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Illness Among Schoolchildren During Influenza Season
Effect on School Absenteeism, Parental Absenteeism From Work, and Secondary Illness in Families
Kathleen M. Neuzil, MD, MPH;
Cynthia Hohlbein, RN;
Yuwei Zhu, MD, MS
Arch Pediatr Adolesc Med. 2002;156:986-991.
ABSTRACT
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Background High attack rates of Influenzavirus among school-aged
children tend to be expected to cause significant disruption of usual activities
at school and at home.
Objective To quantify the effect of influenza season on illness episodes, school
absenteeism, medication use, parental absenteeism from work, and the occurrence
of secondary illness in families among a cohort of children enrolled in an
elementary school during the 2000-2001 influenza season.
Design Prospective survey study.
Setting Kindergarten through eighth grade elementary school in Seattle, Wash.
Patients or Other Participants All children enrolled in the school were eligible for the study. Study
participants were 313 children in 216 families.
Main Outcome Measures The primary outcome measure was missed school days. Secondary outcomes
measures included total illness episodes, febrile illness episodes, medication
usage, physician visits, parental workdays missed, and secondary illnesses
among family members of children in the study cohort. Differences between
the rates of study events among participants when influenza was circulating
and the event rates during the winter season when influenza was not circulating
were used to calculate influenza-attributable excess events.
Results Total illness episodes, febrile illness episodes, analgesic use, school
absenteeism, parental industrial absenteeism, and secondary illness among
family members were significantly higher during influenza season compared
with the noninfluenza winter season. For every 100 children followed up for
this influenza season, which included 37 school days, an excess 28 illness
episodes and 63 missed school days occurred. Similarly, for every 100 children
followed up, influenza accounted for an estimated 20 days of work missed by
the parents and 22 secondary illness episodes among family members.
Conclusion Influenza season has significant adverse effects on the quality of life
of school-aged children and their families.
INTRODUCTION
INFLUENZA CAUSES annual winter epidemics of respiratory disease that
affect all age groups and all segments of the population. Serious complications
and hospitalizations due to Influenzavirus occur
preponderantly in persons younger than 2 years, persons 65 years and older,
and persons with certain chronic medical conditions. Deaths occur preponderantly
in persons older than 70 years.1-7
However, even among otherwise healthy individuals, the health and economic
consequences of influenza are substantial. Annual influenza attack rates vary
from 10% to 30% in adults and 20% to 50% in children during interpandemic
years, and may approach 70% during pandemic years.3-4,8-10
Among adults, influenza infections lead to increased health care visits, medication
usage, work loss, and restricted activity days.11-14
While the epidemic nature of influenza and the high attack rates in
children would be expected to cause significant disruption of usual activities
at school and at home, data on the effects of influenza on school-aged children
are limited. In a study of healthy children aged 5 through 14 years enrolled
in Tennessee Medicaid, influenza was associated with a health care visit in
approximately 8% of the children and with an antibiotic prescription in approximately
7%.5 This study likely underestimated the effect
of influenza on this population, as it did not examine the effects of influenza
on school-aged children who did not seek medical care. Additional adverse
effects of influenza in this population include the discomfort of the illness,
increased over-the-counter medication usage, and school absenteeism.3, 15 Influenza in a child may also affect
the family. Working parents may stay home to care for a sick child, leading
to industrial absenteeism,16 or sick children
may transmit Influenzavirus to other family members.17-20
Considering the potential for influenza to substantially affect the
quality of life of children and their families, targeting school-aged children
for prevention or treatment of influenza may reduce the individual and societal
burden of this disease. This prospective study was designed to quantify the
effect of influenza season on school and industrial absenteeism, on health
care and medication usage, and on secondary illnesses within families, among
a cohort of schoolchildren and their families.
PARTICIPANTS AND METHODS
STUDY DESIGN
We conducted a 1-year prospective study of the effect of influenza season
on a cohort of children enrolled in a large elementary school in Seattle,
Wash. Baseline surveys obtained information on household size, prevalence
of childhood asthma, and receipt of influenza vaccine. When a child was absent
from school during the winter season, from December 4, 2000, through April
13, 2001, surveys were sent to the child's parent or guardian to determine
the reason for the absence, to characterize the types and severity of illnesses
that occurred during the winter season, and to determine the effect of the
illness on medication usage, physician visits, parental industrial absenteeism,
and secondary illnesses within the family.
