Religious Exemptions for Immunization and Risk ofPertussis in New York State, 2000–2011

WHAT’S KNOWN ON THIS SUBJECT: Exemption rates forimmunization requirements have until recently been stable instates permitting religious exemptions. States with easyexemption processes have seen higher rates of vaccine-preventable diseases.

WHAT THIS STUDY ADDS: In New York, the rate of religiousexemptions has increased. Counties with higher rates ofexemption have a greater incidence of pertussis.

abstractOBJECTIVE: The objective of this study was to describe rates of re-ligious vaccination exemptions over time and the association withpertussis in New York State (NYS).

METHODS: Religious vaccination exemptions reported via school sur-veys of the NYS Department of Health from 2000 through 2011 werereviewed by county, and the changes were assessed against incidencerates of pertussis among children reported to the NYS Department ofHealth Communicable Disease Electronic Surveillance System.

RESULTS: The overall annual state mean prevalence (6 SD) of religiousexemptions for $1 vaccines in 2000–2011 was 0.4% 6 0.08% and in-creased significantly from 0.23% in 2000 to 0.45% in 2011 (P = .001). Theprevalence of religious exemptions varied greatly among counties andincreased by .100% in 34 counties during the study period. Countieswith mean exemption prevalence rates of $1% reported a higher in-cidence of pertussis, 33 per 100 000 than counties with lower exemptionrates, 20 per 100 000, P , .001. In addition, the risk of pertussis amongvaccinated children living in counties with high exemption rate increasedwith increase of exemption rate among exempted children (P = .008).

CONCLUSIONS: The prevalence of religious exemptions varies amongNYS counties and increased during the past decade. Counties with higherexemption rates had higher rates of reported pertussis among exemptedand vaccinated children when compared with the low-exemptioncounties. More studies are needed to characterize differences inthe process of obtaining exemptions among NYS schools, andeducation is needed regarding the risks to the community ofindividuals opting out from recommended vaccinations. Pediatrics2013;132:37–43

AUTHORS: Aamer Imdad, MD,a Boldtsetseg Tserenpuntsag,MD, DrPh,b Debra S. Blog, MD, MPH,b Neal A. Halsey, MD,c

Delia E. Easton, PhD,b and Jana Shaw, MD, MPHa

aState University of New York Upstate Medical University,Syracuse, New York; bNew York State Department of Health,Bureau of Immunization, Albany, New York; and cJohns HopkinsBloomberg School of Public Health, Baltimore, Maryland

KEY WORDSimmunization, exemptions, children, pertussis

ABBREVIATIONSDTaP—diphtheria-tetanus-acellular pertussisNYS—New York StateNYSDOH—New York State Department of HealthPBE—personal belief exemptionTdap—tetanus toxoid, reduced diphtheria toxoid, and acellularpertussis, adsorbed

Drs Imdad and Tserenpuntsag contributed equally to this work.

Dr Imdad conceptualized the study, drafted the initialmanuscript, and approved the final manuscript as submitted; DrTserenpuntsag carried out the analyses, reviewed and revisedthe manuscript, and approved the final manuscript assubmitted; Dr Blog coordinated data collection, criticallyreviewed the manuscript, and approved the final manuscript assubmitted; Dr Halsey conceptualized the study, assisted withcritical feedbacks, reviewed and revised the manuscript, andapproved the final manuscript as submitted; Dr Eastoncoordinated and supervised data collection, critically reviewedand revised the manuscript, and approved the final manuscriptas submitted; and Dr Shaw conceptualized the study, reviewedand revised the manuscript, and approved the final manuscriptas submitted.

www.pediatrics.org/cgi/doi/10.1542/peds.2012-3449

doi:10.1542/peds.2012-3449

Accepted for publication Apr 4, 2013

Address correspondence to Jana Shaw, MD, MPH, SUNY UpstateMedical University, 750 East Adams St, Syracuse, NY 13210. E-mail:shawja@upstate.edu

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

Copyright © 2013 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: Dr Halsey receives compensation forparticipation in Safety Monitoring Committees from Merck andNovartis for studies of vaccines unrelated to the vaccines in thisstudy. He is also participating in the defense of a lawsuit forGlaxoSmithKline on patents related to immunization schedules.Dr Shaw was a 1-time speaker for Merck in 2012 and 2011 andreceived an honorarium and travel for the lecture. The otherauthors have indicated they have no financial relationshipsrelevant to this article to disclose.

