Tuberculosis in Zoo Ungulates: Survey Results and Surveillance Plan
IAAAM 2000
Michael Ziccardi1, DVM, MPVM; Susan K. Mikota2, DVM; Robyn B. Barbiers1, DVM; Terry M. Norton3, DVM; P.K. Robbins4, DVM; and the National Tuberculosis Working Group for Zoo and Wildlife Species
1Institute for Wildlife Infectious Disease, Lincoln Park Zoological Gardens, Chicago, IL, USA; 2Audubon Center for Research of Endangered Species, New Orleans, LA, USA; 3St. Catherine's Wildlife Survival Center, Midway, GA, USA; 4Los Angeles Zoo, Los Angeles, CA, USA

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.

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

Michael Ziccardi, DVM, MPVM


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