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An Elementary School Outbreak of Varicella Attributed to Vaccine Failure: Policy Implications

  1. Brian R. Lee1,a,
  2. Shelly L. Feaver1,
  3. Claudia A. Miller1,
  4. Craig W. Hedberg2 and
  5. Kristen R. Ehresmann1
  1. 1Immunization, Tuberculosis, and International Health Section, Infectious Disease Epidemiology, Prevention, Minneapolis
  2. 2Department of Environmental Health, University of Minnesota, Minneapolis
  1. Reprints or correspondence: Brian Lee, Acute Disease Investigation and Control Section, Minnesota Dept. of Health, 717 Delaware St. SE, Minneapolis, MN 55414 (brian.lee{at}health.state.mn.us).

  • ↵a Present affiliation: Acute Disease Investigation and Control Section, Minnesota Department of Health, Minneapolis.

 
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Abstract

Background. Since licensure in the United States, studies have shown that varicella vaccine's overall effectiveness ranges from 44% to 100%, with substantial protection against moderate and severe varicella; however, breakthrough illness has been documented in up to 56% of vaccinated individuals.

Methods. A varicella outbreak occurred in a Minnesota school with 319 students. Phone surveys were conducted with students' parents. Information was collected on students who had recent varicella infections, including onset date, rash characteristics, duration, and underlying medical conditions.

Results. Fifty-four cases occurred after a primary breakthrough case. Twenty-nine (53%) students had been vaccinated. Unvaccinated students had an increased risk of moderate varicella, compared with vaccinated students (relative risk [RR], 4.4 [95% confidence interval {CI}, 2.2–9.1]; P<.001). The vaccine was 56% effective at preventing any varicella and 90% effective against moderate illness. Students vaccinated ⩾5 years before the outbreak had a greater risk of breakthrough varicella than did those vaccinated within ⩽4 years (RR, 2.6 [95% CI, 1.3–5.4]; P<.01).

Conclusions. Vaccinated students presented with milder varicella symptoms than did unvaccinated students. Individuals with breakthrough illness can be highly infectious. Time since varicella vaccination was associated with illness. Despite 29 breakthrough cases, the varicella vaccine conferred a high degree of protection against moderate illness.

Varicella is highly contagious, with secondary attack rates among susceptible household contacts of 60%–90% [1–3]. During the prevaccination era, this common childhood illness was responsible for 11,000 hospitalizations and 100 deaths each year in the United States [4, 5]. A live attenuated varicella vaccine was licensed in the United States in March 1995 [4–6]. The American Academy of Pediatrics, the American Academy of Family Physicians, and the Advisory Committee on Immunization Practices currently recommend that children receive a dose of varicella vaccine at 12 months of age; children ⩾13 years old should receive 2 doses of the vaccine [4].

The vaccine has shown substantial effectiveness against moderate and severe varicella symptoms; however, varicella has been reported in 0%–56% of vaccinated individuals [7–13]. A breakthrough case of varicella is defined as one that occurs >42 days after the vaccination and is caused by the wild-type (wt) virus [14]. These individuals typically have fewer lesions, have fewer complications from varicella, and are less likely to have a fever [7, 12, 15–17]. Previous studies have identified several possible risk factors for breakthrough varicella: receiving the varicella vaccine at 12–15 months of age, history of asthma, having impaired immune function, or receiving the varicella vaccination within 30 days of the measles-mumps-rubella (MMR) vaccine [4, 7–9, 14, 18–23].

Studies have indicated that the effectiveness of the varicella vaccine is 44%–100% (median, 83%) [7–13]; therefore, further evaluation may be necessary to ascertain the duration of immunity, the optimum age for vaccination, and other factors that could potentially affect vaccine effectiveness [4, 7–9, 12, 14, 18, 23–25]. Recent studies have suggested that immunity may wane after vaccination [12, 24]. Others have proposed that exposure to the wt virus serves to boost vaccine-induced immunity; however, this boosting will likely diminish with a decrease in illness incidence caused by vaccination coverage [26–31]. Seward et al. [32] found a 78% average reduction in the number of reported varicella cases among 3 study sites after the introduction of the vaccine. Five recently published reviews of outbreaks identified a substantial proportion of breakthrough cases, despite national vaccination coverage levels >75% [7–9, 12–13]. We examined the effectiveness of the varicella vaccine and the effect of breakthrough illness during an outbreak of varicella among students attending a Minnesota elementary school.

