PEDIATRICS Vol. 100 No. 3 September 1997,
p. e9
Copyright ©1997 by the American Academy of Pediatrics
ELECTRONIC ARTICLE:
Tuberculosis Transmission Among Five School Bus Drivers and
Students in Two New York Counties
Hussain R. Yusuf*,
Christopher R. Braden
,
Abby J. Greenberg§,
Andre C. Weltman
,
Ida M. Onorato, and
Sarah E. Valway
From the * Epidemic Intelligence Service, Epidemiology Program
Office and the Division of TB Elimination, National Center for HIV,
STD, and TB Prevention, Centers for Disease Control and Prevention,
Atlanta, Georgia; § Division of Disease Control, Nassau County
Department of Health, Mineola, New York; and the Bureau of
Tuberculosis Control, New York State Department of Health, Albany, New
York.
ABSTRACT
- INTRODUCTION
- METHODS
- RESULTS
- DISCUSSION
- ACKNOWLEDGMENTS
- ABBREVIATIONS
- REFERENCES
ABSTRACT 
Objective. Between November 1994 and
April 1995, more than 3300 students in 49 schools in two counties in
New York were potentially exposed to five school bus drivers with
tuberculosis. This investigation was carried out to determine the
extent of transmission of Mycobacterium tuberculosis among
students.
Methods. Components of the epidemiologic investigation
included tuberculin skin-test screening and collection of demographic information for students exposed to a driver with tuberculosis, chest
radiography and medical evaluation of individuals with positive skin
tests, and DNA fingerprinting of M tuberculosis isolates. A
positive skin test was defined as 
10 mm induration, and a converter was an individual with an increase in reaction size of 10 mm in the
past 2 years.
Results. The rates of positive skin tests were 0.8%,
0.3%, 9.9%, 1.1%, and 0.7% among US-born students exposed to
drivers 1 through 5, respectively. The relative risk for a positive
tuberculin skin test was significant only for students exposed to
driver 3, and the only secondary case identified among students was
exposed to driver 3. The DNA fingerprint patterns of isolates from
drivers 3 and 4 matched.
Conclusion. There was no clear evidence of transmission of
M tuberculosis to students from drivers 1, 2, 4, or 5. However, evidence suggests that driver 3 transmitted M
tuberculosis to students and another driver. Routine annual
tuberculin skin-test screening of drivers would not have prevented
these tuberculosis exposures.
Key words:
school,
school bus,
student,
transmission,
tuberculosis.
INTRODUCTION
Transmission of Mycobacterium tuberculosis in
schools has been well-documented,1 but less information
is available concerning transmission of M tuberculosis in
buses.5,9 In two accounts,5,9 60% and 80%
of students exposed to source cases on school buses had positive
tuberculin skin tests. The number of students exposed on school buses
in these two reports is not large (a total of 86), and the source cases
in these instances were very infectious and likely responsible for
hundreds of infections in classmates and other students. Public health
interventions required to prevent or respond to more usual exposures
among large numbers of students have not been outlined in the
literature. County, state, and national public health officials
embarked on an investigation of five tuberculosis cases among bus
drivers and a large number of exposed students to determine the extent
of M tuberculosis transmission and the appropriate public
health interventions. This report summarizes the findings of an
epidemiologic investigation carried out to determine the extent of
transmission of M tuberculosis among student contacts of
each driver, to identify cases of tuberculosis epidemiologically linked
to the bus drivers, and to formulate strategies toward preventing the
spread of M tuberculosis in these circumstances.
Between November 1994 and April 1995, five school bus drivers employed
by three bus companies based in the state of New York were diagnosed
with tuberculosis. Driver 1 was employed by bus company A and
transported students in two counties in New York. Drivers 2, 3, and 4 were employed by bus company B and transported students in one of the
two counties. Driver 5 was employed by bus company C and transported
students in this same county. More than 3000 students in 49 schools of
11 school districts in the two counties involved were exposed to these
five bus drivers.
METHODS
Bus Drivers' Case Histories and Records Review
Medical records were reviewed for the five bus drivers with
tuberculosis. Results of the close contact investigations conducted by
the health departments were also reviewed.
