AMERICAN JOURNAL OF EPIDEMIOLOGY
Vol. 129, No. 1
Copyright ffl 1989 by The Johns Hopkins University School of Hygiene and Public Health
All rights reserved
Printed in U.S.A.
AN EXPLOSIVE POINT-SOURCE MEASLES OUTBREAK IN A
HIGHLY VACCINATED POPULATION
MODES OF TRANSMISSION AND RISK FACTORS FOR DISEASE
ROBERT T. CHEN,1 GARY M. GOLDBAUM,2 STEVEN G. F. WASSILAK,1
LAURI E. MARKOWITZ,1 AND WALTER A. ORENSTEIN1
communicable diseases; disease outbreaks; immunization; measles; medical
records; models, theoretical; vaccination; vaccines
Early in this century, Chapin (1) showed
that measles transmission can be interrupted in open wards by preventing direct
contact between patients with measles and
susceptible persons. This finding led to a
widely-held belief that measles could only
be transmitted by direct contact, or in the
absence of direct contact, by local spread
of large respiratory droplets (2). Due to the
rapid settling of the large droplets, effective
Received for publication August 19, 1987, and in
final form March 10, 1988.
Send reprint requests to Technical Information
Service, Center for Prevention Services, Centers for
Disease Control, Atlanta, GA 30333.
1
Division of Immunization, Center for Prevention
Services, Centers for Disease Control, Atlanta, GA.
2
Division of Health Education, Center for Health
Promotion and Education, Centers for Disease Control, Atlanta, GA.
Presented in part to the 113th annual meeting of
the American Public Health Association, Washington,
DC, November 1985.
The authors thank the staff of High School A for
their cooperation; Bob Barger, Ralph March, Janet
Daniels, and Karen McMahon of Illinois Department
of Public Health for their assistance with the outbreak
investigation; and Ira Longini, Herbert W. Hethcote,
Paul E. M. Fine, and Elizabeth R Rovira for their
helpful suggestions in applying the epidemic model.
173
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Chen, R. T. (CDC, Atlanta, GA 30333), G. M. Goldbaum, S. G. F. Wassilak, L. E.
Markowitz, and W. A. Orenstein. An explosive point-source measles outbreak in
a highly vaccinated population: modes of transmission and risk factors for
disease. Am J Epidemiol 1989; 129:173-82.
In 1985, 69 secondary cases, all in one generation, occurred in an Illinois high
school after exposure to a vigorously coughing index case. The school's 1,873
students had a pre-outbreak vaccination level of 99.7% by school records. The
authors studied the mode of transmission and the risk factors for disease in this
unusual outbreak. There were no school assemblies and little or no air recirculation during the schooldays that exposure occurred. Contact interviews were
completed with 58 secondary cases (84%); only 11 secondary cases (19%) of
these may have had exposure to the index case in the classrooms, buses, or out
of school. With the use of the Reed-Frost epidemic model, only 22-65% of the
secondary cases were likely to have had at least one person-to-person contact
with the index case during class exchanges, suggesting that this mode of
transmission alone could not explain this outbreak. A comparison of the first 45
cases and 90 matched controls suggested that cases were less likely than
controls to have provider-verifiable school vaccination records (odds ratio (OR)
= 8.1) and more likely to have been vaccinated at less than age 12 months (OR
= 8.6) or at age 12-14 months (OR = 7.0). Despite high vaccination levels,
explosive measles outbreaks may occur in secondary schools due to 1) airborne
measles transmission, 2) high contact rates, 3) inaccurate school vaccination
records, or 4) inadequate immunity from vaccinations at younger ages.
174
CHEN ET AL.
16 3
1
14 i
10
1
HfWflft. r,
fectiveness. We conducted an investigation
to explore these issues.
MATERIALS AND METHODS
Descriptive epidemiology
A case of measles was defined as an illness characterized by 1) generalized maculopapular rash >3 days duration, 2) fever,
>38.3 C (>101 F), if measured, and 3) at
least one of the following: cough, coryza, or
conjunctivitis. Serologic confirmation was
based on either 1) a fourfold or greater rise
in hemagglutination-inhibition antibody titer between acute and convalescent phase
serum specimens, or 2) the presence of
hemagglutination-inhibition immunoglobulin M (IgM) antibodies.
