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An Evaluation of Voluntary 2-Dose Varicella Vaccination Coverage in New York City Public Schools Margaret K. Doll, MPH, Jennifer B. Rosen, MD, Stephanie R. Bialek, MD, MPH, Hiram Szeto, MS, and Christopher M. Zimmerman, MD, MPH
Varicella vaccine was licensed in the United States in 1995.1 In 1996, the US Advisory Committee on Immunization Practices recommended a single dose of varicella vaccine for routine use among all children aged 12 to 18 months and children aged 19 months to 12 years without a history of varicella disease; 2 doses were recommended for susceptible persons aged 13 years and older.1 Since licensure, varicella vaccination coverage in the United States has rapidly increased,2---4 and sharp decreases in the incidence of varicella disease and varicella-related morbidity and mortality have been observed.5---8 Outbreaks of varicella, however, continued to occur in the United States even among populations with high 1-dose coverage.9---12 In 2006, the Advisory Committee on Immunization Practices updated its recommendation to a universal 2-dose varicella vaccine childhood schedule, with a catch-up vaccination recommendation for susceptible children, adolescents, and adults with only 1 dose of varicella vaccine.13 Since the 2006 recommendation, 35 states and the District of Columbia have adopted 2-dose varicella school-entry requirements.14 As of the 2013 to 2014 school year, New York State was 1 of the 15 remaining states without a 2-dose requirement. New York State Public Health Law §2164 defines immunization requirements for all schools in New York State; since 1999, the law has required 1 dose of varicella for school entry for all students born on or after January 1, 1998, who do not have a physician-documented history of chickenpox or serological evidence of varicella immunity.15 In 2005, the state modified the law to include students born on or after January 1, 1994. With these rolling requirements, the regulation for 1 dose of varicella vaccine applied to all New York City students in kindergarten through 12th grade by the 2011 to 2012 school year.15
Objectives. We assessed coverage for 2-dose varicella vaccination, which is not required for school entry, among New York City public school students and examined characteristics associated with receipt of 2 doses. Methods. We measured receipt of either at least 1 or 2 doses of varicella vaccine among students aged 4 years and older in a sample of 336 public schools (n = 223 864 students) during the 2010 to 2011 school year. Data came from merged student vaccination records from 2 administrative data systems. We conducted multivariable regression to assess associations of age, gender, race/ ethnicity, and school location with 2-dose prevalence. Results. Coverage with at least 1 varicella dose was 96.2% (95% confidence interval [CI] = 96.2%, 96.3%); coverage with at least 2 doses was 64.8% (95% CI = 64.6%, 64.9%). Increasing student age, non-Hispanic White race/ethnicity, and attendance at school in Staten Island were associated with lower 2-dose coverage. Conclusions. A 2-dose varicella vaccine requirement for school entry would likely improve 2-dose coverage, eliminate coverage disparities, and prevent disease. (Am J Public Health. 2015;105:972–979. doi:10.2105/AJPH. 2014.302229)
In the absence of a 2-dose requirement, little is known regarding 2-dose varicella vaccination coverage in New York City public schools, which compose the largest public school system in the United States, with more than 1 million students.16 Two-dose varicella coverage estimates in this population are not available from current national survey data: the Centers for Disease Control and Prevention (CDC) kindergarten vaccination assessment survey does not provide varicella 2-dose estimates where the vaccine is not required for school entry,17---20 the National Immunization Survey of children aged 19 to 35 months only specifies coverage of 1 or more doses of varicella vaccine, 4 and the National Immunization Survey---Teen 2-dose coverage data for New York City is limited to children aged 13 to 17 years.21,22 Recent CDC sentinel data published for New York City children only assessed 2-dose varicella coverage among children at 7 years of age.14 We measured 2-dose varicella vaccination coverage in a sample of New York City public school students aged 4 years and older and assessed student characteristics associated with varicella vaccination.
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METHODS We assessed varicella vaccination coverage among students aged 4 years and older enrolled at 336 New York City public schools during the 2010 to 2011 school year. We selected public schools for inclusion that participated in a New York City Department of Health and Mental Hygiene sentinel varicella outbreak surveillance project, as determined by the school’s submission of either a varicella zero cases report, indicating that the school had no varicella cases, or a varicella case report in September or October 2010 to the health department.
Data Sources We ascertained student enrollment at sample schools and characteristics of the entire public school population in the New York City Department of Education’s Automate the Schools (ATS) administrative data base, a system that has tracked and maintained New York City public school student information since 1988.23 ATS records contain student demographic information, such as student last name,
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first name, date of birth, gender, address, phone number, and parent-reported race/ethnicity. ATS also records student-level immunization data, such as vaccine type and vaccination date for physician-documented vaccinations, and immunization exemption information, including a previous history of disease or evidence of serological immunity to varicella. Although ATS can record multiple varicella doses, schools are not required to report immunizations that are not mandated for school entry. We matched student records from ATS to records in the Citywide Immunization Registry (CIR), New York City’s Immunization Information System. The CIR is a population-based registry that directly loads birth certificate information for all children born in New York City from the city’s Bureau of Vital Statistics.24,25 In 1997, the city’s health code required providers to report immunizations given to all children younger than 8 years in the CIR; the requirement was expanded in 2005 to immunizations administered to all children younger than 19 years.26 Providers can enter vaccine type and date or document a history of varicella disease or serological testing. The CIR is an Immunization Information System sentinel site for the CDC and maintains high data quality completeness and timeliness: more than 90% of children younger than 5 years in the CIR have 2 or more immunizations, 92% of immunizations are reported within 1 month of administration, and 90% of providers report regularly to the CIR.27
Vaccination Assessment In March 2011, we merged immunization histories from ATS and the CIR for each student aged 4 years or older from the selected schools with a software program developed by the Department of Health and Mental Hygiene that used the Open Source ChoiceMaker Technology matching software version 2.5 (ChoiceMaker LLC, Princeton, NJ). The ChoiceMaker software is configured to use machine-learning methods to derive a probabilistic score for potential matches from a combination of student name, date of birth, gender, address, and phone number. The program considered CIR and ATS records with a matching threshold of 96% or higher a match and merged them. Previous assessment
comparing the New York City matching algorithm with CDC gold standard deduplication data found the algorithm to have a sensitivity of 95.6% and a specificity of 100%.25 For students with no CIR match, we ascertained immunization history from ATS records alone. We calculated student age and vaccination status as of February 1, 2011, the midpoint of the 2010 to 2011 school year. We considered varicella doses given more than 4 days prior to the first birthday or less than 28 days after the previous varicella dose invalid and excluded them. We defined students with at least 2 doses of varicella vaccine as having received 2 varicella doses. We investigated provider documentation of varicella disease or serological immunity to varicella from ATS or the CIR for students without any documented doses of varicella vaccine; we classified students with zero documented varicella vaccinations and evidence of immunity from either data source as having evidence of immunity from sources other than vaccination. On the basis of student age, we classified each student as eligible to receive 2 doses of varicella vaccine as part of (1) a routine schedule (students aged < 10 years), (2) a catch-up schedule (students aged 10---16 years), or (3) an alternative schedule (students aged ‡ 17 years). We based these age categories on the extrapolated age of students at the midpoint of the 2007 to 2008 school year, which followed the CDC Morbidity and Mortality Weekly Report June 2007 release of guidance regarding the updated 2-dose varicella recommendation.13 We used the midpoint of the 2007 to 2008 year for consistency with other calculations of student age in our analyses. We assessed tetanus, diphtheria, and acellular pertussis (Tdap) vaccination coverage in parallel to varicella coverage. We merged Tdap doses recorded in ATS or the CIR as of February 1, 2011, and we considered doses given more than 4 days prior to the seventh birthday invalid and excluded them from Tdap coverage analyses. We measured Tdap coverage as an indicator of missed opportunities for varicella vaccination, defined as the proportion of students aged 11 years and older with a Tdap vaccination who did not have 2 doses of varicella.
