Countywide School-Based Influenza Immunization: Direct and Indirect Impact

on Student Absenteeism
Mollie M. Davis, James C. King, Jr, Lauren Moag, Ginny Cummings and Laurence S.
Magder
Pediatrics 2008;122;e260-e265
DOI: 10.1542/peds.2007-2963

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/122/1/e260

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

publication, it has been published continuously since 1948. PEDIATRICS is owned, published,
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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, Laurence S. Magder, PhDb

Departments of aPediatrics and bEpidemiology, University of Maryland School of Medicine, Baltimore, Maryland.

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 What This Study Adds

Children are often the first group to experience influenza during outbreaks, and student Countywide school-based influenza vaccination of elementary students was associated
absenteeism is an early marker for outbreaks. Despite the benefit and cost-effectiveness with reduced absenteeism during an influenza outbreak. The data suggest not only a
of influenza vaccination, population estimates of vaccination remain low even among direct impact on elementary schools but also an indirect impact on high schools.
groups at high risk.

ABSTRACT
OBJECTIVE. Live attenuated influenza vaccine was given to 5319 (44%) of the 12 090
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 www.pediatrics.org/cgi/doi/10.1542/
peds.2007-2963
countywide student absenteeism during the subsequent influenza outbreak.
doi:10.1542/peds.2007-2963
METHODS. This study used existing, anonymous information: census data, community Key Words
influenza tests, and public school absenteeism data. The intervention group was influenza, vaccination, children, school,
Carroll County, years 2005–2006. The control group included Carroll County, years absenteeism
2001–2005, and adjacent Frederick County, years 2001–2006. Weekly student ab- Abbreviations
CDC—Centers for Disease Control and
senteeism was determined during baseline influenza-free periods and influenza
Prevention
outbreak periods for all of the public schools. LAIV—live attenuated influenza vaccine
PW—peak week
RESULTS. The absolute change in absenteeism during the influenza outbreak periods IOP—influenza outbreak period
over baseline in elementary schools was 0.61% for the intervention group and TIV—trivalent inactivated influenza
1.79% for the control group. Similarly, the change in absenteeism during the vaccine
influenza outbreak period over baseline for high schools was 0.32% for the inter- Accepted for publication Jan 22, 2008

vention group and 1.80% for the control group. Although not statistically significant, Address correspondence to Mollie M. Davis,
MD, MPH, Johns Hopkins School of Medicine,
trends in middle schools were similar. Division of General Internal Medicine, 1830 E
Monument St, RM 8011, Baltimore, MD 21205.
CONCLUSIONS. Countywide school-based influenza vaccination was associated with re- E-mail: mdavis93@jhmi.edu
duced absenteeism during an influenza outbreak. The data suggest not only a direct PEDIATRICS (ISSN Numbers: Print, 0031-4005;
impact on elementary schools but also an indirect impact on high schools. School- Online, 1098-4275). Copyright © 2008 by the
American Academy of Pediatrics
based programs provide an efficient method of providing influenza vaccination to
children, and protection may extend to unvaccinated community members. Addi-
tional research is needed to determine whether school-based vaccination of children reduces morbidity and mortality
associated with influenza outbreaks. Pediatrics 2008;122:e260–e265

I NFLUENZA IS A major cause of global morbidity and mortality. In the United States alone, there are ⬃200 000
hospitalizations and 36 000 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 vaccina-
tion 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

