Abstract
Tuberculosis in ungulate species, caused most frequently by Mycobacterium bovis and M. tuberculosis, has been a well-documented health problem for zoological collections as long ago as the late 19th century. More recently, over the past 2 decades, tuberculosis has been reported in hoofstock species from at least 20 American Zoo and Aquarium Association (AZA)-accredited zoological collections, prompting greater concern at both animal and human health regulatory levels. Additionally, because few diagnostic tests have been validated for use in these exotic species, the ability of professionals to detect sub-clinical infections in these animals is severely limited.
These concerns over tuberculosis prevalence and detection were further heightened when elephants at several different institutions were diagnosed with active M. tuberculosis infections in 1996. In conjunction with this outbreak, the Tuberculosis Committee of the United States Animal Health Association recommended that "the USDAY pursue the formation of an inter-industry working group to address the issues of tuberculosis in exotic animal collections." Thus, the National Tuberculosis Working Group for Zoo and Wildlife Species was formed, consisting of members representing the zoological, wildlife, regulatory, and diagnostic fields. The mission of this group has been "to control and ultimately eradicate tuberculosis (M. tuberculosis complex) and control other mycobacterial diseases in zoo and wildlife species." As a significant step towards this goal, the Working Group developed and distributed the Guidelines for the Control of Tuberculosis in Elephants in 1998.
While the formation of these Guidelines has been an advance towards the control of tuberculosis in this species, overall recommendations have not yet been developed for the control of this infection in all hoofstock species. Before such recommendations can be fully developed however, several questions regarding movement, testing and reporting practices, as well as apparent reactor and disease prevalence, need to be addressed. Therefore, the Working Group, in coordination with the USDA, AAZV and the AZA, developed and distributed an intensive survey to all AZA-accredited and related institutions in August 1999 to better address these deficiencies.
As of 1 April 2000, of the 150 AZA-affiliated institutions whose collections include ungulates, 139 (92.7%) have returned this document to the Working Group. A summary of the data compiled from these surveys is included in Tables 1, 2a, and 2b. Currently, these data are being utilized to finalize the Guidelines for ungulate species in zoo environments. This presentation, in combination with a poster presentation from the Working Group, will explore the implications of these data with regard to future management and movement recommendations (including proposed test reporting mechanisms), as well as highlight areas where more intensive work is needed.
Table 1. Summary of movement data from the 1999 AZA/AAZV/USDA ungulate tuberculosis survey.
Data include number of responses and, in parentheses, percentage of total responses within each category.
|
Survey question/
Proportion of ungulates
|
Where animals are acquired from/distributed to
|
|
AZA Zoos
|
Non-AZA Zoos
|
Game Parks
|
Private Dealers
|
Auctions
|
Import/ Export
|
|
From where does your institution acquire ungulates?
|
|
All ungulates
|
20
|
1
|
0
|
1
|
0
|
0
|
|
(14.7)
|
(0.8)
|
(0.0)
|
(0.7)
|
(0.0)
|
(0.0)
|
|
Almost all ungulates
|
50
|
0
|
0
|
2
|
0
|
0
|
|
(36.8)
|
(0.0)
|
(0.0)
|
(1.5)
|
(0.0)
|
(0.0)
|
|
Most ungulates
|
38
|
1
|
0
|
7
|
0
|
1
|
|
(27.9)
|
(0.8)
|
(0.0)
|
(5.2)
|
(0.0)
|
(0.8)
|
|
Some ungulates
|
20
|
26
|
15
|
31
|
0
|
5
|
|
(14.7)
|
(19.7)
|
(11.5)
|
(23.1)
|
(0.0)
|
(3.8)
|
|
Very few ungulates
|
2
|
35
|
23
|
28
|
0
|
18
|
|
(1.5)
|
(26.5)
|
(17.7)
|
(20.9)
|
(0.0)
|
(18.9)
|
|
No ungulates
|
6
|
69
|
92
|
65
|
130
|
106
|
|
(4.4)
|
(52.3)
|
(70.8)
|
(48.5)
|
(100.0)
|
(81.5)
|
|
To where does your institution distribute ungulates?
