PEDIATRICS Vol. 121 No. 6 June 2008, pp. e1548-e1554 (doi:10.1542/peds.2007-2031)
ARTICLE |
Vaccine-Era Varicella Epidemiology and Vaccine Effectiveness in a Public Elementary School Population, 2002–2007
a Public Health Division, Department of Human Services, Portland, Oregon
b Oregon Health and Science University, Portland, Oregon
c Multnomah County Education Services District, Portland, Oregon
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. We conducted ongoing varicella surveillance of public elementary school students to track changes in incidence from 2002 to 2007. In school year 2002–2003, we also conducted a retrospective cohort study to measure varicella vaccine effectiveness, assess relationships between risk factors for varicella in vaccine recipients (breakthrough varicella) identified in earlier studies, and assess the ability of school nurse surveillance to detect varicella cases.
PATIENTS AND METHODS. Varicella was defined as acute illness with maculo-papulo-vesicular rash without another apparent cause persisting >24 hours, regardless of previous episodes of the same or a similar illness. Using case data reported by school nurses, we described breakthrough varicella rates (percentage of vaccinated students with varicella), annual varicella-incidence rates (varicella cases per 100 public elementary school students), vaccine effectiveness, risk factors for breakthrough varicella, clinical characteristics of vaccinated and susceptible varicella patients, and sensitivity and positive predictive value of school nurse surveillance.
RESULTS. During school years 2002–2007, 502 elementary school students met the varicella case definition. Breakthrough varicella rates among exposed students ranged from 6% to 8% per school year; annual incidence rates ranged from 0.2% to 0.3% of public elementary school students; and varicella was more severe and lasted longer in susceptible than in vaccinated students. The positive predictive value of school nurse surveillance was 94%, and sensitivity was 90%. Vaccine effectiveness was 81%.
CONCLUSIONS. School nurse surveillance has both high positive predictive value and sensitivity and is a useful means of tracking varicella occurrence. Annual incidence rates of varicella are low. Vaccine effectiveness and breakthrough varicella rates are comparable to findings of other studies.
Key Words: varicella disease • varicella epidemiology • varicella surveillance • breakthrough varicella rates • annual varicella-incidence rates • vaccine effectiveness • risk factors for breakthrough varicella
Abbreviations: ACIP—Advisory Committee on Immunization Practices • SY—school year • OPHD—Oregon Public Health Division • BVR—breakthrough varicella rate • MMR—measles-mumps-rubella • CI—confidence interval
On March 17, 1995, the varicella vaccine era began in the United States when the US Food and Drug Administration approved the live, attenuated virus vaccine for susceptible individuals 
12 months of age. The American Academy of Pediatrics recommended that varicella vaccine be added to the childhood immunization schedule in May 1995,1 and the Advisory Committee on Immunization Practices (ACIP) followed suit in July 1996.2 In 1999, ACIP recommended that varicella vaccination be required for child care and school entry3 and, in 2006, further recommended that a second dose of varicella vaccine be given at 4 to 6 years of age.4 To assure coverage for the 2000–2001 school year (SY) and thereafter, varicella vaccination was made mandatory for susceptible Oregon children starting kindergarten and 7th grade. By SY 2006–2007, students in kindergarten through 12th grade without previous varicella had all had a varicella vaccine unless they had religious or other exemptions from vaccination.
After an elementary school varicella outbreak in SY 2000–2001,5 the Oregon Public Health Division (OPHD) started school nurse surveillance for varicella among public elementary school students (kindergarten through 5th grade) in Multnomah County, Oregon, and conducted a retrospective classmate cohort study the first year of surveillance (SY 2002–2003).6 Multnomah County has 107 public elementary schools and 26 registered nurses, each assigned to 4 to 5 schools. Approximately 50 000 Oregon children 5 to 10 years of age (
20% of the state's elementary school population) live in Multnomah County, and 85% of those attend public elementary schools. Public elementary schools are in session 42 weeks per year; students spend 5 hours per day in their classrooms.7
This article describes the vaccine-era epidemiology of varicella in public elementary schools over a 5-SY period; vaccine effectiveness after classroom exposure; the relationships between risk factors identified in earlier studies (5,8–11) for breakthrough varicella after classroom exposure; and the ability of school nurse surveillance to detect varicella cases. These activities were conducted by OPHD to measure how effectively the legal requirement for varicella vaccination by the start of kindergarten achieves the goal of reducing varicella incidence. As such, they are considered public health practice and do not constitute human subjects research.