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Statistical Analyses We compared our sample with the total New York City public school population and assessed differences with v2 tests for categorical variables and t tests for continuous variables, with an a criterion level of 0.05. Among students in our sample, we assessed coverage with at least 1 dose of varicella vaccine and with 2 doses and the prevalence of students who were immune without vaccination. For each group, we used the Agresti---Coull interval procedure for binomial proportions to calculate 95% confidence intervals (CIs),28---30 and we used the v2 test statistic and an a criterion level of 0.05 to compare groups. We also separately evaluated 2-dose coverage for (1) students aged 4 to 6 years, for comparison with the CDC kindergarten vaccination assessment survey results for school years 2009 to 2010 and 2011 to 201218,19; (2) students aged 7 years, for comparison with the 2010 CDC sentinel New York City data for children of that age14; and (3) students aged 7 to 9 years, who were eligible for routine vaccination but were older than the recommended ages for routine administration of the second dose. We examined the median and range of school-level 2-dose varicella coverage stratified by school type (i.e., elementary, middle, or high school) and geographic location to identify potential pockets of undervaccinated students. We defined the type of school as elementary, if all of the school’s grades were between a minimum level of prekindergarten and a maximum of sixth grade; middle school, if all grades were between a minimum of sixth grade and a maximum of ninth grade; and high school, if all grades were between a minimum of ninth grade and a maximum of 12th grade. We defined schools with grades from more than 1 of these grade ranges as other. We used binomial regression with an identity link function to examine prevalence differences and 95% CIs for the association of gender, continuous age in years, race/ethnicity, and school location with our primary outcome of 2-dose varicella receipt.31,32 We chose an identity link function because we regarded absolute differences among our independent predictors as more meaningful in this context than relative measures (e.g., rate ratios or odds ratios). We performed univariable (crude) and
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multivariable (adjusted) analyses and conducted a complete case analysis in which we excluded students with missing data for any covariate from multivariable analysis. We planned sensitivity analyses with an inverse probability weighting design for variables with more than 10% missing values. We performed all analyses with SAS version 9.3 (SAS Institute Inc, Cary, NC).
RESULTS We identified 223 864 students aged 4 years and older enrolled at the 336 sample schools at the time of our analysis, representing 21% of the approximately 1.1 million New York City public school students; 89% of the sample students matched to a CIR immunization record. Race/ethnicity data were missing for fewer than 1% of students in the study population (n = 84); age, gender, and school location information were complete for all students. Maximum student age was 21 years; however, 99.6% of students were aged 18 years or younger. On average, students in the study were 1 year younger than the overall school population (Table 1). Our sample included a larger proportion of Asian/Pacific Islander and non-Hispanic White students, and a lower proportion of schools in Manhattan and the Bronx, than the overall New York City public school population (Table 1). Our sample had a greater percentage of elementary schools and lower percentage of high schools than the city’s public schools overall; the proportion of middle schools and schools in our other category were similar (Table 1). Coverage with at least 1 dose of varicella vaccination was 96.2% (95% CI = 96.2%, 96.3%), and 2-dose coverage was 64.8% (95% CI = 64.6%, 64.9%) among students aged 4 years and older. An additional 1.8% (95% CI = 1.8%, 1.9%) of students had evidence of immunity from sources other than vaccination. Students who were age eligible for routine 2-dose varicella vaccination were significantly more likely to have received both doses than students who were eligible for catch-up or alternative schedules (Figure 1). Students in the latter groups, however, were more likely than routine schedule students to have evidence of immunity from sources other than
vaccination: 3.1% (95% CI = 3.0%, 3.2%) of students on the catch-up schedule, 2.9% (95% CI = 2.6%, 3.3%) of those on an alternative schedule, and 0.5% (95% CI = 0.5%, 0.6%) of students on a routine schedule were immune without vaccination. Among students aged 4 to 6 years, 75.8% (95% CI = 75.4%, 76.2%) had received 2 doses of varicella vaccine; only 69.7% (95% CI = 69.4%, 70.1%) of students aged 7 to 9 years had received both doses. Two-dose coverage among children aged 7 years was similar to that of students aged 4 to 6 years, at 75.7% (95% CI = 75.2%, 76.3%). Tdap coverage was 83.9%, (95% CI = 83.7%, 84.2%) among students aged 11 years and older; of these, 39.1% (95% CI = 38.7%, 39.4%) had not received 2 doses of varicella vaccine. The medians and ranges of school-level 2-dose coverage are presented in Figure 2. In general, elementary schools had significantly higher 2-dose coverage than middle schools,
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and middle schools had significantly higher 2-dose coverage than high schools. Univariable and multivariable analyses revealed significant differences in the prevalence of students with 2 doses of varicella by age, race/ethnicity, and school borough location (Table 2). Increasing age, non-Hispanic White race/ethnicity, and attendance at a school in Staten Island were associated with lower 2-dose varicella coverage. Although 2-dose coverage estimates were higher at schools in Queens and Brooklyn, these locations still had lower 2-dose coverage estimates than schools in Manhattan and the Bronx.
DISCUSSION We assessed varicella vaccination coverage among a large cohort of New York City public school students aged 4 years and older in the absence of a 2-dose varicella school-entry requirement. Receipt of at least 1 dose of
TABLE 1—Comparison of Study Sample and All New York City Public Schools: 2010–2011 School Year Variable
Study Sample, No. (%) or Mean 6SD
All Public Schools, No. (%) or Mean 6SD
Studentsa Male gender
114 116 (51)
554 820 (51)
9.8 63.5
10.9 64.2
Asian/Pacific Islander
46 180* (21)
158 895 (15)
Non-Hispanic Black Hispanic
58 368* (26) 74 481* (33)
321 955 (30) 424 140 (39)
Non-Hispanic White
42 692* (19)
153 892 (14)
Brooklyn
82 673* (37)
326 227 (30)
Bronx
21 752* (10)
228 333 (21)
Manhattan
10 547* (5)
168 616 (16)
Queens
87 449* (39)
294 204 (27)
Staten Island
21 443* (10) Schoolsc
Age, y Race/ethnicityb
Location
63 593 (6)
School type Elementary Middle High Other
200* (60)
704 (43)
52 (15)
276 (17)
26* (8) 58 (17)
383 (24) 260 (16)
a
Sample size for the study, n = 223 864; for all public schools, n = 1 086 454. Does not sum to total; excludes other race/ethnicity and students with missing race/ethnicity data. c Sample size for the study, n = 336; for all public schools, n = 1623. *P < .001. b
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≥1-dose
100
2-dose
% of Children With Varicella Vaccine
90 80 70 60 50 40 30 20
Routine Schedule
Catch-up Schedule
Alternative Schedule
10
2-dose coverage: 72.4% (95% CI = 72.1%, 72.7%)
2-dose coverage: 59.4% (95% CI = 59.1%, 59.7%)
2-dose coverage: 32.3% (95% CI = 31.4%, 33.3%)
0 4
5
6
7
8
9
10
11
12
13
14
15
16
17
≥18
Student Age in Years Note. CI = confidence interval.
