Abstract
A 2-yr-old female reindeer with a history of lethargy and dyspnea was diagnosed with multiple pulmonary abscesses radiographically. At necropsy the animal had severe diffuse granulomatous pneumonia and pleuritis with severe multifocal granulomatous myocarditis, lymphadenitis, nephritis, esophagitis, enteritis, and thyroiditis. Mycobacterium kansasii was cultured from pulmonary, renal, hepatic, and lymph node sections. Mycobacterium kansasii is a slow-growing non-tuberculous mycobacterial species that causes disease in severely immunocompromised individuals. The popularity of reindeer in children's zoos, petting zoos, and holiday exhibitions makes diagnosis of M. kansasii in a reindeer a significant public health concern.
Introduction
Mycobacterium kansasii was first characterized in 1953 at the University of Kansas. It is a slow-growing photochromogenic mycobacterium (Runyon group 1) and is the second most common non-tuberculous mycobacterial species isolated in AIDS patients, following mycobacterial species in the M. avium complex (MAC).3 The most common disease presentation in humans is chronic pulmonary infection with cavitation, resembling classic tuberculosis.9 There are infrequent reports of disseminated infections in severely immunocompromised individuals as well as focal dermal and arthritic lesions. Tap water is believed to be the major reservoir in human disease although it has been cultured from lakes, ponds, swimming pools, sewage, and sphagnum moss.3,4,9 Interestingly, there are few reports of M. kansasii in animals in the United States and Europe. This is the first report of disseminated M. kansasii infection in reindeer (Rangifer tarandus).
Case Description and Methods
A 2-yr-old female reindeer from the Binder Park Zoo was noted to be lethargic and dyspneic for approximately 2 mo. The reindeer did not respond to empiric antibiotic therapy. Thoracic radiographs revealed multiple pulmonary abscesses in both lungs. Corynebacterial pneumonia was suspected. Purulent green-white material from the left prescapular lymph node was submitted for bacteriology. Culture was unrewarding. The animal was euthanatized and submitted to the Diagnostic Center for Population and Animal Health (DCPAH) at Michigan State University for a complete necropsy.
At necropsy, the reindeer was extremely thin (approximately 175 pounds) and mildly dehydrated. There were multiple 0.5–3.0 cm3 firm subcutaneous nodules on the face and neck with central areas of caseous necrosis. One submandibular nodule was filled with clear mucinous material and contained multiple 0.2–0.5 cm3 granulomas. The left prescapular lymph node was enlarged and cross sections revealed purulent to caseous gritty material, suggestive of mineralization. There were dozens of tan to yellow 0.2–2.0 cm3 abscesses and mineralized caseogranulomas randomly distributed over the diaphragmatic and thoracic pleura, often arranged linearly, parallel to the ribs. Numerous 0.1–2.0 cm3 abscesses and caseogranulomas were scattered multifocally throughout all lobes of both lungs, in the thoracic, mesenteric and sublumbar lymph nodes, within the esophageal mucosa, the myocardium of both ventricles, the small intestinal submucosa, and both thyroid glands. Both kidneys had 0.2–4.0 cm3 caseogranulomas and multiple wedge-shaped infarcts.
Sections of tissue were collected in 10% buffered formalin and processed routinely for histopathology, and immunohistochemistry. Tissues were submitted to the Michigan Department of Community Health and the bacteriology section at the DCPAH for bacterial culture. Sections of lymph node were submitted to the virology section at the DCPAH to screen for bovine viral diarrhea virus.
Results and Discussion
An impression smear of necrotic material from the left prescapular lymph node revealed large numbers of acid fast positive staining organisms. Histologic examination of tissues revealed variably sized multifocal to coalescing granulomas with central caseation and mineralization in sections of both lungs, heart, liver, both kidneys, both thyroid glands, thoracic, mesenteric, and sublumbar lymph nodes, and within the submucosa of multiple sections of small intestine. Caseogranulomas had acid-fast bacilli with prominent banding within the central necrotic debris and within the cytoplasm of both epithelioid macrophages and multinucleate giant cells.
Immunohistochemical staining of tissue sections was positive for Mycobacteria sp. and negative for chronic wasting disease. Virus isolation tests on sections of lymph node for BVD virus were negative.
Both laboratories isolated M. kansasii from sections of lymph node, lung, kidney, and liver. Identification testing indicated a Mycobacteria sp. other than M. tuberculosis complex, based on genetic probe testing. Mycobacteria kansasii was subsequently confirmed based upon growth characteristics, colony morphology, photochromogenicity, biochemical profile, high pressure liquid chromatography and genetic probe testing.
Mycobacterium kansasii is a photochromogenic, slowly growing mycobacterium species that is most commonly isolated from water (tap water, ponds, lakes, swimming pools, aquariums, and sewage), but rarely from animals and soil. There are individual case reports of M. kansasii in a dog (Canis familiaris),8 a goat (Capra hircus),1 a llama (Llama glama),7 a rhesus monkey (Macca mulatta),6 and four squirrel monkeys (Saimiri sciureus sciureus).2 A survey of lymph nodes from cattle in the United States identified multiple strains of M. kansasii in the lymph nodes of clinically healthy animals.5 The primates and the goat were identified through routine tuberculosis testing. The dog was clinically ill with dyspnea and had a persistent pleural effusion. All reports documented histologic lesions consistent with mycobacteriosis.
