Published online July 1, 2008
PEDIATRICS Vol. 122 No. 1 July 2008, pp. e260-e265 (doi:10.1542/peds.2007-2963)
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ARTICLE

Countywide School-Based Influenza Immunization: Direct and Indirect Impact on Student Absenteeism

Mollie M. Davis, MD, MPHa, James C. King, Jr, MDa, Lauren Moag, BSa, Ginny Cummings, CPNPa and Laurence S. Magder, PhDb

a Departments of Pediatrics
b Epidemiology, University of Maryland School of Medicine, Baltimore, Maryland


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. Live attenuated influenza vaccine was given to 5319 (44%) of the 12090 students enrolled in public elementary schools in Carroll County, Maryland, during the fall of 2005. We examined the impact of this community-based intervention on countywide student absenteeism during the subsequent influenza outbreak.

METHODS. This study used existing, anonymous information: census data, community influenza tests, and public school absenteeism data. The intervention group was Carroll County, years 2005–2006. The control group included Carroll County, years 2001–2005, and adjacent Frederick County, years 2001–2006. Weekly student absenteeism was determined during baseline influenza-free periods and influenza outbreak periods for all of the public schools.

RESULTS. The absolute change in absenteeism during the influenza outbreak periods over baseline in elementary schools was 0.61% for the intervention group and 1.79% for the control group. Similarly, the change in absenteeism during the influenza outbreak period over baseline for high schools was 0.32% for the intervention group and 1.80% for the control group. Although not statistically significant, trends in middle schools were similar.

CONCLUSIONS. Countywide school-based influenza vaccination was associated with reduced absenteeism during an influenza outbreak. The data suggest not only a direct impact on elementary schools but also an indirect impact on high schools. School-based programs provide an efficient method of providing influenza vaccination to children, and protection may extend to unvaccinated community members. Additional research is needed to determine whether school-based vaccination of children reduces morbidity and mortality associated with influenza outbreaks.

Key Words: influenza • vaccination • children • school • absenteeism

Abbreviations: CDC—Centers for Disease Control and Prevention • LAIV—live attenuated influenza vaccine • PW—peak week • IOP—influenza outbreak period • TIV—trivalent inactivated influenza vaccine

Influenza is a major cause of global morbidity and mortality. In the United States alone, there are ~200000 hospitalizations and 36000 deaths attributed to influenza each year.1 The annual economic impact of influenza in the United States has been estimated at between 11 and 18 billion dollars.2–4 Indirect costs because of losses in work productivity by adults and missed school time for children are harder to quantitate and likely underestimated. Vaccination is an effective method of preventing influenza-associated illness and its complications.1

Despite the benefit of influenza vaccination and its cost-effectiveness, population estimates of influenza vaccination remain low even among groups at high risk.1 Data analyzed from the 2005 National Health Interview Survey estimated that 29% of children aged 2 to 17 years with asthma received an influenza vaccination.5 Influenza vaccination guidelines released by the Advisory Committee on Immunization Practices in 2006 stressed routine vaccination for household contacts of people at risk for complications of influenza infection.1 The Centers for Disease Control and Prevention (CDC) estimated that only 10.8% of children aged 5 to 17 years with a household contact at risk of complications from influenza received the recommended vaccination in 2006.6

Children are important primary transmitters and even amplifiers of influenza to their families and communities. Children are often the first group to experience influenza during outbreaks, and student absenteeism is an early marker for influenza outbreaks.7,8 Children are more susceptible to infection, and, once infected, they excrete influenza virus longer and in a greater quantity than adults.9–11 School classroom crowding and hygiene issues of children may also play roles in facilitating influenza transmission. The remarkable degree to which the prevention of influenza in children reduced the impact of an influenza outbreak on their families and communities was demonstrated in a number of investigations.12–18 Prevention of influenza infections in children should be a part of any public health approach to reduce influenza infections in children, families, and communities.

A unique community-based intervention during the 2005–2006 school year in Carroll County, Maryland, offered the opportunity to examine the impact of a large-scale influenza immunization of public elementary school children.19 During the fall of 2005, intranasal licensed live attenuated influenza vaccine (LAIV) was offered to all healthy Carroll County public elementary school children at no charge. We examined the direct and indirect impacts of this program on student absenteeism in public elementary schools, as well as public middle and high schools, during a subsequent influenza outbreak.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Design
This study used existing anonymous information, including laboratory/antigen influenza testing information, electronically collected public school absenteeism records, census data, and information from the public health influenza immunization program. The study was reviewed and approved by the institutional review board at the University of Maryland.

