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Neira-Munoz, Edmundo MMedSc, FFPH*; Smith, Janette BN, Rgn*; Cockcroft, Paul BSc, MBBS, FRCPath; Basher, Damian RGN, MSc; Abubakar, Ibrahim MD, PhD§

The Pediatric Infectious Disease Journal: September 2008 - Volume 27 - Issue 9 - p 836-837
doi: 10.1097/INF.0b013e31816ff7c5
Brief Reports

We report a tuberculosis outbreak in school children caused by exposure to a sputum-smear positive school bus driver. Exposed children were assessed using 2 versions of interferon-gamma release assays. Fifty-five percent (18/34) had a positive interferon-gamma release assays and 4 children developed tuberculosis. This suggests that transmission may be very efficient in this setting and highlights the need for early diagnosis.

From the *Hampshire and Isle of Wight Health Protection Agency, †Portsmouth Hospitals NHS Trust, ‡Portsmouth City Primary Care Trust, Portsmouth PO3 6DP, Hampshire, and §Tuberculosis Section, Centre for Infection, Health Protection Agency, Colindale, London, U.K.

Accepted for publication February 22, 2008.

The funding sources had no role in study design, conduct, reporting, or the decision to submit the paper for publication.

Address for correspondence: Dr Edmundo Neira Munoz, Consultant Physician in Health Protection, Hampshire and Isle of Wight Health Protection Unit, Finchdean House, Milton Road, Portsmouth PO3 6DP, Hampshire, U.K. E-mail:

Infectious tuberculosis cases frequently have contact with vulnerable individuals such as school children or hospital patients leading to significant investigations in schools1,2 and hospitals.3 A number of previous reports have suggested that transmission of tuberculosis is possible among school bus riders.4,5 Most of these outbreaks report transmission in a school and conclude that transmission in the school bus cannot be ruled out. A single study from New York City6 reports a transmission rate of 10% in children exposed to a driver with infectious tuberculosis.

None of the 162 incidents in educational settings with the potential for transmission of Mycobacterium tuberculosis reported between 2004 and 2006 in England, Wales, and Northern Ireland, involved a school bus. Hampshire and the Isle of Wight is a low tuberculosis incidence area (6.3 per 100,000 in 2006). Four of the 114 cases occurred in children less than 16 years of age. Two education-related tuberculosis incidents occurred in Hampshire and the Isle of Wight between 2004 and 2006.

We investigated the extent of transmission to school children using interferon gamma release assays (IGRA) after the diagnosis of smear-positive tuberculosis in a school bus driver.

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The Hampshire and Isle of Wight Health Protection Unit is responsible for the public health management of tuberculosis incidents in the community. For each incident involving potential transmission, especially in settings with vulnerable individuals, such as hospitals and schools, a risk assessment is undertaken to inform further screening of contacts.

A 46-year-old male school bus driver with symptoms suggestive of pulmonary tuberculosis since November 2006 was diagnosed with tuberculosis in April 2007. A sputum sample showed acid fast bacilli on direct microscopy and M. tuberculosis was subsequently confirmed by PCR and culture. All isolates were fully susceptible to rifampin, pyrazinamide, and ethambutol and reported as low grade resistant to isoniazid. After this diagnosis screening of household contacts, according to UK guidelines,7 was carried out. Two of 3 unvaccinated children with a tuberculin skin reaction of 8 and 10 mm were identified. An incident management team was convened and the decision taken to screen children who used the bus.

A form was used to collect the demographic characteristics and risk factors for tuberculosis for each child contact. Date and place of birth, duration of exposure to the index case, and BCG vaccination status (as reported by the parents about BCG vaccination, searching Child Health System, and scar inspection) were recorded. Clinical, radiologic, and microbiologic data for all contacts subsequently found to have evidence of active tuberculosis were collated.

Two commercial versions of the IGRA test are available, T-SPOT TB (Oxford Immunotec) and QuantiFERON—TB Gold (Cellestis). Venous blood samples for the 2 tests were obtained simultaneously from each child. Samples were tested using both commercial assays according to the manufacturers’ recommendations.

The proportion and means of the demographic and clinical characteristics of cases were calculated. A χ2 test (and where appropriate, the exact test) was used to assess significance of categorical variables. For quantitative variables, the Student t test (or a nonparametric equivalent where appropriate) was used to assess significance.

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Eighteen of 33 (54.5%) children were found to have a positive IGRA. There was a high correlation between both IGRA tests, with a kappa of 0.87% (95% CI: 0.5–1.0). Only 1 sample was Quantiferon-gold positive and T-spot TB borderline positive.

Table 1 summarizes the demographic and clinical characteristics of these contacts. The mean age of the population was 13 years (SD: 1.4) and mean duration of cumulative exposure 24 hours (inter quartile range, 19–37). Four children had a parent and/or grandparent born outside the United Kingdom in a high-risk country. Two children were born in and spent more than a month in a high-risk country. There was no difference in the proportion of contacts found to have a positive IGRA by duration of exposure to the index case (P = 0.37). The children did not sit in a consistent position on the bus; therefore, we were unable to assess the contribution of proximity to the index case. There was no significant association between a positive result with either IGRA test and BCG status, duration of exposure or the place of birth of the child, parent, or grandparent (P > 0.05).



