Open Forum Infectious Diseases MAJOR ARTICLE Trends in Kindergarten Rates of Vaccine Exemption and State-Level Policy, 2011–2016 1,2,3,4 1,2 1 5 1,2,3 Saad B. Omer, Rachael M. Porter, Kristen Allen, Daniel A. Salmon, and Robert A. Bednarczyk 1 2 3 4 Hubert Department of Global Health and Department of Epidemiology, Rollins School of Public Health, Emory Vaccine Center, and Department of Pediatrics, School of Medicine, Emory University, Atlanta, Georgia; Institute for Vaccine Safety, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland Background. Kindergarten-entry vaccination requirements have played an important role in controlling vaccine-preventable dis- eases in the United States. Forty-eight states and the District of Colombia oer n ff onmedical exemptions to vaccines, ranging in stringency. Methods. We analyzed state-level exemption data from 2011 to 2012 through 2015 to 2016 school years. States were categorized by exemption ease and type of exemption allowed. We calculated nonmedical exemption rates for each year in the sample and strat- ified by exemption ease, type, and 2 trend categories: 2011–12 through 2012–13 and 2013–14 through 2015–16 school years. Using generalized estimating equations, we created regression models estimating (1) the average annual change in nonmedical exemption rates and (2) relative differences in rates by state classification. Results. e n Th onmedical exemption rate was higher during the 2013–2014 through 2015–2016 period (2.25%) compared to 2011–2012 through 2012–2013 (1.75%); more importantly, the average annual change in the latter period plateaued. The nonmedical exemption rate in states allowing philosophical and religious exemptions was 2.41 times as high as in states allowing only religious exemptions (incidence rate ratio = 2.41; 95% confidence interval, 1.71–3.41). Conclusions. er Th e was an increase in nonmedical exemption rates through the 2012–2013 school year; however, rates stabi- lized through the 2015–2016 school year, showing an important shift in trend. Keywords. epidemiology; vaccination; vaccine exemption; vaccine hesitancy. School entry vaccine mandates have played an important role have played an important role in measles outbreaks aer e ft limin- in controlling childhood communicable diseases in the United ation of endemic measles transmission in the United States . States . Moreover, data on exemptions to these mandates are Recently, a large measles outbreak—first identified among visitors collected at least once a year in schools and reported to state to Disneyland California—was associated with a large proportion health departments throughout the country, hence providing a of cases among individuals with nonmedical exemptions . direct annual measure of vaccine refusal . er Th e have been 2 multiyear assessments of longitudinal Since the late 1990s, there has been an increase in nonmed- trends in nonmedical exemption rates in the United States. Both ical exemptions [3, 4]. Although this increase is likely to have of these analyses—which included data from 1993 through multiple causes, it was preceded by substantial declines in vac- 2004  and 2006 through 2011 —found an increase in non- cine-preventable diseases and coincided with publication of medical exemptions. In fact, the rate of increase was higher in the 2006 through 2011 period compared to the 1993 through a now retracted case series linking the measles, mumps, and 2004 period [3, 4]. Moreover, there was an association between rubella (MMR) vaccine with autism . The study was subse- the administrative ease of obtaining nonmedical exemptions quently found to be fraudulent, and the lead author was deprived and rates on nonmedical exemptions and pertussis . of his medical license by the UK General Medical Council . In recent years, the efforts to address the increase in nonmed- High rates of nonmedical exemptions have been associated ical exemptions have intensified. Professional medical associa- with higher rates of vaccine-preventable diseases [3, 7]. Local clus- tions such as American Academy of Pediatrics, the Centers of ters of vaccine exemptions geographically overlap with outbreaks Disease Control Prevention and Control, and state and local of pertussis [7, 8]. Moreover, nonmedical vaccine exemptions health