Populations
Primary Intervention Group
During the school year 2005–2006, all of the healthy students in all 21 Carroll County public elementary schools were offered the 2005 licensed LAIV during the fall of 2005. A total of 5319 (44%) of the 12090 students enrolled in Carroll County public elementary schools received the LAIV. Private schools were not included in this study. A description of this school-based vaccination program was published previously.19 All of the Carroll County public elementary, middle, and high schools for this year were considered intervention schools for the purposes of this study. None of the elementary schools are attached to middle or high schools. Public school student enrollment for Carroll County in the fall of 2005 was 12090 for elementary, 6888 for middle, and 9696 for high schools. Carroll County is west of Baltimore and includes rural, suburban, and small-town environments.

Control Group
Carroll County public schools from the fall of 2001 through the spring of 2005 were considered the first part of our control group. However, it must be noted that 3 Carroll County elementary schools for the school year 2004–200517 and 1 elementary school for the year 2003–200414 participated in a school-based influenza vaccination program using LAIV and were not included in the analyses. All of the Frederick County public schools from the fall of 2001 through the spring of 2006 were considered control schools and represented the second part of our control group. Public school student enrollment for Frederick County in the fall of 2005 was 17288 for elementary, 9264 for middle, and 12941 for high schools. Frederick County is adjacent to Carroll County and, like Carroll County, consists of rural, suburban, and small-town environments. General demographic information about the 2 counties was obtained from government Web sites.20–23

Influenza Surveillance
Several sources were used to determine the weeks of high influenza activity in Frederick and Carroll counties. First, anonymous positive influenza cultures and/or antigen test results were collected for the fall 2001 through spring 2006 from the University of Maryland Medical Center (Baltimore, MD), Carroll County Medical Center (Westminster, MD), and Frederick Memorial Hospital (Frederick, MD). In addition, anonymous influenza antigen test results were collected from 3 medical practices in Carroll County for the fall of 2002 through the spring of 2005. These data were used to calculate influenza activity in the region and to describe predefined influenza activity periods. These included the peak week (PW), defined as the week with the highest number of positive influenza tests. The influenza outbreak period (IOP) was defined as the PW and its adjacent weeks to include 85% of the season's total positive tests.

Absentee Data
The public school systems for each county provided anonymous all-cause absentee data for each school, by week, for years 2001 through 2006. Only absentee data for weeks in which schools were open for ≥3 full days were included. Absentee rates during the last 2 weeks of September and all of the full weeks in October provided baseline data for periods without influenza activity.

Data Analyses
For each county and year, absolute changes in absenteeism between the baseline period and the influenza-affected periods (PW and IOP) were calculated. To assess the impact of the vaccination program, changes in absenteeism for the intervention (Carroll County 2005–2006) was compared with the 9 other observations (Carroll County 2001–2005 and Frederick County 2001–2006).

These 10 data points were analyzed in a 2-way analysis of variance model allowing for an effect of county and intervention. The model determined whether the observed change in absenteeism in Carroll County 2005–2006 was less than expected by chance alone given the year-to-year variation in change of absenteeism, and it allowed for a constant yearly difference between counties. P values were calculated by using standard analysis of variance methods. Statistical significance was defined as a P value of <.05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The demographic and geographic characteristics of Frederick and Carroll Counties are similar (Table 1). Table 2 shows the IOPs for years 2001 through 2006 that we determined from positive influenza tests at community hospitals and offices. It also shows annual vaccine composition and subsequent, circulating influenza strains detected by the CDC national surveillance network.24–33 Data from the largest hospital in each of the 2 counties also demonstrated that influenza outbreaks occurred at approximately the same time in both counties each year (data available on request).


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  		TABLE 1 Demographics of Maryland Study Counties

 

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  		TABLE 2 Influenza Outbreaks in Central Maryland, Vaccine Composition, and Proportion of US-Sampled Strains Matching the Vaccine Profile From 2001 to 2006

 
Background vaccination status of the students in each county was not obtained during the 2005–2006 school year, but in a previous study, background influenza vaccination status of Carroll County elementary students and their families was determined by survey. An estimated 12% to 17% of Carroll County elementary school students and their household members received trivalent inactivated influenza vaccine (TIV) during 2004–2005.17

Figure 1 shows the percentage of student absenteeism in the elementary, middle, and high schools of each county during baseline, PW, and IOP. There was an expected rise in absenteeism during PW and IOP over baseline for our control group (for all of the years in Frederick County and for years 2001 through 2005 in Carroll County). When compared with the control group, there was a reduced rise in absenteeism over baseline during PW and IOP for all of the schools in Carroll County during the 2005–2006 intervention.


Figure 1
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  		FIGURE 1 Student absenteeism in Frederick and Carroll County public schools during baseline influenza-free period influenza outbreak period (IOP), and peak week (PW) of influenza activity from 2001 to 2006. A, Elementary schools; B, middle schools; C, high schools.