FIGURE 1—Examination of ‡ 1-dose and 2-dose varicella vaccine coverage, by student age in years and vaccination schedule eligibility in New York City public schools: 2010–2011 school year.
varicella vaccine (96.2%) was significantly higher than 2-dose coverage (64.8%). We found that student age was a meaningful predictor of 2-dose coverage levels, with higher coverage (72.4%) among students who were age eligible for vaccination under a routine schedule than among students eligible for 2 doses via a catch-up or alternative schedule; older students, however, were more likely to have evidence of immunity from sources other than vaccination. When we restricted our analyses to students aged 4 to 6 years, 2-dose coverage was 75.8%. These data demonstrate the relative success of the implementation of the 2-dose schedule among children for whom varicella is routinely recommended, even in the absence of a 2-dose school requirement. Varicella 2-dose coverage among students aged 4 to 6 years, however, was still lower than median 2-dose coverage levels reported among kindergartners in jurisdictions with 2-dose school-entry requirements in 2009 to 2010 (90.5%; range = 84.5%---99.7%)19
and in 2011 to 2012 (92.7%; range = 73.5%--99.2%),18 and well below the Healthy People 2020 goal of 95% (objective Immunization and Infectious Diseases 10.5).33 Compliance with immunization requirements among children in New York City public schools was 99% at the end of each of the school years 2010 to 2013, with 99% 2-dose measles---mumps---rubella coverage in June 2013 (J. B. R., unpublished data, February 7, 2014). In light of the effectiveness of New York State school-level immunization laws in achieving high 2-dose measles---mumps---rubella and 1-dose varicella vaccination coverage among New York City public school students, as well as the effectiveness of similar school requirements elsewhere,34---37 we expect that the adoption and enforcement of a 2-dose varicella vaccination school requirement would result in similarly high levels of 2-dose coverage. Achieving high 2-dose varicella coverage is important because of the demonstrated higher effectiveness of 2 doses than 1 in preventing
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varicella disease.38---42 A review of 1-dose vaccine effectiveness found it to be 84.5% effective (range = 44%---100%) in the prevention of varicella.43 Estimates of 2-dose effectiveness range from 93.9% to 98.3%,39,40,44---46 and the incremental vaccine effectiveness of 2 doses versus 1 dose of varicella was recently estimated as 63.6% (95% CI = 32.6%, 80.3%).46 These data support the potential benefit of increasing 2-dose coverage in our sample, even among age groups with relatively high 2-dose coverage. Furthermore, even among immune students who received 1 dose of varicella vaccine, receipt of a second varicella dose may be important: the protection afforded by 1 dose may wane over time,47---49 and increases in both the risk of breakthrough disease and disease severity have been documented with increasing time since administration of 1 dose of varicella vaccine.47,49 Although estimates of receipt of at least 1 dose of varicella vaccine were high among our sample, 2-dose coverage was significantly
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Percentage of Students with 2 Varicella Doses
Elementary Schools
Middle Schools
High Schools
100
80
60
40
20
0
28
69 10
75
18
Sample Size (No. Schools) 2 22 5 16 7
1
17
3
5
0
x
d an Isl en at St ns ee n Qu atta h an M lyn k oo Br x on d Br an Isl en at St ns ee n Qu atta h an M lyn k oo Br x on d Br an Isl en at St ns ee n Qu atta h an n kly
M
oo
Br
on
Br
School Location Note. IQR = interquartile range. We defined the type of school as elementary if all of the school’s grades were between a minimum level of prekindergarten to a maximum of sixth grade. Middle schools had all grades between a minimum level of sixth grade and a maximum of ninth grade, and high schools had grades between a minimum of ninth grade and a maximum of 12th grade. Schools with grades from more than 1 school type are not shown. The middle line in each box plot represents median 2-dose varicella coverage for each group; the diamond within the box represents mean 2-dose coverage. The upper and lower horizontal lines of the rectangle represent the IQR of 2-dose coverage, or the 75th and 25th percentiles, respectively. Error bars, or whiskers, represent 2-dose coverage values £ 1.5 times the IQR of the box plot; outliers that exceed 1.5 times the IQR are represented by dots. As a reference, the number of schools for each school type and geographic location is provided at the bottom of the figure.
FIGURE 2—Box plot of school 2-dose varicella coverage, by school type and geographic location in New York City public schools: 2010–2011 school year.
lower, potentially leaving undervaccinated students at risk for breakthrough varicella. Breakthrough varicella has been documented as a contributory factor in several prolonged school outbreaks of varicella9---12 because breakthrough disease is infectious, it can be difficult to recognize, and schools provide a high-intensity exposure setting for transmission.11,50 Achievement of high 2-dose coverage is also important to establish varicella herd immunity among the school population, to protect individuals who may be contraindicated to receive varicella vaccine. The 2-dose coverage level required to interrupt varicella transmission depends on a series of factors, including population mixing, the average number of secondary cases produced by 1 primary case, vaccine effectiveness, and 1-dose coverage.51 To our knowledge, the precise level of 2-dose
coverage required to establish varicella herd immunity has not yet been determined. Age remained a predictor of lower 2-dose varicella coverage even after adjustment for other variables. On average, students were 2.7% less likely to have 2 doses of varicella for each year of increasing age, after adjustment for other factors, with approximately 43% of students aged 10 years and older potentially undervaccinated. Although lower 2-dose coverage among older students may represent the failure to receive varicella catch-up vaccination, a plausible alternative is that some of the students who received 1 dose may have had a previous history of varicella disease, but we were unable to determine this from the data available. National Immunization Survey---Teen 2010 and 2011 data indicate that approximately one third of New York City
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adolescents aged 13 to 17 years have a history of varicella disease, and overall about 80% are protected against varicella because of either disease history or receipt of 2 doses of varicella vaccine.21,22 Among older students with fewer than 2 doses of varicella vaccine and no history of varicella disease, the medical visit in which a student receives a Tdap vaccination may present an ideal time for varicella catch-up. Despite this opportunity, we found that nearly 40% of students aged 11 years and older who had a Tdap vaccination had not received 2 doses of varicella vaccine, representing a potential missed opportunity for catch-up vaccination. School immunization requirements can be an effective strategy to promote high vaccination coverage, even for catch-up vaccines.37,52---55
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Insurance Plan public funding was linked to the CIR in 2006.24 By combining ATS and CIR data, however, we attempted to reduce gaps in underreporting of vaccinations and to capitalize on differential incentives and strengths of each system. However, we were still unable to ascertain a previous history of varicella disease among students with at least 1 dose of varicella vaccine. As a result, we may have overestimated the true proportion of students who were susceptible to varicella.
TABLE 2—Associations Between Age, Gender, Race/Ethnicity, and School Location and 2-Dose Varicella Vaccine Coverage Among New York City Public School Students: 2010–2011 School Year Variable
Crude PD (95% CI)
Adjusted PD (95% CI)
Age, 1-y increase
–2.57 (–2.62, –2.52)
–2.72 (–2.77, –2.67)
Male gender
–1.31 (–1.71, –0.91)
–0.98 (–1.36, –0.61)
Asian/Pacific Islander Non-Hispanic Black
13.91 (13.27, 14.55) 14.15 (13.54, 14.76)
14.36 (13.71, 15.00) 14.70 (14.08, 15.31)
Hispanic
15.70 (15.12, 16.28)
15.05 (14.46, 15.64)
Other
14.59 (12.51, 16.67)
10.57 (8.59, 12.55)
...
...
Brooklyn
19.23 (18.34, 20.12)
11.60 (10.70, 12.49)
Bronx
11.51 (10.77, 12.25)
8.98 (8.24, 9.72)
Manhattan Queens
17.77 (16.68, 18.86) 9.50 (8.76, 10.24)
13.35 (12.32, 14.38) 4.18 (3.44, 4.92)
...
...
Race/ethnicitya
Non-Hispanic White (Ref)
Conclusions
Location
Staten Island (Ref)
Note. CI = confidence interval; PD = prevalence difference. Sample size for crude PD, n = 223 864; for adjusted PD, n = 223 780. The Wald procedure was used to estimate 95% CIs. a Excluding 84 students with missing race/ethnicity data.
In addition to variation in 2-dose varicella vaccination coverage by age, we also detected meaningful differences in coverage by race/ ethnicity and school location. Lower varicella vaccination coverage places these subpopulations at risk for disease and may facilitate varicella transmission to other communities with higher coverage, as has been seen for measles.56 School-entry vaccination requirements, including regulations for varicella, have demonstrated success in increasing coverage among all students covered by the requirements, irrespective of student demographics or risk factors associated with low coverage,35,37 and in reducing disparities in coverage among subpopulations.57 Therefore, the adoption and enforcement of a 2-dose varicella mandate in New York State would not only be effective in improving 2-dose coverage in our overall sample, but would also likely address coverage disparities we detected among demographic subpopulations.
Limitations The students in our sample were not representative of New York City public school students with regard to race/ethnicity and school location, factors that were significantly associated with varicella 2-dose coverage in our analysis.
