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Case report — Gevalverslag

Tuberculosis in Kafue (Kobus leche kafuensis) and in a bushbuck ( scriptus) on a game ranch in Central Province, Zambia

U Ziegera*, G S Pandeyb, N P J Kriekc and A E Cauldwella

bacteriosis, 2 in Kafue lechwe and 1 in a ABSTRACT bushbuck from a private game ranch near Mycobacteriosis was diagnosed for the first time outside a national park in free-ranging Lusaka. The pathological and histological wild on a game ranch in Zambia. A Kafue lechwe (Kobus leche kafuensis) was found lesions were typical of tuberculosis in all 3 dead with tuberculous lesions on a ranch near Lusaka. Acid-fast bacilli were found in the cases; however, mycobacteria could only affected organs. Mycobacteria were isolated from these tissues. A bushbuck (Tragelaphus be isolated from 1 of the Kafue lechwe. scriptus) was found dead on the same ranch with multiple superficial abscesses in the neck Unfortunately, appropriate biochemical region, extensive granulomatous lesions in the lung, the bronchial and mediastinal lymph tests were not available at the time to nodes and several nodular lesions in the spleen. Few acid-fast bacilli were found in the exudate from the abscesses and lesions in the affected organs. Histologically the lesions confirm without doubt that the isolate resembled those of tuberculosis, but mycobacteria could not be isolated. In addition, 1 Kafue was M bovis. The strong suspicion, lechwe among 37 wild ungulates of 13 shot on the ranch showed typical tuberculous however, that bovine tuberculosis is lesions in the lungs, but the diagnosis was not confirmed by bacterial isolation. The role of present in wildlife on private Zambian the Kafue lechwe as maintenance host for tuberculosis as well as in the possible spread of ranches warrants attention. The danger of this disease to other wildlife are discussed. spreading tuberculosis through wildlife Key words: bushbuck (Tragelaphus scriptus), Kafue lechwe (Kobus leche kafuensis), mycobac- translocations is emphasised. teriosis, tuberculosis, wildlife, Zambia. MATERIALS AND METHODS Zieger U, Pandey G S, Kriek N P J, Cauldwell A E Tuberculosis in Kafue lechwe (Kobus leche kafuensis) and in a bushbuck (Tragelaphus scriptus) on a game ranch in Central Animals Province, Zambia. Journal of the South African Veterinary Association (1998) 69(3): 98–101 (En.). Centre for Wildlife Management, University of Pretoria, Pretoria, 0002 South Africa. All animals came from a private game ranch (15.05 S, 28.15 E) located in the Chisamba District in the Central Province of Zambia, approximately 20 km north of INTRODUCTION endemic in (Syncerus Lusaka. This ranch has operated commer- Tuberculosis, caused by Mycobacterium caffer) and in (Phacochoerus cially as a game ranch since 1990, when bovis, has been described in a variety of aethiopicus) populations in the Queen wildlife was first introduced. Eighteen captive and free-ranging wild animals. Elizabeth National Park in Uganda9,26,27. ungulate species are present at a stocking Among the latter, self-maintaining infec- High prevalence rates of M. bovis infec- rate of approximately 1 large stock unit tions have been reported in the European tions were found in wild olive baboons per 4.7 ha16. badger (Meles meles) in the United King- (Papio cynocephalus anubis) in the Masai A male Kafue lechwe was found freshly dom; in the brush-tailed possum (Tricho- Mara Game Reserve in Kenya20. Recently, dead on the ranch in November 1996. The surus vulpecula) in New Zealand and in an outbreak of tuberculosis in a free- carcass was transported immediately to farmed fallow ( dama) as well as ranging African buffalo population and the Disease Control Laboratory of the ( elaphus) in several other subsequent spread of this disease to other School of Veterinary Science, University countries3,4,6,23,25. The first cases of bovine species was reported from the Kruger of Zambia, for a post mortem examination. tuberculosis in free-ranging wild animals National Park, South Africa2,12,13. This had been dead for presum- in South Africa were reported in 1928 in In Zambia, tuberculosis caused by ably 5–6 hours when the necropsy was greater (Tragelaphus strepsiceros) and M. bovis in free-ranging wild animals has conducted. common (Sylvicapra grimmia)18. been reported only in a single eland A male bushbuck (Tragelaphus scriptus) were later found to be ( )15 and in Kafue lechwe was found dead on the same ranch in endemically infected with M. bovis in the (Kobus leche kafuensis)5,8,15. It was suggested September 1996. A necropsy was Eastern Cape region of South Africa24. that tuberculous that shared the performed immediately on site. It was Tuberculosis caused by M. bovis is grazing on the Kafue flood plains with estimated that the bushbuck had been lechwe introduced this disease to the dead for about 2–3 hours when the susceptible wildlife population8. necropsy was conducted. All organs that aCentre for Wildlife Management, University of Pretoria, In 1989 the legislation in Zambia contained lesions were cooled at 4 °C and Pretoria, 0002 South Africa. pertaining to wildlife was amended and transported to the same laboratory for bSchool of Veterinary Science, University of Zambia, many private game ranches have since diagnosis. Lusaka, Zambia. been established. Several ranches were In addition, 37 wild ungulates were shot cFaculty of Veterinary Science, University of Pretoria, stocked, amongst other species, with on the ranch between December 1995 Onderstepoort, 0110 South Africa. Kafue lechwe that had been captured on and November 1996 for venison, as *To whom correspondence should be addressed. the Kafue flood plains. This report trophies or because of injuries. These Received: February 1998. Accepted: June 1998. presents 3 cases of tuberculosis or myco- animals included 1 Burchell’s zebra