|
|
All ungulates
|
15
|
1
|
0
|
2
|
0
|
0
|
|
(11.3)
|
(0.8)
|
(0.0)
|
(1.5)
|
(0.0)
|
(0.0)
|
|
Almost all ungulates
|
38
|
0
|
1
|
2
|
0
|
0
|
|
(28.6)
|
(0.0)
|
(0.8)
|
(1.5)
|
(0.0)
|
(0.0)
|
|
Most ungulates
|
41
|
2
|
2
|
6
|
0
|
1
|
|
(30.8)
|
(1.5)
|
(1.5)
|
(4.6)
|
(0.0)
|
(0.8)
|
|
Some ungulates
|
23
|
35
|
14
|
28
|
0
|
4
|
|
(17.3)
|
(26.9)
|
(10.8)
|
(21.5)
|
(0.0)
|
(3.1)
|
|
Very few ungulates
|
4
|
34
|
25
|
25
|
2
|
24
|
|
(3.0)
|
(26.2)
|
19.2)
|
(19.2)
|
(1.6)
|
(18.9)
|
|
No ungulates
|
12
|
58
|
88
|
67
|
125
|
98
|
|
(9.0)
|
(44.6)
|
(67.7)
|
(51.5)
|
(98.4)
|
(77.2)
|
Table 2a. Summary of testing data from the 1999 AZA/AAZV/USDA ungulate tuberculosis survey.
Data include number of responses and, in parentheses, percentage of total responses within each category.
a NA = Not applicable.
|
Survey
Question
/Survey
Answer
|
Bovids
|
Camelids
|
Cervids
|
Elephant
|
Giraf-fidae
|
Hippo-potamus
|
Other
Artio-dactylids
|
Rhino-ceros
|
Rumin-ants
|
Swine
|
Tapir
|
|
Testing Frequency
|
|
Never
|
4
|
8
|
9
|
5
|
32
|
36
|
6
|
24
|
16
|
36
|
12
|
|
(3.7)
|
(8.3)
|
(8.0)
|
(6.5)
|
(38.6)
|
(75.0)
|
(7.9)
|
(35.8)
|
(13.4)
|
(47.4)
|
(25.0)
|
|
On
Acquisition
|
56
|
46
|
55
|
24
|
25
|
6
|
41
|
23
|
67
|
23
|
23
|
|
(51.9)
|
(47.9)
|
(49.1)
|
(31.2)
|
(30.1)
|
(12.5)
|
(53.9)
|
(34.3)
|
(56.3)
|
(30.3)
|
(47.9)
|
|
Pre
Shipment
|
81
|
61
|
80
|
21
|
37
|
7
|
63
|
34
|
76
|
24
|
25
|
|
(75.0)
|
(63.5)
|
(71.4)
|
(27.3)
|
(44.6)
|
(14.6)
|
(82.9)
|
(50.7)
|
(63.9)
|
(31.6)
|
(52.1)
|
|
When
Immobilized
|
40
|
20
|
27
|
8
|
19
|
8
|
24
|
18
|
21
|
11
|
12
|
|
(37.0)
|
(20.8)
|
(24.1)
|
(10.4)
|
(22.9)
|
(16.7)
|
(31.6)
|
(26.9)
|
(17.6)
|
(14.5)
|
(25.0)
|
|
Annually
|
13
|
18
|
16
|
50
|
4
|
1
|
7
|
6
|
25
|
8
|
4
|
|
(12.0)
|
(18.8)
|
(14.3)
|
(64.9)
|
(4.8)
|
(2.1)
|
(9.2)
|
(9.0)
|
(21.0)
|
(10.5)
|
(8.3)
|
|
Other
|
3
|
3
|
4
|
5
|
1
|
0
|
1
|
0
|
5
|
0
|
1
|
|
(2.8)
|
(3.1)
|
(3.6)
|
(6.5)
|
(1.2)
|
(0.0)
|
(1.3)
|
(0.0)
|
(4.2)
|
(0.0)
|
(2.1)
|
|
Primary Testing Method
|
|
Single Skin
Test
|
95
|
79
|
90
|
18
|
49
|
11
|
60
|
37
|
96
|
29
|
31
|
|
(88.0)
|
(82.3)
|
(80.4)
|
(23.4)
|
(59.0)
|
(22.9)
|
(78.9)
|
(55.2)
|
(80.7)
|
(38.2)
|
(64.6)
|
|
Comparative
