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Pediatrics
July 2013, VOLUME 132 / ISSUE 1
From the American Academy of Pediatrics
Article

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

Aamer Imdad, Boldtsetseg Tserenpuntsag, Debra S. Blog, Neal A. Halsey, Delia E. Easton, Jana Shaw
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Abstract

OBJECTIVE: The objective of this study was to describe rates of religious vaccination exemptions over time and the association with pertussis in New York State (NYS).

METHODS: Religious vaccination exemptions reported via school surveys of the NYS Department of Health from 2000 through 2011 were reviewed by county, and the changes were assessed against incidence rates of pertussis among children reported to the NYS Department of Health Communicable Disease Electronic Surveillance System.

RESULTS: The overall annual state mean prevalence (± SD) of religious exemptions for ≥1 vaccines in 2000–2011 was 0.4% ± 0.08% and increased significantly from 0.23% in 2000 to 0.45% in 2011 (P = .001). The prevalence of religious exemptions varied greatly among counties and increased by >100% in 34 counties during the study period. Counties with mean exemption prevalence rates of ≥1% reported a higher incidence of pertussis, 33 per 100 000 than counties with lower exemption rates, 20 per 100 000, P < .001. In addition, the risk of pertussis among vaccinated children living in counties with high exemption rate increased with increase of exemption rate among exempted children (P = .008).

CONCLUSIONS: The prevalence of religious exemptions varies among NYS counties and increased during the past decade. Counties with higher exemption rates had higher rates of reported pertussis among exempted and vaccinated children when compared with the low-exemption counties. More studies are needed to characterize differences in the process of obtaining exemptions among NYS schools, and education is needed regarding the risks to the community of individuals opting out from recommended vaccinations.

  • Abbreviations:
    DTaP —
    diphtheria-tetanus-acellular pertussis
    NYS —
    New York State
    NYSDOH —
    New York State Department of Health
    PBE —
    personal belief exemption
    Tdap —
    tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis, adsorbed

    • What’s Known on This Subject:

    Exemption rates for immunization requirements have until recently been stable in states permitting religious exemptions. States with easy exemption processes have seen higher rates of vaccine-preventable diseases.

    What This Study Adds:

    In New York, the rate of religious exemptions has increased. Counties with higher rates of exemption have a greater incidence of pertussis.

    Introduction of vaccines has resulted in dramatic decreases in the incidence of vaccine preventable diseases in the last century.1 One of the effective strategies used in United States to increase vaccine coverage has been state laws mandating vaccination before school entry.2 Immunization requirements in all states permit exemptions due to underlying medical conditions, 48 states permit religious exemption, and 20 states permit philosophical or personal belief exemptions (PBEs).3,4 A PBE allows parents to refuse immunizations based on personal, moral, or philosophical belief.5 New York State (NYS) permits medical and religious exemptions to immunization requirements for school entry. A recent report indicates a religious exemption prevalence of 0.5% among NYS children entering kindergarten.6 Exemption prevalence for states that allowed religious exemptions remained at ∼1% between 1991 and 20045 and increased to 1.6% in 2011.7 Procedures and level of difficulty to obtain exemption to school immunization requirement also vary across the states.3,5 Omer et al reported an increase in exemption rates from 0.99% in 1991 to 2.54% in 2004 in states that allow PBEs.5 Similarly, in states that easily granted exemptions, the exemption rates increased from 1.26% in 1991 to 2.51% in 2004. No significant increase in exemptions was observed in states that allowed religious exemptions only.5 However, recent data have shown a rise of religious exemptions across the United States.7 Children who are exempted from vaccination are more likely to contract vaccine-preventable diseases such as measles and pertussis than nonexempt children.8,9

    Both unvaccinated children and families with similar attitudes and beliefs regarding vaccination cluster geographically.10 For example, 12.3% of all children attending public schools and 18.8% attending day care in Ashland, Oregon, claimed exemptions from mandatory vaccination compared with 2.4% for the entire state.11 Furthermore, multiple outbreaks have been reported in isolated religious communities where most children claim vaccine exemptions.12,13 We evaluated the rates of religious exemptions in NYS over time, geographic clustering of exemptions, and the association between exemption rates and the rates of reported pertussis.