Epidemiologic Investigation
Tuberculin skin test (TST) screening was offered to all students
who rode on a bus with a source case. The respective schools' bus
route rosters were used to identify students who may have been exposed
to any one of the five bus drivers. Because some students who were not
on a roster may have ridden in a bus driven by one of the five drivers,
letters from respective school principals were sent to all parents
requesting skin testing of the student if she/he had been exposed to
one of the drivers in question. Tuberculin skin tests were administered
by the Mantoux method using 5 tuberculin units of purified protein
derivative and were read at 48 to 72 hours. Individuals who were known
to have prior positive tests were exempted from TST screening, but did
undergo an evaluation of symptoms and, if necessary, further clinical and radiologic evaluation. Testing of students was conducted at the
respective schools by the county health departments between January and
June 1995. Students with recent exposure to any of the five drivers and
negative TSTs were retested 3 months after the time of last contact.
Students with exposure that took place at least 3 months before the
screening received only one TST. All exposed students with a TST
response of 5 mm induration received further clinical evaluation
including a chest radiograph. Information with respect to birthplace
and other demographic characteristics of students were obtained from
school records and during skin testing.
Definitions
For greater specificity of epidemiologic analysis, a positive
TST result was defined as 10 mm induration. A student was considered exposed to M tuberculosis if she/he ever rode in a bus with
a driver with tuberculosis from the beginning of the school year to the
last day of work by the driver. A secondary case of tuberculosis was
defined as an individual with contact to a bus driver with no other
exposure to tuberculosis identified, a positive skin test, and signs
and symptoms of tuberculosis. Individuals who had an increase in
reaction size of 10 mm and a negative TST administered within the
past 2 years were classified as TST converters.12
Bacteriology and Laboratory Analysis
Sputum specimens were obtained from all cases for acid-fast
bacilli (AFB) smears and cultures and, if culture-positive,
drug-susceptibility testing. DNA fingerprinting of M
tuberculosis isolates was performed at the New York State
Department of Health Laboratory using a DNA probe for insertion
sequence IS6110 as described previously.13
RESULTS
Case Histories and Close Contact Investigations
All bus drivers except driver 4 presented with signs and symptoms
of tuberculosis before diagnosis of their condition (Table 1). Sputum specimens were AFB
smear-positive for drivers 1, 3, and 5, and negative for drivers 2 and
4. Driver 1 was exposed to a relative with tuberculosis in 1979. Although his TST results from that time are unknown, he did receive
isoniazid (INH) prophylaxis for 3 months. Driver 2 was anergic and died
shortly after her tuberculosis diagnosis. Drug-susceptibility testing
indicated that drivers 3 and 4 were infected with INH-resistant
strains. Driver 4 was evaluated for tuberculosis after he was found to have a positive TST during screening of contacts around driver 3. Driver 4 had a documented negative TST in May 1992.
|
Table 1.
History of Source Cases and Close Contact Investigation
[View Table]
|
A high proportion of family members and friends of drivers 1, 3, and 5 were TST-positive (25% to 100%) (Table 1). Very few close contacts
were identified for drivers 2 and 4. Although drivers 2, 3, and 4 worked for the same bus company, driver 2 did not come in contact with
drivers 3 or 4. However, driver 4 was a friend of driver 3, the likely
source of his infection. Drivers 3 and 4 often sat together in the
closed bus of driver 3 while waiting for students to be dismissed from
school and enter their buses. M tuberculosis isolates of
drivers 3 and 4 were identical by DNA fingerprinting.
Secondary Cases Among Students Exposed to the Bus Drivers
One 14-year-old student was diagnosed with tuberculosis. This
student had a positive TST (18 mm) in March 1995, during screening of
students exposed to driver 3. A few weeks before testing, the patient
had upper respiratory symptoms and was started on clarithromycin but
showed no clinical improvement. A chest radiograph revealed infiltrates
in the left upper and right lower lobes and enlarged left hilar lymph
nodes. Sputum specimens were AFB smear- and culture-negative. The
patient had clinical and radiographic improvement with antituberculosis therapy. Other than contact with driver 3, the patient had no identified risk factor for tuberculosis. None of the chest radiographs for other students were abnormal and no other secondary cases of active
tuberculosis disease were identified with respect to drivers 1, 2, 4, or 5.
TST Screening of Students
Although more than 3300 students were exposed to the five bus
drivers, no student was potentially exposed to more than one driver.
Drivers 1 and 5 were substitute drivers and operated different bus
routes each day. Therefore, students were potentially exposed to these
two drivers only infrequently (once or twice). Drivers 2, 3, and 4 operated regular bus routes.