This study was approved by the Human Subjects Division at the University
of Washington. Baseline surveys and informed consent were sent to all parents
at the school. Parents chose to enroll in the study by returning the baseline
survey and the accompanying informed consent. After receiving the informed
consent from the parents, two of us (K.M.N., C.H.) obtained assent from the
children. These children and their families constituted the study population.
SOURCE POPULATION
The study school is a parochial elementary school (grades kindergarten-8)
located in central Seattle and draws children from 24 ZIP codes within the
city, and 14 ZIP codes from the surrounding suburbs. The school represents
an ethnically and socioeconomically diverse population of children. Of a total
enrollment of 611 children, 18% are nonwhite; almost 20% receive financial
aid.
DATA COLLECTION
Baseline Data
Baseline data on household size, ages of all household members, and
receipt of influenza vaccine by each member of the family was collected from
all of the 216 families who chose to participate. To determine the prevalence
of asthma among the schoolchildren, the survey also included a question asking
whether a physician had ever diagnosed asthma for the child.
Illness Data
Coded, computerized absentee records were obtained by the study coordinator
(C.H.) from the school office at the end of each week. Children who were participating
in the study were identified. From December 4, 2000, through April 13, 2001
(the day before spring break), the parent or guardian of a child listed on
the computerized absentee records was sent a survey inquiring about the child's
reason for missing school. If the child missed school for an illness, then
the parent completed the remainder of the form, which asked details about
the symptoms of the illness, medication usage, health care use, parental industrial
absenteeism, and illnesses among other household members. The following symptoms
were included on the survey: fever, coryza, sore throat, cough, myalgia, earache,
headache, nausea, vomiting, and diarrhea. Parents returned the surveys in
stamped, self-addressed envelopes to the study nurse (C.H.). If the survey
was not received by the study nurse within 2 weeks, a telephone call was placed,
and the details of the absence were ascertained by telephone interview.
Influenza Season
Influenza season was defined by prospective viral surveillance at the
University of Washington Clinical Virology Laboratory at Children's Hospital
and Medical Center.21 Influenza season was
defined as the first day of the first week in which there were at least 5
isolates of Influenzavirus, until the last day of
the last week in which there were at least 5 isolates of Influenzavirus.
MAIN OUTCOME MEASURES
The primary outcome measure was the total number of school days missed
during influenza season compared with the noninfluenza winter season. Secondary
outcomes included the total illness episodes, febrile illness episodes, other
symptoms associated with the illness episodes, number of days that parents
miss work secondary to childhood illness, the number of family members who
become ill within 3 days of the child's illness, and the number of health
care visits and medications dispensed during influenza season.
DATA ANALYSIS
The expected number of study outcomes during influenza season was calculated
based on the rate of study outcomes observed during the noninfluenza winter
season. The observed number of study events during influenza season was then
compared with the expected number, and a relative risk was calculated. Influenza-attributable
excess events were calculated by subtracting the expected outcomes from the
observed outcomes during influenza season. An excess event rate per 100 children
was then generated by dividing by the total number of children in the cohort
(313), then multiplying by 100. The 95% confidence intervals were generated
using StatXact (Cytel Software, Cambridge, Mass).  2 or Fisher
exact test was used as appropriate for symptom comparison between the influenza
and noninfluenza winter season. In an attempt to control for the confounding
effect of respiratory syncytial virus (RSV) circulation, a nested analysis
was performed that was restricted to January 8, 2001, through March 31, 2001,
during which the mean number of RSV isolates per week was equivalent during
the influenza and noninfluenza winter season. All calculations other than
the 95% confidence interval were done using SAS version 8.0 (SAS Institute
Inc, Cary, NC).
RESULTS
Of 428 families with 611 children enrolled at the school, 216 families
with 313 children chose to participate in the study. Baseline characteristics
of the study population are given in Table
1. Participation was equally distributed through all of the grades—with
a low of 9% of the participants being second graders to a high of 14% of participants
being eighth graders. The prevalence of asthma among this study population
was 12%, and 9 (24%) of 37 children with asthma received influenza vaccine
during the study year. Among all participants, 6% of the study children, 25%
of the parents, 37% of the grandparents, and 5% of other household members
reported receiving influenza vaccine.