    Methods

    This study was conducted in collaboration with New York State Department of Health (NYSDOH). Every year all schools in NYS must provide the commissioner with a summary regarding compliance with immunization requirements before school entry. School-based immunization surveys gather student-level details about vaccination histories during the preschool years and report aggregate school-level data to NYSDOH. In contrast to provider-based surveys, school-based surveys include all children including those who have no identified provider or who change providers, and are therefore a useful tool for assessing immunization coverage.14

    Immunization Exemption Process in NYS Schools

    School exemptions are reviewed by the school’s principal either annually each September or upon enrollment of new students. The NYS Education Department guidelines help schools through the exemption process, and all schools, both public and private, are recommended to use them. Each school drafts its own policy based on the NYS Education Department guidelines, and differences may exist between individual schools. The NYS Education Department standardized the exemption guidelines in 2006 and determined that a student may be exempt from vaccination if the parents hold genuine and sincere religious beliefs that are contrary to the practice of immunization regardless of membership in established religious organizations. Those children are referred to as “exemptors” in this article. Requests for exemptions must be written, signed, and notarized by the student or a parent if aged <18.15 If a religious exemption request is denied, parents are informed in writing along with reasons. Parents may appeal by petition to the commissioner of education. If the exemption is denied, the child has to complete vaccinations according to school immunization laws or be exempted from attending school. NYS permits a 14-day grace period to complete required immunizations.

    NYS requires the following vaccinations before attending school (kindergarten through 12th grade) entry: 3 doses of diphtheria-tetanus-acellular pertussis (DTaP); polio and hepatitis B; tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis, adsorbed (Tdap) booster for sixth grade; 2 doses of measles-mumps-rubella; and 1 dose of varicella vaccines (seewww.health.ny.gov/publications/2370.pdf). During the study period, hepatitis B, varicella, DTaP, and Tdap booster vaccines were added to school immunization requirements in 2000, 2004, 2005, and 2007, respectively. The compliance with new school immunization requirements was implemented by schools and NYSDOH incrementally and started at the kindergarten, sixth-grade, or seventh-grade level and moved to each successive year as the age cohort was promoted to the next higher grade level until all grades were covered.

    Immunization Exemption Estimates

    Immunization surveys submitted to NYSDOH are the most complete source of data for monitoring immunization exemptions. School-based immunization surveys include information on total numbers of enrolled and exempted children in each school. We performed a retrospective review of immunization religious exemption rates by county between 2000 and 2011 by using school survey results. Annual religious exemption rates were calculated as the percent of children with religious exemptions among enrolled children by county. Change in exemption rates was calculated as the difference in rates in 2011 compared with rates in 2000 for each county and presented in a state map by county. Overall annual exemption rates for the state were calculated as percentage of all exempted children among all enrolled children by school year and trend over the years was tested by using the χ2 test for trend. For each county, an overall exemption rate was calculated by dividing sum of all exempted by all enrolled children for the study period of 12 years. If county’s overall exemption was ≥1%, the county was grouped in the high-exemption group; the remaining counties were considered to be low-exemption counties.

    Pertussis Incidence Estimates in High- and Low-Exemption Counties

    We counted all pertussis cases among children aged ≤19 years reported to Communicable Disease Electronic Surveillance System. We used US Census Bureau county population estimates between 2000 and 2011 for children aged ≤19 years as the denominator and calculated incidence rates of pertussis for each county. The 5 New York City counties were excluded because county-specific pertussis case reports were not available. Correlation between exemption rate and pertussis incidence by county was assessed by using a simple linear regression. Similarly, incidence rates of pertussis in high- and low-exemption counties were calculated by using all reported cases and US Census Bureau cumulative county population estimates for these 2 groups. The difference in pertussis incidences between high- and low-exemption groups was tested by using Poisson regression.

    Pertussis Incidence Estimates Among Vaccinated and Exempted Children

    Data for cases such as age, county of residence, vaccination status, and reason for no vaccination were collected from Communicable Disease Electronic Surveillance System case reports. For the purpose of the analysis of risk of pertussis among vaccinated and exempted children, we excluded pertussis cases with unknown vaccination or exemption history. Because the age distribution of enrollees in the school survey was not different from the age distribution of the NYS general population, exemption rate was used to estimate the numbers of exempted children and vaccinated children in the counties, using the mean exemption rate for each county. We estimated the annual county population of vaccinated and exempted children by applying the annual proportion of vaccinated and exempted children from the school immunization surveys to the entire annual county population. Incidence of pertussis among vaccinated children was calculated by dividing the total number of cases with reported pertussis vaccination by the estimated cumulative number of vaccinated children in the county by using population estimates from the US Census Bureau. Children were considered vaccinated if they had received ≥1 pertussis vaccination. Similarly, pertussis incidence among exempted children was calculated by dividing number of cases with documented exemption in the case report by estimated number of exempted children by using the county exemption rate and US Census Bureau population estimates. We used a linear regression to assess any correlation between the incidence rates among vaccinated and exempted children. Data analysis was performed by using SAS version 9.2 (SAS Institute, Cary, NC). A P value ≤.05 was considered statistically significant. Because publicly available, aggregate county-level data were used, this study was considered non–human subject research, and institutional review board approval was not required.