98 0038-2809 Tydskr.S.Afr.vet.Ver. (1998) 69(3): 98–101 (Equus burchellii), 2 (Potamocho- tissue was replaced by calcified, white enlarged and up to 120 mm in diameter. erus larvatus), 11 (Aepyceros melam- necrotic material that was hard and Most of them were firm and contained pus), 3 tsessebe ( lunatus gritty to cut. The testes revealed a few necrotic material while 1 contained a lunatus), 1 Lichtenstein’s (Sig- yellowish nodules on their surface. The yellowish-white exudate. The spleen moceros lichtensteinii), 2 eland, 2 bushbuck, urinary bladder was full of turbid urine. showed disseminated miliary lesions, 4 greater kudu, 2 sable (Hippotra- The visceral surface of the bladder many of which were calcified. gus niger), 6 defassa (Kobus showed a few whitish, pinhead-sized The impression smears made from ellipsiprymnus defassa), 1 Kafue lechwe, 1 nodules. exudate obtained from the abscesses (Kobus vardonii) and 1 Large numbers of acid-fast bacilli were revealed only few acid-fast bacteria. (Redunca arundinum). All carcasses were seen in the smears made from the kidneys Microscopically the lesions in the lungs, transported immediately after death to a and the urine sediment while few lymph nodes and the spleen were similar nearby abattoir. In addition to standard acid-fast bacteria were present in the in appearance. The lesions consisted of meat inspection procedures, the thoracic impression smears made from the lungs large masses of caseous necrotic material and visceral organs were examined more and the mediastinal lymph nodes. Micro- enveloped by an attenuated granuloma- thoroughly according to standard scopically the lesions were characterised tous inflammatory reaction. Scattered foci necropsy procedures. by large aggregates of epithelioid cells of calcification occurred in the necrotic and the lack of Langhan’s giant cells. Few tissue. The lesions were further charac- Gross and histopathology acid-fast bacilli were detected in the cyto- terised by the presence of numerous All observed abnormalities were plasm of epithelioid cells. The lesions neutrophils in the reaction. Few scattered, recorded while the necropsies were were typical of tuberculosis. With the acid-fast bacilli were seen in the cyto- performed. Specimens of selected organs exception of severe testicular atrophy, no plasm of Langhan’s giant cells and in the were preserved in 10 % formol saline. other lesions were seen in the testis. necrotic debris. These findings suggest a These were later routinely processed and Colonies of acid-fast bacteria were seen diagnosis of tuberculosis. stained with haematoxylin and eosin for after 5 weeks of incubation on the LJ No growth was obtained on LJ medium histological examination. Selected tissue media slants containing pyruvate inocu- during 10 weeks of incubation. sections as well as smears of exudates lated with material extracted from the were stained with the Ziehl-Neelsen stain kidneys, urine and lungs. The colonies Culled animals for the detection of acid-fast bacteria. were white and had a smooth surface. No Typical tuberculous lesions were found growth was observed on media either in 1 of the 37 animals that were shot. This Bacteriology with or without glycerine during 8 weeks was a 3-year-old Kafue lechwe, which was Specimens of affected organs were of incubation. The culture was found to culled because of a hind-leg injury collected and processed for bacterial be niacin-negative and sensitive to but appeared otherwise healthy. Several isolation and identification1. Petroff’s thiophene carboxylic acid hydrazide. firm nodules varying between 30 and modified concentration method was used The findings that these colonies 55 mm in diameter were found in the lung for the preparation of the inoculum. The appeared only after 5 weeks of incuba- tissue. On cut surface, these nodules had inoculum was smeared over the surface of tion, were not pigmented and smooth, caseous necrotic centres. Histologically each tube of Lowenstein-Jensen (LJ) egg grew only on pyruvate-enriched but not these lesions reflected multifocal, medium containing glycerine, LJ egg on glycerine-containing media, and were necrogranulomatous pneumonia charac- medium without glycerine and LJ egg TCH sensitive indicate that the isolate was terised by large central calcified cores of medium containing pyruvate. These most probably M. bovis. However, a final cellular debris surrounded by attenuated tubes were incubated aerobically at 37 °C differentiation from other members of the collars of granulomatous inflammatory and checked for growth of colonies of M. tuberculosis complex (M. tuberculosis, reaction. The lesions were well-encapsu- acid-fast bacteria after 2 weeks and then M. africanum and M. microti) was not lated and surrounded by areas of atelecta- every week for 8 weeks. The isolates were achieved as other biochemical tests sis. Histologically the lesions resembled further identified by testing their niacin (pyraziamide susceptibility, nitrate those of tuberculosis. However, the production and by their sensitivity to reduction, catalase production, tellurite diagnosis could not be confirmed as no thiophene carboxylic acid hydrazide. reduction) were not available at the acid-fast bacteria were detected on Ziehl- time. Neelsen-stained sections. RESULTS Bushbuck DISCUSSION Natural deaths The carcass was severely emaciated. Bovine tuberculosis has previously been Several large, superficial abscesses were reported from free-living Kafue lechwe in Kafue lechwe visible in the submandibular and retro- Zambia5,8,15. This is the 1st case of tubercu- The carcass was severely emaciated. All pharyngeal regions, along the neck and in losis suspected to be caused by M. bovis lobes of the right lung and the diaphrag- the prescapular region. The abscesses infection in a Kafue lechwe from a private matic lobe of the left lung were consoli- varied from approximately 60 to 150 mm game ranch in Zambia. Mycobacteriosis dated. The mediastinal lymph nodes were in diameter. Two abscesses discharged was also diagnosed in a free-ranging slightly enlarged but lacked gross patho- a yellowish-white exudate through bushbuck for the 1st time. Although the logical changes. There was mild enteritis cutaneous sinuses. On cut surface, all microbiological isolation failed in this and the mesenteric lymph nodes were abscesses contained a similar exudate. case, the typical pathological and histo- slightly enlarged. Both kidneys revealed Both lungs contained multiple firm logical lesions and the presence of acid- large, encapsulated, white, partially nodules varying from 5 to 70 mm in fast bacilli in these lesions are consistent calcified abscesses varying in diameter diameter. On cut surface, numerous with those of tuberculosis. from 20 to 60 mm with central necrosis. necrotic foci were evident in the nodules. The occurrence of tuberculosis in the Approximately 70 % of the normal kidney The thoracic lymph nodes were grossly Kafue lechwe does not come as a surprise.