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Table 1. Baseline Characteristics of 313 Children in 216 Families Participating
in Illness Survey Study*
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INFLUENZA SEASON
Influenza season occurred in the Seattle area from January 8, 2001,
through March 2, 2001. Influenza A (H1N1) and influenza B viruses circulated
during this period. Influenza season included 37 school days. The noninfluenza
winter season occurred from December 4, 2000, through January 5, 2001, and
March 5, 2001, through April 13, 2001, representing 44 school days. Respiratory
syncytial virus circulated in the Seattle area during the entire study period,
from December 4, 2000, through April 13, 2001 (Figure 1). The mean number of RSV isolates per week was higher in
influenza season than in the noninfluenza winter season, at 37 and 23 per
week, respectively. From January 8, 2001, through March 31, 2001, the mean
number of RSV isolates per week was 37 during both influenza season and the
noninfluenza winter season. Parainfluenza virus circulated at relatively constant
levels throughout the study period (Figure
1).
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The number of isolates of influenza (solid line), respiratory syncytial
virus (large dashed line), and parainfluenza (small dashed line) per week
at Children's Hospital and Regional Medical Center, Seattle, Wash, during
the 2000-2001 school year. Adapted from the University of Washington Clinical
Virology Laboratory Web site.21
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OUTCOME RATES
Throughout the school year, weekly rates of absenteeism were monitored.
The weekly percentage of children in the study who missed school was similar
to the percentage of all students who missed school (data not shown). From
December 4, 2000, through April 13, 2001, on notification by the school that
a study participant missed school, 868 surveys were mailed to parents and
804 (93%) were returned. Of these 804 returned surveys, 360 surveys indicated
that either the child did not miss school, or that the child did miss school
but was not ill. On 444 surveys, the parents confirmed that the child missed
school owing to an illness.
Of the 444 illness episodes, 194 (43.7%) occurred during the noninfluenza
winter season, and 250 (56.3%) occurred during influenza season. Among the
313 children monitored throughout the 44 days of the noninfluenza season,
194 illnesses occurred during the 13 772 child-days of follow-up. Using
this rate as the background rate, the expected number of illness episodes
during influenza season was calculated and compared with the observed number.
As given in Table 2, the 250 reported
illnesses during influenza season exceeded the expected number by more than
50%. The 87 excess illness events occurring among 313 children followed up
during winter represents an estimated influenza attack rate of 28%. In addition
to total illness episodes, days of school missed per episode was higher during
influenza season than during the noninfluenza winter season. Febrile illnesses
increased during influenza season, with the difference in illness episodes
entirely accounted for by illness episodes with fever. Analgesic use during
influenza season, and parental work absenteeism, were likewise higher than
expected during influenza season. The observed numbers of antibiotic prescriptions
and health care visits were not statistically significantly greater than expected
during influenza season (Table 2).
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Table 2. Effect of Winter Illness on School and Family Among 313 Schoolchildren
Monitored From December 1, 2000, Through April 13, 2001
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To determine the excess event rate for outcomes during influenza season,
the expected rate during influenza season was subtracted from the observed
rate (Table 2). It is estimated
that for every 100 children followed up for this influenza season, which included
37 school days, an additional 28 illness episodes and 63 missed school days
would occur. Similarly, for every 100 children followed up, influenza accounted
for an estimated 20 excess days of work missed by the parents. When the study
was restricted to periods of peak RSV activity, from January 8, 2001, through
March 31, 2001, estimates of influenza-attributable events were similar (data
not shown).
During influenza season, parents were much more likely to report illness
in other household members in the 3 days following the child's absence from
school compared with the noninfluenza winter season. An estimated 22 excess
secondary illness episodes occurred for every 100 children followed up during
this influenza season (Table 2).
Of the 126 household members who became ill during influenza season within
3 days of the child's illness, 46% were parents, 33% were siblings aged 5
to 17 years, 20% were siblings younger than 5 years, and fewer than 1% were
grandparents.
