Published online March 1, 2006
PEDIATRICS
Vol. 117
No. 3
March 2006, pp.
863-869
(doi:10.1542/peds.2005-1380)
A Tuberculosis Outbreak in a Private-Home Family Child Care Center in San Francisco, 2002 to 2004
Puneet K. Dewan, MDa,
Houmpheng Banouvongb,
Neil Abernethy, PhDc,
Thomas Hoynes, BAb,
Liliana Diaz, MSWb,
Melaku Woldemariamb,
Theresa Ampieb,
Jennifer Grinsdale, MPHb and
L. Masae Kawamura, MDb
a Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, Atlanta, Georgia
b Tuberculosis Control Section, San Francisco Department of Public Health, San Francisco, California
c Medical Informatics, Stanford University School of Medicine, Palo Alto, California
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ABSTRACT
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BACKGROUND. Child care facilities are well known as sites of infectious disease transmission, and California child care facility licensure requirements include annual tuberculosis (TB) screening for on-site adults. In April 2004, we detected an adult with TB living in a private-home family child care center (child care center A).
METHODS. We reviewed patient medical records and conducted a contact investigation. The investigation included all persons at the child care center, the workplace and leisure contacts of the adult patient with TB, and the household contacts of secondary case patients. Contact names were obtained through patient interviews. A positive tuberculin skin test result was defined as induration of 
5 mm. DNA fingerprints of Mycobacterium tuberculosis isolates were analyzed. Outbreak cases were those that had matching DNA fingerprint patterns or were linked epidemiologically, if DNA fingerprint results were not available.
RESULTS. Between August 2002 and July 2004, we detected 11 outbreak cases, including 9 (82%) among children (<18 years of age). All 11 outbreak patients lived or were cared for at child care center A. The 9 pediatric TB patients were young (<7 years of age), United States-born children of foreign-born parents, and 4 (44%) had positive cultures for M tuberculosis. Including isolates recovered from the 2 adult patients, all 6 M tuberculosis isolates shared identical, 7-band, DNA fingerprint patterns. The contact investigation identified 3 (33%) of the 9 pediatric cases; 2 (22%) presented with illness and 4 (44%) were detected by primary care providers during routine TB screening. Excluding case subjects, 36 (54%) of 67 named contacts had latent TB infection.
CONCLUSIONS. Provider adherence to locally adapted pediatric TB screening recommendations proved critical to outbreak control. TB screening compliance by the child care center and more aggressive source-case investigation by the TB program might have prevented or abated this large pediatric TB outbreak.
Key Words: child care • tuberculosis • outbreak • pediatric • day care
Abbreviations: TB—tuberculosis • SFDPH—San Francisco Department of Public Health • AFB—acid-fact bacilli • TST—tuberculin skin test • LTBI—latent tuberculosis infection
Child care facilities are well recognized as common sites of disease transmission. Large outbreaks of diarrheal illness and upper respiratory tract infections are common.1 However, instances of Mycobacterium tuberculosis transmission within child care facilities have been reported rarely. In San Francisco, California, although the rate of tuberculosis (TB) is among the highest of any major US city, pediatric TB is uncommon. In 2003, the San Francisco rate of TB (20.4 cases per 100000 population) was nearly 4 times the national TB case rate of 5.2 cases per 100000 population but only 7 (4.3%) of 162 reported TB cases occurred among children <18 years of age, including just 2 (1.2%) among children <5 years of age.2
In April 2004, an adult residing at a private-home family child care center (child care center A) was diagnosed as having TB by the San Francisco Department of Public Health (SFDPH). A community provider who suspected TB first detected and referred this patient to SFDPH. The patient was foreign-born, had been in the United States since July 2003, and had never previously had a tuberculin skin test (TST). At the time of diagnosis, the patient was symptomatic, with a >1.5-year history of cough. The patient tested negative for HIV, had sputum smears with positive results for acid-fast bacilli (AFB), and demonstrated multiple pulmonary cavities in chest radiographs. Furthermore, the patient reported a history of intermittent self-medication with unknown TB drugs obtained abroad. We report a large TB outbreak among children centered at child care center A, and we review the public health interventions implemented to improve contact investigations and to minimize the likelihood of similar events in the future.