FUNDING: The study was supported by a Resident ResearchGrant from the AAP.

PEDIATRICS Volume 132, Number 1, July 2013 37

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Introduction of vaccines has resulted indramatic decreases in the incidence ofvaccine preventable diseases in the lastcentury.1 One of the effective strategiesused in United States to increase vac-cine coverage has been state lawsmandating vaccination before schoolentry.2 Immunization requirements inall states permit exemptions due tounderlying medical conditions, 48states permit religious exemption, and20 states permit philosophical or per-sonal belief exemptions (PBEs).3,4 A PBEallows parents to refuse immuniza-tions based on personal, moral, orphilosophical belief.5 New York State(NYS) permits medical and religiousexemptions to immunization require-ments for school entry. A recent reportindicates a religious exemption preva-lence of 0.5% among NYS childrenentering kindergarten.6 Exemptionprevalence for states that allowed re-ligious exemptions remained at ∼1%between 1991 and 20045 and increasedto 1.6% in 2011.7 Procedures and levelof difficulty to obtain exemption toschool immunization requirement alsovary across the states.3,5 Omer et alreported an increase in exemptionrates from 0.99% in 1991 to 2.54% in2004 in states that allow PBEs.5 Simi-larly, in states that easily grantedexemptions, the exemption rates in-creased from 1.26% in 1991 to 2.51%in 2004. No significant increase inexemptions was observed in statesthat allowed religious exemptionsonly.5 However, recent data have showna rise of religious exemptions acrossthe United States.7 Children who areexempted from vaccination are morelikely to contract vaccine-preventablediseases such as measles and pertus-sis than nonexempt children.8,9

Both unvaccinated children and fami-lies with similar attitudes and beliefsregarding vaccination cluster geo-graphically.10 For example, 12.3% of allchildren attending public schools and

18.8% attending day care in Ashland,Oregon, claimed exemptions frommandatory vaccination compared with2.4% for the entire state.11 Further-more, multiple outbreaks have beenreported in isolated religious commu-nities where most children claim vac-cine exemptions.12,13 We evaluated therates of religious exemptions in NYSover time, geographic clustering ofexemptions, and the association be-tween exemption rates and the rates ofreported pertussis.

METHODS

This study was conducted in collabo-ration with New York State Departmentof Health (NYSDOH). Every year allschools in NYS must provide the com-missioner with a summary regardingcompliance with immunization require-mentsbefore school entry. School-basedimmunization surveys gather student-level details about vaccination histo-ries during the preschool years andreport aggregate school-level data toNYSDOH. In contrast to provider-basedsurveys, school-based surveys includeall children including those who have noidentified provider or who change pro-viders,andare thereforeauseful tool forassessing immunization coverage.14

Immunization Exemption Process inNYS Schools

School exemptions are reviewed by theschool’s principal either annually eachSeptember or upon enrollment of newstudents. The NYS Education Departmentguidelines help schools through the ex-emption process, and all schools, bothpublic and private, are recommended touse them. Each school drafts its ownpolicy based on the NYS Education De-partment guidelines, and differencesmay exist between individual schools.The NYS Education Department stan-dardized the exemption guidelines in2006 and determined that a studentmay be exempt from vaccination if the

parents hold genuine and sincere re-ligious beliefs that are contrary to thepractice of immunization regardless ofmembership in established religiousorganizations. Those children are re-ferred to as “exemptors” in this article.Requests for exemptions must be writ-ten, signed, and notarized by the studentor a parent if aged,18.15 If a religiousexemption request is denied, parentsare informed in writing along with rea-sons. Parents may appeal by petition tothe commissioner of education. If theexemption is denied, the child has tocomplete vaccinations according toschool immunization laws or beexempted from attending school. NYSpermits a 14-day grace period to com-plete required immunizations.

NYS requires the following vaccinationsbefore attending school (kindergartenthrough 12th grade) entry: 3 doses ofdiphtheria-tetanus-acellular pertussis(DTaP); polio and hepatitis B; tetanustoxoid, reduced diphtheria toxoid, andacellular pertussis, adsorbed (Tdap)booster for sixth grade; 2 doses ofmeasles-mumps-rubella; and 1 dose ofvaricella vaccines (seewww.health.ny.gov/publications/2370.pdf). During thestudy period, hepatitis B, varicella,DTaP, and Tdap booster vaccines wereadded to school immunization require-ments in 2000, 2004, 2005, and 2007,respectively. The compliance with newschool immunization requirements wasimplemented by schools and NYSDOHincrementally and started at the kin-dergarten, sixth-grade, or seventh-gradelevel and moved to each successive yearas the age cohort was promoted to thenext higher grade level until all gradeswere covered.

