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Tuberculosis (TB) among
Travelers Arriving into the
United States, 2006-2009
William L. Jackson, MD, PhD, MSPH, MA
CAPT, Commissioned Corps, U.S. Public Health Service
Quarantine and Border Health Services Branch
Division of Global Migration and Quarantine
2011 USPHS Scientific and Training Symposium:
New Orleans, LA
National Center for Emerging and Zoonotic Infectious Diseases
Division of Global Migration and Quarantine
Presentation Overview
• Outline the distribution of TB in the United States
and globally with respect to travelers who are
infectious with TB
• Report on travelers who are infectious with TB as
documented using the CDC Quarantine Activity
Reporting System (QARS)
Geographic Distribution of
Mycobacterium tuberculosis (MTB)
TB Cases, United States, 1993-2008
Overall TB rate:
4.2 per 100,000
FB 20.6/100K
US 2.1/100K
Div. TB Elimination (CDC/OID/NCHHSTP) :
www.cdc.gov/tb/topic/research/TBESC
TB Case Count and Rate* Among U.S.- and Foreign-born
Persons, by Year — United States, 1993–2010
22
45
No. of TB cases among U.S.-born persons
No. of TB cases among foreign-born persons
TB rate among U.S.-born persons
TB rate among foreign-born persons
Overall nationa TB rate
18
16
40
35
30
14
12
25
10
20
8
15
6
10
4
2
5
0
0
1993
1995
1997
1999
2001
Year
* Per 100,000 population.
Data are updated as of Feb 26, 2011 and are provisional.
2003
2005
2007
2009
Rate
Number (in thousands)
20
Foreign-born US Residents Reported
with TB in United States -- 2009
Countries of Origin
Age Distributions
>65 yrs
(20%)
Philippines
(12%)
<15 yrs
(6%)
15–24 yrs
(11%)
45–64 yrs
(30%)
www.cdc.gov/tb/topic/research/TBESC
25–44 yrs
(34%)
Quarantine Activity Reporting System
(QARS)
• Secure Web-based system used to track diseases
of public health interest and activities at CDC
Quarantine Stations:
–
–
–
–
–
–
Reports of ill and deceased passengers
Inspections of passengers, cargo, and conveyances
Monitoring shipments of nonhuman primate & drugs
Immigrant and refugee processing
Partnership activities: diseases of public health interest
Other
• Administrative log of CDC and partner responses
to travel-related events or incidents
CDC Quarantine Stations by Jurisdictions
Field offices for responding to and documenting
illness in travelers
AK
ME
Minneapolis
Seattle
Chicago
Anchorage
WA
ND
MT
Detroit
MN
OR
VT
ID
MD DE
WY
IA
NE
No.CA
IN
IL
UT
CO
VA
OK
AZ
Los Angeles
Dallas
Philadelphia
Washington, D.C.
NC
TN
So.CA
Newark
WV
KY
MO
KS
New York
OH
NV
San Francisco
CT
NJ
PA
SD
Boston
MA
RI
NY
MI
WI
NH
SC
AR
Atlanta
NM
North TX
MS
AL
GA
San Diego
El Paso
West TX
East TX
LA
FL
Houston
Miami
Honolulu
GU
PR
HI
CDC Quarantine Stations
San Juan
QARS Report Types for Diseases of
Public Health Interest
•Illness reported during
travel
•Illness reported after
travel completed
•Death reported during
travel
•Land border crossing
•Other information
Diseases of Public Health Interest
Quarantinable*
Smallpox, Cholera, Plague, Viral
Hemorrhagic Fevers, Infectious