 
Table 3 provides a statistical comparison of the intervention year (Carroll County 2005–06) to the control group (Carroll County 2001–2005 and Frederick County 2001–2006). We observed statistically significant, reduced absenteeism during the IOP for the 2005–2006 intervention in Carroll County elementary and high schools. Variation in excess absenteeism was observed during each influenza season, but Carroll County's blunted rise in absenteeism during the intervention year was unlikely because of chance alone. Reduced absenteeism during the IOP was not significant for middle schools, but the trend and magnitude were similar to those observed for elementary and high schools. Trends were also similar for the PW of influenza activity but did not reach statistical significance.


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  		TABLE 3 Change in Percentage of Absenteeism During PW and IOP From Baseline in Carroll County 2005–2006 (Intervention) Versus All Other Years in Frederick and Carroll Counties (Control Group)

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The data presented in this study reveal an association between school-based influenza vaccination in Carroll County public elementary schools during the fall of 2005 and reduced absenteeism during a subsequent influenza outbreak. The data suggest not only a direct impact on elementary schools but also an indirect impact on high schools, which did not participate in the vaccination program. This trend, although not statistically significant, was also seen in the middle schools. A smaller number of middle schools as compared with elementary and high schools may account for the wider confidence intervals associated with the estimated differences in absenteeism.

We do not know the proportion of students who received influenza vaccination (LAIV or TIV) outside of our intervention, and this is a limitation of the study. Despite public knowledge of a school-based vaccination effort in Carroll County in 2004–2005, commercial use of LAIV was reportedly low outside of this public health effort (MedImmune data on file). Also, data from previous years suggested that the use of TIV in Carroll County households was low, at 12% to 17%.14,17 The CDC reports a similarly low vaccination rate among school-aged children who are household contacts of individuals at risk.6 We do not think that the association between vaccination and reduced absenteeism was because of background influenza vaccination in the secondary schools of Carroll County.

Previous studies have demonstrated that vaccinating children improved their health status and indirectly improved community health. The vaccination of 86% of school children with inactivated influenza vaccine was associated with reduced student absenteeism and decreased respiratory illnesses in children and adults.13 A relatively modest immunization rate (20%–25%) in school children of Temple-Belton, Texas, was associated with a reduction in medically attended acute respiratory illness in adults when compared with a nonintervention community.34 Vaccinating day care children with inactivated influenza vaccine was associated with a reduction of missed school days by older siblings.18 In a multicenter study, 46% of children received LAIV in an elementary school-based intervention. During the subsequent influenza outbreak, not only were significant reductions of influenza-like illness, physician visits, and lost school days observed among young children, but also fewer influenza-like illness and lost work days were observed among household adults in the intervention school families as compared with nonintervention school families.17 Finally, epidemiologic data from Japan suggest that influenza vaccination of Japanese schoolchildren was associated with reduced mortality in the elderly.12


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
In this study, a modest LAIV vaccination rate of 44% of public school elementary students was associated with reduced absenteeism in elementary and high schools, which suggests that the protective effect of vaccination extended to secondary schools. Our school-based program provided an efficient method of vaccinating children against influenza and directly reduced elementary school absenteeism during the influenza outbreak. Our results also suggest indirect protection that extended to unvaccinated community members. School-based influenza vaccination programs could serve as an important part of public health plans designed to protect children and their community contacts at highest risk for influenza and its complications. Additional research is needed to determine whether these kinds of programs reduce morbidity and mortality associated with influenza outbreaks. Future studies should also address the cost-effectiveness of school-based influenza vaccination programs.


   ACKNOWLEDGMENTS
 
We thank Stephen Guthrie and Marge Hoffmaster, RN (Carroll County Public School system), Elizabeth Ruff, MD, Susan Kiler, and Larry Leitch, MA, MPA (Carroll County Health Department), Helen Monk (Frederick County Public School System), Joan Lawrence (Maryland Department of Health and Mental Hygiene), Dennis Hansford (Frederick Hospital Virology Laboratories), and Bea Jackson (Carroll Medical Center Virology Laboratories) for their contributions to this study.


   FOOTNOTES
 
Accepted Jan 22, 2008.

Address correspondence to Mollie M. Davis, MD, MPH, Johns Hopkins School of Medicine, Division of General Internal Medicine, 1830 E Monument St, RM 8011, Baltimore, MD 21205. E-mail: mdavis93{at}jhmi.edu

Financial Disclosure: MedImmune, Inc donated all of the vaccine doses for the program and provided grant support to Ms Cummings and Drs King and Magder.


What's Known on This Subject

Children are often the first group to experience influenza during outbreaks, and student absenteeism is an early marker for outbreaks. Despite the benefit and cost-effectiveness of influenza vaccination, population estimates of vaccination remain low even among groups at high risk.

 

What This Study Adds

Countywide school-based influenza vaccination of elementary students was associated with reduced absenteeism during an influenza outbreak. The data suggest not only a direct impact on elementary schools but also an indirect impact on high schools.

 


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics




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