Cases of measles were ascertained in
High School A as follows: 1) a letter requesting reporting of measles-like symptoms was sent to all parents on April 25; 2)
all absent students with rash illness were
interviewed by the school nurse; 3) all local
physicians and emergency rooms were enrolled in surveillance; 4) all classes were
surveyed by their teachers during period 4
on May 28 for students who had been absent with a febrile rash illness more than
two days since April 1. Students with suspected measles were further interviewed to
determine whether they met the case definition and where they may have had contact with the index case in and out of
school.
Information on absentees, class schedules of the cases, school assemblies, ventilation system, and floor plan was obtained
•
Ifigh School A (K-70)
•
Othar (N-45)
,r,
Bfln
n«
n H
n n
10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30 5 10 15 20 25 30
April
May
June
Date of rash onset
July
FIGURE 1. Reported measles cases by date of rash onset: High School A, Illinois, April-July 1985.
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transmission by this mode is believed to
require susceptible persons to approach
within approximately one meter of the
source (3). These two modes of transmission are frequently classified together as
person-to-person contact transmission.
In the 1930s, Wells (4) noted the important role that airborne droplet nuclei, the
evaporated residue of small respiratory
droplets, played in transmission of infections without direct contact. Initial evidence for this mode of measles transmission came from studies showing a lower
measles incidence in schools with ultraviolet air disinfection relative to schools
without disinfection (5).
More recent evidence supporting airborne transmission comes from studies
showing that measles virus can survive
more than two hours in aerosolized droplet
nuclei (6, 7). Epidemiologic investigations
of measles outbreaks in physician's offices
(8-10), and other settings (11,12) have also
implicated airborne transmission. While its
occurrence is now well documented, the
relative importance of airborne compared
with contact transmission during a measles
outbreak remains poorly understood.
In April 1986, an explosive point-source
measles outbreak occurred in High School
A in Illinois (figure 1). The large number
of cases that followed, 69, all occurring in
one generation after a single index case,
raised questions about the mode and the
setting of such an efficient transmission.
Concomitantly, the high vaccination level
among the students, 99.7 per cent by school
records, raised questions about vaccine ef-
A MEASLES OUTBREAK IN A HIGHLY VACCINATED POPULATION
175
of the hallway in wing A for the entire five
minutes of the exchange period; 2) the radius of effective contact was equivalent to
that of large droplet dispersion, one meter
around the index case, or approximately 6
Hallway contact model
feet (1.8 m) total diameter; 3) the students
in
the hallway mixed randomly; and 4) all
A linear wing of two floors (wing A, figure
2) houses all the traditional classrooms in susceptibles were exhausted in one generHigh School A, each seating approximately ation.
30 students. The classic Reed-Frost model
Let pi denote the probability that any
(13) calculates the probability of person-to- specified susceptible had at least one effecperson contact between cases and suscep- tive contact with the index case during one
tibles for a homogeneously mixing popula- five-minute exchange period. Then qr = 1
tion. The movement of students within the — pi would be the probability of a particular
hallway of Wing A during exchange periods susceptible not having contact during one
closely approximate these conditions.
exchange period.
If the index case was ill and present in
An effective contact was defined as an
encounter in which the infection is trans- the hallway for X exchange periods, the
mitted from an infected to a susceptible. probability, q2, of a student not having conTo calculate the maximum person-to- tact during X exchange periods is given by
person contact rate in the hallway of wing
92 = (<?l)*
(1)
A, the following assumptions were made: 1)
the index case was stationary in the middle Pi, the probability of at least one contact
from High School A. Temperature information was obtained from the National
Weather Service in Chicago, Illinois.
wing A
Cafeteria
1
1
H i i i i i-d=l
Second Floor
H
:
11I
FIGURE 2. Floor plan of High School A, Illinois, showing site of 1985 measles outbreak. Traditional
classrooms are located on two floors in wing A; ® denotes location where hall monitors counted the number of
passing students.