ILLNESS CHARACTERISTICS
Fever was reported as a component of 67% of illnesses during influenza
season compared with 49% of illnesses during the noninfluenza winter season
(P = .001). Similarly, febrile respiratory illness
(defined as fever with at least one of the following symptoms: cough, runny
nose, or sore throat) was significantly more common in influenza season compared
with the noninfluenza winter season (57% vs 44%, P
= .04). The systemic symptoms of myalgia and headache were significantly more
frequent during influenza season compared with the noninfluenza winter season
among children aged 11 to 14 years, but not among younger children. There
were no differences in the prevalence of nausea, vomiting, diarrhea, or earache
among illnesses in any age group occurring during the influenza and noninfluenza
winter season.
COMMENT
This Seattle population–based study examined the effect of the
influenza season on multiple and diverse outcomes among schoolchildren and
their families during the 2000-2001 winter season. Illness during influenza
season was common, with an estimated 87 excess illness events occurring among
313 children followed up during the winter, for an attack rate of 28%. This
likely represents a minimum estimate, as it only included children who were
sufficiently ill to miss a day of school, and did not include illnesses that
occurred only on weekends or school holidays. This attack rate is consistent
with other studies that report symptomatic attack rates of 23% to 48% among
school-aged children during interpandemic years.22-25
The total number of school days missed during influenza season was likewise
higher than expected based on the noninfluenza winter season baseline. We
estimated that for this influenza season, which encompassed 37 school days,
63 excess school days were missed for every 100 children followed up. Estimates
of school days missed per 100 children due to influenza infection from a randomized,
controlled trial of influenza vaccine among schoolchildren in Russia were
slightly higher at 79 school days missed for every 100 unvaccinated children.26
The increase in absenteeism for illness in our cohort was paralleled
by increases in febrile illnesses and analgesic use. That fever is a major
component of influenza illness in children is well established.27-28
Health care visits and antibiotic use did not increase significantly during
influenza season compared with the noninfluenza winter season. This is in
contrast to other studies that demonstrate significant excess outpatient health
care visits and antibiotic prescriptions among school-aged children during
influenza season.5 The reasons for this discrepancy
are unclear, but may relate to differences in parents' knowledge and attitudes
about viral illness, the threshold for bringing children to a physician, or
our relatively small sample size.
The effect of influenza season on this cohort extended beyond illness
in the schoolchildren. In this study, significant excess industrial absenteeism
occurred among the parents, who missed almost 1 day of work for every 3 days
of school missed by a child attributable to influenza infection. National
data report that 57% of mothers and 97% of fathers of school-aged children
work full-time and, thus, may need to miss work or hire alternative care if
their children miss school.16 Presumably, our
study population included fewer households with 2 working parents, or parents
with more flexibility in their schedules or alternative child care providers.
Rates of parental absenteeism could be higher in other populations. Our estimates
of parental industrial absenteeism were based solely on missing work to care
for a sick child, and did not include work that may have been missed if the
child transmitted influenza to the parent.
Children more frequently shed Influenzavirus
compared with adults,29 and this may facilitate
the transmission of Influenzavirus. In a large general
practice population outside London, England, during the pandemic of 1957,
attack rates in adults who resided with school-aged children were 2 to 3 times
higher than attack rates in adults who did not reside with school-aged children.30 Family studies of influenza transmission in Seattle
and Tecumseh, Mich, during the 1970s found children to be the main introducers
of influenza infection into households during interpandemic periods.17-18,20 In this study, the
number of household members who became ill within 3 days of a child's absence
from school was 2.2 times higher than expected during influenza season. For
every 10 children who miss school for an influenza-related illness, our data
suggest that 8 household members will subsequently become ill. Increased use
of influenza vaccine among children could reduce illness in household or community
contacts. In a 1995 randomized controlled trial of influenza vaccine for preschool-aged
children, influenza-unvaccinated household contacts of influenza-vaccinated
children had 42% fewer febrile respiratory illnesses compared with unvaccinated
household contacts of control children.13 Mass
vaccination of schoolchildren has been correlated with reduced respiratory
illness in Tecumseh31 and with reductions in
all-cause mortality rates in Japan,32 suggesting
that immunization on a larger scale can affect community epidemics.
This was a survey study, and we did not attempt to diagnose the reported
illnesses by clinical or laboratory evaluation. We assumed that noninfluenza
illnesses occurred equally during the influenza and noninfluenza winter season,
so that any excess during influenza season was attributable to influenza infection.
