Journal oj Wfldlffe /Jf.Jcasrs. 22(3).1986. pp 425-429 0 Wildlife Disease Assxiation 19%

Tuberculous Osteomyelitis Caused by Mycobacterium infracellulare in the Brush-tailed Bettong

Kenneth C. Richardson and Richard A. Read, School of Veterinary Studies, Murdoch University, Murdoch, West- em Australia 6150. Australia

The brush-tailed bettong (Bettongia joint. There were several soft circular penicillata) is a rare and endangered swellings each of about 8 mm in diameter species of small kangaroo found in a few over the immediate area of the hock joint. isolated areas of southwestern Australia Two of these swellings were lanced, pu- and Queensland (Christensen, 1983, Com- rulent material was expressed and the plete Book of Australian Mammals, Angus cavity swabbed for bacteriologic culture and Robertson, Sydney, Australia, pp. 184- and its sensitivity tested. Staphylococcus 185).These animals weigh about 1 kg and aureus was cultured and the bettong was are unusual in that their natural diet is then treated for 10 days with procaine thought to be principally the fruiting bod- penicillin G. The swelling only subsided ies of fungi supplemented with tubers, slightly so a second 2-wk course of peni- seeds and insects (Christensen, 1983, For- cillin was implemented. ests Dept. West. Aust. Bull. 91: 1-90). Two mo later there was a similar swell- There has been some breeding success ing in the middle of the tail. Radiographs when these animals were maintained in were taken of the left hock joint and the small enclosures. Occasionally captive tail and these revealed osteolysis with bettongs and other small marsupials (i.e., multiple circular radiolucent areas pres- bandicoots Perameles spp.) developed ent (Fig. 2). There was destruction of the swollen hock joints that resulted in chron- articular surfaces of the hock joints and ic lameness. This paper documents a case one of the intervertebral joints of the tail. of chronic lameness in the hock joints of Culture of the hock joint revealed Proteus a bettong; the tail and the digits of the mirabilis and Staphylococcus epidermi- forelimb were also involved. dis. There was no response to a course of Four bettongs were kept for 3 yr in a treatment with streptomycin. Hematolog- totally enclosed outside pen which had a ic findings at this stage were normal apart concrete pad 3 x 4 m at one end adjoin- from a moderate mature neutrophilia. ing a run of 6 x 4 m with a deep sand After a further 2 mo, similar lesions had floor. Food and water were provided on developed in the right hock joint and the the concrete pad. One bettong developed phalanges of both forefeet. Because of the a firm swelling of the left hock joint (Fig. severe destructive nature of these lesions 1). This was treated by intramuscular in- as seen on radiography, the bettong was jection of a benzathine penicillin/pro- euthanized. Whole body radiography re- caine penicillin suspension over a 10-day vealed that the bony lesions were confined period and the swelling diminished. to the hock joints, tail and forefeet. Eight wk later the swelling recurred and On postmortem examination, the car- resulted in lameness. The swelling was firm cass was in good condition. The patho- for 2-3 cm both above and below the hock logic findings were restricted to the areas surrounding the lesions. In these areas the bone was extensively eroded and replaced Received for publication 21 August 1985. with a mixture of fibrous tissue and thick,

425 426 JOURNAL OF WILDLIFE DISEASES, VOL 22, NO 3, JULY 1986

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FIGURE 1. An adult brush-tailed bettong with multiple swellings around the hock joint white purulent exudate (Fig. 3). In several as above. Direct aerobic and anaerobic areas the lesion extended through all lay- cultures were negative. Staphylococcus ers of the surrounding soft tissue, with oc- epidermidis was identified from two sam- casional ulceration through the skin. In the ples which were enriched in cooked meat left hock joint, the infection had tracked medium. Cultures for fungi and myco- up the sheath of the gastrocnemius tendon plasmata were negative. An acid-fast ba- and a purulent exudate was found at the cillus was cultured after 3 wk on myco- musculotendinous junction. The lymph bacterial media (B83 and a GE6) and nodes that drained all the affected areas identified as Mycobacterium intracellu- appeared normal. lare. Ba c t e r i ol og i c specimens were taken Microscopic sections of the hock joints, from the depths of the lesions in both hock tail and forefoot revealed extensive osteol- joints and from the lesion in the gastrocne- ysis surrounded by an intense pyogranu- mius muscle. Blocks of bone from both lomatous reaction (Fig. 4). hock joints, the tail and a forefoot were There were areas of caseation sur- fixed in formalin and then decalcified in rounded by a dense reactive zone of mac- formic acid. Sections were prepared by rophages and a mixture of neutrophils, routine histologic methods and stained lymphocytes and plasma cells. Large with hematoxylin and eosin and by the numbers of acid-fast bacilli were demon- modified Ziehl-Neelsen technique. Addi- strated in these areas when stained with tional sections from the left gastrocnemius the Ziehl-Neelsen technique. In both hock muscle were fixed, processed and stained joints the articular surfaces and subchon- RESEARCH NOTES/CASE REPORTS 427

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FIGURE2. A lateral radiograph of the tail of a brush-tailed bettong showing extensive bone destruction and remodelling of three coccygeal vertebrae.