Immunization Exemption Estimates

Immunization surveys submitted toNYSDOH are the most complete sourceof data for monitoring immunizationexemptions. School-based immuniza-tion surveys include information on

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total numbers of enrolled and exemptedchildren in each school. We performeda retrospective review of immunizationreligious exemption rates by county be-tween 2000 and 2011 by using schoolsurvey results. Annual religious exemp-tion rateswere calculated as the percentof children with religious exemptionsamong enrolled children by county.Change in exemption rates was calcu-lated as the difference in rates in 2011compared with rates in 2000 for eachcounty and presented in a state map bycounty. Overall annual exemption ratesfor the state were calculated as per-centage of all exempted children amongall enrolled children by school year andtrend over the years was tested by usingthe x2 test for trend. For each county, anoverall exemption rate was calculated bydividing sum of all exempted by all en-rolled children for the study period of 12years. If county’s overall exemption was$1%, the county was grouped in thehigh-exemption group; the remainingcounties were considered to be low-exemption counties.

Pertussis Incidence Estimates inHigh- and Low-Exemption Counties

We counted all pertussis cases amongchildren aged #19 years reported toCommunicable Disease Electronic Sur-veillance System. We used US CensusBureau county population estimatesbetween 2000 and 2011 for childrenaged #19 years as the denominatorand calculated incidence rates of per-tussis for each county. The 5 New YorkCity counties were excluded becausecounty-specific pertussis case reportswere not available. Correlation betweenexemption rate and pertussis incidenceby county was assessed by usinga simple linear regression. Similarly,incidence rates of pertussis in high- andlow-exemption countieswere calculatedby using all reported cases and USCensus Bureau cumulative county pop-ulation estimates for these 2 groups.The difference in pertussis incidences

between high- and low-exemption groupswas tested by using Poisson regression.

Pertussis Incidence EstimatesAmong Vaccinated and ExemptedChildren

Data for cases such as age, county ofresidence, vaccination status, andreason for no vaccination were col-lected from Communicable DiseaseElectronic Surveillance System casereports. For the purpose of the analysisof risk of pertussis among vaccinatedand exempted children, we excludedpertussis cases with unknown vacci-nation or exemption history. Becausethe age distribution of enrollees in theschool survey was not different fromthe age distribution of the NYS generalpopulation, exemption rate was used toestimate the numbers of exemptedchildren and vaccinated children in thecounties, using the mean exemptionrate for each county. We estimated theannual county population of vaccinatedand exempted children by applying theannual proportion of vaccinated andexempted children from the schoolimmunization surveys to the entireannual county population. Incidence ofpertussis among vaccinated childrenwas calculated by dividing the totalnumber of cases with reported per-tussis vaccination by the estimatedcumulative number of vaccinated chil-dren in the county by using populationestimates from the US Census Bureau.Children were considered vaccinated ifthey had received $1 pertussis vacci-nation. Similarly, pertussis incidenceamong exempted children was calcu-lated by dividing number of cases withdocumented exemption in the case re-port by estimated number of exemptedchildren by using the county exemptionrate and US Census Bureau populationestimates. We used a linear regressionto assess any correlation between theincidence rates among vaccinated andexempted children. Data analysis wasperformed by using SAS version 9.2

(SAS Institute, Cary, NC). A P value#.05was considered statistically signifi-cant. Because publicly available, ag-gregate county-level data were used,this study was considered non–humansubject research, and institutional re-view board approval was not required.

RESULTS

There are 62 counties in NYS, includingNew York City. The 12-year mean preva-lence of religious exemptions among the62 counties in NYS ranged from 0.06% to5.58% in 2000–2011 with an overallmean (6 SD) of 0.78% 6 1.08%. Thestatewide mean exemption rate in-creased from 0.23% in 2000 to 0.45% in2011 (P = .001). Thirteen counties hadhigh religious exemption rates in 2011compared with only 4 in 2000 (Fig 1).Thirty-four counties had a more thantwofold increase in religious exemptionrates between 2000 and 2011.