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METHODS
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Public Health Response and Contact Investigation
The adult index case was removed from child care center A and treated with standard anti-TB medications (isoniazid, rifampin, pyrazinamide, and ethambutol) through directly observed therapy. M tuberculosis was recovered from sputum culture, and the isolate was found to be susceptible to all standard anti-TB drugs. Disease control investigators interviewed both the adult index patient and the child care center A operator and requested identification of all adults and children who spent >1 day at the center in the past 2 years. Workplace and leisure contacts of the index patient were also contacted. We called named contacts (or their parents), informed them of TB exposure, and offered medical evaluation for TB.
Medical evaluation of contacts consisted of an initial symptom review and a Mantoux TST with intradermal administration of 5 tuberculin units of purified protein derivative (Tubersol; Connaught Laboratories, Toronto, Canada). A positive TST result was defined as measured induration of 5 mm 48 to 72 hours after administration, regardless of BCG vaccination status. TST conversion was defined as a documented change within 2 years from negative to positive TST results, with a 10-mm increase in TST induration. For each contact, the TST was conducted as soon as possible and, if negative results were obtained, the TST was repeated 3 months after the last documented exposure to the presumed site of transmission (ie, child care center A). Contacts were evaluated with chest radiographs and medical examinations if they had positive TST results, were <5 years of age, or had symptoms indicating TB.3 Diagnostic specimens were obtained through inpatient collection of early-morning gastric aspirates (if <5 years of age) or outpatient sputum induction (if 5 years of age).
All TB suspects were the subjects of complete contact investigations. For children <5 years of age with positive TST results, all household members (adults and children) were also evaluated through TST and symptom review, in an attempt to identify and to evaluate all possible sources of the child's TB infection. The SFDPH notified community pediatricians about the outbreak by fax, by using a registry of providers, and disseminated current SFDPH and American Academy of Pediatrics TB screening guidelines.
Treatment of TB and Latent TB Infection
TB suspects were treated with standard anti-TB medications through directly observed treatment. Their TB diagnoses were verified if M tuberculosis was isolated from a clinical specimen or if they had radiographic and clinical evidence of TB disease with improvement after 3 months of treatment with anti-TB medications.
Contacts with latent TB infection (LTBI) who were 
15 years of age or immunocompromised were offered 9 months of treatment with isoniazid (10 mg/kg per day, up to 300 mg); all other contacts with LTBI were offered 6 months of isoniazid treatment, according to SFDPH guidelines. Contacts 15 years of age with initial negative TST results were also offered window prophylaxis4 (isoniazid) if <3 months had elapsed since their most recent exposure at child care center A or to the presumed source case; if the follow-up TST yielded negative results, then isoniazid treatment was discontinued and the patient was classified as uninfected. Contacts with a documented history of completed prior treatment for LTBI and <8 hours of exposure at child care center A were not offered treatment.
Laboratory Investigation
Isolates were tested for drug susceptibility to standard anti-TB medications with radiometric respirometry with the BACTEC 460 system (Becton Dickinson, Franklin Lakes, NJ). We performed DNA fingerprint analysis with restriction fragment length polymorphism assays with IS6110 as a probe, by using standardized methods.5
Epidemiologic Investigation
We reviewed medical and public health records of all pediatric patients with TB reported from April 2002 through November 2004. Records were reviewed for epidemiologic links to child care center A or any persons living at this private home. Exposure at child care center A was defined as >24 hours of cumulative time in the center between August 2002 and April 2004. An outbreak case was defined as TB in a person sharing a DNA fingerprint with the index patient. If DNA fingerprint results were not available, then an outbreak case was defined as TB in a person named as a contact by the index patient or exposed to child care center A. Case subjects and contacts were mapped into a diagram showing the relationships between individuals (social network). Contacts named by 2 case subjects were reinterviewed and asked to provide names of any persons at child care center A.
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RESULTS
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Case Subject Characteristics
Of the 78 persons identified during this outbreak investigation, 11 had outbreak-associated TB, including 2 adults (the index patient and 1 other adult) and 9 children <7 years of age (Table 1 and Fig 1). Besides the index patient, the other adult with outbreak-associated TB (patient A2 in Table 1) had sputum smears with AFB-positive results and cultures positive for M tuberculosis but reported just 3 months of symptoms, far less than the index patient. Both adults tested negative for HIV.