departments have developed and disseminated resources to address vaccine hesitancy and refusal. The 2014–2015 measles Received 10 August 2017; editorial decision 31 October 2017; accepted 14 November 2017. outbreak that started in California, the so-called “Disneyland Correspondence: S. B. Omer, MBBS, MPH, PhD, 1518 Clifton Road, Atlanta, GA 30322 outbreak,” received considerable media attention, focusing on the (email@example.com). ® individual and community risk of vaccine refusal . Moreover, Open Forum Infectious Diseases © The Author(s) 2018. Published by Oxford University Press on behalf of Infectious Diseases several states have enacted legislation to increase administrative Society of America. This is an Open Access article distributed under the terms of the Creative scrutiny of requests to obtain nonmedical exemptions. Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/ by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any Although there have been a few recent reports of nonmed- medium, provided the original work is not altered or transformed in any way, and that the work ical exemption rates in various states, we are not aware of a is properly cited. For commercial re-use, please contact firstname.lastname@example.org. longitudinal analysis of recent national trends in nonmedical DOI: 10.1093/ofid/ofx244 Vaccine Exemptions and State-Level Policy • OFID • 1 Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofx244/4628136 by Ed 'DeepDyve' Gillespie user on 16 March 2018 exemption rates accounting for administrative ease of nonmed- 2012. Aer ini ft tial analysis of the data by school year, we chose to ical exemptions. In this study, we evaluated secular trends in stratify the data into year trend categories: one category includ- nonmedical exemptions in the United States between the 2011– ing years 2011–2012 and 2012–2013, and another category 2012 and 2015–2016 school years (inclusive) and evaluated the including years 2013–2014 through 2015–2016 (Table 2). association between exemption rates and ease of obtaining non- Over the course of the study period, 7 notable legislative medical exemptions and types of exemptions permitted. changes went into effect. Each legislative change during the study period led to nonmedical exemptions being more difficult METHODS to obtain (Table 3). All changes in exemption ease classification were reflected in the dataset by coding each individual year with In the United States, during the 2011–2012 through 2015–2016 the corresponding ease classification. California and Vermont school years, 48 states (excluding West Virginia and Mississippi) passed vaccine exemption legislation in 2016: California and the District of Colombia (DC) permitted nonmedical removed all nonmedical exemptions, and Vermont removed exemptions to vaccination requirements for school entry to kin- philosophical exemptions. Both of these bills went into effect dergarten (California passed a law in 2016 removing all nonmed- on July 1, 2016, which fell just outside of our study period. ical exemptions, which went into effect after the study period). We calculated nonmedical exemption rates using the number These state-level laws vary by administrative ease of obtaining of exemptions reported per year by states in the numerator and nonmedical exemptions. For this analysis, we obtained data com- dividing by the total number of reported enrolled kindergarten- piled yearly by the Centers for Disease Control and Prevention ers per year, by state. We then stratified the sample by type of (CDC) on the number of exemptions filed for incoming kinder- exemption allowed in states per year and ease of exemption cat- garteners [11–15]. We used publicly available documentation egory in states per year (Figure 1). For the 7 states that enacted on state-level vaccine policies for this analysis . A secondary new legislation in the study period, we changed ease and/or type reviewer verified each state’s vaccine exemption policy through of exemption category for subsequent years to reflect the provi- state legislative and health department websites. sions of the new law. We used t tests to compare mean nonmedi- We categorized states by the type of nonmedical exemption cal exemption rates between states by exemption type and policy. allowed—only