Abstract

In May 2000, Francisella tularensis was isolated from tissues collected during the necropsy of a golden lion tamarin (Leontopithecus rosalia) that had died at the Phoenix Zoo. This was the sixth acute death in the tamarin collection within 2 months. Six of the zoo’s 15 tamarins died. Mortalities occurred in four different species: golden-headed tamarin (Leontopithecus chrysomelas), golden lion tamarin (L. rosalia), red-handed tamarin (Saguinus midas), and cotton-top tamarin (S. oedipus). A Goeldi’s marmoset (Callimico goeldii) died with similar clinical symptoms during this time frame and was later confirmed to have had tularemia. The most prominent clinical symptoms were severe depression, painful abdomen, generalized hypoglycemic symptoms, hyperthermia (depending on stage of progression) and peracute death. The primary differential for this presentation was scorpion stings, which are fairly common in the southwest United States. After the final diagnosis was confirmed, two additional tamarins were successfully treated for tularemia with the aminoglycoside, amikacin (4.5–6.8 mg/kg BID to TID either IM or IV). Review of medical records and preserved tissues identified an additional fatal case of tularemia in a siamang (Hylobates syndactylus) in January 2000. The histopathology, fairly consistent in all the deceased specimens, revealed a necrosuppurative enteritis, hepatitis and splenitis.

Tularemia or “rabbit fever” is a bacterial zoonosis caused by Francisella tularensis.^1-4 The disease is endemic in northern Arizona, but it is not known to be enzootic in wildlife or insects in central or southern Arizona at elevations below 4000 feet. Francisella tularensis had not previously been documented in this zoologic collection. Due to the zoonotic disease potential to guest and staff members and the health threat to the collection animals, preventive measures were immediately initiated. Zoo and public health officials at the state, county and federal (Centers for Disease Control and Prevention) levels conducted a joint epidemiologic investigation.

Surveillance for human illness consisted of a health status questionnaire filled out by every zoo employee, serologic testing of employees who were exposed to the ill animals, and a letter to local physicians. Active case surveillance among zoo animals involved serologic testing of carnivores, petting zoo animals, non-human primates, and other animals housed adjacent to the affected animals. Local veterinary practitioners were requested to provide samples from their patients to survey the pet population for comparative purposes. The zoo’s veterinary records and necropsy reports were reviewed for other undiagnosed cases. Wild rodents, rabbits, insects, and water samples from the zoo grounds were collected and tested. Caging was examined for evidence of rodents, collecting samples for testing and to determine methods of minimizing further risk. Zookeeper interviews were conducted to accurately assess human risk and discuss behavioral traits of the animals that might help determine the mode of transmission.

Francisella tularensis type B was confirmed by the Centers for Disease Control and Prevention in the six tamarins and one marmoset. Four percent (6/145) of the rodents and rabbits, specifically rock squirrels (Spermophilus variegates), cotton rats (Sigmodon arizonae), round-tail ground squirrels (Spermophilus tereticaudus), and cottontail rabbits (Sylvilagus audubonii), were infected with tularemia. Tests were negative on limited samples of mosquitos, triatomes and water. No ticks were found in the area. None of the zoo employees, visitors, or other collection animals developed illness; however, two exhibit coyotes, a feral cat, and eight livestock animals from the petting zoo had significant serologic titers. Pathology reports and histories implicated ingestion of infected rodents as the most likely mode of transmission for the fatal non-human primate cases.

The potential for persistence of F. tularensis type B in the rodent/rabbit population in this area is unknown. A longitudinal ecologic study involving monthly trapping and testing of rodents/rabbits is ongoing. There have been no other positive wild animals since the initial testing. The original source of the tularemia also remains unknown.

Acknowledgments

The Phoenix Zoo—Linda Cava, Paula Swanson, RVT, and Lisa Elliot, RVT
University of Arizona Veterinary Diagnostic Laboratory—Dr. Greg Bradley
Arizona Department of Health Services

1.  Epidemiology: Dave Engelthaler and Craig Levy

2.  Laboratory: Jed Clinch and Blaine Matheson

3.  Centers for Disease Control: Drs. May Chu and Sherif Zaki

4.  Maricopa County Health Department: Steven Kearing

Literature Cited

1.  Calle, P., et al. 1993. Nonhuman primate tularemia epizootic in a zoologic park. J. Zoo Wildl. Med. 24(4): 459–468.

2.  Clark, J.D. and E.D. Olfert. 1986. Rodents (Rodentia). In: Fowler, M. (ed.). Zoo and Wild Animal Medicine, 2nd ed. W.B. Saunders Co., Philadelphia, PA. Pp. 65, 740–741.

3.  Nayar, G.P., et al. 1979. Tularemia in a group of nonhuman primates. J. Am. Vet. Med. Assoc. 175(9): 962–963.

4.  Quan, T.J. 1993. Plague and tularemia in rodent populations. In: Fowler, M. (ed.). Zoo and Wild Animal Medicine: Current Therapy 3. W.B. Saunders Co., Philadelphia, PA. Pp. 54–56.

5.  Preiksaitis, J.K., et al. 1979. Human tularemia at an urban zoo. Calif. Med. Assoc. J. 121: 1097–1099.