This case of M. kansasii in a reindeer is of significant public health concern because reindeer are popular animals for exhibition in children's zoos, petting zoos, and holiday exhibitions. This young animal had disseminated granulomatous disease that was grossly and microscopically indistinguishable from M. bovis, a member of the M. tuberculosis complex. Definitive identification of mycobacterial species requires bacterial culture and PCR. This reindeer had been screened for Johne’s disease (M. avium ssp paratuberculosis) via a radiometric fecal culture several months prior to the development of clinical illness. Mycobacterium kansasii had been identified in fecal material and was not considered a primary pathogen at the time of identification. The information was filed and forgotten until the post-mortem diagnosis of mycobacteriosis, thereby perpetuating the potential transmission of M. kansasii to animal care staff and other animals in adjacent exhibits. Fortunately, there was no direct contact with zoo visitors.
The source of this mycobacterial infection in the reindeer was not identified. The reindeer had been housed with one other female reindeer from the time she was acquired as a calf. There is no record of direct contact with any other animals. The hoofstock at the zoo are housed in a large barn with a common air handling system. The most likely source of infection in this case is drinking water. Mycobacterium kansasii has been cultured from municipal water sources (tap water), lakes, ponds, swimming pools, sewage, and rarely, soil. There have been no reports of human-to-human,3 animal-to-animal, or animal-to-human transmission of M. kansasii.
Disseminated mycobacteriosis in animals and humans is typically associated with immunocompromised individuals. Human cases of M. kansasii have been reported in patients with AIDS, systemic lupus erythematosus, chronic pulmonary disease, and those undergoing immunosuppressive therapy.4,9 There are a few reported cases of focal dermal and arthritic infections in humans with a history of localized trauma.3 The majority of these people have a history of immunosuppressive disease or therapy. There are rare individual case reports of immunocompetent individuals with M. kansasii.3 The severity of this reindeer’s disseminated disease and the fact that she was shedding the organism in her feces prior to exhibiting clinical illness suggest immunosuppressive disease or compromised immune function. Virus isolation tests performed on sections of lymph node for BVD virus, which causes immunosuppression in ruminants, were negative. Other factors considered as possible stressors and thus causes of immune suppression included the stress of captivity and display, and the fact that this animal was behaviorally subordinate to the other reindeer it was housed with. There is little information about this reindeer prior to its arrival at the zoo. It is not known if the dam raised it and it received passive maternal immunity or if it was “hand raised” and fed milk replacer, which may have had a marked effect on its immune status as a calf.
No other animals housed at the zoo, including the other reindeer, have been diagnosed with mycobacteriosis prior to, or subsequent to this reindeer’s demise. Mycobacterium kansasii should be considered a primary pathogen in animals and should be added to the list of differential diagnoses for animals with nonspecific signs of illness. Animals infected with M. kansasii may pose significant zoonotic risk to zoo visitors and employees.
Acknowledgments
We wish to thank Dr. David Rost and Dr. Robert Emery for submission of this case.
Literature Cited
1. Acosta, B., F. Real, O. Ferrer, S. Deniz, and B. Poveda. 1998. Isolation of Mycobacterium kansasii from a tuberculin-positive goat. Vet. Rec. 142:195–196.
2. Brammer, D.W., C.M. O’Rourke, L.A. Heath, C.E. Chrisp, G.K. Peter, and G.L. Hofing. 1995. Mycobacterium kansasii infection in squirrel monkeys (Saimiri sciureus sciureus). J. Med. Primatol. 24:231–235.
3. Chaves, A., A. Torrelo, I.G. Mediero, M. Menendez-Rivas, A. Ortega-Calderon, and A. Zambrano. 2001. Primary cutaneous Mycobacterium kansasii infection in a child. Pediatr. Dermatol. 18:131.
4. Hsu, P.Y., Y.H. Yang, C.H. Hsiao, P.I. Lee, and B.L. Chiang. 2002. Mycobacterium kansasii infection presenting as cellulitis in a patient with systemic lupus erythematosis. J. Formos. Med. Assoc. 101: 581–584.
5. Jarnagin, J.L., E.M. Himes, W.D. Richards, D.W. Luchsinger, and R. Harrington. 1983. Isolation of Mycobacterium kansasii from lymph nodes of cattle in the United States. Am. J. Vet. Res. 44:1853–1855.
6. Jackson, R.K., R.A. Juras, S.M. Stiefel, and J.E. Hall. 1989. Mycobacterium kansasii in a rhesus monkey. Lab. Anim. Sci. 39:425–428.
7. Johnson, C.T., C.E. Winkler, E. Boughton, and J.W. Penford. 1993. Mycobacterium kansasii infection in a llama. Vet. Rec. 133:243-244.
8. Pressler, B.M., E.M. Hardie, C. Pitulle, R.M. Hopwood, S. Sontakke, and E.B. Breitschwerdt. 2002. Isolation and identification of Mycobacterium kansasii from pleural fluid of a dog with persistent pleural effusion. J. Am. Vet. Med. Assoc. 220:1336–1340.
9. Taillard, C., G. Greub, R. Weber, G.E. Pfyffer, T. Bodmer, S. Zimmerli, R. Frei, S. Bassetti, P. Rhoner, J. Pifferetti, E. Bernasconi, J. Bille, A. Telenti, and G. Prod’jhom. 2003. Clinical implications of Mycobacterium kansasii species heterogeneity: Swiss National Survey. J. Clin. Microbiol. 41:1240–1244.