level.

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Page 8: Mandatory Vaccination in Europe · Vaccination in Europe. Pediatrics. 2020;145(2):e20190620 aDepartments of Epidemiology and cBiostatistics and Bioinformatics, bHubert Department

4. Gostin LO, Wiley LF. Public Health Law:Power, Duty, Restraint. Berkeley, CA:University of California Press; 2016

5. Goodman RA. Law in Public HealthPractice. Oxford, United Kingdom:Oxford University Press; 2007

6. Ward JK, Colgrove J, Verger P. WhyFrance is making eight new vaccinesmandatory. Vaccine. 2018;36(14):1801–1803

7. Ravagli M. Amid measles outbreak, Italymakes childhood vaccinationsmandatory. 2017. Available at: https://www.npr.org/sections/parallels/2017/06/19/533481635/amid-measles-outbreak-italy-makes-childhood-vaccinations-mandatory. Accessed April15, 2018

8. European Centre for Disease Preventionand Control. Monthly Measles andRubella Monitoring Report. Stockholm,Sweden: European Centre for DiseasePrevention and Control; 2018

9. Haverkate M, D’Ancona F, Giambi C,et al; VENICE project gatekeepers andcontact points. Mandatory andrecommended vaccination in the EU,Iceland and Norway: results of theVENICE 2010 survey on the ways ofimplementing national vaccinationprogrammes. Euro Surveill. 2012;17(22):17

10. World Health Organization. GlobalHealth Observatory (GHO) data: aboutthe GHO. 2018. Available at: www.who.int/gho/about/en/. Accessed April 15,2018

11. WHO Regional Office for Europe. CISIDhome. Available at: http://data.euro.who.int/cisid/?TabID=456118. AccessedApril 15, 2018

12. Eurostat. What we do. Available at:http://ec.europa.eu/eurostat/about/overview/what-we-do. Accessed April15, 2018

13. European Centre for Disease Preventionand Control. Vaccination schedules forindividual European countries andspecific age groups. 2018. Available at:

https://ecdc.europa.eu/en/immunisation-vaccines/EU-vaccination-schedules. Accessed April 15, 2018

14. Fra�nková R. Court underminesmandatory Czech vaccination regime.Radio Praha. Available at: http://www.radio.cz/en/section/curraffrs/court-undermines-mandatory-czech-vaccination-regime. Accessed April 15,2018

15. Vaksinko. Vaccinations: frequentlyasked questions. Available at: http://vaksinko.bg/faq/. Accessed April 15,2018

16. Likumi. Regulations of the Cabinet ofMinisters Nr. 33002000. Available at:https://likumi.lv/doc.php?id=11215.Accessed April 15, 2018

17. Tasz; HCLU. Vaccination 1x1: Társasága Szabadságjogokért. Available at:https://tasz.hu/cikkek/vedooltas-1x1.Accessed April 15, 2018

18. Szczepienia Info. Mandatoryvaccinations in Poland - history andrationale. 2017. Available at: http://szczepienia.pzh.gov.pl/en/stories/mandatory-vaccinations-in-poland/.Accessed April 15, 2018

19. National Institute of Public Health of theRepublic of Slovenia. Vaccination ofChildren - Parents’ Booklet. Ljbuljana,Republic of Slovenia: National Instituteof Public Health; 2018

20. Sprievodcaockovanim. Frequentquestions about vaccination. 2018.Available at: www.sprievodcaockovanim.sk/caste-otazky-o-ockovani/ktore-pravne-predpisy-upravuju-ockovanie-na-slovensku.html.Accessed April 15, 2018

21. Eurostat. Purchasing power parities.Available at: http://ec.europa.eu/eurostat/cache/metadata/en/prc_ppp_esms.htm. Accessed April 15, 2018

22. Austin PC. An introduction to propensityscore methods for reducing the effectsof confounding in observationalstudies. Multivariate Behav Res. 2011;46(3):399–424

23. Haukoos JS, Lewis RJ. The propensityscore. JAMA. 2015;314(15):1637–1638

24. Omer SB, Pan WK, Halsey NA, et al.Nonmedical exemptions to schoolimmunization requirements: seculartrends and association of state policieswith pertussis incidence. JAMA. 2006;296(14):1757–1763

25. Sheikh S, Biundo E, Courcier S, et al. Areport on the status of vaccination inEurope. Vaccine. 2018;36(33):4979–4992

26. O’Connor P, Jankovic D, Muscat M, et al.Measles and rubella elimination in theWHO Region for Europe: progress andchallenges. Clin Microbiol Infect. 2017;23(8):504–510

27. Plotkin SL, Plotkin SA. A Short History ofVaccination. In: Plotkin SA, OrensteinWA, eds. Vaccines, 4th ed. Philadelphia,PA: Saunders; 2004:1–15

28. Cherry JD. The epidemiology ofpertussis and pertussis immunizationin the United Kingdom and the UnitedStates: a comparative study. Curr ProblPediatr. 1984;14(2):1–78

29. Eurostat. Glossary: GINI coefficientstatistics explained: 2014. Available at:https://ec.europa.eu/eurostat/statistics-explained/index.php/Glossary:Gini_coefficient. Accessed November 23,2019

30. World Health Organization. Trackinguniversal health coverage (UHC): onlineQ&A. Available at: www.who.int/health_financing/topics/financial-protection/qa-tracking-uhc/en/. Accessed April 15,2018

31. Walkinshaw E. Mandatory vaccinations:the international landscape. CMAJ.2011;183(16):E1167–E1168

32. Leask J, Danchin M. Imposing penaltiesfor vaccine rejection requires strongscrutiny. J Paediatr Child Health. 2017;53(5):439–444

33. WHO Regional Office for Europe. TheGuide to Tailoring ImmunizationProgrammes. Copenhagen, Denmark:WHO Regional Office for Europe; 2013

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