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JfllMIMI
176
CHEN ET AL.
during X exchange periods is then
p 2 = 1 - q2.
(2)
If there are S susceptibles, the expected
number of susceptibles (E) who had at least
one contact with the index case after X
exchange periods is given by
E = (p 2 )S.
(3)
95 per cent CI
= ±(1.96)[(p 2 )( 92 )Sp.
(4)
The probability, p^, of all S susceptibles
having had at least one contact with the
index case in the hallway during X exchange periods is given by
RESULTS
Overview of the high school
High School A is one of two high schools
located in a community of over 60,000 west
of
Chicago, Illinois. High School A was
(5)
i = (P2)s.
constructed in 1962 and Wing A was added
The number of persons passing a fixed in 1966.
point during the five-minute inter-class exHigh School A had a total enrollment of
change period was counted in two locations 1,873 students with 531, 474, 433, and 392
in wing A and then averaged (marked by ® students in grades 9-12, respectively, and
in figure 2). This was done during the ex- 43 in special education. The school day was
change period before periods 3, 4, and 5 of divided into nine periods with five minutes
between classes. All periods were 50 mina typical school day, May 30.
utes in duration, with the exception of the
Vaccination record study
lunch periods—the 5th, 6th, and 7th peA case-control study was conducted to riods—which were 20 minutes each. There
examine the risk factors for measles among were, therefore, a total of 10 exchange
High School A students. Vaccination rec- periods daily, eight between classes, one
ords were validated by verification with before the 1st period, and one after the 9th
providers. Validated records were then used period.
to examine the difference between cases
Since 1979, Illinois has had a comprehenand controls for age at vaccination and the sive vaccination requirement for children
number of doses of vaccine received.
who attend registered preschool through
Two controls were randomly selected for the 12th grade. Between 1981 and this outthe first 45 reported High School A cases break, fewer than two cases of measles had
matched for sex and grade. The vaccination been reported annually in the county in
record of each case and control was re- which the school is located.
viewed, first from High School A files, then
Descriptive epidemiology
from provider files. Vaccination was only
considered verified if a specific date of meaThe index case was a 16-year-old female
sles vaccination could be confirmed by the student in the 10th grade at High School
provider of the vaccine. Whep the school A. She denied any recent travel or known
and provider dates of vaccination were dis- exposure to someone with febrile rash illcrepant, the date recorded with the vaccine ness. The student reported being comprovider was used to calculate the age at pletely well until the onset of mild cough,
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The 95 per cent confidence interval (CI)
around S can be determined by the equation
vaccination. If a provider was unable to be
contacted, the record was considered
unverified. Providers were unaware of
whether they were verifying the record for
a case or a control student. Age at vaccination (in months) was defined as the number of calendar months completed.
Odds ratios and 95 per cent confidence
intervals were calculated for each potential
risk factor using conditional probability
analysis (14), with strata of grade-matched
cases and controls. Stratification by sex
was not performed as both sexes were affected equally.
A MEASLES OUTBREAK IN A HIGHLY VACCINATED POPULATION
system is controlled and continuously monitored for malfunctions by a computer. The
fans are turned on during the first 45 minutes of each period, and then turned off
during the last five minutes of the period
and during the five-minute exchange
period. The hallways have neither ventilation outlets nor windows. The amount of
indoor air recirculation is adjusted by the
computer depending on the outside temperature. On April 12 and 15, the outside daytime temperature of 15 C would have resulted in 0-10 per cent recirculation (i.e.,
the vents were supplying 90-100 per cent
fresh outside air). No malfunctions in the
ventilation system or the computer were
found.
Contact interviews were completed with
58 (84 per cent) of the secondary cases. For
11 (19 per cent) of the interviewed secondary cases, a possible setting for person-toperson contact transmission with the index
case could be established. Excluding lunch
period, three secondary cases had at least
one class in common with the index case.
Another two shared the same study period
(located in the cafeteria). Three took the
same city bus route, but not necessarily the
same bus as the index case, and three others
were friends of the index case.