A total 3278 students were screened. Five hundred ninety-one students
(18.0%) exposed to drivers 1, 3, or 4 were skin tested twice because
the initial test was performed before the elapse of 3 months from the
time of last contact with the respective driver. Of the total, 91 (2.8%) students were born outside of the United States (US) and
birthplace was unknown for 714 (21.8%) students. Among foreign-born
students and students whose birthplace was unknown, the proportion who
were TST-positive were 8.8% and 1.7%, respectively.
To avoid confounding of the epidemiologic analysis by infections
acquired outside of the US, Bacille bilié de
Calmette-Guérin vaccination, and boosting, we analyzed TST
results for US-born students separately. The median age of US-born
students varied by driver, ranging from 5.3 years for those exposed to
driver 2 to 15.6 years for those exposed to driver 5 (Table
2). The proportion of US-born students
who were TST-positive was relatively low for drivers 1, 2, 4, and 5 (range, 0.3% to 1.1%), but was significantly higher (9.9%) for
driver 3. Driver 3 transported students from four different schools,
and for one school, 8 (44%) of 18 US-born students exposed to this
driver were TST-positive. Compared with students with the lowest TST
positivity rate, ie, those exposed to driver 2, only students who were
exposed to driver 3 were significantly more likely to be TST-positive
(relative risk = 39.3; 95% confidence interval, 8.8, 174.8)
(Table 3).
|
Table 2.
Results of Tuberculin Skin Test (TST) Screening of US-Born Students, by
Bus Driver
[View Table]
|
|
Table 3.
Relative Risk of a Positive Tuberculin Skin Test Among US-Born
Students, by Bus Driver With Active Tuberculosis
[View Table]
|
Two US-born students, 1 exposed to driver 3 and 1 to driver 4, had TST
conversions (Table 2). The student exposed to driver 3 was a 6-year-old
child who had a negative TST (0 mm) in March 1995 and a positive one
(10 mm) in May 1995. A 13-year-old student who was exposed to driver 4 had a negative TST (0 mm) in April 1995, followed by a positive
one (11 mm) in June 1995. Neither of these students had signs and
symptoms of active tuberculosis disease.
DISCUSSION
Previous studies that have investigated exposure to a source case
with tuberculosis on a bus document that substantial transmission of
M tuberculosis can result from exposure in such a closed
setting.5,9 In these reports, students exposed on a bus
to a tuberculosis case were 2 to 20 times more likely to have a
positive TST compared with students who were not exposed to M
tuberculosis on a bus.
In the current investigation, there is no definite evidence of
transmission of M tuberculosis to students from drivers 1, 2, or 5. Among US-born students potentially exposed to these three drivers, the prevalence of positive TST reactions was low. There were
no secondary cases of tuberculosis or TST conversions associated with
any of these three drivers. The sputum of Driver 2 was AFB smear-negative and therefore unlikely to transmit M
tuberculosis. Although the sputum of drivers 1 and 5 was AFB
smear-positive and a substantial proportion of their family members and
close contacts were TST-positive (100% and 25%, respectively),
indicating that both drivers were infectious, the transmission of
M tuberculosis to students probably did not occur because
both were substitute drivers and the frequency of their contacts with
any 1 student was low.
It is possible that 1 of the 2 students who had a TST conversion may
have been infected by driver 4. However, this result is discrepant with
the findings that none of the other 87 students exposed to this driver
were TST-positive and because sputum specimens from driver 4 were
AFB-negative. Other possible explanations for this student's TST
conversion include an unidentified exposure to another patient with
tuberculosis, a misreading of the TST, or a false-positive TST
reaction. Such false-positive reactions have been described when the
TST is used in low disease prevalence populations.14
The highest risk for M tuberculosis infection was found for
students exposed to driver 3. This driver had AFB smear-positive sputum
and 65% of his close contacts were TST-positive. Compared with US-born
students with the lowest TST positivity rate (those potentially exposed
to driver 2), US-born students exposed to this driver were
significantly more likely to be TST-positive, with 1 student having a
documented conversion and another having active tuberculosis disease. A
greater percentage of students exposed to driver 3 were TST-positive
compared with students exposed to the other drivers. With respect to
the school where 44% of students exposed to driver 3 were
TST-positive, it was learned that in this particular case he would
arrive at the school with the children 15 to 20 minutes early. School
policy did not allow the children to disembark before the scheduled
time. Therefore, the children waited on the bus with the driver and,
because it was winter, the windows were closed. This may have
contributed to prolonged exposure of the students to infectious
airborne droplet nuclei in a poorly ventilated environment.