The county mean annual incidences ofpertussis among children in NYS rangedfrom 8 to 124 per 100 000 during the 12-year period. Counties with mean re-ligious exemption prevalence rates of$1% had a higher incidence of repor-ted pertussis than counties with lowerreligious exemption rates, 33.1 per100 000 versus 20.1 per 100 000, re-spectively, P , .001, with an incidenceratio of 1.71 (95% confidence interval:1.60–1.83; Fig 2). The overall pertussisincidence increased on average by 5 per100 000 for each 0.1% increase in ex-emption rate (data not shown). Figure 3illustrates a linear relationship betweenpertussis incidence and increase in ex-emption rate. For example, in countieswith a high exemption rate, a twofoldincrease in the exemption rate corre-lated with pertussis incidence of 32 per100 000. Counties with low exemptionrates did not show significant increasein pertussis incidence with increasingrate change (Fig 3).

Among all vaccinated children, 77% re-ceived $4 doses of pertussis vaccine.

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County pertussis incidence amongexempted and vaccinated childrenranged from 6 to 1000 per 100 000 and5 to 98 per 100 000, respectively. Themean incidence of pertussis amongexempted children living in all countieswas 14 times greater than the meanincidence of pertussis among vacci-nated children, 302 per 100 000 and 22per 100 000 children (P = .02), re-spectively (Fig 4). High exemption ratesin the community increased pertussisrisk for both vaccinated and exemptedchildren (Fig 4) and especially amongvaccinated and exempted children living

in counties with high exemption rates(P = .008). In counties with overall lowexemption rates, the incidence of pertus-sis in vaccinated children was not signif-icantly influenced by pertussis infectionsamong exempted children (P = .76).

DISCUSSION

Religious exemptions to immunizationsin NYS have nearly doubled from 0.23%to 0.45% over the past decade. Thisincreasewas not uniformly distributed,and some counties had high exemptionrates. The incidence of pertussis washigher in counties with higher rates of

exemptions. These findings are consis-tentwith studies in other states that haveshown geographic clustering of exemp-tionsandanincreasedriskofpertussis incommunities with higher exemptionrates.3,5,9,10 In addition, high county ex-emption rates pose an increased risk ofpertussis not only to exemptors but alsoto vaccinated children.

The increase in religious exemptions isin contrast to a previously publishedstudy that showed rates of exemptionsto be stable in states with medical andreligious exemptions only5 but is inagreement with a recent report.7 Inaddition, the increased rate of religiousexemptions in NYS is comparable tothose states that permit easy non-medical exemptions.5 We suspect thatparents seek religious exemptions toschool immunization requirements asa way of addressing personal beliefsand concerns regarding vaccine safetyand efficacy. NYS is one of the states inwhich obtaining religious exemptionsto vaccination was considered to be of“moderate difficulty” when comparedwith other states.16 The reasons forrising rates of religious exemptionsare not known and deserve furtherstudy.

Migration or changes in local religiousor ethnic groups may have influencedvaccination exemptions in certaincounties. NYS has seen growth of theAmish population over the past decadewith an increase by 22% between2010–2012.17 Although not all Amishgroups refuse to immunize their chil-dren, Amish children are underimmu-nized.18 In addition to the possible effectof the growth of Amish communities onexemption rates, previous researchsuggests that other groups of un-vaccinated children tend to be white, tohave a mother who is married and hasa college degree, to live in a householdwith an annual income exceeding$75 000, and to have parents who ex-press concerns regarding the safety of

FIGURE 1County religious exemption rates in NYS schools in 2000 and 2011.

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vaccines.10 It is unclear at this pointwhether the pediatric populationexempted for religious reasons in NYS

is represented by specific religiousgroups, simply by parents who sharepersonal belief objections to vacci-

nations and use religious exemptionsto gain entry to school for their chil-dren, or by some other group. It is likelythat a combination of ethnic, socioeco-nomic, and religious groups are reflectedin exemption rates. Additional researchis needed to determine the predominantgroup, if any, comprising exemptionrates.

Our study had several limitations. First,this was a retrospective study, andtemporal differences in administrativerequirements for exemptions at theschool and state levels could not beaddressed. For example, hepatitis B,varicella, DTaP, and Tdap booster vac-cines were added to school immuni-zation requirements during the studyperiod, and the review process wasimplemented over time. It is possiblethat our exemption rates represent anunderestimate of true exemption rates.Second, vaccination status and reasonsfor “no vaccine” were missing for 15%of pertussis cases, thus the number ofcases among exemptors may beunderestimated. If cases with unknownvaccination status were all exemptors,our reported incidence among ex-emptors would be an underestimate.Third, the school immunization surveyssubmitted to the NYSDOH do not include

FIGURE 2Incidence of pertussis per 100 000 NYS children, excluding New York City, stratified by exemption rate category, 2000–2011.