For the other 47 cases without an attributable exposure (81 per cent), the two remaining settings where transmission may
have occurred are the cafeteria during
lunch period and the hallway of wing A.
The large number of students in both of
these settings makes accurate contact tracing by recall extremely difficult. However,
the probability of person-to-person contact
exposure in the hallway can be estimated
by an adaptation of the Reed-Frost model
(13).
Hallway contact model
An average of 329 students passed one
point in the hallway of wing A during the
five-minute exchange period. The hallways
in this wing were 11 feet (3.4 m) wide. Only
6/11 or 179 of these students were likely to
have passed within the 6 feet (1.8 m) di-
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rhinorrhea, conjunctivitis, and sore throat
on Friday, April 12, during which time she
attended all of her classes. A hacking nonproductive cough developed in addition
over the weekend and continued on Monday, April 15, when a rash appeared. Nonetheless, the index case attended all of her
classes that day. From April 16 through
April 24, she stayed at home and was diagnosed by a physician as having measles;
this was subsequently confirmed serologically.
A total of 69 secondary High School A
cases had onset of rash 9-18 days after the
rash onset in the index case; 13 (19 per
cent) were seroconfirmed. The attack rate
for the 9th through the 12th grades were
6.0, 4.4, 1.6, and 2.8 per cent, respectively,
for an overall High School A attack rate of
4.1 per cent. No cases were reported among
the special education students, faculty, or
staff. Twenty-three secondary cases (33 per
cent) reported attending school during the
prodromal period of their disease. No subsequent cases were detected in High School
A despite the described surveillance. A total
of 45 cases were reported from the community in the ensuing weeks, however (figure 1).
The index case commuted to and from
High School A by city bus daily, including
April 12 and 15, the two days she was ill
and attended school. All of her classes were
located in wing A or immediately adjacent
(the cafeteria and gymnasium). She had
lunch during period 6, the middle of three
lunch periods. Due to the malaise associated with measles, the student's movements on these two days were limited to
passage to and from her scheduled classes.
She denied participating in any extracurricular activities either at High School A or
in the community while ill. There were no
school assemblies, performances, or sporting events at High School A on April 12
and 15.
Wing A has its own air handling unit
separate from the rest of High School A,
designed to supply 8.5 m3 (300 ft3) per
minute to each classroom in this wing. The
177
178
CHEN ET AL.
case would now most likely have effective
contact during one schoolday with 28 secondary cases (p2 = 0.40). Further reducing
Pi to one-fourth of the maximum possible
value results in an estimate of 15 effective
contacts (P2 = 0.22). With both of these
revised assumptions, the probability that
all cases (p^) had at least one contact with
the index case approaches zero.
Vaccination record study
According to school records, 1,867 (99.7
per cent) High School A students had a
history of measles vaccination and six (0.3
per cent) had a valid religious or medical
exemption (none became cases in this outbreak). The index case's school record
showed a measles vaccination date of May
1973 at the age four years; this could not
be verified with the provider, however.
With the use of school records, there was
no difference between cases and controls in
the age at vaccination or the number of
doses of vaccine received. However, lack of
provider verification of school records was
more likely among cases than controls
(odds ratio (OR) = 8.1, 95 per cent CI =
2.2-30.1) (table 1), suggesting cases were
less likely to have a valid vaccination than
controls. Cases were also more likely to
have been vaccinated at a younger age.
Compared with controls with providerverified records, cases with provider-verified records were more likely to have been
TABLE 1
Risk factors for measles: case-control study of students at High School A, Illinois, 1985
Cases
Controls
No.
95%
ratio*
No.
<%)
Lacked provider verification
Vaccinated at age <12 monthst
Vaccinated at age 12-14 monthst
Received two vaccinations
Subtotal
23
3
6
42
(61.1)
(6.7)
(22.2)
(13.3)
(93.3)
23
3
12
26
64
(25.6)
(3.3)
(13.3)
(28.9)
(71.1)
8.1
8.6
7.0
1.9
Vaccinated at age £15 monthst
Total
3
45
(6.7)
(100.0)
26
90
(28.9)
(100.0)
1.0
10
(*)
interval
2.2-30.1
1.1-64.4
1.6-30.2
0.4-8.6
' Case-control odds ratio is relative to at least one provider-verified vaccine dose at age a 15 months and was
obtained by conditional probability analysis, based on grade matching,
t Single-dose physician-verified vaccination.