Thus, our coverage results may not be generalizable to all New York City public school students. Our estimate of 2-dose coverage among students aged 7 years was similar, however, to 2010 CDC sentinel data from New York City that assessed coverage among all New York City children aged 7 years (75.7% in our sample vs 77.6% in CDC data).14 Furthermore, because our sample comprised nearly one quarter of a million students—or one quarter of the New York City public school population—our results may have highly relevant implications regarding the potential for varicella transmission among New York City public school students. Because our analyses relied on documented vaccinations and evidence of varicella immunity, we may have underestimated varicella coverage and immunity levels. A second varicella dose may be less likely to be recorded in ATS because it is not required for school entry. Varicella doses may be less likely to be documented in the CIR if they were administered prior to enactment of legal requirements to report vaccinations or were funded by sources other than public funds, because health care facility accountability for administration of vaccine purchased via Vaccines For Children and New York State Children’s Health
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Since adoption of a routine 2-dose varicella vaccination schedule in 2006, varicella incidence and outbreaks in the United States have continued to decline.58,59 Data from the largest public school system in the United States demonstrated early success in implementation of the 2-dose schedule, even in the absence of a 2-dose school requirement. Although these findings are encouraging, 2-dose coverage was still well below recommended levels, leaving New York City public school students at higher risk of varicella disease and outbreaks. Our results underscore the need for a 2-dose varicella vaccination school-entry requirement to achieve near universal 2-dose coverage among New York City public school students and eliminate differences in coverage among subgroups. j
About the Authors At the time of the study, Margaret K. Doll, Jennifer B. Rosen, and Christopher M. Zimmerman were with the Bureau of Immunization, New York City Department of Health and Mental Hygiene, Queens, NY. Hiram Szeto is with the Bureau of School Health, New York City Department of Health and Mental Hygiene, Queens. Stephanie R. Bialek is with the National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA. Correspondence should be sent to Jennifer B. Rosen, MD, Bureau of Immunization, New York City Department of Health and Mental Hygiene, 42-09 28th St, FL 5, Queens, NY 11101 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link. This article was accepted July 24, 2014.
Contributors M. K. Doll helped develop the project, conducted analyses, and led the writing of the article. J. B. Rosen helped manage and develop the project. S. R. Bialek helped develop the project and critically revised the article. H. Szeto gathered the data. C. M. Zimmerman conceptualized and helped manage the project. All authors interpreted results and edited the article.
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Acknowledgments This research was funded by a grant from the CDC, with funding from the American Recovery and Reinvestment Act. We thank Luiz Homem de Mello, Vikki Papadouka, Alexandra Ternier, and Jane Zucker of the New York City Department of Health and Mental Hygiene and Scott Grytdal, Adriana Lopez, Mona Marin, and Jane Seward of the CDC National Center for Immunization and Respiratory Diseases. Note. The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the CDC.
Human Participant Protection No protocol approval was required because the study was considered to be part of routine program evaluation activities and not research.
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12. Tugwell BD, Lee LE, Gillette H, Lorber EM, Hedberg K, Cieslak PR. Chickenpox outbreak in a highly vaccinated school population. Pediatrics. 2004;113(3): 455---459. 13. Marin M, Güris D, Chaves SS, et al. Prevention of varicella: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2007;56(RR-4):1---40.
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16. New York City Dept of Education. About our schools. 2012. Available at: http://schools.nyc.gov/ AboutUs/schools/default.htm. Accessed December 10, 2012.
31. Petersen MR, Deddens JA. Re: “Easy SAS calculations for risk or prevalence ratios and differences.” Am J Epidemiol. 2006;163(12):1158---1159; author reply 1159---1161.
17. Centers for Disease Control and Prevention. Vaccination coverage among children in kindergarten—United States, 2012---13 school year. MMWR Morb Mortal Wkly Rep. 2013;62(30):607---612.
32. Spiegelman D, Hertzmark E. Easy SAS calculations for risk or prevalence ratios and differences. Am J Epidemiol. 2005;162(3):199---200.
18. Centers for Disease Control and Prevention. Vaccination coverage among children in kindergarten—United States, 2011---12 school year. MMWR Morb Mortal Wkly Rep. 2012;61(33):647---652. 19. Centers for Disease Control and Prevention. Vaccination coverage among children in kindergarten—United States, 2009---10 school year. MMWR Morb Mortal Wkly Rep. 2011;60(21):700---704.
4. Centers for Disease Control and Prevention. National Immunization Survey. Available at: http://www. cdc.gov/vaccines/stats-surv/nis/data/tables_2008. htm#overall. Accessed December 18, 2012.
20. Centers for Disease Control and Prevention. Vaccination coverage among children in kindergarten—United States, 2006---07 school year. MMWR Morb Mortal Wkly Rep. 2007;56(32):819---821.
5. Marin M, Meissner HC, Seward JF. Varicella prevention in the United States: a review of successes and challenges. Pediatrics. 2008;122(3):e744---e751.
21. Centers for Disease Control and Prevention. 2010 NIS---Teen vaccination coverage table data, overall coverage by state and selected area, vaccines routinely recommended during childhood (adolescent catch-up vaccines). 2011. Available at: http://www.cdc.gov/ vaccines/stats-surv/nisteen/data/tables_2010.htm#overall. Accessed December 18, 2012.
7. Davis MM, Patel MS, Gebremariam A. Decline in varicella-related hospitalizations and expenditures for children and adults after introduction of varicella vaccine in the United States. Pediatrics. 2004;114(3):786---792. 8. Nguyen HQ, Jumaan AO, Seward JF. Decline in mortality due to varicella after implementation of varicella vaccination in the United States. N Engl J Med. 2005;352(5):450---458. 9. Centers for Disease Control and Prevention. Outbreak of varicella among vaccinated children—Michigan, 2003. MMWR Morb Mortal Wkly Rep. 2004;53 (18):389---392.
29. Brown LD, Cai TT, DasGupta A. Interval estimation for a binomial proportion. Stat Sci. 2001;16(2)101---117.
15. New York State Dept of Health Bureau of Immunization. New York State immunization requirements for school entrance/attendance. 2012. Available at: http:// www.health.ny.gov/publications/2370.pdf. Accessed December 13, 2012.
3. US Dept of Health and Human Services. Healthy people 2010: increase routine vaccination coverage levels for adolescents. 2000. Available at: http://www. healthypeople.gov/2010/document/html/objectives/ 14-27.htm. Accessed June, 15, 2012.
6. Seward JF, Watson BM, Peterson CL, et al. Varicella disease after introduction of varicella vaccine in the United States, 1995---2000. JAMA. 2002;287(5): 606---611.
26. New York City Health Code. §11.07, Article 11, Reportable Diseases and Conditions. Chapter 24, Rules of the City of New York.
22. Centers for Disease Control and Prevention. 2011 NIS---Teen vaccination coverage table data, overall coverage by state and selected area, vaccines routinely recommended during childhood (adolescent catch-up vaccines). 2012. Available at: http://www.cdc.gov/ vaccines/stats-surv/nisteen/data/tables_2011.htm#overall. Accessed December 18, 2012. 23. Kumar KS. Higher education: a lesson in mainframe server automation. 2000. Available at: http://esj.com/ articles/2000/03/01/higher-education-a-lesson-inmainframe-server-automation.aspx. Accessed June 10, 2012.
10. Lee BR, Feaver SL, Miller CA, Hedberg CW, Ehresmann KR. An elementary school outbreak of varicella attributed to vaccine failure: policy implications. J Infect Dis. 2004;190(3):477---483.
24. Metroka AE, Hansen MA, Papadouka V, Zucker JR. Using an immunization information system to improve accountability for vaccines distributed through the Vaccines for Children program in New York City, 2005---2008. J Public Health Manag Pract. 2009;15(5): E13---E21.
11. Lopez AS, Guris D, Zimmerman L, et al. One dose of varicella vaccine does not prevent school outbreaks: is it time for a second dose? Pediatrics. 2006;117(6): e1070---e1077.
25. Papadouka V, Schaeffer P, Metroka A, et al. Integrating the New York citywide immunization registry and the childhood blood lead registry. J Public Health Manag Pract. 2004;Nov(suppl):S72---S80.