Four children developed active tuberculosis diagnosed based on clinical and radiologic features. None of these cases had a positive smear or microbiologic confirmation to allow comparison with the genotype of the index case.

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This investigation found evidence of a high level of transmission among contacts of an infectious bus driver. More than half of the children who regularly travel on the bus had been infected. Four of these 18 children had already developed evidence of active tuberculosis. This is a very high infection rate in comparison to other tuberculosis incidents where children have been exposed to an infectious case on a school bus;4,5 the highest reported rate was 46% in Spain.8 However, in these studies the case was a child and contact might not have been limited to the bus.

An alternative explanation for the high transmission rate is the presence of a secondary case among the children transmitting to other children on the bus. We have, however, found no evidence for this as none of the secondary cases developed infectious tuberculosis. That transmission had occurred in this instance from the driver is supported by the fact that only 4 children had additional risk factors, none of whom had active disease. Furthermore, there was no known contact with other infectious cases or link with a high incidence country. All the children had prolonged contact with the source case because of a delay in the diagnosis. Delayed diagnosis is a common feature of outbreaks with evidence of transmission to or between children.1,2

Although UK guidelines7 do not recommend the routine investigation of contacts on a bus, this incident highlights the need to prioritize the investigation of exposures in this setting. This contrasts with the investigation of the recent multidrug resistant tuberculosis case in an air passenger from the United States, which led to a significant amount of contact tracing. To date, there has been no documented case of active tuberculosis disease after exposure on an airplane.9 A key reason cited for greater transmission potential in aircrafts is that when in operation, the ventilation systems are closed. The bus involved in this incident had, like an aircraft, a closed ventilation system, combined with a heating system that blows hot air toward the infectious driver and then into the remainder of the bus potentially exposing all the children on the bus to droplets containing mycobacterium. Furthermore, passengers on a school bus are more likely to have a longer cumulative period of exposure to the same individual compared with commercial airline passengers.

Results from the 2 IGRA tests were very similar in this population. IGRA tests are increasingly used in screening contacts of tuberculosis cases and have been recommended to replace tuberculin skin testing in the United States.10

The conclusions that can be drawn from this investigation are limited by the small number of exposed individuals (33); nonetheless, the high proportion of individuals infected suggests that transmission in this setting can be very efficient. This incident shows a high transmission rate to school children after prolonged cumulative exposure to an infectious adult on a bus. It highlights the need for early diagnosis of infectious cases and screening of exposed vulnerable contacts.

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1.Howard J, Paranjothy S, Thomax S, Bracebridge S, Lilley M, McEvoy M. Outbreak of tuberculosis in a junior school in south-eastern England. Euro Surveill. 2007;12:E070628.1.
2.Ewer K, Deeks J, Alvarez L, et al. Comparison of T-cell-based assay with tuberculin skin test for diagnosis of Mycobacterium tuberculosis infection in a school tuberculosis outbreak. Lancet. 2003;361:1168–1173.
3.Breathnach AS, de Ruiter A, Holdsworth GM, et al. An outbreak of multi-drug-resistant tuberculosis in a London teaching hospital. J Hosp Infect. 1998;39:111–117.
4.Curtis AB, Ridzon R, Vogel R, et al. Extensive transmission of Mycobacterium tuberculosis from a child. N Engl J Med. 1999;341:1491–1495.
5.A school- and community-based outbreak of Mycobacterium tuberculosis in northern Italy, 1992–1993. The Lodi Tuberculosis Working Group. Epidemiol Infect. 1994;113:83–93.
6.Yusuf HR, Braden CR, Greenberg AJ, Weltman AC, Onorato IM, Valway SE. Tuberculosis transmission among five school bus drivers and students in two New York counties. Pediatrics. 1997;100:E9.
7.National Collaborating Centre for Chronic Conditions. Tuberculosis: clinical diagnosis and management of tuberculosis, and measures for its prevention and control. London: Royal College of Physicians; 2006.
8.Extremera MF, Moyano AR, Gomez PB, et al. Exposure to Mycobacterium tuberculosis during a bus travel. Med Clin (Barc). 2001;116:182–185.
9.World Health Organisation. Tuberculosis and Air Travel: Guidelines for Prevention and Control. 2nd ed. Geneva: World Health Organisation; 2006.
10.Centers for Disease Control and Prevention. Guidelines for the investigation of contacts of persons with infectious tuberculosis and guidelines for using the QuantiFERON-TB Gold test for detecting Mycobacterium tuberculosis infection, United States. MMWR Morb Mortal Wkly Rep. 2005;54(No RR-15).

tuberculosis; extensive transmission; school bus

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