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ameter assumed for effective contact. Thus,
the probability of a student having had
contact during a five-minute exchange
period is p, = 179/1,722 = 0.10, where the
denominator is the total number of students (1,873) minus the index case and 150
absentees (the average daily absenteeism at
High School A during April). The probability of a student not having contact is
simply Qi = 1 — pi = 0.90.
Since there were 10 exchange periods
daily, the probability (<72) of a student not
having contact in the hallway with the index case during one schoolday would be
(0.90)10 = 0.35. The probability of any single student having at least one contact during one schoolday would be P2 = 1 — 92 =
0.65. The expected number of all secondary
cases who had at least one contact with the
index case is E = p2(69) = 45 (95 per cent
confidence interval (CI) = 37-53). The
probability that all 69 secondary cases had
at least one contact in the hallway, on the
other hand, is extremely small, p 3 = (0.65)69
= 1.2 x 10~13.
These calculations are based on assumptions of maximal exposure to the index case
in the hallway. If we now assume that the
index case was not in the hallway for the
entire five minutes of each exchange period,
that she did not stay in the center of the
hallway, and that the cumulative effect of
these factors would half the contact rate
during one exchange period (pi), the index
A MEASLES OUTBREAK IN A HIGHLY VACCINATED POPULATION
vaccinated at age less than 12 months (OR
= 8.6, 95 per cent CI = 1.1-64.4), or at age
12-14 months (OR = 7.0, 95 per cent CI =
1.6-30.2) than to have received one dose at
age 15 months or more. Number of doses
of vaccine received did not significantly
differ between cases and controls with
provider-verified records.
DISCUSSION
occurred at High School A on April 12 and
15. Classrooms also did not appear to have
been an important setting for transmission;
only three secondary cases were in the same
class as the index case and only one other
case was in the same classroom as the index
case one period later.
A more efficient setting for mass exposure in this outbreak was probably the unventilated hallway in wing A. All traditional classrooms where the students spend
the majority of their schoolday were located
in this wing. The movement of the students
in the hallway during exchange periods
would have dispersed widely the infective
aerosol left behind by the coughing index
case as she travelled between classrooms.
Some mass airborne exposure may also
have occurred in the cafeteria.
The unusual architecture at High School
A and the time course of this outbreak also
permit us to roughly estimate the relative
roles played by contact and airborne transmission in this outbreak. The maximum
potential role played by contact transmission can be estimated by establishing the
proportion of secondary cases who may
have person-to-person contact with the index case. By exclusion, cases for whom such
contact could not be established are more
likely to have been infected via airborne
exposure.
Contact tracing in the index student's
classes, city bus route, and friends identified potential person-to-person contact for
a maximum of 11 (19 per cent) of the secondary cases. Application of the contact
model to the hallway of Wing A further
suggests that, depending on the assumptions of the index case's movements during
exchange periods, between 22 and 65 per
cent of the secondary cases may have had
effective person-to-person contact with the
index case during one schoolday.
To complete the analysis for contact
transmission, the remaining potential setting for exposure to the index case, the
cafeteria during lunch period, needed to be
studied. Unfortunately, neither contact
tracing nor modeling could be effectively
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In 1980, Langmuir (2) predicted that as
the measles elimination program proceeds,
"sharp outbreaks of short duration" will be
observed due to "superspreaders" who "pick
out" the few remaining susceptibles in a
large group of immunes. The characteristics of this outbreak are notably similar.
The exposure of 1,722 students to a vigorously coughing index case resulted in 69
secondary cases, all in one generation. This
would require an "astronomic" person-toperson contact rate by classic epidemic theory (2).
Airborne transmission, on the other
hand, via the large number of suspended
virus particles, can result in such an "astronomic" contact rate (2). Furthermore, the
type of "hacking" cough described by the
index case is known to aerosolize large
numbers of virus particles (15).