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33. US Dept of Health and Human Services. Healthy people 2020: immunization and infectious diseases. 2010. Available at: http://www.healthypeople.gov/2020/ topicsobjectives2020/objectiveslist.aspx?topicId=23. Accessed August 21, 2013. 34. Abrevaya J, Mulligan K. Effectiveness of state-level vaccination mandates: evidence from the varicella vaccine. J Health Econ. 2011;30(5):966---976. 35. Davis MM, Gaglia MA. Associations of daycare and school entry vaccination requirements with varicella immunization rates. Vaccine. 2005;23(23):3053---3060. 36. Kolasa MS, Klemperer-Johnson S, Papania MJ. Progress toward implementation of a second-dose measles immunization requirement for all schoolchildren in the United States. J Infect Dis. 2004;189(suppl 1):S98---S103. 37. Averhoff F, Linton L, Peddecord KM, Edwards C, Wang W, Fishbein D. A middle school immunization law rapidly and substantially increases immunization coverage among adolescents. Am J Public Health. 2004;94 (6):978---984. 38. Brisson M, Melkonyan G, Drolet M, De Serres G, Thibeault R, De Wals P. Modeling the impact of one- and two-dose varicella vaccination on the epidemiology of varicella and zoster. Vaccine. 2010;28(19):3385---3397. 39. Kuter B, Matthews H, Shinefield H, et al. Ten year follow-up of healthy children who received one or two injections of varicella vaccine. Pediatr Infect Dis J. 2004; 23(2):132---137. 40. Shapiro ED, Vazquez M, Esposito D, et al. Effectiveness of 2 doses of varicella vaccine in children. J Infect Dis. 2011;203(3):312---315. 41. Macartney K. Prevention of varicella: time for twodose vaccination. Lancet. 2014;383(9925):1276---1277. 42. Prymula R, Bergsaker MR, Esposito S, et al. Protection against varicella with two doses of combined measles-mumps-rubella-varicella vaccine versus one dose of monovalent varicella vaccine: a multicentre, observer-blind, randomised, controlled trial. Lancet. 2014;383(9925):1313---1324.
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43. Seward JF, Marin M, Vazquez M. Varicella vaccine effectiveness in the US vaccination program: a review. J Infect Dis. 2008;197(suppl 2):S82---S89. 44. Spackova M, Wiese-Posselt M, Dehnert M, MatysiakKlose D, Heininger U, Siedler A. Comparative varicella vaccine effectiveness during outbreaks in day-care centres. Vaccine. 2010;28(3):686---691. 45. Cenoz MG, Martinez-Artola V, Guevara M, Ezpeleta C, Barricarte A, Castilla J. Effectiveness of one and two doses of varicella vaccine in preventing laboratoryconfirmed cases in children in Navarre, Spain. Hum Vaccin Immunother. 2013;9(5):1172---1176. 46. Thomas CA, Shwe T, Bixler D, et al. Two-dose varicella vaccine effectiveness and rash severity in outbreaks of varicella among public school students [published online ahead of print June 6, 2014]. Pediatr Infect Dis J. 2014. 47. Chaves SS, Gargiullo P, Zhang JX, et al. Loss of vaccine-induced immunity to varicella over time. N Engl J Med. 2007;356(11):1121---1129. 48. Vázquez M, LaRussa PS, Gershon AA, et al. Effectiveness over time of varicella vaccine. JAMA. 2004; 291(7):851---855. 49. Galil K, Lee B, Strine T, et al. Outbreak of varicella at a day-care center despite vaccination. N Engl J Med. 2002;347(24):1909---1915. 50. Seward JF, Zhang JX, Maupin TJ, Mascola L, Jumaan AO. Contagiousness of varicella in vaccinated cases: a household contact study. JAMA. 2004;292(6): 704---708. 51. Anderson RM, May RM. Immunisation and herd immunity. Lancet. 1990;335(8690);641---645. 52. Wilson TR, Fishbein DB, Ellis PA, Edlavitch SA. The impact of a school entry law on adolescent immunization rates. J Adolesc Health. 2005;37(6):511---516. 53. Bugenske E, Stokley S, Kennedy A, Dorell C. Middle school vaccination requirements and adolescent vaccination coverage. Pediatrics. 2012;129(6):1056---1063. 54. Centers for Disease Control and Prevention. Effectiveness of a seventh grade school entry vaccination requirement—statewide and Orange County, Florida, 1997---1998. MMWR Morb Mortal Wkly Rep. 1998; 47(34):711---715. 55. Olshen Kharbanda E, Stockwell MS, Colgrove J, Natarajan K, Rickert VI. Changes in Tdap and MCV4 vaccine coverage following enactment of a statewide requirement of Tdap vaccination for entry into sixth grade. Am J Public Health. 2010;100(9):1635---1640. 56. Santoli JM, Setia S, Rodewald LE, O’Mara D, Gallo B, Brink E. Immunization pockets of need: science and practice. Am J Prev Med. 2000;19(3, suppl):89---98. 57. Morita JY, Ramirez E, Trick WE. Effect of a schoolentry vaccination requirement on racial and ethnic disparities in hepatitis B immunization coverage levels among public school students. Pediatrics. 2008;121(3): e547---e552. 58. Bialek SR, Perella D, Zhang J, et al. Impact of a routine two-dose varicella vaccination program on varicella epidemiology. Pediatrics. 2013;132(5):e1134---e1140. 59. Centers for Disease Control and Prevention. Evolution of varicella surveillance—selected states, 2000--2010. MMWR Morb Mortal Wkly Rep. 2012;61(32): 609---612.
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An Evaluation of Voluntary 2-Dose Varicella Vaccination Coverage in New York City Public Schools Margaret K. Doll, MPH, Jennifer B. Rosen, MD, Stephanie R. Bialek, MD, MPH, Hiram Szeto, MS, and Christopher M. Zimmerman, MD, MPH
Varicella vaccine was licensed in the United States in 1995.1 In 1996, the US Advisory Committee on Immunization Practices recommended a single dose of varicella vaccine for routine use among all children aged 12 to 18 months and children aged 19 months to 12 years without a history of varicella disease; 2 doses were recommended for susceptible persons aged 13 years and older.1 Since licensure, varicella vaccination coverage in the United States has rapidly increased,2---4 and sharp decreases in the incidence of varicella disease and varicella-related morbidity and mortality have been observed.5---8 Outbreaks of varicella, however, continued to occur in the United States even among populations with high 1-dose coverage.9---12 In 2006, the Advisory Committee on Immunization Practices updated its recommendation to a universal 2-dose varicella vaccine childhood schedule, with a catch-up vaccination recommendation for susceptible children, adolescents, and adults with only 1 dose of varicella vaccine.13 Since the 2006 recommendation, 35 states and the District of Columbia have adopted 2-dose varicella school-entry requirements.14 As of the 2013 to 2014 school year, New York State was 1 of the 15 remaining states without a 2-dose requirement. New York State Public Health Law §2164 defines immunization requirements for all schools in New York State; since 1999, the law has required 1 dose of varicella for school entry for all students born on or after January 1, 1998, who do not have a physician-documented history of chickenpox or serological evidence of varicella immunity.15 In 2005, the state modified the law to include students born on or after January 1, 1994. With these rolling requirements, the regulation for 1 dose of varicella vaccine applied to all New York City students in kindergarten through 12th grade by the 2011 to 2012 school year.15
Objectives. We assessed coverage for 2-dose varicella vaccination, which is not required for school entry, among New York City public school students and examined characteristics associated with receipt of 2 doses. Methods. We measured receipt of either at least 1 or 2 doses of varicella vaccine among students aged 4 years and older in a sample of 336 public schools (n = 223 864 students) during the 2010 to 2011 school year. Data came from merged student vaccination records from 2 administrative data systems. We conducted multivariable regression to assess associations of age, gender, race/ ethnicity, and school location with 2-dose prevalence. Results. Coverage with at least 1 varicella dose was 96.2% (95% confidence interval [CI] = 96.2%, 96.3%); coverage with at least 2 doses was 64.8% (95% CI = 64.6%, 64.9%). Increasing student age, non-Hispanic White race/ethnicity, and attendance at school in Staten Island were associated with lower 2-dose coverage. Conclusions. A 2-dose varicella vaccine requirement for school entry would likely improve 2-dose coverage, eliminate coverage disparities, and prevent disease. (Am J Public Health. 2015;105:972–979. doi:10.2105/AJPH. 2014.302229)
In the absence of a 2-dose requirement, little is known regarding 2-dose varicella vaccination coverage in New York City public schools, which compose the largest public school system in the United States, with more than 1 million students.16 Two-dose varicella coverage estimates in this population are not available from current national survey data: the Centers for Disease Control and Prevention (CDC) kindergarten vaccination assessment survey does not provide varicella 2-dose estimates where the vaccine is not required for school entry,17---20 the National Immunization Survey of children aged 19 to 35 months only specifies coverage of 1 or more doses of varicella vaccine, 4 and the National Immunization Survey---Teen 2-dose coverage data for New York City is limited to children aged 13 to 17 years.21,22 Recent CDC sentinel data published for New York City children only assessed 2-dose varicella coverage among children at 7 years of age.14 We measured 2-dose varicella vaccination coverage in a sample of New York City public school students aged 4 years and older and assessed student characteristics associated with varicella vaccination.