Tuberculosis, Yellow Fever, Diphtheria,
SARS, Novel Influenza Virus (pandemic
potential)
Public Health Concern (examples)
* Executive Order 13375:
Revised List of Quarantinable
Communicable Diseases,
President George W. Bush,
April 1, 2005
Rabies, malaria, dengue, measles,
mumps, rubella, varicella,
meningococcal, zoonotic poxvirus,
polio, legionellosis, pertussis
Objectives
• Review of analysis methodology for tuberculosis
surveillance
• Reports on TB in travelers documented using the CDC
Quarantine Activity Reporting System (QARS)
• Characteristics and trends of travelers with infectious TB
• Baselines and trend changes for TB reporting
METHODOLOGY
Tuberculosis Surveillance Definitions in the
CDC Quarantine Activity Reporting
System (QARS)
Major QARS Report Categories for
Travel-Related TB Surveillance
Sea
Air
Land
Before Travel
During Travel
After Travel
Illness reported
prior to initiation of
transit
Illness/death
reported while
person in transit
Illness reported
after person
reached final
destination
American Thoracic Society (ATS)
CDC TB-Classification System
Tuberculosis Status
• No TB exposure
• TB exposure
• Latent TB infection
• Active TB disease
• Clinically inactive TB
• TB suspect
TB-Class:
† No-active (inactive)
Stage
Class 0†
Class 1†
Class 2†
Class 3‡
Class 4†
Class 5*
‡Active
*Temporary(deleted)
QARS Tuberculosis
Report Confirmation
Clinical criteria
Laboratory criteria
Confirmation requires direct or indirect evidence
of ALL clinical elements in QARS records
Clinical criteria = all below
Clinical (AFB+) specimen MTB complex detection
by nucleic acid amplification (NAA) OR culture
Lab criteria = any below
Acid-fast
bacilli (AFB+)
sputum smear
Chest x-ray
Medical exam
TB skin test
Anti-TB
therapy
Culture
Nucleic acid
amplification
Selected Timelines
• QARS activated and current CDC Quarantine
Station configurations set by end 2005
• Analysis dates 01JAN2006 - 31DEC2009 permit
multiple end point analysis
– Yearly trends between traveler demographics
– Monthly comparisons for TB activity class
– Contrast of pre/post-effects and comparisons for
2007 media events on TB(+) traveler(s)
• Time segments permit use of USDoT BTS travel
statistics to estimate rates (denominators)
TB in Travelers Arriving in US:
Analysis Methods 2006-09
Record extraction from QARS
552,759
QARS Entries
104,530
Illness Reports
6,596
TB-related
Reports
Record rev iew
• 949 reports met TB case definition after medical officer review
Categorize • SAS text-searc h with Medic al Offic er duplic ate c hec ks
Classif y
• 873 TB-c ases met Americ an Thorac ic Soc iety definitions
• Medic al Offic er c onsultation with Q-Stations or health departments
Analyze
• Confirmation reviews for report c ase definition assignment
• Epi-info 3. 5 analysis and evaluations
RESULTS
Tuberculosis Surveillance
Annual Volume of QARS TB Reports compared
with Traveler Volumes, 2006-2009 (N=873)
300
80
70
250
200
Case Reports
50
150
40
30
100
20
50
10
0
0
2006
2007
2008
2009
Years
Active
No-Active
US-Inbound Traveler Vol.
