Abstract

Johne's disease (paratuberculosis) is a fatal and often clinically invisible transmissible disease of hoofstock. The infection has been reported in many captive or free-ranging artiodactyl species. Animals are infected by the etiologic agent (Mycobacterium avium ss. paratuberculosis (Map)) in the first few months of life. They may appear healthy for years afterwards but during this long subclinical phase the animal is capable of infecting offspring and herdmates by shedding the organism in its feces and milk. When clinical signs do appear, they are non-specific (weight loss and diarrhea in some species) and are often masked by other common health problems (e.g., enteroparasites). The pathobiology of the disease hampers the effectiveness of standard diagnostic assays (late production of antibody, sporadic shedding of the slow-growing organism, minimal gross pathology in subclinical and in some species clinical disease). Additional aggravating aspects of the infection include interference with TB testing and the unresolved question of Map's zoonotic potential.

How much effort should go towards Map infection control in the zoo industry? The level of attention that should be focused on any disease should match the risk it represents to the national collection. Disease risk is a function of health impact (morbidity/mortality), the balance between prevention vs. eradication (what does it take in time and money to keep it out vs. stamp it out?) and prevalence (how likely is it that you will buy the infection along with the next pair of bongos?). For Map infection in the zoo industry the effects are as follows.

 Health impact: Debilitating and eventually fatal.

 Prevention: Feasible.

 Eradication: Both expensive and difficult.

 Prevalence: Unknown.

A study is underway with the assistance of American Zoo and Aquarium Association (AZA) accredited facilities to assess the risk factors for introduction of this disturbing infection to captive artiodactyl species. Other goals are to establish a baseline prevalence of the infection against which to measure the progress of control efforts and to share current knowledge about Johne's disease in captive non-domestic hoofstock.

A short Johne's disease survey was mailed to all AZA accredited institutions with hoofstock species in their collection. A summary of responses from the133 respondents (90% response rate) appears below. Elements of particular pertinence are:

1.  Cases of infection: 42 facilities (32% of respondents) report having had at least one test-positive animal. (No data were collected on JD prevalence, risk factors, etc. for animals managed by private hoofstock dealers.)

2.  Surveillance: One-third of respondents never test for Map infection. Another third report that a diagnostic surveillance program is in place but it appears the majority of these programs test single animals pre or post shipment only. This means that effective surveillance for the infection does not occur at up to 66% of responding facilities.

3.  Potential exposure through transfers: Multi- and single species exhibits have been developed and expanded with animals from sources outside the reporting zoo within the last 5 yr according to a majority of respondents.

4.  Human-animal contact areas:These exhibits exist at 107 (80%) of responding institutions and deserve particular attention for two reasons. First, goats, sheep and cows are common to these exhibits. These species may be the most likely to have been exposed to Map given the prevalence of the infection and the patterns of husbandry in domestic agriculture. The most commonly listed test-positive species was the goat. Secondly, a link between Map and a human inflammatory bowel disease (Crohn's Disease) has been hypothesized. The hypothesis has been supported and contradicted in about equal measure; the true zoonotic nature of the organism likely will not be clarified for years. In the meantime, it is perhaps tactically injudicious not to know the JD status of animals handled by children at your facility.

Additional facets of the study are still underway. They include site visits to up to 20 zoos chosen to represent different types and sizes of collections, geographic locations and husbandry patterns. The Map infection status of these zoos range from never having seen a case to confirmed infection in one or more exhibits. Fecal culture (individually identified or randomly sampled) will be completed for these and other facilities to expand surveillance for the infection. Five years of pathology and clinical records will be reviewed both to compare surveillance protocols and to screen for any hint of an undetected case.

Given the preliminary Map infection prevalence findings of this study, facilities managing hoofstock face a real risk of currently harboring or introducing Map infection to their collections. Now is the best time to limit the spread of the infection to safeguard captive endangered and genetically valuable species. As with many issues, prevention is both less costly and more effective than attempts at eradication.

Table 1. American Zoo and Aquarium Association--CEF Johne's Disease (JD) Survey Results

Dr. Becky Manning (University of Wisconsin--Madison); Dr. Michael Ziccardi (Lincoln Park Zoo)
Institutions surveyed = 147; Institutions responding = 133 (90.4%).

Domestic and non-domestic ungulate husbandry

 Animal contact areas?

 Yes: 107 (80%)

 No: 26 (20%)

 Seasonal exhibits?

 Yes: 38 (29%)

 No: 93 (70%)

 Introductions?

 None: 10 (8%)

 1-20: 74 (56%)

 21-50: 35 (26%)

 > 50: 13 (10%)

 Births?

 None: 11 (8%)

 1-10: 74 (56%)

 11-20: 22 (17%)

 > 20: 24 (18%)

 Hand-rearing?

 Never: 25 (19%)

 Sometimes: 91 (68%)

 Frequently: 5 (4%)

 Always: 0

JD testing

 JD Testing of any kind?

 Yes: 92 (69%)

 No: 41 (31%)

 JD testing methods:

 Serum: ELISA: 44 (48%)

 Comp. Fixation: 13 (14%)

 AGID: 32 (35%)

 Feces:

 Fecal culture: 76 (83%)

 Direct acid-fast: 17 (18%)

 Direct IS900 probe: 14 (15%)

 Tissue:

 Necropsy: 48 (52%)

 Histopathology: 47 (51%)

 Immunohistochem: 3 (3%)

 Tissue culture: 18 (20%)

 Biopsy: 7 (8%)

 Other:

 Gamma interferon: 1 (1%)

 Skin test: 3 (3%)

Test-positive ungulate information

 JD Test-positive animals?

 Yes: 42 (32%)

 No: 90 (68%)

 Disposition of test-positive animals:

 Quarantined animal(s): 18 (43%)

 Tested adjacent enclosure(s): 8 (19%

 Retested, same method: 15 (36%)

 Tested all animals in enclosure: 16 (38%)

 Retested, different method: 18 (43%)

 Euthanatized animal(s)/slaughter: 22 (52%)

 No action taken: 1 (2%)

 Euthanatized ALL animals in enclosure: 6 (14%)

 Tested all hoofstock in collection: 8 (19%)

 Animal(s) died: 16 (38%)

Hoofstock with unconfirmed diagnoses

 Undiagnosed deaths? Yes: 27 (20%) No: 103 (77%)

 Undiagnosed results? Yes: 16 (12%) No: 114 (86%)

JD testing and surveillance

 JD surveillance program?

 No program: 70 (53%)

 Program in the next 12 mo: 13 (10%)

 Program in place: 47 (35%)

 Interested in JD Testing? Yes: 35 (26%)

 Interested but would need more info: 54 (41%) No: 7 (5%)

Johne's disease importance amongst other health issues:

 Primary: 4 (3%)

 High: 25 (19%)

 Moderate: 45 (34%)

 Slight: 44 (33%)

 None: 13 (10%)

Acknowledgments

Funds for this study were provided by American Zoo and Aquarium Association's Conservation Endowment Fund.