Eliminating bovine tuberculosis from Australia

Mycobacterium bovis belongs in the Mycobacterium tuberculosis complex, a closely related group of organisms that causes TB in humans and other mammals. The traditional members of the complex are M. tuberculosis, M. africanum, M. bovis (and M. bovis BCG) and M. microti. Mycobacterium tuberculosis and M. africanum primarily affect humans and M. microti is mainly associated with tuberculous disease of voles.

It is well known that M. bovis has the widest host range of any of the M. tuberculosis complex species¹. The list of animals susceptible to M. bovis is extensive, including domesticated animals such as cattle, farmed buffalo, goats, various species of deer, sheep and pigs, as well as a variety of free living and captive wildlife species that may be maintenance, spill over or end hosts for M. bovis². The 44 recorded wild animal hosts of M bovis, or a closely related variant, include not only ruminants such as buffalo (3 spp.) and deer, antelope, and goats (11 spp.), but also large and small carnivores from cats to lions (7 spp.), omnivores such as bears and pigs (3 spp.), primates (2 spp.), mustelids such as badgers (Meles meles) and ferrets (4 spp.), rabbits and hares (2 spp.), some other small mammals (4 spp.), seals and dolphins (7 spp.), and even a marsupial, the Australian brushtail possum (Trichosurus vulpecula). Another 17 species have been recorded as hosts in captivity, including 6 additional primates, and two species of rhinoceros.

In Australia in the 1930’s, 25% of the cases of TB in children were due to M. bovis³, caused mainly by ingestion of infected cow’s milk. Following the implementation of pasteurisation in the mid ’50s and a successful bovine TB eradication campaign, Australia was declared free of TB according to international standards in 1997 (the last case of animal M. bovis was recorded in 2002). A significant feature of the campaign was the involvement of industry who worked in partnership with government to fund and make policy decisions. Eradication was underpinned by a test and slaughter program but included a number of novel interventions such as age culling, tracking of residual animals on crown and private land using radio collars, strategic use of depopulation, an enhanced abattoir monitoring program. Research funded by government and industry provided new knowledge to assist policy decisions. Buffalo were recognised as a maintenance host for M. bovis and were included in the test and slaughter program from the early 1980’s, when attention was focussed on northern Australia. M. bovis also infected feral pigs but these were confirmed as spill over hosts. Incidental cases of M. bovis were confirmed in deer and a goat but neither of these presented a risk to the eradication program.

Despite the success of the program, an average of five cases per year of human infection (range 2-25) caused by M. bovis were recorded from 1975-2004⁴ and 2-5 cases were recorded up to 2010. During 1975-1994 M. bovis infection was recorded in cattle workers and three cases were recorded in laboratory workers, however the majority of cases resulted from reactivation of previous infection or were in people infected prior to arrival in Australia. Considerable concern has been raised about the increased risk of M. bovis causing TB in developing countries with a high HIV/AIDS burden such as South Africa and SE Asia⁵, but this has not yet been recognized as a significant problem.

Wildlife species such as badgers, brushtail possums, white-tailed deer (Odocoileus virginianus), bison (Bison bison) and African buffalo (Syncerus caffer) are maintenance hosts for M. bovis and may be reservoirs for infection of both domestic animals and other wildlife species. In particular, the badger, possum and buffalo have caused almost insurmountable difficulties for conventional control and eradication programmes in Great Britain and Ireland, New Zealand and South Africa respectively. Australia was fortunate it didn’t have a wildlife maintenance host other than imported water buffalo. The inclusion of buffalo in the test and slaughter campaign, along with large-scale depopulation of feral buffalo contributed to Australia's success in eradication of bovine tuberculosis from its cattle herds.

Organisms once considered ‘garden variety’ M. bovis isolated from goats, antelopes and seals have been further characterised as new members within the M. tuberculosis complex, evolving from an M. tuberculosis-like ancestor. For example, TB in Spanish goats, originally considered to have been caused by M. bovis, is now recognised as being caused by a particular clone of the M. tuberculosis complex known as M. caprae⁶ and TB in seals and sea lions is now known to be caused by a new species called M. pinnipedii⁷, which is also known to be zoonotic⁸. The presence of M. pinnipedii in seals, sea lions, and more recently a bottle nosed dolphin (unpublished data) remain a risk for humans, and information sharing and cooperation between wildlife specialists, veterinarians and physicians is required to minimise exposure and infection in wildlife species and humans who work with them.