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METHODS We assessed varicella vaccination coverage among students aged 4 years and older enrolled at 336 New York City public schools during the 2010 to 2011 school year. We selected public schools for inclusion that participated in a New York City Department of Health and Mental Hygiene sentinel varicella outbreak surveillance project, as determined by the school’s submission of either a varicella zero cases report, indicating that the school had no varicella cases, or a varicella case report in September or October 2010 to the health department.
Data Sources We ascertained student enrollment at sample schools and characteristics of the entire public school population in the New York City Department of Education’s Automate the Schools (ATS) administrative data base, a system that has tracked and maintained New York City public school student information since 1988.23 ATS records contain student demographic information, such as student last name,
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first name, date of birth, gender, address, phone number, and parent-reported race/ethnicity. ATS also records student-level immunization data, such as vaccine type and vaccination date for physician-documented vaccinations, and immunization exemption information, including a previous history of disease or evidence of serological immunity to varicella. Although ATS can record multiple varicella doses, schools are not required to report immunizations that are not mandated for school entry. We matched student records from ATS to records in the Citywide Immunization Registry (CIR), New York City’s Immunization Information System. The CIR is a population-based registry that directly loads birth certificate information for all children born in New York City from the city’s Bureau of Vital Statistics.24,25 In 1997, the city’s health code required providers to report immunizations given to all children younger than 8 years in the CIR; the requirement was expanded in 2005 to immunizations administered to all children younger than 19 years.26 Providers can enter vaccine type and date or document a history of varicella disease or serological testing. The CIR is an Immunization Information System sentinel site for the CDC and maintains high data quality completeness and timeliness: more than 90% of children younger than 5 years in the CIR have 2 or more immunizations, 92% of immunizations are reported within 1 month of administration, and 90% of providers report regularly to the CIR.27
Vaccination Assessment In March 2011, we merged immunization histories from ATS and the CIR for each student aged 4 years or older from the selected schools with a software program developed by the Department of Health and Mental Hygiene that used the Open Source ChoiceMaker Technology matching software version 2.5 (ChoiceMaker LLC, Princeton, NJ). The ChoiceMaker software is configured to use machine-learning methods to derive a probabilistic score for potential matches from a combination of student name, date of birth, gender, address, and phone number. The program considered CIR and ATS records with a matching threshold of 96% or higher a match and merged them. Previous assessment
comparing the New York City matching algorithm with CDC gold standard deduplication data found the algorithm to have a sensitivity of 95.6% and a specificity of 100%.25 For students with no CIR match, we ascertained immunization history from ATS records alone. We calculated student age and vaccination status as of February 1, 2011, the midpoint of the 2010 to 2011 school year. We considered varicella doses given more than 4 days prior to the first birthday or less than 28 days after the previous varicella dose invalid and excluded them. We defined students with at least 2 doses of varicella vaccine as having received 2 varicella doses. We investigated provider documentation of varicella disease or serological immunity to varicella from ATS or the CIR for students without any documented doses of varicella vaccine; we classified students with zero documented varicella vaccinations and evidence of immunity from either data source as having evidence of immunity from sources other than vaccination. On the basis of student age, we classified each student as eligible to receive 2 doses of varicella vaccine as part of (1) a routine schedule (students aged < 10 years), (2) a catch-up schedule (students aged 10---16 years), or (3) an alternative schedule (students aged ‡ 17 years). We based these age categories on the extrapolated age of students at the midpoint of the 2007 to 2008 school year, which followed the CDC Morbidity and Mortality Weekly Report June 2007 release of guidance regarding the updated 2-dose varicella recommendation.13 We used the midpoint of the 2007 to 2008 year for consistency with other calculations of student age in our analyses. We assessed tetanus, diphtheria, and acellular pertussis (Tdap) vaccination coverage in parallel to varicella coverage. We merged Tdap doses recorded in ATS or the CIR as of February 1, 2011, and we considered doses given more than 4 days prior to the seventh birthday invalid and excluded them from Tdap coverage analyses. We measured Tdap coverage as an indicator of missed opportunities for varicella vaccination, defined as the proportion of students aged 11 years and older with a Tdap vaccination who did not have 2 doses of varicella.
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Statistical Analyses We compared our sample with the total New York City public school population and assessed differences with v2 tests for categorical variables and t tests for continuous variables, with an a criterion level of 0.05. Among students in our sample, we assessed coverage with at least 1 dose of varicella vaccine and with 2 doses and the prevalence of students who were immune without vaccination. For each group, we used the Agresti---Coull interval procedure for binomial proportions to calculate 95% confidence intervals (CIs),28---30 and we used the v2 test statistic and an a criterion level of 0.05 to compare groups. We also separately evaluated 2-dose coverage for (1) students aged 4 to 6 years, for comparison with the CDC kindergarten vaccination assessment survey results for school years 2009 to 2010 and 2011 to 201218,19; (2) students aged 7 years, for comparison with the 2010 CDC sentinel New York City data for children of that age14; and (3) students aged 7 to 9 years, who were eligible for routine vaccination but were older than the recommended ages for routine administration of the second dose. We examined the median and range of school-level 2-dose varicella coverage stratified by school type (i.e., elementary, middle, or high school) and geographic location to identify potential pockets of undervaccinated students. We defined the type of school as elementary, if all of the school’s grades were between a minimum level of prekindergarten and a maximum of sixth grade; middle school, if all grades were between a minimum of sixth grade and a maximum of ninth grade; and high school, if all grades were between a minimum of ninth grade and a maximum of 12th grade. We defined schools with grades from more than 1 of these grade ranges as other. We used binomial regression with an identity link function to examine prevalence differences and 95% CIs for the association of gender, continuous age in years, race/ethnicity, and school location with our primary outcome of 2-dose varicella receipt.31,32 We chose an identity link function because we regarded absolute differences among our independent predictors as more meaningful in this context than relative measures (e.g., rate ratios or odds ratios). We performed univariable (crude) and
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multivariable (adjusted) analyses and conducted a complete case analysis in which we excluded students with missing data for any covariate from multivariable analysis. We planned sensitivity analyses with an inverse probability weighting design for variables with more than 10% missing values. We performed all analyses with SAS version 9.3 (SAS Institute Inc, Cary, NC).