*
*Source: Bureau of Travel Statistics (BTS) of the US Department of Transportation
Traveler Volume x 106
60
Active-TB Case Reports in relation to Travel,
2006-2009 (N=949)
400
350
300
TB-Case Reports
250
200
150
100
50
0
Before Travel
During Travel
Years
2006
2007
After Travel
2008
2009
Agency Sources for TB Reporting to CDC
Quarantine Stations, 2006-2009 (N=949)
Time Periods
Before Travel
During Travel
After Travel
Federal
US Customs* Travel industry Health Dept. Care Provider International Other
*US Customs = CBP of US DHS, Federal = all US Government agencies excluding CBP
Comparison: TB and Other Illness Reports,
2006-2009
No-Active TB
Active TB (Class 3)
QARS Illness Reports
50
45
800
Novel H1N1
TB(+) Traveler
Media Event
700
40
600
500
TB-Reports
30
25
400
20
300
15
200
10
100
5
0
0
Month
TB infected travelers recorded in QARS Illness Reports 01JAN2006-31DEC2009
QARS Illness Reports
35
Countries of Origin for Persons
Reported with TB in United States
Passport
Proportions by
country of origin
travelers with TB
recorded in QARS:
2006-2009
Mexico
(13%)
Philippines
(10%)
Other Countries
(58%)
India
(8%)
(1.5%)
Ethiopia/Kenya
Pakistan
China
(4%)
Vietnam
(3%)
Korea
(2%)
Countries of citizenship for non US-citizens
with TB reported in QARS, 2006-2009
80
70
60
C
A
S
E
S
50
40
Active
Non-Active
30
20
10
0
COUNTRIES
TB infected travelers recorded in QARS Illness Reports 01JAN2006-31DEC2009
Countries of Origin for Persons
Reported with TB in United States
Travelers recorded in QARS
2006-09
Foreign-born US Residents
2009
Mexico
(13%)
Philippines
(10%)
Other Countries
(58%)
Philippines
(12%)
www.cdc.gov/tb/topic/research/TBESC
India
(8%)
China
(4%)
Vietnam
(3%)
Korea
(2%)
(1.5%)
Ethiopia/Kenya/Pakistan
QARS TB Reports, by Age: 2006-09
Foreign-born US Residents
2009
>65 yrs
(20%)
45–64 yrs
(30%)
Travelers recorded in QARS
2006-09
<15 yrs
<15 yrs
(6%)
15–24 yrs
(11%)
25–44 yrs
(34%)
http://www.cdc.gov/tb/topic/research/TBESC
(3%)
>65 yrs
(16%)
15–24 yrs
(16%)
45–64 yrs
(25%)
25–44 yrs
(40%)
Ratios and Rates of Total TB Reporting to
CDC Quarantine Stations, 2006-2009
Monthly
2006
2007
2008
2009
TB Reports per 100 6.67
QARS Illness Reports [3.31]
13.74
[7.44]
15.44
[5.67]
8.97
[5.73]
TB Reports per
1.17
Million Air Trave le rs [0.47]
2.51
[1.56]
3.17
[0.99]
*3.22
[0.63]
M ean [Std. D eviation] *p < 0.001 (F-tes t)
Rates of Total TB Reporting to CDC
Quarantine Stations, 2006-2009
Monthly
Jan 06-May 07 Jun 07-Dec 09
TB Re ports pe r 100
QARS Illne ss Re ports
5.4 [2.6]
*9.3 [4.7]
TB Reports per Million
Air Travelers
1.18 [0.45]
**3.18 [0.78]
M ean [Std. D eviation] *p < 0.001 **p < 0.001 (F-test)
Monthly TB Report Trends for Active v. Non-active
Cases, Adjusted for Travel Volume
3
2.5
Cases per Traveler x 106
Active
Slope1 p < 0.10
2
1.5
Rate-Active
Rate-Non
1
Non-Active
0.5
Slope2 p < 0.01
0
0
10
20
TB(+) Traveler
Media Event
2006
2007
30
MONTHS
40
2008
50
60
2009
Summary
• Countries of citizenship for travelers with TB
reported in QARS consistent with
– WHO estimates of TB incidence by country
– TB in foreign-born US residents
• TB-reporting to CDC Quarantine Stations
increased significantly after high-profile
media events in May 2007
– Sustained for Active TB disease > inactive disease
– Difference persisted into 2009
Limitations
• QARS functions as a passive surveillance
system for communicable diseases
– Reliant on reportage of partners outside of CDC
– Reflects only fractions of actual infected travelers
• Passports act as surrogates to traveler
countries-of-origin
– Unable to precisely discern microbial origins
– Unable to discern any episodes of microbial
transmission
Conclusions
• Majority of TB cases reported in QARS were active
pulmonary disease
• Majority of all TB cases reports came from state or
local public health partners after travel completed
• Increased TB-reporting rates after 2007 may reflect
enhanced Federal, State and local public health
surveillance partnerships for infectious TB in
travelers
• Sustained growth in pre-travel reports from public
health partners (2008-09) likely reflect the
institution of a public health “Do Not Board”
program by CDC
Next Steps
• Conduct further evaluation to
characterize high-risk travelers who are
not included in current pre-travel
screening systems (e.g. , students,
temporary workers)
• Additional analyses will establish
baseline TB report rates and inform
strategies to control TB in travelers and
prevent spread to US communities
Acknowledgments
Division of Global Migration and Quarantine and
Quarantine Station Officers
Daniel Fishbein
Nina Marano
Brian Miars
An Nguyen
LaTonia Richardson
Chris Schembri
Ciji Adams
Francisco Alvarado-Ramy
Kirsten Buckley
Peter Houck
Tonyka Jackson
Curi Kim
Laura Leidel
Brian Schmidt
Paige Szymanowski
Questions?