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Materials And Methods

Outbreak setting. In November 2002, the Minnesota Department of Health was notified of an outbreak of varicella in students attending an elementary school in northern Minnesota. A total of 319 students attended preschool, kindergarten, or grades 1–5. At the time of the outbreak, Minnesota did not require varicella vaccination for school attendance. The school design consisted of 2 wings with connecting hallways. Except for the preschoolers, the school cafeteria was shared by all grades.

Case definition. A case of varicella was defined as a student who had an acute maculopapulovesicular rash, with no other apparent cause, between 1 July 2002 and 1 January 2003. The 6-month study window was used to ensure that all cases in the outbreak were identified. Each illness was classified on the basis of the reported number of lesions [9, 12, 13]. A mild case was defined as <50 lesions, a moderate case as 51–500 lesions, and a severe case as <500 lesions. A breakthrough case was defined as a varicella illness in a vaccinated student with onset 142 days after vaccination [4]. Students were removed from the analysis if they had received the varicella vaccine within 42 days of illness, which excluded illnesses that could be attributed to the varicella vaccine. Students were identified as having a history of varicella or no history on the basis of information provided by their parents. Students with no history of varicella were classified as vaccinated or unvaccinated. Students were excluded from the analysis of risk factors and vaccine effectiveness if they had a history of varicella or if they had received the varicella vaccine at age <12 months. The study was approved by the University of Minnesota Institutional Review Board; all parents provided informed consent.

Interviews. Phone surveys with the students' parents were conducted to collect demographic information, vaccination history, medical risk factors, history of varicella, extracurricular and social activities, the amount of time spent at the school, and use of school transportation. Additional information was collected on students with outbreak-associated varicella infections, regarding the date of rash onset, illness severity, rash duration and type (macule, papule, and vesicle), and outcomes of the illness.

Follow-up. Clinics and vaccination centers were contacted to verify varicella vaccination history, including the vaccination date and the vaccine lot number. Information was also collected on any vaccinations within 30 days of the varicella vaccination. Follow-up was conducted with the school to examine attendance records for students with varicella during the time frame of the outbreak. These records were used to verify the date of rash onset (using the first day of absence from school as the determinate of onset) and the number of school days missed.

Statistical analysis. The data were analyzed using Epi Info (version 2000; Centers for Disease Control and Prevention [CDC]) and SAS (version 8.0; SAS Institute) software. Relative risks (RRs) and 95% confidence intervals (CIs) were performed in stratified calculations, Fisher's exact test was used to compare proportions, and 2-sided P values were reported, with P<.05 considered to indicate statistical significance. Medians were compared by use of the Wilcoxon rank-sum test. Logistic regression was used to examine the relationship between the length of time since vaccination and the risk of breakthrough varicella. Similar to other studies [7–9, 12, 13, 24] that have documented vaccine effectiveness, we used the attack rate in the vaccinated (ARV) and the attack rate in the unvaccinated (ARU) to calculate the vaccine effectiveness as [(ARU - ARV)/ARU]×100.

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Results

Student population characteristics. Of 319 students identified by the school, 12 did not attend school during the outbreak; these individuals were excluded from the investigation. Of the remaining 307 eligible participants, 252 interviews were completed (82% response rate). The population characteristics (e.g., grade, sex, and age) did not differ between students interviewed and those not interviewed. The study population ranged in age from 4 to 11 years (median, 8 years); 137 (54%) were female. Three students were excluded because they had been immunized at !12 months of age. Ninety-five (38%) of the remaining 249 students reported a history of varicella before the outbreak, 118 (47%) had documented varicella vaccination, and 36 (14%) were unvaccinated (table 1). Of the 154 students who did not report a history of varicella, 77% (n = 118) were documented as having been vaccinated.

A total of 55 cases were associated with the outbreak (including 6 in students with a reported history of varicella), which lasted from 16 October to 5 December 2002 (figure 1). These students were 5–11 years old (median, 7 years), and 31 of them (56%) were female. Of the 49 students with no history of varicella, 29 (59%) had documented varicella vaccination and 20 (41%) were unvaccinated. No student had a varicella illness that occurred within 42 days of the varicella vaccination.

Figure 1.
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Figure 1.