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TABLE 1 Outbreak-Associated TB Case Characteristics in the Child Care Center A TB Outbreak in San Francisco, 2002 to 2004
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FIGURE 1 Outbreak of TB among children and adults in child care center A in San Francisco, 2002 to 2004. All boxes indicate children <7 years of age who were diagnosed as having TB, except those marked A for adult.
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For the 9 pediatric patients, the median age was 3.4 years (range: 0.5–6 years). All pediatric patients were United States-born Hispanic children of foreign-born parents, and none had been vaccinated with BCG vaccine. At the time of diagnosis, all 9 demonstrated positive TST results (median measured induration: 19 mm; range: 10–30 mm). Six children had prior documented TST results within 2 years, all of which were negative (0-mm induration); therefore, these 6 children were classified as having experienced TST conversion. Four (44%) of the 9 cases were symptomatic. Radiographic abnormalities included pulmonary infiltrates in 6 (67%) of the 9 cases and lymphadenopathy alone in 3 (33%). Either induced sputum or gastric aspirate specimens were submitted in all 9 cases; specimens from 4 patients (44%) were culture-positive for M tuberculosis. No parents were known to be HIV positive, and all denied HIV risk factors; HIV testing was offered to pediatric patients and parents but was declined by all. Isolates from the 4 culture-positive pediatric patients and the 2 adult patients had identical, 7-band, DNA fingerprint patterns and were sensitive to all standard anti-TB drugs.
Contact Investigation and Treatment of Infected Contacts
Excluding the 11 active TB cases, 67 unique persons were named during the contact investigations of outbreak-associated cases; medical evaluation of contacts was completed for 61 (91%), including all 19 (28%) pediatric contacts <18 years of age (Table 2). Four (21%) of 19 pediatric contacts were foreign-born, and 15 (79%) were United States-born children of foreign-born parents. In contrast, 47 (98%) of 48 adult contacts were foreign-born, all from either Mexico or Central America. A large proportion of contacts (36 of 67 contacts, 54%) had LTBI, including 8 (12%) with TST conversion. Of those 8 contacts, 4 (50%) were adults; they were not parents of pediatric case subjects. Treatment for LTBI was initiated for 27 (93%) of 29 eligible patients and was completed for 18 (62%), including all 5 children and 13 (54%) of 24 eligible adults.
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TABLE 2 Outbreak-Associated Contact Evaluation and Treatment Outcomes in the Child Care Center A TB Outbreak in San Francisco, 2002 to 2004
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Epidemiologic Investigation
Child care center A was a private apartment in a predominantly Hispanic neighborhood. It had been operating as a child care center for several years but was not licensed for child care. Residents and employees of this private-home child care center had not been screened for TB before the first pediatric TB case (August 2002). The index patient had lived intermittently at child care center A since June 2002 but was not named in a contact investigation until December 2003. Child care center A was the only common exposure setting among all 11 case patients (Fig 2). The operator was also a common contact for all 11 but was found to have only LTBI and not active TB. Although few patients (or their parents) named the index patient specifically, all had child care center A exposure during the period of time that the index patient was presumed to be infectious and residing at child care center A. Of the 77 persons identified during this outbreak investigation (excluding the index patient), 24 (31%) reported exposure to child care center A and 53 (69%) were exposed at sites other than child care center A. Among the 24 persons with reported exposure to child care center A, 10 (42%) had TB and 10 (42%) had LTBI, for an overall attack rate for TB infection of 84% (Table 3). TST conversion was documented for 9 (38%) of 24 child care center A contacts, including 5 TST conversions that occurred among TB patients. At the workplace of the index patient, 7 (78%) of 9 contacts had LTBI, including 4 (44%) with prior positive TST results and 1 with documented TST conversion. A smaller proportion of household contacts of the secondary case patients had LTBI (19 of 44 contacts, 43%), including 3 (6.8%) with TST conversion and 5 (11%) with prior positive TST results. Reinterviews of adult contacts named by 2 patients failed to generate additional contacts or potential sites of transmission.