0038-2809 Jl S.Afr.vet.Ass. (1998) 69(3): 98–101 99 Kafue lechwe are endemic to the Kafue susceptible wild animals during this time REFERENCES flats in Zambia and it has been well may have facilitated the spread of the 1. Baker F J 1997. Hand book of bacteriological known since 1972 that prevalence rates of disease via droplet infection and the bush- techniques (2nd edn). Butterworth, London M. bovis infections in this population are buck could thus have been infected. 2. Bengis R G, Kriek N P J, Keet D F, Raath J P, De Vos V, Huchzermeyer H F A K 1996 high. Prevalence rates of 36.0 %, 33.0 % Tubercle bacilli can also be shed via urine, An outbreak of bovine tuberculosis in a and 43.4 %, respectively, were found in 3 faeces, vaginal secretions, semen or free-living African buffalo (Syncerus caffer- extensive surveys that were conducted discharging abscesses and thus contami- Sparrman) population in the Kruger here5,8,15. Free-living lechwe have been nate soil, water and plants14,19. The National Park: a preliminary report. Onder- captured on the Kafue flats and translo- survival time and infectivity of these stepoort Journal of Veterinary Research 63: 15– 18 cated to private game ranches within organisms in the environment have 3. Bülske G, Englund L, Wahlström H, De Zambia since late 1989 without having recently been reviewed in detail by Lisle G W, Collins D M, Croston P S 1995 been tested for tuberculosis. Morris et al.17. The practical significance of Bovine tuberculosis in Swedish deer farms: It is likely that lechwe now serve as persistence of tubercle bacilli in the epidemiological investigations and tracing constant sources of infection for other environment as a source of infection using restriction fragment analysis. Veteri- nary Record 136: 414–417 animals on private ranches. The reported appears to be small. However, the bacilli 4. Cheeseman C L, Wilesmith J W, Stuart F A, high prevalence rates in Kafue lechwe can remain infective for several days Mallison P J 1988 Dynamics of tuberculosis indicate that the infection can be self- depending on climatic conditions and this in a naturally infected badger population. maintaining in these populations. M. bovis may contribute to the spread of the Revue 18: 61–72 has an exceptionally wide host range and disease through oral and/or percutaneous 5. Clancey J K 1977 The incidence of tubercu- losis in lechwe (marsh antelope). Tubercle the presence of 1 maintenance host in an infection of new hosts. Percutaneous 58: 151–156 ecosystem is sufficient to spread bovine infection as a result of scratching the ears 6. 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Gallagher J, Macadam I, Sayer J, Van Lavieren L P 1972 Pulmonary tuberculosis Kruger National Park, South Africa, have will consequently be slow and the bush- in free-living lechwe antelope in Zambia. been incriminated as the source of bovine buck can thus be considered a spill-over Tropical Animal Health and Production 4: 204– tuberculosis, spreading the disease to host. However, with 1 maintenance host 213 other hosts such as lion (Panthera leo), being present, it is possible that tubercu- 9. Guilbride P D L, Rollinson D H L, McAnulty cheetah (Acinonyx jubatus) and chacma losis could manifest itself also in gregari- E G, Alley J G, Wells J G 1963 Tuberculosis 13 in free living African (Cape) buffalo baboon (Papio ursinus) . The bushbuck ous animals other than Kafue lechwe. It (Syncerus caffer Sparrman). Journal of reported here must have contracted appears that this has not yet occurred on Comparative Pathology and Therapeutics 73: tuberculosis on the game ranch. This the game ranch investigated, as none of 337–348 animal was only 3 years old and no the other animals examined showed 10. Grange J M, Collins C H 1987 Bovine tuber- animals had been introduced after 1991. It tuberculous lesions. cle bacilli and disease in animals and man. Epidemiology and Infection 92: 221–234 is likely that the bushbuck contracted the Further tests are still required to confirm 11. Huchzermeyer H F A K, Brückner G K, Van disease from the lechwe population. the presence of M. bovis. The suspicion Heerden A, Kleeberg H H, Van Rensburg The mode of transmission of M. bovis that bovine tuberculosis is present in wild- I B J, Koen P, Loveday R K 1994 Tuberculo- among wildlife remains speculative. life on private Zambian game ranches sis. In Coetzer J A W, Thomson G R, Tustin Possible routes of infection are respira- should be followed up, as tuberculosis is R C (eds) Infectious diseases of livestock with special reference to southern Africa, Vol. 2. tory, alimentary, congenital, cutaneous considered a serious health hazard. Some Oxford University Press, Cape Town: 1425– 11 and venereal . In cattle, infection is of the wild ungulates kept on Zambian 1444 acquired almost exclusively aerogenously ranches, such as Lichtenstein’s harte- 12. Keet D F, Kriek N P J, Huchzermeyer H, by the inhalation of infected droplets from beest, ( equinus) Bengis R G 1994 Advanced tuberculosis in an animal with open pulmonary tubercu- and , are sought after as an African buffalo (Syncerus caffer, Sparrman). Journal of the South African losis or from infected dust particles. breeding animals for other ranches within Veterinary Association 65: 79–83 Usually close contact between infected the country and for export. Veterinary 13. Keet D F, Kriek N P J, Penrith M-L, Michel and non-infected animals is required7. control measures must be considered and A, Huchzermeyer H 1996 Tuberculosis in However, tuberculosis has been found in implemented urgently before bovine buffaloes (Syncerus caffer) in the Kruger extensively farmed cattle in southern tuberculosis becomes widely established National Park: spread of the disease to other species. Onderstepoort Journal of Veterinary Africa and Australia, possibly owing to on game ranches and poses a threat to the Research 63: 239–244 their habit of congregating in large country’s wildlife industry. 14. Kleeberg H H 1961 The tuberculin test in numbers at watering points under dusty cattle. Journal of the South African Veterinary conditions11. Kafue lechwe are gregarious ACKNOWLEDGEMENTS Medical Association 32: 482–486 15. Krauss H, Roetcher D, Weiss R, Danner K, ungulates that utilise a semi-aquatic We are grateful to Mr and Mrs 21 Hübschle O J B 1984 Wildtiere als Infektion- habitat throughout the year . On the M O’Donnell who provided us with squelle für Nutztiere: Untersuchungen in game ranch under investigation they accommodation on their game ranch and Zambia. Beiträge der Klinischen Veterinär- occupy a small area around 1 of the few permitted us to undertake this study. medizin zur Verbesserung der tierischen permanent water sources. Large numbers We thank Mr C Harvey for permission to Erzeugung in den Tropen, Vol. 10. Justus- Liebig Universität, Giessen of wildlife congregate here, particularly use his abattoir facilities and Mr W Ulaya 16. Meissner H H 1982 Theory and application during the dry season. The close contact and Mr H Chimana for technical assis- of a method to calculate forage intake of between the Kafue lechwe and other tance. wild southern African ungulates for