religious exemptions or allowing religious and Using generalized estimating equations, we created negative philosophical exemptions—in addition to medical exemptions. binomial regression models to estimate (1) the average annual We also categorized states by ease of obtaining a nonmedical change in nonmedical exemption rates and (2) relative dif- exemption, using categories easy, medium, and difficult, adapted ferences in rates by state classification (ie, type of exemption from Omer et al  (Table 1). This method of classification was allowed; difficulty of exemption policy). All estimates were chosen because ease of exemption has been shown to be asso- generated as incidence rate ratios (IRRs), and they were com- ciated with higher rates of disease . In addition, we wanted puted for the full time period as well as stratified into 2 tem- our work to be comparable with other studies in this field, which poral periods of 2011–2012 through 2012–2013 school years have used the Omer et al  ease classifications, published in and 2013–2014 through 2015–2016 school years. The models accounted for correlations among repeated state-level meas- Table 1. Ease of Exemption Classification Standards ures during the study period, with state used as the clustering b c d term and assumed independence between states. In addition to Type of Requirement Easy Medium Difficult unadjusted models, we generated models adjusted for potential Form with parent signature required x X x confounding variables of income (10 categories), race (9 cat- Form available at school x Form available online x egories), education (5 categories), and population density. For Form available at health department only x x adjusted models, data for all covariates for each state and year of Parent personal statement required x x this analysis came from the US Census Bureau [18–23]. All data Parent visit to health department required x x analyses were conducted using SAS 9.4 (Cary, NC). Form must be notarized x To estimate the average annual change in nonmedical exemp- Signature of state official or religious leader x required tion rates, we estimated the IRR considering school year as the Yearly recertification required x primary predictor. Because we used state-level data in this ana- Adapted from Omer SB, Pan WK, Halsey NA, et al. Nonmedical exemptions to school lysis, institutional review board approval was not required. immunization requirements: secular trends and association of state policies with pertussis incidence. JAMA 2006;296:1757–63. b RESULTS States were classified as easy if they required at least 1 standard from the easy list and nothing from the medium or difficult list. c Over the full study period, a total of 245 state-years were States were classified as medium if they required at least 2 standards from the medium list in addition to things from the easy list. These states did not have requirements from included in the analysis. From 2011–2012 through 2015–2016, the difficult list. d 29 states and DC allowed for exemptions based on religious States were classified as difficult if they required at least 3 standards from the difficult list in addition to anything from the medium or easy list. beliefs, and 19 states allowed for both exemptions based on 2 • OFID • Omer et al Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofx244/4628136 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Table 2. State Nonmedical Exemption Rates, 2011–2012 and 2013–2015, Overall and Stratified in Two Trend Categories: Type of Exemption Permitted and Ease of Obtaining an Exemption Type of Incidence Rate Ratio, by Ease of State Exemption Annual Change in Exemption Rate Policy or Type of Exemption Permitted Permitted by Incidence Rate Ratio (95% CI) (95% CI) States For State-Years Average Nonmedical a b b Kindergarten (N) Exemption Rate (%) Unadjusted Adjusted Unadjusted Adjusted Overall 245 2.04% 1.09 (1.05–1.14) 1.11 (1.04–1.18) - - Years 2011–2012 98 1.75% 1.29 (1.07–1.55) 1.45 (1.15–1.83) - - Years 2013–2015 147 2.25% 0.98 (0.95–1.02) 1.00 (0.96, 1.05) - - Type of Exemption Permitted by States For Kindergarten Overall Only religious 149 1.27% 1.20 (1.13–1.27) 1.12 (1.02–1.24) Reference Reference exemption Philosophical 96 3.25% 1.03 (1.00–1.08) 1.07 (1.00–1.15) 2.41 (1.71–3.41) 2.15 (1.68–2.76) exemption Years 2011–2012 Only religious 60 1.01% 1.52 (1.56–2.01) 1.72 (1.27–2.34) Reference Reference exemption Philosophical 38 2.94% 1.17 (0.93–1.47) 1.17 (0.88–1.56) 2.91 (1.90–4.46) 2.53 (1.75–3.68) exemption Years 2013–2015 Only religious 90 1.45% 1.04 (1.00–1.07) 1.05 (1.01–1.11) Reference Reference exemption Philosophical 57 3.45% 0.95 (0.91–0.99) 0.99 (0.93–1.07) 2.38 (1.70–3.32) 2.06 (1.65–2.56) exemption Exemption Ease Categoried Overall Difficult 97 1.84% 1.10 (1.03–1.17) 1.38 (1.21–1.58) Reference Reference Medium 100 1.77% 1.08 (1.05–1.12) 0.94 (0.86–1.03) 0.86 (0.40–1.85) 1.08 (0.67–1.74) Easy 48 2.97% 1.16 (1.06–1.25) 1.26 (1.11–1.44) 1.08 (0.86–1.38) 1.22 (0.90–1.66) Years 2011–2012 Difficult 35 1.37% 0.99 (0.80–1.23) 1.07 (0.76–1.51) Reference Reference Medium 42 1.71% 1.32 (1.04–1.67) 1.51 (1.00–2.29) 1.12 (0.65–1.93) 2.24 (1.28–3.93) Easy 21 2.44% 1.59 (0.97–2.59) 1.37 (0.72–2.65) 1.26 (0.90–1.77) Years 2013–2015 Difficult 62 2.11% 1.04 (1.00–1.08) 1.16 (1.04–1.28) Reference Reference Medium 58 1.83% 0.99 (0.95–1.02) 1.05 (0.96–1.15) 1.33 (0.92–1.93) 1.29 (0.85–1.98) Easy 27 3.36% 0.95 (0.89–1.01) 0.89 (0.80–0.98) 1.15 (0.97–1.37) 1.15 (0.96–1.39) Abbreviation: CI, confidence interval. For unadjusted estimates. Adjusted for income (10 categories), race (9 categories), education (5 categories), and population density. States permitting only religious exemptions: AL, AK, CT, DE, DC, FL, GA, HI, IL, IN, IA, KS, KY, MD, MA, MO, MT, NE, NV, NH, NJ, NM, NY, NC, RI, SC, SD, TN, VA, WY. States permitting philosophical exemptions: AZ, AR, CA, CO, ID, LA, MA, MI, ND, OH, OK, OR, PA, TX, UT, VT, WA, WI. States with easy exemption policies: AZ, CO, HI, MD, ND, RI, VT, WI. States with medium exemption policies: DC, FL, ID, IN, KS, LA, ME, MA, MO, NV, NJ, NY, NC, OH, OK, PA, SD, TN. e f g h i j States with difficult exemption policies: AL, AK , AR, CA , CT , DE, GA, IL , IA, KY, MI , MN, MT, NE, NH, NM, OR , SC, TX, UT, VA, WA, WY. Medium exemption policy from 2011 to 2102. Easy exemption policy in 2011–2012. Easy exemption policy from 2011 to 2014. Medium exemption policy from 2011 to 2014. Medium exemption policy from 2011 to 2014. Easy exemption policy from 2011 to 2013. There is insufficient data to run a fully adjusted model. However, sufficient data exist to run the unadjusted model. religious beliefs and philosophical or personal belief reasons. to be reclassified. Of these 10 states, all but 1 enacted policy During the study period, 8 states were classified as having easy changes to make nonmedical exemptions harder to obtain. exemption policies, 18 states were classified as having medium From 2011–2012 through 2015–2016, the average non- exemption policies, and 23 states were classified as having dif- medical exemption rate increased to 2.04%, from the average ficult exemption policies during at least 1 year of the analysis of 1.58% reported in a similar analysis conducted in 2011 . (Table 1). Over the course of the study period, 10 states enacted e n Th onmedical exemption rate in states allowing philosophi- new legislative changes, leading to the states exemption policy cal and religious exemptions was 2.41 times as high as in states Vaccine Exemptions and State-Level Policy • OFID • 3 Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofx244/4628136 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Table 3. Legislative Changes from 2011 to 2016 That Impacted Nonmedical Exemption Ease Classifications State Year of Change Previous Classification New Classification Description California 2011 Easy Difficult New law requires signature from healthcare provider and counseling about vaccine benefits before exemption is granted Alaska 2013 Medium Difficult New law requires notarization of exemption form, and yearly recertification Oregon 2014 Easy Difficult New law requires education from healthcare provider or through online portal to receive exemption forms Illinois 2015 Medium Difficult Signature of healthcare provider is required on exemption form, with a parent personal statement Connecticut 2015 Medium Difficult Exemption form requires notarization Missouri 2015 Easy Medium Exemption form can only be obtained in person at the county or district health department Michigan 2015 Medium Difficult