Skin Test
|
7
|
6
|
11
|
3
|
2
|
1
|
6
|
3
|
8
|
7
|
5
|
|
(6.5)
|
(6.3)
|
(9.8)
|
(3.9)
|
(2.4)
|
(2.1)
|
(7.9)
|
(4.5)(6.7)
|
(9.2)
|
(10.4)
|
|
|
Culture
|
0
|
0
|
1
|
58
|
0
|
1
|
0
|
2
|
1
|
0
|
4
|
|
(0.0)
|
(0.0)
|
(0.9)
|
(75.3)
|
(0.0)
|
(2.1)
|
(0.0)
|
(3.0)
|
(0.8)
|
(0.0)
|
(8.3)
|
|
Primary Skin Test Site
|
|
Tail Fold
|
67
|
29
|
22
|
11
|
26
|
3
|
26
|
16
|
81
|
20
|
16
|
|
(65.0)
|
(33.7)
|
(21.4)
|
(16.4)
|
(50.1)
|
(27.3)
|
(37.1)
|
(38.1)
|
(78.6)
|
(48.8)
|
(44.4)
|
|
Cervical
|
38
|
23
|
78
|
4
|
26
|
0
|
36
|
1
|
23
|
7
|
4
|
|
(36.9)
|
(26.7)
|
(75.7)
|
(6.0)
|
(50.1)
|
(0.0)
|
(51.4)
|
(2.4)
|
(22.3)
|
(17.1)
|
(11.1)
|
|
Ear
|
0
|
0
|
0
|
9
|
1
|
5
|
0
|
23
|
0
|
13
|
4
|
|
(0.0)
|
(0.0)
|
0.0
|
13.4
|
2.0
|
45.5
|
0.0
|
54.8
|
13
|
31.7
|
11.1
|
|
Axilla
|
0
|
33
|
1
|
0
|
0
|
0
|
1
|
0
|
0
|
0
|
5
|
|
(0.0)
|
(38.4)
|
(1.0)
|
(0.0)
|
(0.0)
|
(0.0)
|
(1.4)
|
(0.0)
|
(0.0)
|
(0.0)
|
(13.9)
|
|
Inguinal
|
0
|
2
|
0
|
3
|
0
|
0
|
0
|
0
|
0
|
0
|
8
|
|
(0.0)
|
(2.3)
|
(0.0)
|
(4.5)
|
(0.0)
|
(0.0)
|
(0.0)
|
(0.0)
|
(0.0)
|
(0.0)
|
(22.2)
|
|
Other
|
3
|
2
|
1
|
0
|
1
|
1
|
5
|
2
|
2
|
2
|
0
|
|
(2.9)
|
(2.3)
|
(1.0)
|
(0.0)
|
(2.0)
|
(9.1)
|
(7.1)
|
(4.8)
|
(1.9)
|
(4.9)
|
(0.0)
|
Table 2b. Summary of testing data from the 1999 AZA/AAZV/USDA ungulate tuberculosis survey.
Data include number of responses and, in parentheses, percentage of total responses within each category. a NA = Not applicable.
|
Survey
Question
/Survey
Answer
|
Bovids
|
Camelids
|
Cervids
|
Elephant
|
Giraf-fidae
|
Hippo-potamus
|
Other
Artio-dactylids
|
Rhino-ceros
|
Rumin-ants
|
Swine
|
Tapir
|
|
Primary Test Results
|
|
No
|
74
|
66
|
62
|
61
|
45
|
9
|
66
|
33
|
78
|
40
|
27
|
|
Positive
|
(68.5)
|
(68.8)
|
(55.4)
|
(79.2)
|
(54.2)
|
(18.8)
|
(86.8)
|
(65.5)
|
(65.5)
|
(51.3)
|
(56.3)
|
|
Positive
|
30
|
21
|
40
|
7
|
3
|
0
|
4
|
7
|
23
|
0
|
7
|
|
Primary
|
(27.8)
|
(21.9)
|
(35.7)
|
(9.1)
|
(3.6)
|
(0.0)
|
(5.3)
|
(19.3)
|
(19.3)
|
(0.0)
|
(14.6)
|
|
Positive Primary Test Follow-Up Actions
|
|
Retest, Same Method
|
4
|
6
|
3
|
1
|
0
|
NAa
|
0
|
1
|
0
|
NA
|
0
|
|
(13.3)
|
(28.6)
|
(7.5)
|
(14.3)
|
(0.0)
|
|
(0.0)
|
(14.3)
|
(0.0)
|
|
(0.0)
|
|
Retest,
Different
Method
|
30
|