The distribution of the onsets of rash in
the 69 High School A secondary cases, 918 days after Monday, April 15, is similar
to the classic range of incubation period
described for measles (16). This distribution, along with its unimodal shape, suggest
that these 69 cases probably had a point
source exposure. The presence of an undetected co-index case in this outbreak would,
therefore, have been unlikely. The epidemic
curve further suggests that despite the presence of prodromal symptoms in the index
case on April 12, effective transmission
probably did not occur until April 15 with
the onset of vigorous coughing; otherwise,
the curve might have been bimodal and
wider by three days.
In contrast to an earlier school-based
airborne measles outbreak (11), no school
assemblies and little or no air recirculation
179
180
CHEN ET AL.
pared to those vaccinated at age 15 months
or over (18). In this study, further stratification of this age group indicates that only
those vaccinated at age 12 months were at
increased risk. The number of cases vaccinated at ages 13 and 14 months was small,
however, and the power to detect a difference was low. The Immunization Practices
Advisory Committee (19) has recommended that revaccination of persons vaccinated
at 12-14 months be considered in outbreak
settings, particularly in junior and senior
high schools.
This outbreak illustrates how measles
outbreaks can occur in a highly vaccinated
population. First, in the absence of measles
outbreaks in the county where High School
A was located for several years, susceptibles
may have accumulated. Second, despite
school vaccination laws, a small percentage
of students still are not immune against
measles due to a) nonreceipt of vaccine with
inaccurate school documentation; b) vaccination at an age when maternal antibody
interfered with vaccine virus replication;
and c) the 2-10 per cent primary vaccine
failure rate (18). Third, as shown by this
outbreak, measles is one of the most contagious diseases known to man, especially
when airborne transmission occurs. Finally, the contact rate is an extremely important determinant of the epidemic potential in a population, irrespective of the immunity level (20).
Students of high school and college age
are frequently found in settings of crowding
where high contact rates are probable (e.g.,
buses, dances, school hallways, and dormitories). An increase in the incidence of measles in this age cohort has been observed in
recent years (21). This may represent the
effect of a "gap" in measles immunity in
this birth cohort due to missing either natural infection or vaccination, superimposed
on high contact rates common for this age
group.
Reports of explosive airborne measles
outbreaks with large numbers of cases are
relatively uncommon, however (21, 22). We
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applied to this setting; there were too many
students for the former and the students
were too sedentary for the latter. Even excluding the cafeteria, however, the above
analysis suggests that a significant proportion of secondary cases may have had
person-to-person contact with the index
case. This analysis further emphasizes that,
irrespective of the mode of transmission,
extremely high contact rates between infectious and susceptible students can occur in
schools, especially in the hallways during
exchange periods.
The lack of a third generation of cases in
High School A suggests that all susceptibles
in the school were exhausted. It is possible,
however, that the surveillance may have
been incomplete. It is also possible that,
unlike the index case, none of the secondary
cases became "spreaders" by continuing to
attend school after they developed contagion-enhancing symptoms such as coughing. Because of the lack of "spreader-tospreader" contact, a third generation may
have not occurred despite the presence of
additional susceptibles (17). Supportive
evidence for this comes from the fact that,
based on the same 4.1 per cent susceptibility rate as the attendees on April 15, one
would have expected six susceptibles
among the 150 absentees.
Our investigation also identified three
risk factors in this highly vaccinated population: lack of provider verification, vaccination at age less than 12 months, and
vaccination at age 12-14 months. All of
these risk factors have been identified in
previous studies (18). The lack of provider
verification suggests that some of the students whose school records indicated that
they had been vaccinated may not actually
have received vaccine.
Children vaccinated before the first
birthday are more likely to have a lower
seroconversion rate due to persisting maternal antibodies. In several previous outbreaks, children who received vaccine at
age 12-14 months have been found to be at
increased risk of acquiring measles com-
A MEASLES OUTBREAK IN A HIGHLY VACCINATED POPULATION
181
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are aware of only one other measles out- prospects for measles elimination in the
break with more secondary cases in one United States.
generation after an index case—84 (Roger
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