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METHODS |
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Case Definitions
"Varicella absentees" were defined as students absent for parent-reported or school nurse-observed varicella. "Varicella" was defined as acute illness with maculo-papulo-vesicular rash without other apparent cause persisting >24 hours, regardless of previous episodes of the same or a similar illness (case definition). "Breakthrough varicella" was defined as varicella with onset
42 days after varicella vaccination. "Sporadic varicella" was defined as 1 varicella case in a school with no other cases reported there within 21 days (1 incubation period). "Clustered varicella" was defined as 2 to 4 varicella cases in a school in 1 consecutive incubation periods. "Varicella outbreaks" were defined as 5 varicella cases in a school in 1 consecutive incubation periods.
Case Classifications
Students with varicella (and their classmates in the cohort study) were classified as "previous varicella" (parent-reported past varicella episodes), "vaccinated" (varicella vaccination dates found in school records, medical charts, or the state immunization registry), "susceptible" (neither previous varicella nor vaccination), "unknown" (previous varicella or vaccination unknown), or "other" (both previous varicella and varicella vaccination).
SY 2002–2003 Retrospective Classmate Cohort Study
Classmates were defined as students exposed to varicella as a result of sharing a classroom with a varicella case within 5 days of the cases rash onset. School nurses provided classmate registration and vaccination data. OPHD conducted structured interviews with classmates’ parents or guardians ("parents") to find varicella that occurred 7 to 21 days after exposure (defined as cases rash-onset date). Furthermore, classmates’ vaccination data were checked against the state immunization registry or, when data were not in the registry, medical charts from vaccination providers. Registry or medical chart dates were used if they differed from those in the school records. Only vaccinated classmates with verified vaccination dates were included in the analyses of vaccine effectiveness and risk factors for breakthrough varicella.
SYs 2002–2007 School Nurse Surveillance
School nurses provided demographic data and vaccination dates from school records for each varicella absentee. Using a translator service as needed, OPHD conducted structured interviews with parents of varicella absentees to collect information about vaccination, previous varicella, parent-reported asthma, eczema, oral steroid use, rash onset date, signs and symptoms, parental assessment of illness severity, nurse or physician examinations or consultations, complications, and hospitalizations. Varicella was verified either by physicians or nurses examining varicella absentees or by OPHD interviewers applying the case definition to the illness described by parents.
Exclusions
In all of the analyses, elementary school students vaccinated before 12 months of age were excluded. In descriptive epidemiologic analysis, cases detected by structured interviews but not reported by school nurses were excluded (except in the analysis of surveillance system sensitivity). Cases with previous varicella or unknown histories, and their classmates when they were the only cases in the classroom, were excluded from analyses of vaccine effectiveness and risk factors for breakthrough varicella in the classmate cohort study and in the computation of breakthrough varicella rates and annual incidence rates.
Statistical Analyses
Retrospective classmate cohort study data (SY 2002–2003) permitted the calculation of sensitivity (percentage of varicella cases detected by school nurses), overall varicella vaccination rate (percentage of varicella vaccination in the entire classmate cohort, including vaccinated classmates both with and without previous varicella and excluding classmates whose vaccination status is unknown), varicella vaccination coverage rate (percentage of varicella vaccination among classmates without previous varicella), breakthrough varicella rate (BVR; percentage of vaccinated classmates with varicella), attack rate in susceptibles (percentage of susceptible classmates with varicella), and vaccine effectiveness (the reduction in incidence among vaccinated classmates that is attributable to vaccination [1 – (BVR/attack rate in susceptibles)]. Multiple logistic regression was used to assess relationships between risk factors for breakthrough varicella identified in earlier studies (time 5 years since vaccination, vaccination at 12–15 months of age, timing of measles-mumps-rubella [MMR] and varicella vaccination, and preexisting asthma).