RESULTS We identified 223 864 students aged 4 years and older enrolled at the 336 sample schools at the time of our analysis, representing 21% of the approximately 1.1 million New York City public school students; 89% of the sample students matched to a CIR immunization record. Race/ethnicity data were missing for fewer than 1% of students in the study population (n = 84); age, gender, and school location information were complete for all students. Maximum student age was 21 years; however, 99.6% of students were aged 18 years or younger. On average, students in the study were 1 year younger than the overall school population (Table 1). Our sample included a larger proportion of Asian/Pacific Islander and non-Hispanic White students, and a lower proportion of schools in Manhattan and the Bronx, than the overall New York City public school population (Table 1). Our sample had a greater percentage of elementary schools and lower percentage of high schools than the city’s public schools overall; the proportion of middle schools and schools in our other category were similar (Table 1). Coverage with at least 1 dose of varicella vaccination was 96.2% (95% CI = 96.2%, 96.3%), and 2-dose coverage was 64.8% (95% CI = 64.6%, 64.9%) among students aged 4 years and older. An additional 1.8% (95% CI = 1.8%, 1.9%) of students had evidence of immunity from sources other than vaccination. Students who were age eligible for routine 2-dose varicella vaccination were significantly more likely to have received both doses than students who were eligible for catch-up or alternative schedules (Figure 1). Students in the latter groups, however, were more likely than routine schedule students to have evidence of immunity from sources other than
vaccination: 3.1% (95% CI = 3.0%, 3.2%) of students on the catch-up schedule, 2.9% (95% CI = 2.6%, 3.3%) of those on an alternative schedule, and 0.5% (95% CI = 0.5%, 0.6%) of students on a routine schedule were immune without vaccination. Among students aged 4 to 6 years, 75.8% (95% CI = 75.4%, 76.2%) had received 2 doses of varicella vaccine; only 69.7% (95% CI = 69.4%, 70.1%) of students aged 7 to 9 years had received both doses. Two-dose coverage among children aged 7 years was similar to that of students aged 4 to 6 years, at 75.7% (95% CI = 75.2%, 76.3%). Tdap coverage was 83.9%, (95% CI = 83.7%, 84.2%) among students aged 11 years and older; of these, 39.1% (95% CI = 38.7%, 39.4%) had not received 2 doses of varicella vaccine. The medians and ranges of school-level 2-dose coverage are presented in Figure 2. In general, elementary schools had significantly higher 2-dose coverage than middle schools,
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and middle schools had significantly higher 2-dose coverage than high schools. Univariable and multivariable analyses revealed significant differences in the prevalence of students with 2 doses of varicella by age, race/ethnicity, and school borough location (Table 2). Increasing age, non-Hispanic White race/ethnicity, and attendance at a school in Staten Island were associated with lower 2-dose varicella coverage. Although 2-dose coverage estimates were higher at schools in Queens and Brooklyn, these locations still had lower 2-dose coverage estimates than schools in Manhattan and the Bronx.
DISCUSSION We assessed varicella vaccination coverage among a large cohort of New York City public school students aged 4 years and older in the absence of a 2-dose varicella school-entry requirement. Receipt of at least 1 dose of
TABLE 1—Comparison of Study Sample and All New York City Public Schools: 2010–2011 School Year Variable
Study Sample, No. (%) or Mean 6SD
All Public Schools, No. (%) or Mean 6SD
Studentsa Male gender
114 116 (51)
554 820 (51)
9.8 63.5
10.9 64.2
Asian/Pacific Islander
46 180* (21)
158 895 (15)
Non-Hispanic Black Hispanic
58 368* (26) 74 481* (33)
321 955 (30) 424 140 (39)
Non-Hispanic White
42 692* (19)
153 892 (14)
Brooklyn
82 673* (37)
326 227 (30)
Bronx
21 752* (10)
228 333 (21)
Manhattan
10 547* (5)
168 616 (16)
Queens
87 449* (39)
294 204 (27)
Staten Island
21 443* (10) Schoolsc
Age, y Race/ethnicityb
Location
63 593 (6)
School type Elementary Middle High Other
200* (60)
704 (43)
52 (15)
276 (17)
26* (8) 58 (17)
383 (24) 260 (16)
a
Sample size for the study, n = 223 864; for all public schools, n = 1 086 454. Does not sum to total; excludes other race/ethnicity and students with missing race/ethnicity data. c Sample size for the study, n = 336; for all public schools, n = 1623. *P < .001. b
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≥1-dose
100
2-dose
% of Children With Varicella Vaccine
90 80 70 60 50 40 30 20
Routine Schedule
Catch-up Schedule
Alternative Schedule
10
2-dose coverage: 72.4% (95% CI = 72.1%, 72.7%)
2-dose coverage: 59.4% (95% CI = 59.1%, 59.7%)
2-dose coverage: 32.3% (95% CI = 31.4%, 33.3%)
0 4
5
6
7
8
9
10
11
12
13
14
15
16
17
≥18
Student Age in Years Note. CI = confidence interval.
FIGURE 1—Examination of ‡ 1-dose and 2-dose varicella vaccine coverage, by student age in years and vaccination schedule eligibility in New York City public schools: 2010–2011 school year.
varicella vaccine (96.2%) was significantly higher than 2-dose coverage (64.8%). We found that student age was a meaningful predictor of 2-dose coverage levels, with higher coverage (72.4%) among students who were age eligible for vaccination under a routine schedule than among students eligible for 2 doses via a catch-up or alternative schedule; older students, however, were more likely to have evidence of immunity from sources other than vaccination. When we restricted our analyses to students aged 4 to 6 years, 2-dose coverage was 75.8%. These data demonstrate the relative success of the implementation of the 2-dose schedule among children for whom varicella is routinely recommended, even in the absence of a 2-dose school requirement. Varicella 2-dose coverage among students aged 4 to 6 years, however, was still lower than median 2-dose coverage levels reported among kindergartners in jurisdictions with 2-dose school-entry requirements in 2009 to 2010 (90.5%; range = 84.5%---99.7%)19
and in 2011 to 2012 (92.7%; range = 73.5%--99.2%),18 and well below the Healthy People 2020 goal of 95% (objective Immunization and Infectious Diseases 10.5).33 Compliance with immunization requirements among children in New York City public schools was 99% at the end of each of the school years 2010 to 2013, with 99% 2-dose measles---mumps---rubella coverage in June 2013 (J. B. R., unpublished data, February 7, 2014). In light of the effectiveness of New York State school-level immunization laws in achieving high 2-dose measles---mumps---rubella and 1-dose varicella vaccination coverage among New York City public school students, as well as the effectiveness of similar school requirements elsewhere,34---37 we expect that the adoption and enforcement of a 2-dose varicella vaccination school requirement would result in similarly high levels of 2-dose coverage. Achieving high 2-dose varicella coverage is important because of the demonstrated higher effectiveness of 2 doses than 1 in preventing
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varicella disease.38---42 A review of 1-dose vaccine effectiveness found it to be 84.5% effective (range = 44%---100%) in the prevention of varicella.43 Estimates of 2-dose effectiveness range from 93.9% to 98.3%,39,40,44---46 and the incremental vaccine effectiveness of 2 doses versus 1 dose of varicella was recently estimated as 63.6% (95% CI = 32.6%, 80.3%).46 These data support the potential benefit of increasing 2-dose coverage in our sample, even among age groups with relatively high 2-dose coverage. Furthermore, even among immune students who received 1 dose of varicella vaccine, receipt of a second varicella dose may be important: the protection afforded by 1 dose may wane over time,47---49 and increases in both the risk of breakthrough disease and disease severity have been documented with increasing time since administration of 1 dose of varicella vaccine.47,49 Although estimates of receipt of at least 1 dose of varicella vaccine were high among our sample, 2-dose coverage was significantly
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Percentage of Students with 2 Varicella Doses
Elementary Schools
Middle Schools
High Schools
100
80
60
40
20
0
28
69 10
75
18
Sample Size (No. Schools) 2 22 5 16 7
1
17
3
5
0
x
d an Isl en at St ns ee n Qu atta h an M lyn k oo Br x on d Br an Isl en at St ns ee n Qu atta h an M lyn k oo Br x on d Br an Isl en at St ns ee n Qu atta h an n kly
M
oo
Br
on
Br
School Location Note. IQR = interquartile range. We defined the type of school as elementary if all of the school’s grades were between a minimum level of prekindergarten to a maximum of sixth grade. Middle schools had all grades between a minimum level of sixth grade and a maximum of ninth grade, and high schools had grades between a minimum of ninth grade and a maximum of 12th grade. Schools with grades from more than 1 school type are not shown. The middle line in each box plot represents median 2-dose varicella coverage for each group; the diamond within the box represents mean 2-dose coverage. The upper and lower horizontal lines of the rectangle represent the IQR of 2-dose coverage, or the 75th and 25th percentiles, respectively. Error bars, or whiskers, represent 2-dose coverage values £ 1.5 times the IQR of the box plot; outliers that exceed 1.5 times the IQR are represented by dots. As a reference, the number of schools for each school type and geographic location is provided at the bottom of the figure.
