A varicella outbreak in a school with high one-dose vaccination coverage, Beijing, China

doi:10.1016/j.vaccine.2012.05.072

Vaccine

Volume 30, Issue 34, 20 July 2012, Pages 5094-5098

https://doi.org/10.1016/j.vaccine.2012.05.072 Get rights and content

Abstract

Background

Varicella vaccine is available in the private sector in China, with a single dose currently recommended for children aged ≥12 months. We investigated a varicella outbreak in a school in Beijing with high varicella vaccination coverage to describe the outbreak, examine risk factors for vaccine failure, and calculate vaccine effectiveness.

Methods

A varicella case was defined as an acute generalized maculopapular rash without other apparent cause in a student without prior varicella attending the elementary school during August 30–December 28, 2010. Varicella among vaccinated students (breakthrough varicella) was defined as varicella occurring >42 days after vaccination. Students’ vaccination status was verified with immunization records and clinical presentations were collected from health care practitioners.

Results

Of the 951 students, 934 (98%) had no prior varicella history. Among these students, 916 had received 1 dose of varicella vaccine and 2 had received 2 doses (98% vaccination coverage) before the outbreak. A total of 87 cases occurred during the outbreak; most had breakthrough varicella (86/87, 99%) and mild disease (83/87, 95%). Age at vaccination (<15 months vs. ≥15 months) and time since vaccination before outbreak (<5 years vs. ≥5 years) were not associated with development of breakthrough varicella. Single-dose varicella vaccination was 89% effective in preventing any varicella and 99% in preventing moderate/severe varicella.

Conclusion

Single-dose varicella vaccination is highly effective in reducing varicella incidence and mitigating disease severity, but not high enough to prevent outbreak. A two-dose program might help to prevent varicella outbreaks in Beijing.

Highlights

► The outbreak in school with high single-dose vaccination coverage may last long (4 months here). ► Most (86/97) cases are vaccinated cases with mild clinical manifestation. ► Single-dose varicella vaccine effectiveness is high, but not sufficient to eliminate outbreak.

Introduction

Varicella (chickenpox) is a highly contagious disease caused by infection with varicella zoster virus (VZV), and is characterized by a generalized pruritic vesicular rash. Although varicella is usually self-limiting and resolves within a week, severe complications, including death, can occur [1].

Varicella vaccines are now widely available globally for prevention and control of varicella. In China, varicella vaccine first was licensed for use as single dose in 1998. The vaccine has been shown to be highly effective in preventing varicella disease [2]. Currently, the vaccine is available for private purchase but is not included in national or provincial routine immunization programs. To control school-based outbreaks, single-dose vaccination has been provided free of charge by Beijing government since 2006 to unvaccinated students in Beijing schools. The vaccine is offered immediately after an outbreak is detected, a strategy which in some settings has been demonstrated to be effective [3], [4].

In September 2010, the Beijing Center for Disease Control and Prevention (CDC) was notified of an outbreak in an elementary school. Because almost all students in the school had received varicella vaccine before the outbreak, most cases were among vaccinated students. Beijing CDC investigated this outbreak to (1) describe its epidemiology, (2) delineate transmission patterns, (3) examine varicella vaccine effectiveness (VE), and (4) assess whether age at vaccination or time since vaccination were related to vaccine failure. This article summarizes findings from this investigation and discusses the implications for varicella outbreak control and vaccination policy in Beijing, China.

Section snippets

Outbreak setting

The outbreak occurred in a public elementary school for Grades 1 and 2 (hereafter referred to as “School A”) in Beijing. During the outbreak, School A had 951 students. The 3-story school building includes 22 classrooms, 11 for each grade, with 7–8 classrooms on each floor. Mixing of students occurred in the classrooms, hallways, play areas, on school buses, and at after-school activities (e.g., drawing, dancing, and martial arts groups).