The findings of this investigation provide no convincing evidence of
transmission of M tuberculosis to students exposed to four
of the five bus drivers with active tuberculosis. However, there is
strong evidence that driver 3 transmitted M tuberculosis to
student contacts in his bus route and to driver 4.
Several factors that may have influenced transmission on the buses
could not be analyzed in this investigation. Most importantly, the
extent of ventilation on all buses is not known. All of these drivers
were diagnosed with tuberculosis in the winter months and it is likely
that windows on the buses were closed. The duration of routes within
these school districts were roughly equivalent, ranging from 25 to 35 minutes, and we had no information concerning the seating of children
on the buses. Therefore, any difference among students exposed to
different drivers according to these factors could not be ascertained.
An issue brought forth as a result of this investigation is whether or
not the health of school children can be better protected by requiring
annual TST screening of all school bus drivers. There were strong
community and media requests that public health officials require such
testing. Our findings suggest that transmission of M
tuberculosis to students would not have been prevented by annual TST screening. Driver 1 was previously exposed to a family member with
tuberculosis and had been prescribed INH prophylaxis. Driver 2 would
have tested negative as she was anergic. Driver 3 had immigrated from a
country with a high incidence of tuberculosis and was likely previously
infected, because he had disease consistent with tuberculosis
reactivation (ie, right upper lobe consolidation). Even if he had been
found to be TST-positive via annual screening, he would not have been a
candidate for INH prophylaxis because he was older than
35.15 Driver 4 seems to have been recently infected (after
the beginning of the school year) by driver 3. Therefore, screening at
the beginning of the school year would not have been effective in
preventing development of tuberculosis disease in this patient. Bus
company C, the employer of driver 5, required TST screening of its
drivers once every 2 years. Although driver 5 was a new employee, he
was not screened by the company before his diagnosis because he had a
negative TST in December 1993. Whether driver 5 would have had been
found to be TST-positive if screened at the beginning of the 1994 to
1995 school year is unknown.
Currently, the only occupational groups identified as being at
high-risk for M tuberculosis infection are health care
workers, migrant workers, and employees of high-risk congregate
settings such as correctional facilities, mental institutions, and
shelters for the homeless.12 A recent study investigating
the association between occupation and tuberculosis found the rates of
M tuberculosis infection among unemployed individuals,
certain categories of health care workers, and those with jobs with
extensive animal contact to be higher than expected when age, sex,
race, and country of birth were accounted for.16 The rate
among bus drivers was not higher than expected.16 However,
the Centers for Disease Control and Prevention recommends that local
health departments identify groups at high-risk for M
tuberculosis transmission and infection using surveillance data
from their populations.12 A substantial proportion of
employees of the three bus companies involved in this investigation
were foreign-born (between 16% and 30% among those for whom the place
of birth was known; data not shown). Immigrants from countries where
tuberculosis is common are at a higher risk of having tuberculosis
infection.12 These findings support the development of
prevention strategies, such as TST screening of certain occupational
groups, based on the epidemiologic factors within the respective
community.
Effective prevention strategies must also ensure adequate and prompt
access to health care for persons at risk for tuberculosis so that
tuberculosis disease can be quickly diagnosed and treated before there
is exposure of large numbers of other individuals. Four of the five
drivers involved in this investigation continued to work for several
days or weeks after becoming symptomatic. Communities and employers
need to be informed of the need for proper medical attention for
individuals with the signs and symptoms of tuberculosis, and of the
need to implement measures for reducing the risk of transmission of
tuberculosis. Employers also should implement mechanisms that encourage
sick employees to promptly seek health care and evaluation for
tuberculosis without fearing loss of salary.
FOOTNOTES
Received for publication Nov 5, 1996; accepted Apr 1, 1997.
Reprint requests to (H.R.Y.) Centers for Disease Control and
Prevention, 4770 Buford Hwy, Mailstop E52, Atlanta, GA 30341.
ACKNOWLEDGMENTS
We gratefully acknowledge the assistance provided by Richard E. Edstrom, MD, Suffolk County Department of Health Services, Suffolk
County, NY; Jennifer Lightdale, MD, San Francisco General Hospital, San
Francisco, CA; Tara Cooperman, DO, and Elaine Hlaing, RN, Nassau County
Department of Health, Nassau County, NY; and Kin Lay Maw, Chris Larken,
and Yuling Chen, New York City Department of Health, New York, NY.
ABBREVIATIONS
TST, tuberculin skin test.
AFB, acid-fast bacilli.
INH, isoniazid.
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