outbreak of mycobacterium tuberculosis among employees of ... · mycobacterium tuberculosis...
TRANSCRIPT
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Rendi Murphree, PhD CDR, USPHS
CDC Epidemic Intelligence Service Officer
Tennessee Department of Health
Communicable and Environmental Disease Services
Outbreak of Mycobacterium tuberculosis Among Employees of an Elephant Refuge
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The Outbreak
• Notification
– October 2009
– 5 tuberculin skin test (TST) conversions among employees of an elephant refuge
• Refuge
– Known to house elephants previously exposed to Mycobacterium tuberculosis
– Rumors that one elephant had tuberculosis disease
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Tuberculosis (TB)
• Caused by Mycobacterium tuberculosis (Mtb)
• Spread on airborne droplet nuclei
• Transmitted during close, prolonged contact
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TB in Humans and Elephants: Inactive Infection
Humans Elephants
Detection method
Symptoms
Infectious to others
Preventive therapy
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TB in Humans and Elephants: Inactive Infection
Humans Elephants
Detection method Positive TST or IGRA
Symptoms No
Infectious to others No
Preventive therapy Recommended
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TB in Humans and Elephants: Inactive Infection
Humans Elephants
Detection method Positive TST or IGRA Validation needed
Symptoms No No
Infectious to others No Probably not
Preventive therapy Recommended Efficacy unknown
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TB in Humans and Elephants: Active Disease
Humans Elephants
Diagnosis
Symptoms
Infectious to others
Treatment
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TB in Humans and Elephants: Active Disease
Humans Elephants
Diagnosis Sputum or chest x-ray
Symptoms Yes
Infectious to others Yes
Treatment Required
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TB in Humans and Elephants: Active Disease
Humans Elephants
Diagnosis Sputum or chest x-ray Saline trunk wash
Symptoms Yes Rare
Infectious to others Yes Yes
Treatment Required Recommended;
efficacy unknown
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TB in Humans and Elephants: Treatment for Disease
Humans Elephants
Antibiotics
Duration
Delivery
Efficacious
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TB in Humans and Elephants: Treatment for Disease
Humans Elephants
Antibiotics
Izoniazid, rifampin, ethambutol,
pyrazinamide
Duration 6 months
Delivery Oral
Efficacious Yes
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TB in Humans and Elephants: Treatment for Disease
Humans Elephants
Antibiotics
Izoniazid, rifampin, ethambutol,
pyrazinamide
Izoniazid, rifampin, ethambutol,
pyrazinamide
Duration 6 months 12 months
Delivery Oral Oral or rectal
Efficacious Yes Unknown
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Important Literature
• 1998 Michalak et al. (EID) – TB outbreak among 4 elephants in Illinois
– One employee had TB — isolate matched the elephants
– 11 employees positive TST — timing of conversion unknown
– Prompted action from USDA — annual Mtb testing required
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Captive Elephants in North America
270 Asian elephants 12% infected with Mtb
220 African elephants 2% infected with Mtb
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Elephant Refuge in Tennessee
• Established in 1995 with 1 elephant
• Care of sick, old, or abused elephants
• Nonprofit organization
• Accredited and licensed
• Closed to the public
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Elephant Refuge in Tennessee
• 2,700 acres and 14 elephants
• 3 areas with a barn and dedicated staff
– African area — 2 African elephants
– Asian area — 6 Asian elephants
• 3 from Illinois herd
– Quarantine area — 7 Asian elephants
• All from Illinois herd
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www.elephants.com
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www.elephants.com
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The Outbreak
• Notification
– October 2009
– 5 TST conversions
– 1 elephant with TB
• Response
– Gained access to the refuge
– Initiated onsite investigation
– December 2009
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Investigation Objectives
• Determine extent of outbreak
• Identify risk factors for TST conversion in humans
• Prevent ongoing transmission
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Cohort Study
• Interviews
• Occupational health records
– Preemployment and annual TST results
– Respirator fit testing dates
– Employment dates
• TST screening increased to quarterly
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TST Conversion
• Refuge employee or intern
• 2006–2009
• Documented negative (<10 mm) TST
• ≥10 mm increase in TST induration within 2 years
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Onsite Assessment
• Barn management
• Elephant husbandry practices
• Environmental sampling in targeted areas
• CDC National Institutes of Occupational Safety and Health (NIOSH)
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Record Review
• Refuge and TN Wildlife Resources Agency (TWRA)
• Timeline of events
– Elephants
– Employees
• Mtb culture results for respiratory secretions
– Trunk wash
– Participating elephants