School nurse surveillance data permitted the calculation of positive predictive value (varicella among varicella absentees), annual BVRs (as above), and annual varicella-incidence rates (varicella per 100 public elementary school students). To estimate denominators of annual BVRs (vaccinated classmates), we multiplied the total number of students in classrooms with varicella cases7 by the overall varicella vaccination rate (expressed as a proportion) from the retrospective classmate cohort study [(total classmates)(overall vaccination rate) = vaccinated classmates]. We needed to use a single proportion for annual BVR calculations because the state immunization program does not collect grade- or school-specific overall varicella vaccination rates. Annual varicella-incidence rates per 100 persons were estimated using 2002–2007 population estimates of Multnomah County children ages 5 to 10 years12–16 multiplied by 0.85, the proportion attending public elementary schools. Clinical characteristics of vaccinated and susceptible cases were compared by 
2 analysis. For all of the analyses, statistical significance was set at P < .05; SPSS 15.0 for Windows (SPSS Inc, Chicago, IL) was used for data analysis.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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SY 2002–2003 Retrospective Classmate Cohort Study
The SY 2002–2003 retrospective classmate cohort study was conducted from September 19, 2002, to June 1, 2003 (36 weeks of the 42-week SY) and included only vaccinated students with verified varicella vaccination dates. In a cohort of 1327 classmates with verified vaccinations exposed to 112 varicella cases, parents of 1176 (89%) were interviewed. Active case finding detected 13 unreported cases. Sixty-three classrooms in 30 schools were affected.
Of 1176 classmates, 710 (60%) had not had previous varicella, 355 (30%) had previous varicella, 69 (6%) had both previous varicella and vaccination, and 42 (4%) had unknown histories. Sixteen cases with previous varicella or unknown histories were excluded from analyses of vaccine effectiveness and risk factors for breakthrough varicella. Two of these 16 varicella cases were, however, detected by active surveillance and, therefore, were included in the analysis of surveillance system sensitivity. Varicella vaccine coverage was 92% among 710 classmates without previous varicella; 60 (8%) were susceptible (Fig 1). Classmates had been vaccinated a median of 5 years before exposure. The overall varicella vaccination rate was 63% (719 of 1134).
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Vaccine effectiveness was calculated for the 710 classmates without previous varicella. The breakthrough varicella rate was 11.2% (73 of 650), and the attack rate among susceptible classmates was 60% (36 of 60); vaccine effectiveness was 80.8% (Fig 1).
Risk Factors for Breakthrough Varicella
Time 5 years since vaccination was not a risk factor for breakthrough varicella in trend analysis (P = .07) or when data were categorized to compare classmates with time <5 years since vaccination (10.9%) to those with time 5 years since vaccination (11.5%; relative risk: 0.95 [95% confidence interval (CI): 0.94–1.10]; Table 1). Early age at vaccination was likewise not a risk factor for breakthrough varicella when varicella cases vaccinated at 12 to 15 months of age (11%) were compared with varicella cases vaccinated after 15 months (11.3%; relative risk: 0.98 [95% CI: 0.70–2.00]). Finally, none of the following risk factors were independently associated with breakthrough varicella in logistic regression analysis: time 5 years since vaccination, vaccination at 12 to 15 months, MMR timing (nonsimultaneous administration of MMR vaccine within 30 days of the varicella vaccination), and asthma; only noncase classmates reported eczema, and none reported oral steroid use (Table 2).
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School Nurse Surveillance
Positive Predictive Value and Sensitivity
During SYs 2002–2007, elementary school nurses reported 595 varicella absentees to OPHD; parents of 532 (89%) were interviewed; 502 met the case definition (positive predictive value: 94%; Table 3). Fifty-four percent of varicella cases were provider-diagnosed after physical examination; 46% had parent-reported varicella that met the case definition. In the SY 2002–2003 classmate cohort study, demographic and vaccination data were available for classmates of 112 varicella cases. Active case finding detected 13 unreported varicella cases; sensitivity of school nurse surveillance was 90% (112 of 125).