Cases of varicella among students attending elementary school A, by date of rash onset and vaccination status. Data from 5 students for whom no date of rash onset was available are left out.

Outbreak. The primary case occurred in a vaccinated 6-year-old boy who had a rash onset date of ∼16 October 2002 (figure 1). This student was reported to be ill for 3 days, had ∼40 lesions, and had fever for 2 days. According to school records, the boy had attended school for all 3 days of his illness. He likely transmitted varicella directly to 32 students. A total of 54 cases occurred after the primary case. This student was reported to have no known exposure to varicella zoster outside of the school during the 3 weeks before the onset of his rash. An unvaccinated 9-year-old student with a suspicious illness with an onset date of 26 September was identified and may have been the source of infection for the primary case. However, given the incubation period for varicella (typically 14–16 days), it is quite unlikely that this 9-year-old student could have been the source of the 54 secondary cases beginning in November 2002 (∼35 days' difference). With regard to the outbreak time line, we evaluated cases occurring early or late by likely exposure type (e.g., home or school) and found no difference.

Illness severity and vaccine effectiveness. On the basis of the number of lesions, mild varicella was reported in 23 students (47%), and 25 students (51%) had moderate varicella (table 2). No cases were identified as severe varicella. Hospitalization was necessary for 1 unvaccinated student, who was receiving immunosuppressive therapy. Three students had pneumonia complications after their varicella illness. The median duration of the illness among vaccinated students was 3 days, compared with 4 days among unvaccinated students (P = .02). Of the 29 breakthrough cases, 76% had <50 lesions present during the illness. The varicella attack rate for vaccinated students was 25%, compared with 56% for unvaccinated students (P<.001); the attack rate for students who had a history of varicella was 6% (table 1). Overall, vaccine effectiveness was 56% for any varicella illness. Vaccine effectiveness against moderate illness was 90%.

Table 1.
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Table 1.

Selected demographics of elementary school students at the time of the varicella outbreak—interviewed population.

Risk factors. The length of time since varicella vaccination was a significant risk factor for developing breakthrough varicella. Students vaccinated ⩾5 years before the start of the outbreak had a greater risk of developing varicella illness, compared with those vaccinated ⩽4 years before the start of the outbreak (RR, 2.6 [95% CI, 1.3–2.4]; P = .009). The median length of time since vaccination was 5 years for ill students and 4 years for vaccinated students who did not become ill (P = .004). On the basis of logistic regression analysis, the odds of developing varicella increased, overall, 1.5 times with each year since the time of vaccination. Receiving the varicella vaccine between ⩾12 and <16 months of age was associated with developing breakthrough varicella (RR, 2.1 [95% CI, 1.1–4.1]; P = .03). Vaccinated students who became ill had a significantly lower age at varicella vaccination than did vaccinated students without outbreak-associated varicella (median, 15 vs. 20 months, respectively; P = .04). No common lot number was associated with the risk of developing varicella.

Certain medical conditions were associated with the risk of varicella. Chronic ear infections were not associated with breakthrough illness among students without a history of varicella (RR, 1.9 [95% CI, 1.0–3.5]; P = .07). Students with a history of respiratory syncytial virus infection, pneumonia, or other similar lung conditions had an increased risk of developing breakthrough varicella (RR, 3.0 [95% CI, 1.5–5.8]; P = .03). Asthma, cystic fibrosis, diabetes, allergies, heart disease, and bronchitis were not identified as risk factors of varicella in our analysis.

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Discussion

The varicella vaccine was 56% effective in preventing varicella illness entirely and 90% effective against moderate illness in this outbreak setting. Although the overall vaccine effectiveness in the present investigation may have been lower than that reported nationally, school outbreaks may represent a unique scenario for demonstrating the effectiveness of a vaccine. Attack rates may be greater in school-outbreak settings as a result of the closed environment and the intense, repeated exposure to the virus among students.

Immunized students had fewer lesions, were less likely to have a fever, were sick for fewer days, and missed less school than unvaccinated students. Our results correspond with those of a day-care center outbreak investigated by Galil et al. [12], in which vaccine effectiveness was 44% against all varicella and 86% against moderate and severe varicella. In that study, children who had been vaccinated presented with milder varicella symptoms than did unvaccinated children.