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FIGURE 2 Social network of child care center A pediatric TB outbreak in San Francisco, 2002 to 2004. Persons with >24 cumulative hours in child care center A were considered exposed and are grouped inside the dotted line. I indicates the index case; MTB, outbreak strain of M tuberculosis.
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TABLE 3 TB Infection Status Among All Contacts, According to Exposure Setting, in the Child Care Center A TB Outbreak in San Francisco, 2002 to 2004
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We reviewed case histories to determine missed opportunities for outbreak detection before April 2004. Of the 9 pediatric outbreak-associated cases, 4 (44%) had been diagnosed before identification of the index patient (Fig 1). Identification of the first patient (patient P1) in August 2002 sparked a large contact investigation that included screening of all adults identified at child care center A. No other source patient was identified despite home visits to the household of patient P1 and child care center A, with screening of all identified adults. The index patient, although living at child care center A and symptomatic at the time, was not named or detected in that 2002 contact investigation. The second patient (patient P2) was diagnosed in a neighboring county in September 2002; although child care center A was reported to SFDPH by the neighboring jurisdiction as a site of possible exposure, no connection was made at the time, and the TB program did not revisit the site. Furthermore, the M tuberculosis isolate recovered from patient P2 was evaluated with restriction fragment length polymorphism assays at a different laboratory than subsequent isolates. No data were shared between laboratories; therefore, no DNA fingerprint comparison with results for subsequent patients was made before the outbreak investigation. The third patient (patient P3), whose infection was diagnosed in December 2003, was a 6-month-old infant who had no exposures except family members and child care center A. At that time, the individual identified subsequently as the index patient (patient A1) was reported as a contact (for the first time) but could not be located despite multiple health worker visits to child care center A. The source of the TB infection of patient P3 was thought initially to be an elderly family member who was reported to have pulmonary symptoms but who had left the country and could not be evaluated. Also, although gastric aspirate cultures were positive for M tuberculosis, DNA fingerprint results were not available for 2 months (because of transport time between laboratories and a batch-processing method), by which time the outbreak had been detected. The fourth patient (patient P4) was not known initially to have been exposed at child care center A; complete exposure history was obtained only in reinterviews during the outbreak investigation.
Routine primary care TB screening with TSTs led to detection of 4 children (44%) with TB. In each of these 4 cases, the child was asymptomatic and the primary care physicians had no knowledge of the TB outbreak. TB screening with TSTs was performed on the basis of epidemiologic risk factors, in accordance with American Academy of Pediatrics and SFDPH guidelines (Table 4), and subsequent investigation of TST-positive results led to case diagnosis.
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TABLE 4 Recommendations for Primary Care Providers for Screening for Risk Factors for LTBI Among Children and Adolescents3
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DISCUSSION
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Extensive prolonged transmission of TB from an adult resident of a private-home child care center led to one of the largest reported pediatric TB outbreaks in the United States in the past 30 years.6 Although TB outbreaks among school-aged children and adolescents have been reported frequently, this outbreak is unusual because of its occurrence in a child care center and the involvement of multiple young children with active TB.
A second adult with TB living at the site might have contributed to transmission, although the duration of symptoms and the extent of disease were substantially less than those of the presumed index case. We cannot exclude the possibility of child-to-child TB transmission; 4 (44%) of 9 pediatric TB patients had cultures positive for M tuberculosis, including 2 with a history of cough and pulmonary infiltrates. TST conversion was noted for 3 (6.8%) of 44 household contacts of secondary cases. However, TB transmission from young children has been reported very rarely. Generally, the burden of disease among young children is much lower than that among adults; in particular, cavitary disease is very uncommon. Also, young children may not have a cough strength adequate to generate droplet nuclei.7 Patients with low-burden disease, defined by sputum smears with negative results for AFB, demonstrate markedly less TB transmission than patients with AFB smear-positive results.8 Furthermore, in several smaller pediatric outbreaks in school and nursery settings that were reported recently, the sources of disease were usually either adolescents or adults.9–14 In this outbreak involving very young children, child-to-child or child-to-adult transmission of TB was thus unlikely.