New law requires parent or guardian to attend education session at health department before exemption waiver is granted allowing only religious exemptions (IRR = 2.41; 95% confidence States classified as having an easy exemption policy had an interval [CI], 1.71–3.41). Although the overall average non- overall average nonmedical exemption rate of 2.97%, com- medical exemption rate was higher for the states allowing phil- pared to medium exemption policy states (1.77% nonmedical osophical exemptions than for the states allowing only religious exemption rate) and difficult exemption policy states (1.84% exemptions (3.25% to 1.27%, respectively), the average annual nonmedical exemption rate). However, the differences in state- rate increase for states allowing only religious exemptions level nonmedical exemption rates by exemption ease were not (IRR = 1.20; 95% CI, 1.13–1.27) was higher than the average significant (Table 1). annual rate increase for states allowing religious and philosoph- Although the overall nonmedical exemption rate was higher ical exemptions (IRR = 1.03; 95% CI, 1.00–1.08) (Table 1). in the later years of the study period (2.25% during 2013–2014 Overall Results (excluding Religious Exemptions Only Philosophical Exemptions Misissippi and West Virginia) Permitted 10 10 9 9 8 8 7 7 6 6 5 5 4 4 3 3 2 2 1 1 1 0 0 2011 2012 2013 2014 2015 2011 2012 2013 2014 2015 2011 2012 2013 2014 2015 Easy Exemption Policies Dicult Exemption Policies Medium Exemption Policies 6 6 3 3 2 2 1 1 1 0 0 2011 2012 2013 2014 2015 2011 2012 2013 2014 2015 2011 2012 2013 2014 2015 Figure 1. Overall means (and 95% confidence intervals) for the rate of nonmedical exemptions in the United States (excluding Mississippi and West Virginia, including the District of Columbia) by year from the 2011–2012 school year through the 2015–2016 school year, stratified by states that allow only religious exemptions, and by states that allow for both religious and philosophical exemptions, ease of exemption category. 4 • OFID • Omer et al Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofx244/4628136 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Nonmedical Exemption Rate (%) Nonmedical Exemption Rate (%) Nonmedical Exemption Rate (%) Nonmedical Exemption Rate (%) Nonmedical Exemption Rate (%) Nonmedical Exemption Rate (%) through 2015–2016 compared to 1.75% during 2011–2012 (and, therefore, from each child). The US Census Bureau data through 2012–2013), the average annual change in exemption indicate that 86% of the US population resides in these states rates leveled off to a null change in the later years. . Therefore, we believe our overall results to be generalizable to the US population. As already mentioned, we are not able DISCUSSION to quantitatively explore the causes for changes in exemption rates and most particularly the leveling off we have identified. Our study shows an increase in nonmedical exemptions through However, our comparisons of exemption rates between states the 2012–13 school year, which then plateaued. This is the first based upon the type of nonmedical exemption and administra- time since the late 1990s that we have seen such stabilization. tive procedures for granting exemptions provides vaccine pol- There are many potential explanations as to why this leveling icy approaches that are associated with exemption rates. off has occurred, including considerable efforts by medical and public health authorities to address vaccine hesitancy and media CONCLUSIONS attention focused on outbreaks of disease involving vaccine refus- als and nonmedical exemptions. The slight increase between Continued monitoring of exemption rates is critically impor- medium and difficult policy states could be attributed to the lag- tant to ensure that the plateau in rates identified by our study is time in enacting new laws to enforcing those laws on the school sustained. Improvements can also be made to within-state col- level. However, like other studies evaluating national phenomena, lection of exemption data to improve this surveillance system this study is not able to directly assess the specific factors that have moving forward. States will be well served by enacting legisla- affected changes in exemption rates. The risk of vaccine refusal tion