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Employee Cohort, 2006–2009
• 57 current and former employees
• 46/57 (81%) interviewed
– 30 caregivers
– 11 administrators
– 5 maintenance workers
• 9/46 (20%) had positive TST
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Characteristics of Employees with Positive TST (n=9)
• 7 female
• Mean age 40 years (range 25–62 years)
• TST ranged 12–24 mm induration
• 1 conversion in 2006
– Prolonged exposure to a known source of TB
• 8 with documented conversion in 2009
• 6 began preventive therapy
• None have active TB disease
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
International travel 5 19 26 4 27 14 1.8 (0.6–5.8)
Foreign-born 2 6 33 7 40 18 1.9 (0.5–7.1)
Exposure to person(s) with TB 0 4 0 9 42 21 –
Healthcare facility work 1 8 13 8 38 21 0.6 (0.1–4.1)
Correctional facility work 0 4 0 9 42 21 –
Homeless shelter work 0 1 0 9 45 20 –
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST+ Total %
Close elephant contact 2 11 18 7 35 20 0.9 (0.2–3.8)
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST– Total %
Close elephant(s) contact 2 11 18 7 35 20 0.9 (0.2–3.8)
Quarantine area exposure 2009 8 13 62 1 33 3 20.3
(2.8–146.7)
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Potential Risk Factors for TB Among Refuge Employees, 2006–2009
Potential risk factor Exposed Unexposed Relative
Risk (95% CI)
TST+ Total % TST– Total %
Close elephant(s) contact 2 11 18 7 35 20 0.9 (0.2–3.8)
Quarantine area exposure 2009 8 13 62 1 33 3 20.3
(2.8–146.7)
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Quarantine Area
www.elephants.com
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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TST Conversion Timeline Among Quarantine Area Employees, 2009
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Characteristics of Quarantine Area Employees, 2009 (n = 13)
Conversion (n = 8)
No. (%)
TST Negative (n = 5)
No. (%)
Position Caregiver Administrative Maintenance
5 (63) 3 (38) 0 ( 0)
3 (60) 0 ( 0) 2 (40)
Close contact with elephant(s) 1 (13) 2 (40)
Participated in elephant(s) trunk wash 0 ( 0) 1 (20)
Pressure washed 5 (63) 3 (60)
Annual N95 fit testing 2 (25) 3 (60)
―Always‖ compliant with N95 wear 2 (25) 3 (60)
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Characteristics of Quarantine Area Employees, 2009 (n = 13)
Conversion (n = 8)
No. (%)
TST Negative (n = 5)
No. (%)
Position Caregiver Administrative Maintenance
5 (63) 3 (38) 0 ( 0)
3 (60) 0 ( 0) 2 (40)
Close contact with elephant(s) 1 (13) 2 (40)
Participated in elephant(s) trunk wash 0 ( 0) 1 (20)
Pressure washed 5 (63) 3 (60)
Annual N95 fit testing 2 (25) 3 (60)
―Always‖ compliant with N95 wear 2 (25) 3 (60)
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Characteristics of Quarantine Area Employees, 2009 (n = 13)
Conversion (n = 8)
No. (%)
TST Negative (n = 5)
No. (%)
Position Caregiver Administrative Maintenance
5 (63) 3 (38) 0 ( 0)
3 (60) 0 ( 0) 2 (40)
Close contact with elephant(s) 1 (13) 2 (40)
Participated in elephant(s) trunk wash 0 ( 0) 1 (20)
Pressure washed 5 (63) 3 (60)
Annual N95 fit testing 2 (25) 3 (60)
―Always‖ compliant with N95 wear 2 (25) 3 (60)
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Characteristics of Quarantine Area Employees, 2009 (n = 13)
Conversion (n = 8)
No. (%)
TST Negative (n = 5)
No. (%)
Position Caregiver Administrative Maintenance
5 (63) 3 (38) 0 ( 0)
3 (60) 0 ( 0) 2 (40)
Close contact with elephant(s) 1 (13) 2 (40)
Participated in elephant(s) trunk wash 0 ( 0) 1 (20)
Pressure washed 5 (63) 3 (60)
Annual N95 fit testing 2 (25) 3 (60)
―Always‖ compliant with N95 wear 2 (25) 3 (60)
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High Risk Work Practices
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Unrestricted Air Flow
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Environmental Sampling
• Barn housing the Mtb-infected elephant
• Standard methods
• Mtb not isolated
– Elephant stool (n = 14) – Water (n = 12) – Barn surface swabs (n = 23) – Air filter (n = 3)
• M. fortuitum isolated from 6 specimens
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More on Elephant L Mtb Culture Isolation
• Transferred from Illinois herd in 2006 and housed in quarantine
• Respiratory secretions obtained by trunk-wash method annually
• Mtb culture-positive in 2009
– Susceptible to all 4 first-line antibiotics
– Mtb genotype PCR01621
• 2004 CA human patient
• 2005 TN elephant died with TB (Illinois herd)
• 2006 TN elephant died with TB (Illinois herd)
• 2008 MO elephant
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Summary
• Employees exposed to the quarantine area in 2009 were 20 times more likely to have TB infection
– RR 20.3; 95% CI 2.8–146.7
• 8 TST conversion documented in 2009
– 3 administrators without elephant contact
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Factors Contributing to Transmission
• Delayed response to Mtb isolation
• Inadequate infection control
– Aerosol-generating work practices
– Inconsistent use of respirators
– Unrestricted air flow
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Immediate Interventions
• Relocate nonessential personnel
• Increase use of respirators
• Revise infection control practices
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Limitations
• 11 former employees not contacted
– None employed during 2009