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FIGURE3. A longitudinal section of the same region of the tail of a brush-tailed bettong as in Figure 2. In addition to the generalized swelling, there is an admixture of fibrous tissue and caseous material as well as the absence of recognizable bone. 428 JOURNAL OF WILDLIFE DISEASES, VOL 22. NO 3. JULY 1986

FIGURE4. Remnants of necrotic bone surrounded by caseation and a dense zone of macrophages in the affected tail of a brush-tailed bettong. H & E. ~90. dral bone were severely eroded; it was dif- fection in two quokkas (Setonix brachy- ficult to determine where the joint spaces urus) resulted in encapsulated granu- had been. Small fragments of necrotic lomatous lesions in the thorax of one bone were still present in some areas, but animal and similar lesions in the mesen- there was no evidence of osteogenesis, even teries of the other (Kakulas, 1964, Aust. J. at the periphery of the lesions. Sections of Sci. 27: 115-116). the gastrocnemius muscle also revealed In the brush-tailed possum (Trichosu- extensive caseation surrounded by a sim- rus vulpecula) Mycobacterium bovis was ilar pyogranulomatous reaction contain- a common causal agent of visceral tuber- ing acid-fast bacilli. culosis in wild animals in New Zealand Naturally occurring tuberculosis prin- (Ekdahl et al., 1970, N.Z. Vet. J. 18: 44- cipally affecting the viscera was reported 45), but was virtually absent in Australian in the rat kangaroo (Aepyprymnus rufes- populations (Corner and Presidente, 1980, cens) (Lucas, 1925, J. Pathol. Bacteriol. Vet. Microbiol. 5: 309-321). 28: 123-124). Barker et al. (1963, Vet. Bull. Mycobacterium intracellulare has been 33: 539-544) reviewed the Occurrence of found rarely in marsupials. Moore et al. a number of diseases in marsupials. They (1961, J. Infect. Dis. 123: 569-578) re- reported that Mycobacterium avium was ported that it caused a proliferative pneu- the cause of most tuberculous lesions in monitis and caseous lesions of the mesen- kangaroos. An atypical mycobacterial in- teric lymph nodes, spleen and liver of the RESEARCH NOTESCASE REPORTS 429

opossum, Didelphis mursupiulis virginiu- joints of rabbits when inoculated intrave- nu. nously (Armstrong et al., 1967, Am. Rev. Mycobacterial infection in marsupials Respir. Dis. 95: 20-32). These lesions are principally affecting the musculoskeletal characterized by granuloma formation and system has not been reported previously. osteolysis as well as necrotizing tendinitis The osseous lesions were typical of tuber- and bursitis. The lesions in this bettong culous osteomyelitis (skeletal tuberculoses) were all located in weight-bearing areas in man and other species (Murray and Ja- and hence were possibly sites subject to cobson, 1977, The Radiology of Skeletal superficial abrasion, particularly on the Disorders, Churchill Livingstone, New concrete pad at one end of the run. It is York, 2,033 pp.). The infection usually be- postulated that the organism gained entry gins in cancellous bone and in man, ver- via this route. This hypothesis is supported tebral lesions are the most common. The by the finding that animals kept in natu- lesions are destructive with occasional se- rally grassed enclosures at a number of questrum formation. Involvement of ma- zoos have not developed lesions of this na- jor joints is also common in man, with ture, nor have they been found in wild- gradual destruction of articular surfaces caught animals. However, it is also possi- and invasion of adjacent bone (Murray and ble that the multiple lesions resulted from Jacobson, 1977, op. cit.). The formation of hematogenous spread from a primary fo- caseous abscesses frequently leads to ne- cus. Although no such primary lesion was crosis of the overlying skin and secondary found on postmortem examination, the infection. This occurred in the present case original lesion in the left hock joint may since Proteus mirabilis and Staphylococ- have been the primary source for hema- cus epidermidis were isolated from cul- togenous spread to other sites. tures of the affected areas. In man, as the The current environmental conditions infection subsides, reactive sclerosis de- in Perth may favor the proliferation and velops, but in the bettong the lesions were spread of mycobacterial infections of an- progressing actively and there was no ra- imals. Over the recent 12 mo four cases diographic evidence of a reactive sclerotic (two cats and two dogs) of panniculitis zone. There was also no histologic evi- caused by Mycobacterium smegmatis dence of new bone formation around the have been confirmed in the Murdoch Uni- periphery of the lesions. Absence of re- versity Veterinary Hospital. It is possible generative osteophyte formation is typical that many more cases of mycobacterial in- of skeletal tuberculosis in animals, as is the fection causing chronic lamenesses in spread of the infection into surrounding marsupials may have escaped diagnosis soft tissues as seen in this case (Jubb et al., due to failure to use specific mycobacte- 1985, Pathology of Domestic Animals, 3rd rial culture techniques. Ed., Vol. 1, Academic Press, Inc., New Financial support for this research was York, 574 pp.). provided by the E. A. Weston and I. E. Skeletal tuberculosis in man is believed Fernie Research Fund and by a Special to be caused by hematogenous spread from Research Grant from Murdoch Universi- a primary focus (Murray and Jacobson, ty. We appreciate the assistance of John 1977, op. cit.). Some strains of M. intra- Atherton, Geoff Griffiths and Judy Rob- cellulare cause abscesses in and around the ertson.