FIGURE 2—Box plot of school 2-dose varicella coverage, by school type and geographic location in New York City public schools: 2010–2011 school year.
lower, potentially leaving undervaccinated students at risk for breakthrough varicella. Breakthrough varicella has been documented as a contributory factor in several prolonged school outbreaks of varicella9---12 because breakthrough disease is infectious, it can be difficult to recognize, and schools provide a high-intensity exposure setting for transmission.11,50 Achievement of high 2-dose coverage is also important to establish varicella herd immunity among the school population, to protect individuals who may be contraindicated to receive varicella vaccine. The 2-dose coverage level required to interrupt varicella transmission depends on a series of factors, including population mixing, the average number of secondary cases produced by 1 primary case, vaccine effectiveness, and 1-dose coverage.51 To our knowledge, the precise level of 2-dose
coverage required to establish varicella herd immunity has not yet been determined. Age remained a predictor of lower 2-dose varicella coverage even after adjustment for other variables. On average, students were 2.7% less likely to have 2 doses of varicella for each year of increasing age, after adjustment for other factors, with approximately 43% of students aged 10 years and older potentially undervaccinated. Although lower 2-dose coverage among older students may represent the failure to receive varicella catch-up vaccination, a plausible alternative is that some of the students who received 1 dose may have had a previous history of varicella disease, but we were unable to determine this from the data available. National Immunization Survey---Teen 2010 and 2011 data indicate that approximately one third of New York City
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adolescents aged 13 to 17 years have a history of varicella disease, and overall about 80% are protected against varicella because of either disease history or receipt of 2 doses of varicella vaccine.21,22 Among older students with fewer than 2 doses of varicella vaccine and no history of varicella disease, the medical visit in which a student receives a Tdap vaccination may present an ideal time for varicella catch-up. Despite this opportunity, we found that nearly 40% of students aged 11 years and older who had a Tdap vaccination had not received 2 doses of varicella vaccine, representing a potential missed opportunity for catch-up vaccination. School immunization requirements can be an effective strategy to promote high vaccination coverage, even for catch-up vaccines.37,52---55
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Insurance Plan public funding was linked to the CIR in 2006.24 By combining ATS and CIR data, however, we attempted to reduce gaps in underreporting of vaccinations and to capitalize on differential incentives and strengths of each system. However, we were still unable to ascertain a previous history of varicella disease among students with at least 1 dose of varicella vaccine. As a result, we may have overestimated the true proportion of students who were susceptible to varicella.
TABLE 2—Associations Between Age, Gender, Race/Ethnicity, and School Location and 2-Dose Varicella Vaccine Coverage Among New York City Public School Students: 2010–2011 School Year Variable
Crude PD (95% CI)
Adjusted PD (95% CI)
Age, 1-y increase
–2.57 (–2.62, –2.52)
–2.72 (–2.77, –2.67)
Male gender
–1.31 (–1.71, –0.91)
–0.98 (–1.36, –0.61)
Asian/Pacific Islander Non-Hispanic Black
13.91 (13.27, 14.55) 14.15 (13.54, 14.76)
14.36 (13.71, 15.00) 14.70 (14.08, 15.31)
Hispanic
15.70 (15.12, 16.28)
15.05 (14.46, 15.64)
Other
14.59 (12.51, 16.67)
10.57 (8.59, 12.55)
...
...
Brooklyn
19.23 (18.34, 20.12)
11.60 (10.70, 12.49)
Bronx
11.51 (10.77, 12.25)
8.98 (8.24, 9.72)
Manhattan Queens
17.77 (16.68, 18.86) 9.50 (8.76, 10.24)
13.35 (12.32, 14.38) 4.18 (3.44, 4.92)
...
...
Race/ethnicitya
Non-Hispanic White (Ref)
Conclusions
Location
Staten Island (Ref)
Note. CI = confidence interval; PD = prevalence difference. Sample size for crude PD, n = 223 864; for adjusted PD, n = 223 780. The Wald procedure was used to estimate 95% CIs. a Excluding 84 students with missing race/ethnicity data.
In addition to variation in 2-dose varicella vaccination coverage by age, we also detected meaningful differences in coverage by race/ ethnicity and school location. Lower varicella vaccination coverage places these subpopulations at risk for disease and may facilitate varicella transmission to other communities with higher coverage, as has been seen for measles.56 School-entry vaccination requirements, including regulations for varicella, have demonstrated success in increasing coverage among all students covered by the requirements, irrespective of student demographics or risk factors associated with low coverage,35,37 and in reducing disparities in coverage among subpopulations.57 Therefore, the adoption and enforcement of a 2-dose varicella mandate in New York State would not only be effective in improving 2-dose coverage in our overall sample, but would also likely address coverage disparities we detected among demographic subpopulations.
Limitations The students in our sample were not representative of New York City public school students with regard to race/ethnicity and school location, factors that were significantly associated with varicella 2-dose coverage in our analysis.
Thus, our coverage results may not be generalizable to all New York City public school students. Our estimate of 2-dose coverage among students aged 7 years was similar, however, to 2010 CDC sentinel data from New York City that assessed coverage among all New York City children aged 7 years (75.7% in our sample vs 77.6% in CDC data).14 Furthermore, because our sample comprised nearly one quarter of a million students—or one quarter of the New York City public school population—our results may have highly relevant implications regarding the potential for varicella transmission among New York City public school students. Because our analyses relied on documented vaccinations and evidence of varicella immunity, we may have underestimated varicella coverage and immunity levels. A second varicella dose may be less likely to be recorded in ATS because it is not required for school entry. Varicella doses may be less likely to be documented in the CIR if they were administered prior to enactment of legal requirements to report vaccinations or were funded by sources other than public funds, because health care facility accountability for administration of vaccine purchased via Vaccines For Children and New York State Children’s Health
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Since adoption of a routine 2-dose varicella vaccination schedule in 2006, varicella incidence and outbreaks in the United States have continued to decline.58,59 Data from the largest public school system in the United States demonstrated early success in implementation of the 2-dose schedule, even in the absence of a 2-dose school requirement. Although these findings are encouraging, 2-dose coverage was still well below recommended levels, leaving New York City public school students at higher risk of varicella disease and outbreaks. Our results underscore the need for a 2-dose varicella vaccination school-entry requirement to achieve near universal 2-dose coverage among New York City public school students and eliminate differences in coverage among subgroups. j
About the Authors At the time of the study, Margaret K. Doll, Jennifer B. Rosen, and Christopher M. Zimmerman were with the Bureau of Immunization, New York City Department of Health and Mental Hygiene, Queens, NY. Hiram Szeto is with the Bureau of School Health, New York City Department of Health and Mental Hygiene, Queens. Stephanie R. Bialek is with the National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA. Correspondence should be sent to Jennifer B. Rosen, MD, Bureau of Immunization, New York City Department of Health and Mental Hygiene, 42-09 28th St, FL 5, Queens, NY 11101 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link. This article was accepted July 24, 2014.
Contributors M. K. Doll helped develop the project, conducted analyses, and led the writing of the article. J. B. Rosen helped manage and develop the project. S. R. Bialek helped develop the project and critically revised the article. H. Szeto gathered the data. C. M. Zimmerman conceptualized and helped manage the project. All authors interpreted results and edited the article.
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Acknowledgments This research was funded by a grant from the CDC, with funding from the American Recovery and Reinvestment Act. We thank Luiz Homem de Mello, Vikki Papadouka, Alexandra Ternier, and Jane Zucker of the New York City Department of Health and Mental Hygiene and Scott Grytdal, Adriana Lopez, Mona Marin, and Jane Seward of the CDC National Center for Immunization and Respiratory Diseases. Note. The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the CDC.
Human Participant Protection No protocol approval was required because the study was considered to be part of routine program evaluation activities and not research.
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