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Breakthrough Varicella, Annual Incidence, Outbreaks, and Monthly Distribution
An average of 100 varicella cases occurred per SY, with the fewest number reported in SY 2006–2007. Breakthrough varicella rates ranged from 6.0% to 8.0% per SY; annual incidence rates ranged from 0.2% to 0.3% of public elementary school students. The percentage of vaccinated varicella cases increased commensurate with annual increases in varicella vaccination coverage17 (Table 4).
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From SY 2002–2007, there occurred 95 sporadic varicella cases, 71 clusters of 2 to 4 varicella cases, and 27 outbreaks of
5 varicella cases (Table 5). The majority (53%) of varicella cases occurred in outbreaks. Varicella occurrence was highest early in the SY (October and November) and steady until June, when late-occurring varicella cases were lost to follow-up after school closed for the summer.
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Clinical Characteristics of Varicella Case Subjects
During SYs 2002–2007, provider-diagnosed varicella and parent-reported varicella were more severe in susceptible than in vaccinated students. The former were more likely to have generalized rashes with >50 lesions (74% vs 19%); to have rashes accompanied by fever, headache, sore throat, malaise, and anorexia; to have all of these symptoms at once (60% vs 28%); and to have fever (86% vs 62%). To their parents, 65% of susceptible students but only 13% of vaccinated students seemed moderately or severely ill. Susceptible students’ rash duration was a median of 2 days longer than vaccinated students’ rash duration. Finally, 1 vaccinated and 1 susceptible student had complications (bacterial skin infections and conjunctivitis, respectively; Table 6).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Since licensure on March 17, 1995, progressively widespread use of varicella vaccine in the United States has significantly altered varicella epidemiology, with the Centers for Disease Control and Prevention reporting incidence reductions of
84% from 1990 to 2001 in selected states and surveillance sites.18 However, varicella outbreaks in schools and child care centers with vaccination coverage ranging from 30% to 97% engendered discussion about the need for a booster dose of the varicella vaccine. Measured vaccine effectiveness in these outbreaks ranged from 46% to 76%, and, in some studies, time 5 years since vaccination was associated with breakthrough varicella, suggesting that vaccine-induced immunity waned over time.5,9,19–21 With uncertainty about long-term vaccine effectiveness, in June 2006, ACIP recommended a second dose of varicella vaccine for persons 12 months of age without evidence of immunity.4
Estimates of vaccine effectiveness based on outbreak investigations can underestimate vaccine effectiveness in the general population when high case counts are needed to trigger investigations, small populations are investigated, and vaccine failure clusters within a community.22 With these issues in mind, our retrospective cohort study included sporadic varicella cases, clusters of 2 to 4 varicella cases, and varicella cases in outbreaks, along with noncase classmates of varicella cases. Using classrooms assured that vaccinated and susceptible students had similar opportunities for exposure to varicella-zoster virus and increased the accuracy of our estimate.23 Finally, effectiveness was calculated with school record-based vaccination dates plus 1 independent verification source (state immunization registry or provider medical charts), thus reducing uncertainty about the accuracy of vaccination data. Uncertainty remains about whether noncase classmates reported as susceptible to varicella were indeed susceptible, because antibody testing was not conducted; in a 1998 study, 25% of children whose parents reported a "definite" negative varicella history were serologically positive.24 When susceptibles identified by patient history are not truly susceptible, vaccine effectiveness could be underestimated.