e260 DAVIS et al
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children may also play roles in facilitating influenza TABLE 1 Demographics of Maryland Study Counties
transmission. The remarkable degree to which the pre- Demographic Characteristics Carroll County Frederick County
vention of influenza in children reduced the impact of 22,23
Population (2006 estimated), n 170 260 222 938
an influenza outbreak on their families and communities
Population Density (2000),22,23 336 295
was demonstrated in a number of investigations.12–18 persons per square mile
Prevention of influenza infections in children should be No. of schools (2005;
a part of any public health approach to reduce influenza enrollment)20,21
infections in children, families, and communities. Elementary 21 (11 471) 35 (14 406)
A unique community-based intervention during the Middle 9 (6888) 12 (9154)
2005–2006 school year in Carroll County, Maryland, High 7 (9696) 9 (12 424)
offered the opportunity to examine the impact of a Other 3 (164) 5 (346)
large-scale influenza immunization of public elementary School attendance rate
(2004–2005),20,21 %
school children.19 During the fall of 2005, intranasal
Elementary 95.6 95.7
licensed live attenuated influenza vaccine (LAIV) was
Middle 95.2 94.7
offered to all healthy Carroll County public elementary High 94.6 93.2
school children at no charge. We examined the direct Race/ethnicity (2005
and indirect impacts of this program on student absen- estimated),22,23 %
teeism in public elementary schools, as well as public White 94.7 87.2
middle and high schools, during a subsequent influenza Black 3.0 7.8
outbreak. Hispanic 1.5 4.6
Mean travel time to work 34.1 31.9
(2000),22,23 min
METHODS Median income (2003 66 617 66 493
Design estimated),22,23 $
Education attainment,22,23 %
This study used existing anonymous information, in-
High school graduate 33 30
cluding laboratory/antigen influenza testing informa- Bachelor’s degree 16 19
tion, electronically collected public school absenteeism Master’s degree or higher 9 11
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.
analyses. All of the Frederick County public schools from
the fall of 2001 through the spring of 2006 were consid-
Populations ered control schools and represented the second part of
Primary Intervention Group our control group. Public school student enrollment for
During the school year 2005–2006, all of the healthy Frederick County in the fall of 2005 was 17 288 for
students in all 21 Carroll County public elementary elementary, 9264 for middle, and 12 941 for high
schools were offered the 2005 licensed LAIV during the schools. Frederick County is adjacent to Carroll County
fall of 2005. A total of 5319 (44%) of the 12 090 stu- and, like Carroll County, consists of rural, suburban, and
dents enrolled in Carroll County public elementary small-town environments. General demographic infor-
schools received the LAIV. Private schools were not in- mation about the 2 counties was obtained from govern-
cluded in this study. A description of this school-based ment Web sites.20–23
vaccination program was published previously.19 All of
the Carroll County public elementary, middle, and high Influenza Surveillance
schools for this year were considered intervention Several sources were used to determine the weeks of
schools for the purposes of this study. None of the ele- high influenza activity in Frederick and Carroll counties.
mentary schools are attached to middle or high schools. First, anonymous positive influenza cultures and/or an-
Public school student enrollment for Carroll County in tigen test results were collected for the fall 2001 through
the fall of 2005 was 12 090 for elementary, 6888 for spring 2006 from the University of Maryland Medical
middle, and 9696 for high schools. Carroll County is Center (Baltimore, MD), Carroll County Medical Center
west of Baltimore and includes rural, suburban, and (Westminster, MD), and Frederick Memorial Hospital
small-town environments. (Frederick, MD). In addition, anonymous influenza an-
tigen test results were collected from 3 medical practices
Control Group in Carroll County for the fall of 2002 through the spring
Carroll County public schools from the fall of 2001 of 2005. These data were used to calculate influenza
through the spring of 2005 were considered the first part activity in the region and to describe predefined influ-
of our control group. However, it must be noted that 3 enza activity periods. These included the peak week
Carroll County elementary schools for the school year (PW), defined as the week with the highest number of
2004 –200517 and 1 elementary school for the year 2003– positive influenza tests. The influenza outbreak period
200414 participated in a school-based influenza vaccina- (IOP) was defined as the PW and its adjacent weeks to
tion program using LAIV and were not included in the include 85% of the season’s total positive tests.

PEDIATRICS Volume 122, Number 1, July 2008 e261

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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 ⱖ3 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 anal-
ysis 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 absentee-
ism, and it allowed for a constant yearly difference be-
tween counties. P values were calculated by using stan-
dard analysis of variance methods. Statistical significance
was defined as a P value of ⬍.05.
RESULTS
The demographic and geographic characteristics of Fred-
erick 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 com-
position 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).
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 stu-
dents 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.
Table 3 provides a statistical comparison of the inter-
vention year (Carroll County 2005– 06) to the control
group (Carroll County 2001–2005 and Frederick County
2001–2006). We observed statistically significant, re-
duced 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 absen-
teeism 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.

TABLE 2 Influenza Outbreaks in Central Maryland, Vaccine Composition, and Proportion of US-Sampled Strains Matching the Vaccine Profile
From 2001 to 2006
Season PW Influenza Outbreak Period Influenza Vaccine Composition24–28 Proportion of US
Sampled Strains
Matching Vaccine
Profile29–33
2001–2002 January 1, 2002 December 2, 2002, to March 3, 2002 A/Moscow/10/99–like (H3N2), 393/393 H3N2 strains
A/New Caledonia/20/99–like (H1N1), 30/30 H1N1 strains
B/Sichuan/379/99–like antigens 61/267 B strains
2002–2003 February 2, 2003 January 19, 2003 to March 16, 2003 A/Moscow/10/99–like (H3N2), 121/143 H3N2 strains
A/New Caledonia/20/99–like (H1N1), 287/287 H1N1 strains
B/Hong Kong/330/2001–like antigens 268/269 B strains
2003–2004 December 21, 2003 November 30, 2003 to January 11, 2004 A/Moscow/10/99–like (H3N2), 106/949 H3N2 strains
A/New Caledonia/20/99–like (H1N1), 3/3 H1N1 strains
B/Hong Kong/330/2001–like antigens 5/71 B strains
2004–2005 February 6, 2005 January 2, 2005 to March 13, 2005 A/Fujian/411/2002–like (H3N2), 156/706 H3N2 strains
A/New Caledonia/20/99–like (H1N1), 11/11 H1N1 strains
B/Shanghai/361/2002–like antigens 219/355 B strains
2005–2006 March 12, 2006 January 22, 2006 to April 16, 2006 A/California/7/2003–like (H3N2), 410/563 H3N2 strains
A/New Caledonia/20/99–like (H1N1), 131/135 H1N1 strains
B/Shanghai/361/2002–like antigens 59/321 B strains
PW is the week with the highest number of positive influenza tests. Influenza outbreak period includes the PW and its adjacent, consecutive weeks containing 85% of positive influenza tests.