    Results

    There are 62 counties in NYS, including New York City. The 12-year mean prevalence of religious exemptions among the 62 counties in NYS ranged from 0.06% to 5.58% in 2000–2011 with an overall mean (± SD) of 0.78% ± 1.08%. The statewide mean exemption rate increased from 0.23% in 2000 to 0.45% in 2011 (P = .001). Thirteen counties had high religious exemption rates in 2011 compared with only 4 in 2000 (Fig 1). Thirty-four counties had a more than twofold increase in religious exemption rates between 2000 and 2011.

    FIGURE 1
    FIGURE 1

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

    The county mean annual incidences of pertussis among children in NYS ranged from 8 to 124 per 100 000 during the 12-year period. Counties with mean religious exemption prevalence rates of ≥1% had a higher incidence of reported pertussis than counties with lower religious exemption rates, 33.1 per 100 000 versus 20.1 per 100 000, respectively, P < .001, with an incidence ratio of 1.71 (95% confidence interval: 1.60–1.83; Fig 2). The overall pertussis incidence increased on average by 5 per 100 000 for each 0.1% increase in exemption rate (data not shown). Figure 3 illustrates a linear relationship between pertussis incidence and increase in exemption rate. For example, in counties with a high exemption rate, a twofold increase in the exemption rate correlated with pertussis incidence of 32 per 100 000. Counties with low exemption rates did not show significant increase in pertussis incidence with increasing rate change (Fig 3).

    FIGURE 2
    FIGURE 2

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

    FIGURE 3
    FIGURE 3

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

    Among all vaccinated children, 77% received ≥4 doses of pertussis vaccine. County pertussis incidence among exempted and vaccinated children ranged from 6 to 1000 per 100 000 and 5 to 98 per 100 000, respectively. The mean incidence of pertussis among exempted children living in all counties was 14 times greater than the mean incidence of pertussis among vaccinated children, 302 per 100 000 and 22 per 100 000 children (P = .02), respectively (Fig 4). High exemption rates in the community increased pertussis risk for both vaccinated and exempted children (Fig 4) and especially among vaccinated and exempted children living in counties with high exemption rates (P = .008). In counties with overall low exemption rates, the incidence of pertussis in vaccinated children was not significantly influenced by pertussis infections among exempted children (P = .76).

    FIGURE 4
    FIGURE 4

    Estimated pertussis incidences per 100 000 vaccinated or exempted NYS children living in counties with low (<1%) and high (≥1%) immunization exemption level, 2000–2011.

    Discussion

    Religious exemptions to immunizations in NYS have nearly doubled from 0.23% to 0.45% over the past decade. This increase was not uniformly distributed, and some counties had high exemption rates. The incidence of pertussis was higher in counties with higher rates of exemptions. These findings are consistent with studies in other states that have shown geographic clustering of exemptions and an increased risk of pertussis in communities with higher exemption rates.3,5,9,10 In addition, high county exemption rates pose an increased risk of pertussis not only to exemptors but also to vaccinated children.

    The increase in religious exemptions is in contrast to a previously published study that showed rates of exemptions to be stable in states with medical and religious exemptions only5 but is in agreement with a recent report.7 In addition, the increased rate of religious exemptions in NYS is comparable to those states that permit easy nonmedical exemptions.5 We suspect that parents seek religious exemptions to school immunization requirements as a way of addressing personal beliefs and concerns regarding vaccine safety and efficacy. NYS is one of the states in which obtaining religious exemptions to vaccination was considered to be of “moderate difficulty” when compared with other states.16 The reasons for rising rates of religious exemptions are not known and deserve further study.

    Migration or changes in local religious or ethnic groups may have influenced vaccination exemptions in certain counties. NYS has seen growth of the Amish population over the past decade with an increase by 22% between 2010–2012.17 Although not all Amish groups refuse to immunize their children, Amish children are underimmunized.18 In addition to the possible effect of the growth of Amish communities on exemption rates, previous research suggests that other groups of unvaccinated children tend to be white, to have a mother who is married and has a college degree, to live in a household with an annual income exceeding $75 000, and to have parents who express concerns regarding the safety of vaccines.10 It is unclear at this point whether the pediatric population exempted for religious reasons in NYS is represented by specific religious groups, simply by parents who share personal belief objections to vaccinations and use religious exemptions to gain entry to school for their children, or by some other group. It is likely that a combination of ethnic, socioeconomic, and religious groups are reflected in exemption rates. Additional research is needed to determine the predominant group, if any, comprising exemption rates.