that changes the balance of convenience in favor of vacci- and exemptions remains an important issue in many localities nation and away from nonmedical exemptions . where much higher exemption rates are seen. These clusters of Acknowledgments exemptions have been associated with outbreaks of pertussis and Disclaimer. e f Th under had no role in the design and conduct of the remain an important threat to the public’s health . study; collection, management, analysis, or interpretation of the data; or We found that states allowing philosophical and easy-to-ob- preparation, review, or approval of the manuscript. Financial support. This work was funded in part by National Institutes tain exemptions continue to be associated with higher rates of of Health grant K01AI106961 (to R. A. B.). exemptions [3, 4, 24]. In the wake of the recent Disneyland mea- Potential coni fl cts of interest. In the past, D. A. S. has served as a con- sles outbreak, California eliminated all nonmedical exemptions. sultant for Merck and conducted sponsored research for Crucell and Pfizer. e im Th pact of this policy, including its implementation, is not All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the con- yet apparent, because it will take many years of data to evalu- tent of the manuscript have been disclosed. ate postimplementation trends. e Th majority of states have not gone as far as to eliminate exemptions, because there is evidence References pointing to successes in curbing nonmedical exemptions by 1. Omer SB, Salmon DA, Orenstein WA, et al. Vaccine refusal, mandatory immu- nization, and the risks of vaccine-preventable diseases. N Engl J Med 2009; restricting exemptions rather than fully eliminating them [3, 4]. 360:1981–8. Our study suggests that eliminating philosophical exemptions 2. Salmon DA, Smith PJ, Navar AM, et al. Measuring immunization coverage among and making the exemption procedures more stringent may be preschool children: past, present, and future opportunities. Epidemiol Rev 2006; 28:27–40. useful policy approaches in states that are waiting to learn from 3. Omer SB, Pan WK, Halsey NA, et al. Nonmedical exemptions to school immuni- the California experience of eliminating nonmedical exemp- zation requirements: secular trends and association of state policies with pertussis incidence. JAMA 2006; 296:1757–63. tions or where such a policy approach is not politically feasible. 4. Omer SB, Richards JL, Ward M, Bednarczyk RA. 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Am J Epidemiol 2008; 168:1389–96. random sample, 3 states relied on voluntary response, and 6 9. Phadke VK, Bednarczyk RA, Salmon DA, Omer SB. Association between vaccine states relied on a mix of sampling methods to obtain exemption refusal and vaccine-preventable diseases in the United States: a review of measles and pertussis. JAMA 2016; 315:1149–58. rates . A breakdown of reporting for each state by year can 10. Zipprich J, Winter K, Hacker J, et al. Measles outbreak–California, December be found in the yearly MMWR [11–15] report that details vac- 2014-February 2015. MMWR Morb Mortal Wkly Rep 2015; 64:153–4. 11. Centers for Disease Control and Prevention (CDC). Vaccination coverage among cine coverage among children in kindergarten across the United children in kindergarten — United States, 2011–12 school year. MMWR Morb States, by school year. In some states, all schools report data Mortal Wkly Rep 2012; 61:647–52. 12. Seither R, Shaw L, Knighton CL, Greby SM, Stokley S. 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National, state, and selected local area l?pid=ACS_16_1YR_B01001&prodType=table Accessed 30 July 2016. vaccination coverage among children aged 19–35 months - United States, 2014. 19. American Community Survey - Race. 2010. Avalilable at: https://factfinder. MMWR Morb Mortal Wkly Rep 2015; 64:889–96. census.gov/faces/tableservices/jsf/pages/productview.xhtml?pid=ACS_15_5YR_ 26. Omer SB. How to Handle the Vaccine Skeptics. The New York Times, 2015. B02001&prodType=table Accessed 3 August 2016. February 6, 2015;Sect. The Opinion Pages. 6 • OFID • Omer et al Downloaded from https://academic.oup.com/ofid/article-abstract/5/2/ofx244/4628136 by Ed 'DeepDyve' Gillespie user on 16 March 2018
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