e262 DAVIS et al
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 10
A Baseline
9 PW
IOP
8

,QWHUYHQWLRQ\HDU
7

Absenteeism, %
6

0
Fred Carr Fred Carr Fred Carr Fred Carr Fred Carr
2001–2002 2002–2003 2003–2004 2004–2005 2005–2006
School year

B 10
Baseline
9 PW
IOP
8

,QWHUYHQWLRQ\HDU
7
Absenteeism, %

6
FIGURE 1
Student absenteeism in Frederick and Carroll County public 5
schools during baseline influenza-free period influenza out- 4
break period (IOP), and peak week (PW) of influenza activity
from 2001 to 2006. A, Elementary schools; B, middle schools; 3
C, high schools.
2

0
Fred Carr Fred Carr Fred Carr Fred Carr Fred Carr
2001–2002 2002–2003 2003–2004 2004–2005 2005–2006
School year

C 10
Baseline
9 PW
IOP
8

,QWHUYHQWLRQ\HDU
7
Absenteeism, %

0
Fred Carr Fred Carr Fred Carr Fred Carr Fred Carr
2001–2002 2002–2003 2003–2004 2004–2005 2005–2006
School year

DISCUSSION and reduced absenteeism during a subsequent influenza

The data presented in this study reveal an association outbreak. The data suggest not only a direct impact on
between school-based influenza vaccination in Carroll elementary schools but also an indirect impact on high
County public elementary schools during the fall of 2005 schools, which did not participate in the vaccination

PEDIATRICS Volume 122, Number 1, July 2008 e263

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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)
Type of Comparison Change in Percentage of Absenteeism
School
Control Group
(Carroll 2001–2005;
Frederick 2001–2006)
Elementary IOP vs baseline 1.79
PW vs baseline 2.31
Middle IOP vs baseline 1.84
PW vs baseline 2.56
High IOP vs baseline 1.80
PW vs baseline 2.32
a Data were analyzed in a 2-way analysis of variance model allowing for an effect of county and intervention.
program. This trend, although not statistically signifi-
cant, 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 previ-
ous years suggested that the use of TIV in Carroll County
households was low, at 12% to 17%.14,17 The CDC re-
ports 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 im-
proved community health. The vaccination of 86% of
school children with inactivated influenza vaccine was
associated with reduced student absenteeism and de-
creased 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 inacti-
vated 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 influ-
enza 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 fam-
ilies as compared with nonintervention school families.17
Finally, epidemiologic data from Japan suggest that in-
fluenza vaccination of Japanese schoolchildren was as-
sociated with reduced mortality in the elderly.12
e264 DAVIS et al
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Estimated Difference P
(95% Confidence
Intervention
Interval)a
(Carroll County
2005–2006)
0.61 1.0 (0.1 to 1.9) .029
0.05 2.3 (⫺0.1 to 4.7) .057
0.61 1.0 (⫺0.3 to 2.2) .12
⫺0.07 2.9 (⫺1.3 to 7.1) .15
0.32 0.9 (0.1 to 1.7) .028
0.07 2.0 (⫺0.6 to 4.6) .11
CONCLUSIONS
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 pro-
gram provided an efficient method of vaccinating chil-
dren 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 influ-
enza vaccination programs could serve as an important
part of public health plans designed to protect children
and their community contacts at highest risk for influ-
enza and its complications. Additional research is needed
to determine whether these kinds of programs reduce
morbidity and mortality associated with influenza out-
breaks. Future studies should also address the cost-effec-
tiveness 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 (Mary-
land Department of Health and Mental Hygiene), Dennis
Hansford (Frederick Hospital Virology Laboratories), and
Bea Jackson (Carroll Medical Center Virology Laborato-
ries) for their contributions to this study.
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PEDIATRICS Volume 122, Number 1, July 2008 e265
Countywide School-Based Influenza Immunization: Direct and Indirect Impact
on Student Absenteeism
Mollie M. Davis, James C. King, Jr, Lauren Moag, Ginny Cummings and Laurence S.
Magder
Pediatrics 2008;122;e260-e265
DOI: 10.1542/peds.2007-2963
Updated Information including high-resolution figures, can be found at:
& Services http://www.pediatrics.org/cgi/content/full/122/1/e260
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