In our SY 2002–2003 retrospective classmate cohort study, vaccine coverage was 92%, vaccine effectiveness was 81% (95% CI: 79%–85%), and time 5 years since vaccination was not a risk factor for breakthrough varicella. Vaccine effectiveness in our study was comparable to estimates of 87% (95% CI: 81%–91%), 83% (95% CI: 69%–91%), and 85% (95% CI: 78%–90%) from studies with designs other than observational studies of varicella outbreaks (11,25,26), as well as to the 79% (95% CI: 70%–85%) vaccine effectiveness found in a household contact study, the setting with "the most intense conditions of exposure."27
Breakthrough varicella rates of 6% to 8% from 2002 to 2007 derived from school nurse surveillance data were higher than the 3% to 4% reported elsewhere.25,28 BVRs may be overestimated, however, because the proportion used to estimate the number of vaccinated classmates was held constant. Varicella incidence from 2002 to 2007 derived from school nurse surveillance data ranged from 0.2% to 0.3% of children ages 5 to 10 years, considerably less than the 9% average annual incidence in the prevaccine era.29 Although this, strictly speaking, is not an annual incidence rate, because Multnomah County does not have a 12-month SY, it is a close approximation given that varicella-zoster virus activity has historically diminished in the summer months.29–31 These rates are lower than the annual (2000) varicella-incidence rate of 2% of the 5- to 9-year-old population of a Centers for Disease Control and Prevention varicella active surveillance site (Antelope Valley, CA)18 and represent population-based estimates.
Surveillance data have several limitations related to case detection and classification (as vaccinated or susceptible). In the vaccine era, varicella has become a milder illness than it was in the prevaccine era and is now easier both to miss and to misdiagnose. Because elementary school nurse reporting depends on both parent reporting and direct observation by the nurse, the system would not have detected varicella that parents had failed to report for students who did not attend school while ill; that was mild enough to escape notice; or that occurred and resolved during school breaks. Likewise, students with a rash illness that was not varicella may have been misclassified as varicella because laboratory confirmation was not undertaken. Unless misdiagnoses occurred disproportionately among susceptible students, they would bias our estimates of vaccine effectiveness toward the null.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Because varicella is uncommonly confirmed by laboratory testing, we used a nonconventional surveillance system (ie, school-based surveillance). From SYs 2002–2007, only 6% of school nurse-reported varicella absentees did not meet the varicella case definition and, during the SY 2002–2003 cohort study, school nurses missed only 10% of varicella absentees who did. Together these indicate that school nurse surveillance has both high positive predictive value and sensitivity and is a useful means of tracking varicella occurrence in a large percentage of school-aged children in the county and state. School-based surveillance has the further advantage of detecting more varicella case subjects than would be detected by physician or laboratory-based reporting and, therefore, produces a more accurate description of vaccine-era varicella epidemiology.
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ACKNOWLEDGMENTS |
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This work was funded in part by Emerging Infections Program Cooperative Agreement U01 CI000306 between the Oregon Department of Human Services and the Centers for Disease Control and Prevention.
We thank Steven Ladd-Wilson, Linda V. Duke, Thomas Brundage, Peg Murray, Yangdol Sherpa, Michelle Barber, and Tammy Cochell for database design, statistical programming, data collection, and data entry; Anna Robins and Lisa Rogers for verifying varicella vaccination with immunization providers and the Oregon Immunization Registry; Janice Betton for providing demographic and vaccination data for varicella-exposed classmates of varicella cases; Robert J. Nystrom for helping us find the right people to whom to talk; Brian Reeder and Cliff Brush at the Oregon Department of Education for providing school attendance data; Lorraine Duncan, Juventila Liko, MD, June Bancroft, MPH, and Frederick Hoesley, MD, for reviewing the article; and Susan Darnell, RN, and all of the elementary school nurses employed by the Multnomah Education Service District who reported varicella absentees. We also thank Gary Oxman, MD, Amy D. Sullivan, PhD, and Jan Poujade, RN, from the Multnomah County Department of Health and Barna De Tugwell, MD.
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FOOTNOTES |
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Accepted Dec 3, 2007.
Address correspondence to Lore E. Lee, MPH, Oregon State Health, 800 NE Oregon St, Portland, OR 97211. E-mail: lore.e.lee{at}state.or.us
The authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject We are already aware of changes in varicella epidemiology since vaccine introduction; vaccine effectiveness under field conditions; and risk factors for varicella after vaccination (breakthrough disease).
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| What This Study Adds We have confirmed vaccine-effectiveness findings from other studies by using different methodologies; present population-based annual incidence rates of varicella; and describe a method of collecting varicella-incidence data with high positive predictive value and sensitivity.
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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics
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