William L. Jackson, MD, PhD, MSPH, MA
CAPT, U.S. Public Health Service Commissioned Corps
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.
National Center for Emerging and Zoonotic Infectious Diseases
Division of Global Migration and Quarantine
International Health Regulations
(June,2007)
• Global agreements about procedures to
protect public health
• Adopted at the World Health Assembly &
binding on all WHO’s Member States (unless
they reject or reserve)
• Legal language in a document containing
66 articles and 9 annexes
• Supported by technical (compliance)
guidelines
www.who.int/ihr/en/
Illness Reports in QARS, 2010
(N=2,003)
Illness
Frequency
(%)
H1N1/ILI
252 (31)
Varicella
195 (24)
Tuberculosis
171 (21)
Mumps
31 (4)
Measles
30 (4)
Malaria
27 (3)
Pertussis
22 (3)
Dengue fever
18 (2)
Typhoid fever
16 (2)
Cholera
12 (1)
Meningococcal
12 (1)
Hepatitis
16 (1)
Legionnaires’ disease
9 (1)
YEAR
Female
Active
TB
Female
Inactive
TB
Male
Active
TB
Male
Inactive
TB
2006
27
8
44
18
2007
47
31
99
49
2008
102
34
99
49
29
11.7%
40.7
[20.7]
105
39.7%
43.6
[18.2]
53
19.3%
41.2
[18.0]
2009
79
Pct(+)TB 29.2%
MeanAge 40.9
[StdDev] [19.3]
TOTALS
(Pct. Male)
N=873
97
(63.9%)
226
(65.5%)
284
(52.1%)
266
(59.4%)
100%
42.1
[18.7]
Chi-square: GENDER=6.3370(df 3 )p<0.0963; F-statistic=3.229: T-Statistic=1.797(df 1) p<0. 0728
TB Cases reported in QARS, by age,
2006-2009
MTB Observe Mean
Disease d
Age
Cases
Female
Active
Male
Active
Female
Non-Active
Male
Non-Active
Std Dev
241
40.9
19.3
380
43.6
18.2
94
40.7
20.7
165
41.2
18.0
F-statistic = 3.2291: T-Statistic = 1.7970 (GENDER) = 6.3370 (df 1) p<0. 0728
Major QARS Report Categories
for TB Surveillance
• Illness Reported During Travel
– Ill individual reported before s/he reached final
destination
– Individuals who are currently on a conveyance
(airplane, cruise ship, etc) at a port or otherwise in
transit
•
•
•
•
Illness Reported After Travel Completed
Death Reported During Travel
Land Border Crossing
Other Information
Major QARS Report Categories
for TB Surveillance
• Illness Reported During Travel
• Illness Reported After Travel Completed
– Ill individual reported after s/he reached his/her
final destination for a leg of a trip
– Frequently but not always a residence
• Death Reported During Travel
• Land Border Crossing
• Other Information
Major QARS Report Categories
for TB Surveillance
•
•
•
•
•
Illness Reported During Travel
Illness Reported After Travel Completed
Death Reported During Travel
Land Border Crossing
Other Information
– Captures activities or events that do not fit prior report
types
– Examples: Before Travel Illness, public health Do Not
Board and Lookout Lists, Foreign Notification of
Case/Contact, Human Remains
Modi, et al; Clin. Inf. Dis. 2009:49
885
1 June 2006 – 31 May2008
TB Reports by Quarantine Station, 2006-09
2006
mean