Case definition and data collection

A case of varicella was defined as an acute generalized

Study population

Among the 951 students in School A, 17 who had a history of varicella before the outbreak were excluded for further analysis (Fig. 1). No staff or faculty developed varicella during the outbreak and all analyses were restricted to students. Among the 934 students without disease history, 16 were unvaccinated and 918 had received vaccine before the outbreak (2 of these had received 2 doses). During the outbreak, 11 of the unvaccinated students received vaccine and were excluded from further

Discussion

In our investigation of a varicella outbreak that lasted for 4 months in a Beijing elementary school where one-dose varicella vaccine coverage before the outbreak was nearly 100%, disease was introduced by a vaccinated student and occurred almost exclusively among vaccinated students exposed at school. This study confirms that children vaccinated with a single-dose of varicella vaccine may both contract and transmit varicella, and high single-dose varicella vaccination coverage may not provide

Acknowledgments

We highly appreciate the help from the school nurses and the clinical practitioners in this outbreak investigation, scientific comments from Dr. Jane Seward, and contribution from Ms. Mary McCauley on manuscript preparation. We are also indebted to the parents for their participation.

Conflict of interest statement: No conflicts of interest relevant to this article were reported.

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Cited by (43)

Impact of a 2-dose voluntary vaccination strategy on varicella epidemiology in Beijing, 2011–2017
2020, Vaccine
One-dose voluntary varicella vaccination for children was introduced in Beijing since 1998. In Oct 2012, a second dose varicella vaccine (VarV) was recommended to further decrease varicella disease and the outbreaks. We describe the impact of the 2-dose voluntary vaccination strategy on varicella epidemiology in Beijing, China.
Varicella incidence rates and outbreak characteristics in 2011–2017 was examined using surveillance data. Varicella vaccination coverage among children born in 2007–2012 was estimated through Beijing children immunization registry system. Vaccine effectiveness (VE) for VarV₂ was estimated by screening method.
Overall varicella incidence decreased by 37.8% from 103.2 per 100,000 population in 2011 to 64.2 per 100,000 population in 2017. Incidence declines in children aged <15 years with most significantly decrease by 82.3% in children aged 5–9 years, while no significant change happened in adolescent and adults. A total of 251 outbreaks with 3239 outbreak-related cases were reported in 2011–2017, the number of outbreaks decreased significantly by 50.7% from 69 in 2011 to 34 in 2017. The VarV₁ coverage ranged from 85.4% to 92.6% among children 4 year of age and the VarV₂ coverage ranged from 40.1% to 72.9% among children 6 year of age in the 2007–2012 birth cohort. Overall VE estimates against all varicella disease was 94.4% (95% CI: 89.9–98.9%) for VarV₂.
Moderate VarV₂ coverage has been achieved in Beijing resulting in remarkable declining of the incidence in children. Varicella outbreaks has not been eliminated suggested that measures such as including a 2-dose varicella vaccination in routine immunization program should be taken in the future.
Varicella outbreak trends in school settings during the voluntary single-dose vaccine era from 2006 to 2017 in Shanghai, China
2019, International Journal of Infectious Diseases
To investigate varicella outbreak trends among schoolchildren during the voluntary single-dose varicella vaccine (VarV) era in Shanghai, China.
Trends in school varicella outbreaks from 2006 to 2017 were assessed using joinpoint regression models. The impacts of changes in single-dose VarV coverage among schoolchildren and implementation of post-exposure prophylaxis (PEP) strategies on outbreak trends were further analyzed.
In total, 265 varicella outbreaks involving 3263 cases were reported in Shanghai from 2006 to 2017. The number of outbreaks showed an increasing trend from 2006 to 2017 (t = 2.62, p = 0.026), especially in kindergartens. The proportion of breakthrough varicella cases among all outbreak-related cases showed an increasing trend from 30.4% in 2008 to 85.7% in 2017 (t = 7.45, p < 0.001). Single-dose VarV coverage among schoolchildren was 88.1%, and showed a significant increase from the 1996 to the 2008 birth cohorts, followed by a non-significant decline from the 2008 to the 2014 birth cohorts. During school outbreaks in which PEP campaigns were conducted, the varicella attack rate was significantly lower than those in outbreaks without PEP campaigns (1.2% vs. 1.4%; Chi-square = 23.35, p < 0.001).