M tuberculosis transmission in child care centers has been reported rarely,6,15 but this outbreak demonstrated that child care centers should be considered and investigated as potential sites of exposure when children are identified as having TB infection. In California, licensure requirements for child care facilities include annual TB screening of adults who work or live at the facility.16 In this outbreak, child care center A was unlicensed, and residents and employees of this private home were not screened for TB until the contact investigation occurred. Although in this instance we were able to implement routine TB screening at child care center A, unlicensed private-home child care centers by their very nature are unlikely to meet health and safety code requirements routinely.
Each contact investigation conducted for the 4 pediatric outbreak-associated cases that occurred before April 2004 was a missed opportunity for earlier detection of the infectious adult source patient. Factors such as poor communication between the child care center A operator and SFDPH disease control investigators, incomplete contact investigations, and poor data management all contributed to ongoing TB transmission and instances of preventable disease. Although we did not collect information about immigration status, it is possible that some individuals were undocumented. Fear of deportation might have been a barrier to cooperation with the contact investigation and might have contributed to delayed diagnosis of infectious cases. Subsequent cooperation with contact investigations might have been improved in 2004 when disease control investigators began to incorporate early discussions of confidentiality protections with case subjects, contacts, and parents. Other program interventions to improve contact investigations have included improved data management through a new TB patient management relational database,17 designed to notify staff members when contacts or sites were named in previous contact investigations and to facilitate network analysis. Most importantly, however, finding children with active TB should prompt aggressive investigation of adult exposures, including those outside the child's home, with particular attention to exposure at current or previous child care facilities. These instances represent important opportunities to find the source patient and halt ongoing TB transmission. Unfortunately, pediatric contact investigations frequently are unsuccessful in identifying source cases. An evaluation of 111 contact investigations around pediatric TB cases in 8 California jurisdictions (not including San Francisco) reported that additional patients with undiagnosed TB disease were found in just 10 (9%) investigations, which demonstrates substantial room for contact investigation improvement.18
Primary care providers played a critical role in case diagnosis and outbreak abatement. By performing routine, risk factor-based, TB screening in accordance with SFDPH guidelines, primary care providers detected 4 of 9 outbreak-associated pediatric TB cases. Early detection of TB might have prevented significant morbidity among these very young children, because they are generally considered to have greater susceptibility to severe forms of disease. Recommendations for LTBI screening by primary care providers are summarized in Table 4.3
Prospective application of social network or genotyping analysis might have allowed detection of the outbreak and the site of transmission earlier. When it became clear that not all contacts had been reported, we ensured the completeness of the contact investigation by reinterviewing contacts named more than twice. Although this effort failed to yield any previously unnamed contacts, it reduced uncertainty about the full scope of the outbreak. DNA fingerprint results for all San Francisco TB cases are now centralized in 1 database, and all isolates are submitted to the National Tuberculosis Genotyping and Surveillance Network.19 With the application of newer, more-rapid, genotyping technologies, such as spoligotyping and mycobacterial interspersed repetitive unit-variable numbers of tandem repeats assays, DNA fingerprint results are now available for use in ongoing contact investigations.
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CONCLUSIONS
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A large outbreak of pediatric TB resulted from prolonged TB transmission in a private-home family child care center, from an infectious adult. Primary care providers played a key role in case detection, through adherence to existing pediatric TB screening guidelines. Intensification of contact investigations surrounding children and systematic improvements in data management by TB programs may improve future outbreak control efforts.
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ACKNOWLEDGMENTS
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We acknowledge Charles Crane for the cooperation of Costra Conta County with the investigation, Roxanne Aga and Midori Kato of the Stanford Center for Tuberculosis Research for DNA fingerprinting assistance, Andi Shane (University of California, San Francisco) for her review of this manuscript, and Ann Lanner (Centers for Disease Control and Prevention) for editorial assistance.
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FOOTNOTES
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Accepted Aug 16, 2005.
Address correspondence to Puneet K. Dewan, MD, Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, 1600 Clifton Rd, Atlanta, GA 30333. E-mail: phd8{at}cdc.gov
The authors have indicated they have no financial relationships relevant to this article to disclose.
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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics
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ABSTRACT
METHODS