We have reported the first documented varicella outbreak in an elementary school setting with a primary case occurring in a vaccinated child; he had a mild clinical presentation, yet there was likely direct transmission to 32 students with 22 subsequent cases. This suggests that, although breakthrough illness in vaccinated children is significantly milder, infectiousness may not necessarily be reduced.

The results from this outbreak are in agreement with those of earlier studies that have suggested that the age at varicella vaccination is a potential risk factor for varicella illness [7, 8, 12, 18, 23, 24]. Students who received the varicella vaccine at ⩽15 months of age had a significantly higher risk of breakthrough varicella illness. Furthermore, because the median age of varicella vaccination was significantly different between vaccinated and unvaccinated students, the data suggest a possible relationship between younger age at vaccination and vaccine failure.

These data suggest that the length of time since vaccination is a risk factor for breakthrough varicella illness, which is similar to the results from another documented varicella outbreak [12]. Students who had received their vaccination at least 5 years before the outbreak were at a higher risk of breakthrough varicella illness than were those who had been immunized more recently. The results from the present study and others suggest that booster doses of the vaccine may be beneficial. Further study is necessary to evaluate the duration of varicella immunity.

Improper storage and handling of the varicella vaccine has been suggested as a risk factor for breakthrough illness [4]. No breakthrough illness patterns were found to be related to varicella vaccine lot numbers. The majority of students (56%) had received the varicella vaccination from 1 clinic in the area. A 2001 Minnesota Department of Health inspection of this clinic indicated proper vaccine storage protocols per CDC recommendations; however, there was no documentation of prior vaccine storage and handling practices.

Previously identified risk factors of asthma or receiving the varicella vaccine within 30 days of the MMR vaccine [4, 9, 22, 23] were not associated with an increased risk of breakthrough varicella illness in our investigation. No association was found between breakthrough varicella illness and the amount of time spent at the elementary school, including participation in extracurricular or social activities. Additionally, there was no relationship between the number of siblings, including those attending the same school, and the risk of breakthrough varicella illness.

There are several limitations to the present study. The characteristics and duration of illness for each student were reported by parents. Any misdiagnosis of varicella could result in overestimated or underestimated vaccine effectiveness; however, the school nurse identified a majority of cases. There was also the possibility of recall bias, because some parents had difficulty remembering the date of rash onset. Examining attendance records to ascertain the date of rash onset was used in attempt to limit these biases. Dates of rash onset generally occurred 1 day before the first day of school missed. There were 5 cases with no reported date of rash onset. These data could affect the case distribution of the epidemiological curve; however, the parents of these 5 students indicated that each had an approximate date of rash onset during November or December 2002. Parents were asked to report their assessment on the severity of their child's illness (mild, moderate, or severe); this question was asked to validate the reported number of lesions for each child (table 2). The parental assessment was in general agreement with case definition of severity (number of lesions). Health-care providers were not contacted to verify any history of varicella.

Table 2.
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Table 2.

Characteristics of illness among students a without history of varicella.

The present results have a number of important public health implications. The varicella vaccine demonstrated effectiveness against moderate varicella illness. Vaccinated students had significantly milder illness, as measured by the number of lesions, days of school missed, presence of fever, and duration of illness. Our data illustrate the importance of keeping children with varicella out of school, regardless of whether the child has received the varicella vaccine. In our investigation, the child with the primary illness was vaccinated and likely transmitted the infection to 32 students. An isolated breakthrough case that results in <50 lesions and/or an unexplained fever should be considered to be highly infectious. Given the substantial number of breakthrough cases that occurred during this outbreak, it is important to continue to maintain and improve the national level of vaccination against varicella zoster and to consider whether a booster dose will offer additional protection.

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Acknowledgments

We thank Harry Hull, Richard Danila, and Kirk Smith, for their critical review of the manuscript; staff at Minnesota Department of Health, who assisted with the investigation; the Centers for Disease Control and Prevention, for providing a prototype questionnaire; Michael Severson and Judy Rian, for their prompt report of the outbreak; the school staff who assisted us with the investigation (Erin Suemnick, Mary Lastovich, and Kathy Olson); and the parents of the students, for their contribution of data for the article.

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Footnotes

  • Financial support: Centers for Disease Control and Prevention, National Immunization Program.

  • The contents of the present study are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention.

  • Received January 6, 2004.
  • Accepted February 2, 2004.
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  1. J Infect Dis. (2004) 190 (3): 477-483. doi: 10.1086/422041
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