Even with high coverage, single-dose VarV is insufficient to prevent school outbreaks. The administration of VarV as PEP is an appropriate intervention for varicella outbreak control prior to implementing a two-dose VarV schedule.
Effectiveness of second-dose varicella vaccination as post-exposure prophylaxis: a prospective cohort study
2019, Clinical Microbiology and Infection
Citation Excerpt :
Additionally, the exposures examined in our study mainly focused on school contacts, and some transmission events probably occur outside the school (for instance, on the school bus or at home). Varicella outbreaks in school settings continue to occur, despite more than 80% of students receiving one-dose VarV in this study and other outbreaks [22–25]. This may be because the protection conferred by one-dose VarV had waned since the time of vaccination [26–28].
Although administration of a second dose of varicella vaccine (2^nd-dose VarV) to individuals who have previously received one-dose VarV has been recommended as a post-exposure prophylaxis (PEP) strategy for outbreak control, the effectiveness of this strategy remains unclear. We evaluated the vaccine effectiveness (VE) of 2^nd-dose VarV as PEP among students involved in 129 varicella outbreaks in Shanghai, China from 2013 to 2016.
Students who had received one-dose VarV more than 5 years prior to varicella exposure were eligible to receive 2^nd-dose VarV as PEP. We evaluated the VE using the following formula: VE = (1 – hazard ratio (HR)) × 100%.
A total of 6762 students were eligible for 2^nd-dose VarV, of whom 58.6% accepted PEP after varicella exposure. The adjusted VE of 2^nd-dose VarV as PEP was 77% (95% confidence interval 64–85%). In addition, the adjusted VE of 2^nd-dose VarV as PEP in affected classrooms with high vaccine uptake was higher than that in classrooms with lower vaccine uptake (87% vs. 69%). The adjusted VE was also higher in students who received 2^nd-dose VarV within 3 days of exposure than those who received it more than 3 days post exposure (77% vs. 64%).
These Results suggest that administration of 2^nd-dose VarV as PEP is an appropriate intervention for outbreak control in countries where two-dose VarV has not been adopted.
Effectiveness of post-exposure prophylaxis during varicella outbreaks among primary and middle school students in Shanghai: An analysis of three-year surveillance data
2018, Vaccine
Citation Excerpt :
Further, we collected data on the varicella vaccination status of students, obtained from their immunization records, and from guardians providing information on prior varicella history through phone interviews conducted with school healthcare professionals. According to prior studies, no difference in the incidence rate of varicella between girls and boys has previously been shown [9,10,21]; therefore, data concerning the sex of the students was not collected in this study. Secondary cases were defined according to the disease onset and vaccination dates.
To evaluate the effectiveness of post-exposure prophylaxis conducted during varicella outbreaks among students in Shanghai.
Surveillance data were collected from September 1, 2013 to December 31, 2016 involving 3524 susceptible students in 109 primary and middle school classes where emergency vaccinations (EVs) had been administered. Students were divided into two groups according to their prior vaccination (PV) varicella vaccine status. A secondary attack rate was used to compare EV and non-EV groups using a chi-squared test. Stratification analyses were performed, adjusting for the EV administration date, the vaccination coverage rate, and the number of cases prior to the EV.
The effectiveness rate was 92.2% (95% confidence interval (CI): 37.1–99.0%) when EV was applied within 3 days following the outbreak onset date, and 95.2% (95% CI: 79.9–98.8%) when vaccination coverage was ≥80% among students with PV. When students with PV received an EV for varicella within 3 days, the effectiveness rate was 100%.
EV showed high protective effectiveness for varicella during outbreaks, especially if administered within 3 days of an outbreak and in conjunction with a high coverage rate.
Effectiveness of varicella vaccine as post-exposure prophylaxis during a varicella outbreak in Shanghai, China
2018, International Journal of Infectious Diseases
Varicella vaccine (VarV) is recommended as effective post-exposure prophylaxis (PEP) within 3–5 days to control outbreaks. However, the effectiveness of PEP at >5 days after exposure and the administration of a second dose to those with a history of one dose prior to exposure have not been fully examined. This study evaluated the vaccine effectiveness (VE) of PEP in preventing disease during a varicella outbreak in Shanghai, China in 2013.