– 2 employed during 2008
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Conclusions
• Mtb transmitted from elephant to humans
– Elephant L source of Mtb
• Indirect exposure associated with Mtb infection
• Inadequate infection control practices contributed
• Immediate interventions implemented
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Recommendations
• Reduce aerosol-generating work practices and restrict unfiltered air flow
• Educate workers and provide a comprehensive occupational health program
• Develop and comply with evidence-based TB control guidelines to protect employees working in the elephant industry
• Improve methods for diagnosis and treatment of Mtb infection in elephants
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Acknowledgments
• Elephant refuge
– Employees
– Leadership
• Tennessee Wildlife Resources Agency
– Walter Cook
• TN South-central Regional Health Office
– Lang Smith
– Joy Smith
• Lewis County Health Department
• Tennessee Department of Health
– Jon V. Warkentin
– John R. Dunn
– Timothy F. Jones
• Vanderbilt University School of Medicine
– William Schaffner
• CDC EIS Field Assignments Branch
– W. Randolph Daley
– Diana Bensyl
– Kris Bisgard
• CDC Division of TB Elimination
– Maryam Haddad
– Adam Langer
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For more information please contact Centers for Disease Control and Prevention
1600 Clifton Road NE, Atlanta, GA 30333 Telephone, 1-800-CDC-INFO (232-4636)/TTY: 1-888-232-6348 E-mail: [email protected] Web: www.cdc.gov
The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
zazzle.com
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EXTRA SLIDES
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New Serologic Assays for Detecting Mtb Exposure in Elephants
• ElephantTB STAT-PAK® – Lateral-flow technology
– Detects reactive antibody to M. tuberculosis and Mycobacterium bovis antigens
– Simple, rapid, and can be performed onsite
• MAPIA (multiantigen print immunoasay) – Detects reactive antibodies in serum specimens
– After a STAT-PAK-positive result, MAPIA has been used as a confirmatory test for M. tuberculosis
– Monitoring the treatment of elephants with active TB
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Important Literature
• 1998 Michalak et al. (EID) – TB outbreak among 4 elephants in Illinois
– One employee had TB — isolate matched the elephants
– 11 employees positive TST — timing of conversion unknown
– Prompted action from USDA — annual Mtb testing required
• 2002 Oh et al. (EID) – TB infection among multiple species at California zoo
– 55 employees positive TST — 10 with probable conversion
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Important Literature
• 1998 Michalak et al. (EID) – TB outbreak among 4 elephants in Illinois
– One employee had TB — isolate matched the elephants
– 11 employees positive TST — timing of conversion unknown
– Prompted action from USDA — annual Mtb testing required
• 2002 Oh et al. (EID) – TB infection among multiple species at California zoo
– 55 employees positive TST — 10 with probable conversion
• 2002 Payeur et al. (Ann NY Acad Sci) – 5 Mtb genotypes circulating among 6 elephant herds
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Important Literature
• 1998 Michalak et al. (EID) – TB outbreak among 4 elephants in Illinois
– One employee had TB — isolate matched the elephants
– 11 employees positive TST — timing of conversion unknown
– Prompted action from USDA — annual Mtb testing required
• 2002 Oh et al. (EID) – TB infection among multiple species at California zoo
– 55 employees positive TST — 10 with probable conversion
• 2002 Payeur et al. (Ann NY Acad Sci) – 5 Mtb genotypes circulating among 6 elephant herds
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Culture Isolation of Mtb from Elephant Respiratory Secretions
• Obtained by trunk-wash method
– 30–60 mL of saline
– Raise then lower trunk to collect saline
– 3 samples collected over 1 week
– Standard methods for mycobacterial species
• Method has low sensitivity
– Mtb isolation confirms active TB disease
– Negative result does not exclude active disease
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Trunk Wash Collection
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Trunk Wash Results
• Provided by TWRA
• 2006–2008, all trunk-wash results received were Mtb culture-negative
• 2009, Mtb isolated from 1 of 14 elephants
• Elephant L
– Mtb culture-positive
– Housed in quarantine area
– Arrived in 2006
– Transferred from Illinois herd
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Elephant L Trunk Wash Timeline
• Dec 2008
– Secretions collected
• Mar 2009
– Mtb isolated
• Jul 2009
– Culture confirmed
• Oct 2009
– Heightened infection control
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Elephant L Isolate
• Mtb susceptible to all 4 first-line antibiotics
– Isoniazid, rifampin, ethambutol, pyrazinamide
• Genotype PCR01621
– 2004 CA human patient
– 2005 TN elephant died with TB
– 2006 TN elephant died with TB
– 2008 MO elephant
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Elephant L Isolate
• Mtb susceptible to all 4 first-line antibiotics
– Isoniazid, rifampin, ethambutol, pyrazinamide
• Genotype PCR01621
– 2004 CA human patient
– 2005 TN elephant died with TB (exposure in IL)
– 2006 TN elephant died with TB (exposure in IL)
– 2008 MO elephant