20
|
40
|
6
|
1
|
NA
|
4
|
7
|
21
|
NA
|
6
|
|
(100.0)
|
(95.2)
|
(100.0)
|
(85.7)
|
(33.3)
|
(100.0)
|
(100.0)
|
(91.3)
|
|
|
(85.7)
|
|
Test Entire
Herd
|
8
|
3
|
7
|
3
|
0
|
NA
|
0
|
1
|
2
|
NA
|
1
|
|
(26.7)
|
(14.3)
|
(17.5)
|
(42.9)
|
(0.0)
|
|
(0.0)
|
(14.3)
|
(8.7)
|
|
(14.3)
|
|
Test
Adjacent
Herd
|
3
|
1
|
1
|
1
|
0
|
NA
|
0
|
1
|
1
|
NA
|
0
|
|
(10.0)
|
(4.8)
|
(2.5)
|
(14.3)
|
(0.0)
|
|
(0.0)
|
(14.3)
|
(4.3)
|
|
(0.0)
|
|
Euthanatize
Animal
|
5
|
1
|
6
|
0
|
0
|
NA
|
0
|
0
|
3
|
NA
|
0
|
|
(16.7)
|
(4.8)
|
(15.0)
|
(0.0)
|
(0.0)
|
|
(0.0)
|
(0.0)
|
(13.0)
|
|
(0.0)
|
|
No
|
0
|
0
|
0
|
1
|
0
|
NA
|
0
|
0
|
1
|
NA
|
1
|
|
Action
|
(0.0)
|
(0.0)
|
(0.0)
|
(14.3)
|
(0.0)
|
|
(0.0)
|
(0.0)
|
(4.3)
|
|
(14.3)
|
|
Secondary Testing Results
|
|
No
|
1
|
0
|
1
|
1
|
0
|
NA
|
0
|
0
|
0
|
NA
|
1
|
|
Retest
|
(3.3)
|
(0.0)
|
(2.5)
|
(14.3)
|
(0.0)
|
|
(0.0)
|
(0.0)
|
(0.0)
|
|
(14.3)
|
|
No
|
18
|
18
|
27
|
5
|
3
|
NA
|
3
|
5
|
19
|
NA
|
4
|
|
Positive
|
(60.0)
|
(85.7)
|
(67.5)
|
(71.4)
|
(100.0)
|
|
(75.0)
|
(71.4)
|
(82.6)
|
|
(57.1)
|
|
Positive
|
10
|
2
|
12
|
1
|
0
|
NA
|
1
|
2
|
4
|
NA
|
2
|
|
Secondary
|
(33.3)
|
(9.5)
|
(30.0)
|
(14.3)
|
(0.0)
|
|
(25.0)
|
(28.6)
|
(17.4)
|
|
(28.6)
|
|
Secondary Methods Used
|
|
Comparative
Skin Test
|
21
|
15
|
27
|
2
|
1
|
NA
|
2
|
2
|
19
|
NA
|
5
|
|
(75.0)
|
(75.0)
|
(69.2)
|
(33.3)
|
(33.3)
|
|
(50.0)
|
(28.6)
|
(82.6)
|
|
(83.3)
|
|
Necropsy
|
9
|
4
|
10
|
0
|
0
|
NA
|
1
|
0
|
5
|
NA
|
0
|
|
(32.1)
|
(20.0)
|
(25.6)
|
(0.0)
|
(0.0)
|
|
(25.0)
|
(0.0)
|
(21.7)
|
|
(0.0)
|
|
Culture
|
8
|
3
|
9
|
4
|
0
|
NA
|
2
|
2
|
3
|
NA
|
3
|
|
(28.6)
|
(15.0)
|
(23.1)
|
(66.7)
|
(0.0)
|
|
(50.0)
|
(28.6)
|
(13.0)
|
|
(50.0)
|
|
Serologic
Method
|
8
|
1
|
5
|
4
|
0
|
NA
|
2
|
0
|
2
|
NA
|
2
|
|
(28.6)
|
(5.0)
|
(12.8)
|
(66.7)
|
(0.0)
|
|
(50.0)
|
(0.0)
|
(8.7)
|
|
(33.3)
|
|
Tissue
Method
|
2
|
1
|
3
|
1
|
0
|
NA
|
1
|
0
|
1
|
NA
|
0
|
|
(7.1)
|
(5.0)
|
(7.7)
|
(16.7)
|
(0.0)
|
|
(25.0)
|
(0.0)
|
(4.3)
|
|
(0.0)
|
Acknowledgments
The authors would like to thank all zoo veterinarians who took the time to respond to this fairly lengthy survey. Also, we would like to thank Jane Fouser for her tireless efforts on data compilation and entry.