FIGURE 3Increase in the incidence of pertussis per 100 000 NYS children by fold increase in exemption rate incounties with low (,1%) and high ($1%) immunization exemption level, 2000–2011.

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data on type of vaccine refused byparent. Therefore, it was not possiblefor us to determine whether theexempted children missed 1 or allvaccinations, and the population atrisk for pertussis might have beenoverestimated. However, the biaswould underestimate the risk of per-tussis among exemptors. Fourth,passive surveillance of pertussis likelyresulted in an underestimate of a truepertussis burden during the study pe-riod because not all children with cough

will either seek or receive testing andtreatment of pertussis. Finally, our datadid not capture exemptions amonghomeschooled children because they arenot routinely collected by the NYSDOH.Although immunization coverage ratesamong homeschooled children are notwell studied, some parents may chooseto homeschool their children to avoidvaccination because studies have shownthat, in general, they often lack con-fidence in vaccines’ importance andsafety.19

This is the first study to examine themagnitude of nonmedical exemptionsof childhood vaccinations in schoolswith moderately difficult and stan-dardized exemption processes. Weshow that unvaccinated children posenot only a risk to themselves and toother children who cannot be pro-tected by vaccines because of their ageor an underlying medical condition,but also to vaccinated children incommunities with high exemptionrates. Undervaccination due to vaccineexemptions in schools and waningimmunity with acellular pertussisvaccine could be one of the manyfactors influencing emerging increa-ses of outbreaks of pertussis.9,20

Consistent with Omer and others,5,9

data in this study show possibleassociations between exemption rateand pertussis incidence and highlightthe importance of public, media, andprofessional efforts to increase publicconfidence in vaccines and their ac-ceptance.

CONCLUSIONS

The prevalence of religious exemptionsvaries among NYS counties and hasincreased during the past 12 years.Counties with high exemptions hadoverall higher rates of reported per-tussis. Undervaccination in 1 commu-nity puts not only unvaccinated but alsovaccinated children at increased risk.More studies are needed to determinethe impact of exemptions to schoolimmunizations on other vaccine pre-ventable diseases in NYS. Religiousreasons behind parental refusal de-serve additional study because theydrive the exemption rates in NYS.

REFERENCES

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FIGURE 4Estimated pertussis incidences per 100 000 vaccinated or exempted NYS children living in countieswithlow (,1%) and high ($1%) immunization exemption level, 2000–2011.

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15. New York State Education Department. Guid-ance field memo for implementing requests

for religious exemption to immunization.March 2006. Available at: www.p12.nysed.gov/sss/schoolhealth/schoolhealthservices/fieldmemoreligiouseximmunprocedures.html.Accessed October 12, 2012

16. Rota JS, Salmon DA, Rodewald LE, Chen RT,Hibbs BF, Gangarosa EJ. Processes forobtaining nonmedical exemptions to stateimmunization laws. Am J Public Health.2001;91(4):645–648

17. Amish Studies, Young Center for Ana-baptist and Pietist Studies at Elizabeth-town College. Amish population trends1991–2010, twenty-year highlights. Avail-able at: http://www2.etown.edu/amish-studies/Population_Trends_1991_2010.asp.Accessed October 15, 2012

18. Wenger OK, McManus MD, Bower JR,Langkamp DL. Underimmunization in Ohio’sAmish: parental fears are a greater ob-stacle than access to care. Pediatrics. 2011;128(1):79–85

19. Kennedy AM, Gust DA. Parental vaccinebeliefs and child’s school type. J SchHealth. 2005;75(7):276–280

20. Wendelboe AM, Van Rie A, Salmaso S,Englund JA. Duration of immunity againstpertussis after natural infection or vacci-nation. Pediatr Infect Dis J. 2005;24(suppl5):S58–S61

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DOI: 10.1542/peds.2012-3449 originally published online June 3, 2013; 2013;132;37Pediatrics 

Easton and Jana ShawAamer Imdad, Boldtsetseg Tserenpuntsag, Debra S. Blog, Neal A. Halsey, Delia E.

2011−State, 2000 Religious Exemptions for Immunization and Risk of Pertussis in New York

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2011−State, 2000 Religious Exemptions for Immunization and Risk of Pertussis in New York

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