100 0038-2809 Tydskr.S.Afr.vet.Ver. (1998) 69(3): 98–101 purposes of estimating carrying capacity. 20. Sapolsky R M, Else J G 1987 Bovine tubercu- African Veterinary Medical Association 11: 3– South African Journal of Wildlife Research 12: losis in a wild baboon population: 10 41–47 epidemiological aspects. Journal of Medical 25. Towar D T, Scott R M, Goyings L S 1965 17. Morris R S, Pfeiffer D U, Jackson R 1994 The Primatology 16: 229–235 Tuberculosis in a captive deer herd. Ameri- epidemiology of Mycobacterium bovis infec- 21. Sheppe W, Osborne T 1971 Patterns of use can Journal of Veterinary Research 26: 339–346 tions. Veterinary Microbiology 40: 153–177 of a floodplain by Zambian . 26. Woodford M H 1982a Tuberculosis in wild- 18. Paine R, Martinaglia G 1928 Tuberculosis in Ecological Monographs 41: 179–205 life in the Ruwenzori National Park, wild buck living under natural conditions. 22. Skinner J D, Smithers R H N 1990 The Uganda. I. Tropical Animal Health and Pro- Journal of the South African Veterinary Medical mammals of the southern African subregion. duction 14: 81–88 Association 1: 87 University of Pretoria, Pretoria 27. Woodford M H 1982b Tuberculosis in wild- 19. Robinson R C, Phillips P H, Stevens G, 23. Stuart F A, Manser P A, McIntosh F G 1988 life in the Ruwenzori National Park, Storm P A 1989 An outbreak of Mycobac- Tuberculosis in imported red deer (Cervus Uganda. II. Tropical Animal Health and terium bovis infection in fallow deer (Dama elaphus). The Veterinary Record 122: 508–511 Production 14: 155–160 dama). Australian Veterinary Journal 66: 195– 24. Thorburn J A, Thomas A D 1940 Tuberculo- 197 sis in the Cape kudu. Journal of the South