    Our study had several limitations. First, this was a retrospective study, and temporal differences in administrative requirements for exemptions at the school and state levels could not be addressed. For example, hepatitis B, varicella, DTaP, and Tdap booster vaccines were added to school immunization requirements during the study period, and the review process was implemented over time. It is possible that our exemption rates represent an underestimate of true exemption rates. Second, vaccination status and reasons for “no vaccine” were missing for 15% of pertussis cases, thus the number of cases among exemptors may be underestimated. If cases with unknown vaccination status were all exemptors, our reported incidence among exemptors would be an underestimate. Third, the school immunization surveys submitted to the NYSDOH do not include data on type of vaccine refused by parent. Therefore, it was not possible for us to determine whether the exempted children missed 1 or all vaccinations, and the population at risk for pertussis might have been overestimated. However, the bias would underestimate the risk of pertussis among exemptors. Fourth, passive surveillance of pertussis likely resulted in an underestimate of a true pertussis burden during the study period because not all children with cough will either seek or receive testing and treatment of pertussis. Finally, our data did not capture exemptions among homeschooled children because they are not routinely collected by the NYSDOH. Although immunization coverage rates among homeschooled children are not well studied, some parents may choose to homeschool their children to avoid vaccination because studies have shown that, in general, they often lack confidence in vaccines’ importance and safety.19

    This is the first study to examine the magnitude of nonmedical exemptions of childhood vaccinations in schools with moderately difficult and standardized exemption processes. We show that unvaccinated children pose not only a risk to themselves and to other children who cannot be protected by vaccines because of their age or an underlying medical condition, but also to vaccinated children in communities with high exemption rates. Undervaccination due to vaccine exemptions in schools and waning immunity with acellular pertussis vaccine could be one of the many factors influencing emerging increases of outbreaks of pertussis.9,20 Consistent with Omer and others,5,9 data in this study show possible associations between exemption rate and pertussis incidence and highlight the importance of public, media, and professional efforts to increase public confidence in vaccines and their acceptance.

    Conclusions

    The prevalence of religious exemptions varies among NYS counties and has increased during the past 12 years. Counties with high exemptions had overall higher rates of reported pertussis. Undervaccination in 1 community puts not only unvaccinated but also vaccinated children at increased risk. More studies are needed to determine the impact of exemptions to school immunizations on other vaccine preventable diseases in NYS. Religious reasons behind parental refusal deserve additional study because they drive the exemption rates in NYS.

    Footnotes

      • Accepted April 4, 2013.
    • Address correspondence to Jana Shaw, MD, MPH, SUNY Upstate Medical University, 750 East Adams St, Syracuse, NY 13210. E-mail: shawja{at}upstate.edu

    • Dr Imdad conceptualized the study, drafted the initial manuscript, and approved the final manuscript as submitted; Dr Tserenpuntsag carried out the analyses, reviewed and revised the manuscript, and approved the final manuscript as submitted; Dr Blog coordinated data collection, critically reviewed the manuscript, and approved the final manuscript as submitted; Dr Halsey conceptualized the study, assisted with critical feedbacks, reviewed and revised the manuscript, and approved the final manuscript as submitted; Dr Easton coordinated and supervised data collection, critically reviewed and revised the manuscript, and approved the final manuscript as submitted; and Dr Shaw conceptualized the study, reviewed and revised the manuscript, and approved the final manuscript as submitted.

    • FINANCIAL DISCLOSURE: Dr Halsey receives compensation for participation in Safety Monitoring Committees from Merck and Novartis for studies of vaccines unrelated to the vaccines in this study. He is also participating in the defense of a lawsuit for GlaxoSmithKline on patents related to immunization schedules. Dr Shaw was a 1-time speaker for Merck in 2012 and 2011 and received an honorarium and travel for the lecture. The other authors have indicated they have no financial relationships relevant to this article to disclose.

    • FUNDING: The study was supported by a Resident Research Grant from the AAP.

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    Religious Exemptions for Immunization and Risk of Pertussis in New York State, 2000–2011
    Aamer Imdad, Boldtsetseg Tserenpuntsag, Debra S. Blog, Neal A. Halsey, Delia E. Easton, Jana Shaw
    Pediatrics Jul 2013, 132 (1) 37-43; DOI: 10.1542/peds.2012-3449
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