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TB in llamas caused by Mycobacterium bovis
  1. D. F. Twomey1,
  2. T. R. Crawshaw1,
  3. J. E. Anscombe1,
  4. L. Farrant2,
  5. L. J. Evans2,
  6. W. S. McElligott3,
  7. R. J. Higgins4,
  8. G. Dean5,
  9. M. Vordermeier5,
  10. K. Jahans5 and
  11. R. de la Rua-Domenech6
  1. 1 Veterinary Laboratories Agency (VLA) — Starcross, Staplake Mount, Starcross, Exeter EX6 8PE
  2. 2 SVS, Clyst House, Winslade Park, Clyst St Mary, Exeter EX5 1DY
  3. 3 St Boniface Veterinary Clinic, 47 Mill Street, Crediton, Devon EX17 3AA
  4. 4 VLA — Lasswade, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ
  5. 5 VLA — Weybridge, New Haw, Addlestone, Surrey KT15 3NB
  6. 6 Tuberculosis Division, DEFRA, 1A Page Street, London SW1P 4PQ

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SIR, — We would like to report the diagnosis of tuberculosis (tb) associated with Mycobacterium bovis (the bovine tubercle bacillus) infection in llamas from a commercial herd in Devon.

The herd was established in Devon eight years ago with animals reared outside the county. At the time of disclosure of infection, it comprised 84 adult llamas and their crias. They graze outdoors all year round with occasional supplementary hay fed on the ground, and are only handled for routine vaccinations and worming. Water is provided in troughs, but the llamas also drink from a stream. The only other domestic animals on the premises are a dog, a cat and two donkeys, which all appear healthy. The only contiguous cattle herd has had repeated tb breakdowns since 2000. Direct nose-to-nose contact is not possible between the llama and cattle herds along the common boundary. There are many other tb breakdowns in cattle herds in the locality (19 confirmed cases within a 5 km radius since 2001). Three active badger setts are located on the farm and one in immediately adjacent woodland. Wild deer have not been seen on the farm, although the area does have a reasonable population of roe deer. There are regular llama movements on and off the holding. For example, females from other premises visit for mating, and approximately 30 crias are sold, mainly as pets, each year.

In February 2006, an adult female on the holding was euthanased on welfare grounds following chronic weight loss with terminal dyspnoea. At postmortem examination, multifocal caseous lesions were identified in the lungs, pericardium, and bronchial and mediastinal lymph nodes. Acid-fast bacteria morphologically similar to Mycobacterium species were identified on Ziehl-Neelsen-stained smears of these tissues, and M bovis was subsequently isolated.

At the beginning of May 2006, soon after the isolation of M bovis from this initial case, the State Veterinary Service (svs) in Exeter placed the herd under movement restrictions using powers in Article 17 of the Tuberculosis (England) Order 2006. They also reported the incident to the local consultant in communicable disease control in light of the zoonotic risk. Although there are no statutory requirements to register and identify South American camelids, or powers to test them for tb, the owner agreed to have the remainder of the herd tested. A programme of repeated intradermal herd tests at 90-day intervals was instigated using bovine and avian tuberculins injected in each axillary site. The first two tests, in June and September, yielded negative results by the interpretation used.

Despite the negative herd test results, similar clinical signs to the initial case were seen in another adult female in August, which eventually required euthanasia. Again, tb was suspected at postmortem examination (Fig 1) and M bovis was subsequently isolated. In light of this second clinical case and the previous negative herd test result in June, it was decided to blood sample other llamas in the herd to screen for antibodies to M bovis using a novel, non-validated in vitro lateral-flow assay, the Vettb stat-pak or ‘Rapid’ test (Waters and others 2006). On the basis of either a positive serology result or being considered as dangerous contacts to the previous confirmed cases, 19 more adult llamas and two crias were culled and examined postmortem between August and November. tb associated with M bovis infection was confirmed in four of the adults. Two other adults and a cria also died over this period and on gross postmortem examination showed lesions typical of tb. Specific mycobacterial cultures are still in progress from these three animals.

FIG 1

Severe pulmonary necrosis associated with tuberculosis in an adult llama

A third comparative intradermal tuberculin herd test was carried out in two stages at the end of December 2006 and beginning of January 2007. Blood samples were taken for serological testing both on the day of tuberculin injection and approximately three weeks later. Three tuberculin reactors and at least four seropositive llamas, one of which was a tuberculin reactor, have been identified. The results of postmortem and bacteriological examinations on all these llamas were not available at the time of writing, although one of the seropositive llamas, which had to be euthanased in extremis shortly after testing, presented with gross lesions of advanced tb.

It is intended to continue the tuberculin testing programme of this herd until two successive herd tests with negative results are obtained. This regimen will be supplemented with serological testing as required. Tracings have so far been completed on 14 of the approximately 30 llamas that left the farm in the 12 months before the identification of the first clinical case. None of those animals showed positive reactions to the intradermal tuberculin tests.

The six M bovis isolates to date have been confirmed as spoligotype SB0274 (vla type 11). This is the spoligotype most commonly isolated from tuberculous cattle and road traffic accident survey badgers in the same part of Devon. There is no record of M bovis isolates from deer in this area. In all histologically confirmed cases to date, tubercular lesions were characterised by granulomata with caseous necrosis, mineralisation, acid-fast bacteria, and variable fibrous encapsulation. Langhans' giant cells were not a prominent feature.

This incident illustrates the susceptibility of llamas to M bovis infection and highlights the difficulty of making an accurate antemortem diagnosis using the tests currently available for this species. Unlike bovids, cervids, primates and humans, no in vitro assay is commercially available for measuring the production of interferon-γ in camelids. We would like to reiterate the advice of Barlow and others (1999) that tb should be considered in the differential diagnosis of illthrift in llamas, with or without obvious respiratory involvement, particularly where the animals have been raised in areas of endemic tb in cattle and indigenous wildlife. We would ask veterinary surgeons who suspect tb in carcases or pathological material of South American camelids to report these to the svs as required by the legislation, and encourage owners to cooperate with control measures for this disease. People handling South American camelids with suspected tb should be warned of the zoonotic risk.

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