Book review — Boekresensie Genetic resistance to animal diseases

M Müller and G Brem (coordinators)

1998. Office International des Épizooties, Revue Scientifique et Technique 17 (1), 392 pp., soft cover. Price: FrF 270, US$ 45 (including airmail postage). ISBN 92 9044 466 5.

This special issue of the Scientific and Technical Review of the OIE regions of the world because financial, logistical and political (Office International des Épizooties – the world organisation for realities are making the conventional control of animal diseases animal health) provides a compendium of 27 papers on a subject in Africa increasingly difficult and sometimes impossible to im- of growing importance for the worldwide future of livestock plement. Genetic resistance to disease may help to ameliorate health and production, more especially in Africa. Its major ap- these constraints in some circumstances. peal will lie primarily in the rare quality of many of the papers From a personal perspective the chapters on the biological and the balance it strikes in presenting the scientific basis of principles of heredity and resistance to disease (Horin) and disease resistance and the methods – from conventional breed- genomic approaches to the improvement of disease resistance in ing to gene transfer – that can be employed to achieve it. A minor farm animals (Soller and Andersson) were particularly useful. It deficiency is the lack, as far as one can judge, of a single African could be argued from the same perspective that there are too among the 59 contributors and the passing lip-service it pays to many papers dealing with conventional immunological topics mammalian diversity in Africa. That diversity contains much of such as non-specific immunity, immunoglobulin diversity, T-cell the genetic potential for addressing a whole range of infectious receptors, cytokines and major histocompatibility complexes be- disease problems in Africa and elsewhere. cause this information is available from other sources. On the Genetic resistance to animal disease, i.e. the heritable diversity other hand, there has been a clear effort in the selection of these in the susceptibility of species, breeds and individuals, has been papers to concentrate on farm animals rather than using mouse recognised for a long time, but has only been fitfully exploited. and human models or examples that one finds regularly in texts Perhaps the best local examples were the pioneering observa- purporting to address animal diseases. These chapters are there- tions of J.C. Bonsma on differences between breeds of cattle to fore likely to be a ready source of summarised information for tick infestation and heartwater and the subsequent develop- non-specialists. ment of the Bonsmara breed. Genetic variability in the resistance The papers are divided into 9 groups, viz. mechanisms of of poultry breeds to Marek’s disease and avian leukosis has also defence against infectious diseases; genetic resistance to para- long been appreciated. A more recent example from Australia, sites; bacteria; viruses; prions; conventional breeding pro- described in this volume, is aimed at the problems of gastroin- grammes; marker-assisted selection and identification of disease testinal nematode infestations, flystrike (cutaneous myiasis) and traits; study of genetic resistance by targeted disruption of gene footrot in Merino sheep (Raadsma, Gray and Woolaston). Other function; and genetic resistance through gene transfer. Some than these, however, practical success stories, as opposed to groups, however, contain only one paper. The papers have interesting scientific phenomena, are hard to find. obviously been carefully edited because few editorial errors were Therein lies this volume’s probable value, i.e. in successfully encountered and the papers themselves are clear and easy to making the major issues with respect to disease resistance avail- read. able to a wide audience concerned with the control of animal For anyone interested in disease resistance in farm animals this disease. It adequately demonstrates the paucity of progress volume contains a fund of useful and interesting information as made because of the complexity of the subject but, at the same well as valuable references. time, points out the future potential. The realisation of this G R Thomson potential is arguably more important for Africa than it is for other ARC - Onderstepoort Institute for Exotic Diseases

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