Self-administered questionnaires were used to obtain the students’ varicella history, vaccination status, and willingness to receive PEP. One dose of VarV was provided free of charge to eligible students. The VE of PEP was calculated as [1 − relative risk (RR)] × 100%. Analyses were restricted to grade 8 students, as no students from the other grades or teachers developed varicella during the outbreak.
Twenty-seven varicella cases were identified, 16 (59%) of which were infected after the PEP campaign. Sixty-five students received one dose of VarV on day 13 or 19 after the index case. Attack rates were 28% (9/32), 16% (15/94), 0% (0/10), and 6% (3/55) among unvaccinated, one-dose Pre-PEP, first dose as PEP, and second dose as PEP recipients, respectively. Cases among second dose as PEP recipients tended to have less fever compared with unvaccinated or one-dose Pre-PEP recipients. Compared with unvaccinated students, the VE of first dose as PEP recipients was 100% and of the second dose as PEP recipients was 60% (95% confidence interval −72% to 91%).
Post-exposure vaccination should be given as soon as possible after exposure. Nevertheless, vaccination is still recommended even at more than 5 days post-exposure to control varicella outbreaks.
Varicella outbreak in a highly-vaccinated school population in Beijing, China during the voluntary two-dose era
2017, Vaccine
Citation Excerpt :
Future analyses of surveillance data on reported varicella in Beijing before and after the two-dose recommendation will document whether similar changes occur in Beijing. It is well documented that one-dose breakthrough varicella is contagious; even persons who present with only maculopapular rash may transmit infection to susceptible individuals [21], and can cause outbreaks in school and daycare settings [5,9,22–25]. However, outbreaks started by a two-dose breakthrough varicella have not been previously documented.
Two-dose varicella vaccination has been available in Beijing since 2012 in the private sector. We investigated a varicella outbreak in a highly vaccinated elementary school population.
A cohort study was carried out and a varicella case was defined as an acute onset of generalized maculopapulovesicular rash without other apparent cause in a student attending the school from March 29 through May 17, 2015. Breakthrough varicella was defined as varicella >42 days after the last vaccine dose among both 1- or 2-dose varicella vaccine recipients. Vaccination information was collected from immunization records; information on prior varicella and clinical presentations was collected by surveying students’ parents.
Of the 1056 students in the school, 1027 (97.3%) reported no history of varicella. Prior to the outbreak, 98.6% of students had received ≥1 dose of varicella vaccine, and most (63.2%) students received two doses. Twenty varicella cases were identified for an overall attack rate of 2.0%. Half of the cases occurred in the classroom of the index case-patient, a two-dose recipient who was not isolated after symptom onset. Breakthrough varicella accounted for 95% of cases (19/20) with attack rates of 14.3% (1/7), 1.6% (6/362) and 2.0% (13/649) among unvaccinated, one-dose, and two-dose students, respectively. Most case-patients (18/20, 90%) had <50 lesions. No difference in clinical presentations was found between one-dose and two-dose recipients with breakthrough varicella.
Moderate two-dose varicella vaccine coverage was insufficient to prevent a varicella outbreak. Two-dose recipients with breakthrough varicella are contagious. High two-dose varicella vaccine coverage and timely isolation of cases may be needed for varicella outbreak prevention in the two-dose era.

View all citing articles on Scopus

^☆: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention, U.S. Department of Health and Human Services.

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A varicella outbreak in a school with high one-dose vaccination coverage, Beijing, China☆

Abstract

Background

Methods

Results

Conclusion

Highlights

Introduction

Section snippets

Outbreak setting

Case definition and data collection

Study population

Discussion

Acknowledgments

Varicella-zoster virus

Clin Microbiol Rev

The effectiveness of varicella vaccine in China

Pediatr Infect Dis J

Postexposure effectiveness of varicella vaccine

Pediatrics

Effectiveness of varicella vaccines as postexposure prophylaxis

Pediatr Infect Dis J

Postlicensure effectiveness of varicella vaccine during an outbreak in a child care center

JAMA

Loss of vaccine-induced immunity to varicella over time

N Engl J Med

Effectiveness over time of varicella vaccine

JAMA

Varicella disease among vaccinated persons: clinical and epidemiological characteristics, 1997–2005

J Infect Dis

Varicella outbreak epidemiology in an active surveillance site, 1995–2005

J Infect Dis

Chickenpox outbreak in a highly vaccinated school population

Pediatrics

One dose of varicella vaccine does not prevent school outbreaks: is it time for a second dose?

Pediatrics