Using a similar method, our estimates of influenza-associated hospitalizations
and outpatients visits in children correlated well with laboratory documented
rates of influenza disease.5, 8
That most of the excess illness in this study was febrile illness is consistent
with the clinical picture of Influenzavirus in children.9, 23-24,27-28
Likewise, our secondary analysis that was restricted to peak RSV season yielded
results similar to our primary analysis, suggesting that RSV was not a significant
confounder.
This study included only 1 influenza season, in which influenza type
B and type A (H1N1) strains circulated. The effect of influenza varies from
year to year, and may be influenced by circulating strains and the underlying
immunity in the population. While in adults morbidity is generally believed
to be greatest when H3N2 viruses are circulating,33-35
the effect of different viral strains on morbidity in school-aged children
is not well established, as all 3 strains may cause high attack rates or serious
illness.25-26,28, 36
Studies that include multiple influenza seasons are needed to adequately address
this issue.
CONCLUSIONS
Among a cohort of children followed up during the winter season, total
illness episodes, school days missed, workdays missed by parents, and subsequent
illnesses among household members were significantly increased when Influenzavirus circulated in the community. These data
should aid pediatric health care providers and parents when deciding whether
to immunize a healthy school-aged child with influenza vaccine. When planning
important school events during influenza season, school administrators should
be cognizant of the potential for significant increases in school absenteeism.
Finally, this study reinforces the recommendation to vaccinate children if
they reside in households with persons who are at increased risk for complications
of Influenzavirus, to reduce the potential for transmission.4
| What This Study Adds
Symptomatic influenza illness is frequent among school-aged children.
However, studies evaluating the effect of influenza illness on quality of
life in such children are unavailable. This prospective, population-based
study quantifies a major effect of Influenzavirus
on multiple and diverse outcomes in schoolchildren and their families, including
significant increases in school absenteeism, analgesic use, parental industrial
absenteeism, and secondary illness among family members. Such information
is important for both individual and public policy decisions regarding the
use of influenza vaccine in school-aged children.
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AUTHOR INFORMATION
Accepted for publication May 10, 2002.
This study was funded through a research grant from GlaxoWellcome Worldwide
Epidemiology. GlaxoWellcome Worldwide Epidemiology had no role in the design,
conduct, collection, analysis, or interpretation of the data and did not review
or approve the manuscript prior to submission.
We are indebted to the students, parents, and staff at St Joseph's School
for their enthusiastic participation in this study, and to Anne Cent, Children's
Hospital and Regional Medical Center, Seattle, for her dedication to organizing
and maintaining the viral surveillance data.
Corresponding author and reprints: Kathleen M. Neuzil, MD, MPH, University
of Washington School of Medicine, Veterans Affairs Puget Sound Health Care
System, 1660 S Columbian Way, Seattle, WA 98108 (e-mail:kneuzil{at}u.washington.edu).
From the Department of Medicine, University of Washington School of
Medicine (Dr Neuzil) and the Veterans Affairs Puget Sound Health Care System
(Dr Neuzil and Ms Hohlbein), Seattle; and the Department of Pediatrics, Vanderbilt
University School of Medicine, Nashville, Tenn (Dr Zhu).
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Influenza vaccination in asthmatic children: effects on quality of life and symptoms
Bueving et al.
Eur Respir J 2004;24:925-931.
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Burden of influenza in healthy children and their households
Principi et al.
Arch. Dis. Child. 2004;89:1002-1007.
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Clinical Predictors of Influenza in Children
Friedman and Attia
Arch Pediatr Adolesc Med 2004;158:391-394.
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Incidence of Outpatient Visits and Hospitalizations Related to Influenza in Infants and Young Children
O'Brien et al.
Pediatrics 2004;113:585-593.
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Every Nose Counts: A New Influenza Vaccine for All Healthy Schoolchildren?
Gaglani and Herschler
CLIN PEDIATR 2004;43:35-41.
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Direct and Total Effectiveness of the Intranasal, Live-Attenuated, Trivalent Cold-Adapted Influenza Virus Vaccine Against the 2000-2001 Influenza A(H1N1) and B Epidemic in Healthy Children
Gaglani et al.
Arch Pediatr Adolesc Med 2004;158:65-73.
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Severe acute respiratory syndrome: Capture-recapture method should be used to count how many cases of SARS really exist
Lange and LaPorte
BMJ 2003;326:1396-1396.
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