Feral ferrets (Mustela furo) as hosts and sentinels of tuberculosis in New Zealand.

The control and eventual eradication of bovine tuberculosis (TB) poses major challenges in New Zealand, given the variety of wildlife species susceptible to TB, many of which are capable of onwards transmission of Mycobacterium bovis infection. Here we discuss the role of feral ferrets (Mustela furo), focussing on potential transmission or risk pathways that have implications for management of TB. Firstly inter-specific transmission to ferrets. Ferrets scavenge potentially infected wildlife, including other ferrets, thus prevalence of TB can be amplified through ferrets feeding on tuberculous carcasses, particularly brushtail possums (Trichosurus vulpecula). Secondly intra-specific transmission between ferrets. The rate of ferret-ferret transmission depends on population density, and in some places ferret densities exceed the estimated threshold for disease persistence. TB can therefore potentially be maintained independently of other sources of infection. Thirdly transmission from ferrets to other wildlife. These include the main wildlife maintenance host, brushtail possums, that will occasionally scavenge potentially tuberculous ferret carcasses. Fourthly transmission from ferrets to livestock. This is considered to occur occasionally, but the actual rate of transmission has never been measured. Fifthly geographical spread. M. bovis-infected ferrets can travel large distances and cause new outbreaks of TB at locations previously free of TB, which may have caused an expansion of TB-endemic areas. Ferrets play a complex role in the TB cycle in New Zealand; they are capable of contracting, amplifying and transmitting M. bovis infection, sometimes resulting in ferret populations with a high prevalence of TB. However, ferret population densities are usually too low to sustain infection independently, and transmission to other wildlife or livestock appears a rarer event than with possums. Nevertheless, management of ferrets remains a key part of the National Pest Management Strategy for TB. Control is prudent where M. bovis-infected ferret populations exist in high numbers, to reduce the onward transmission risk of any self-sustained infection to livestock. When ferret numbers are well below the theoretical disease maintenance threshold, ferret control is still sometimes warranted because of the animals' ability to acquire infection when young and, through dispersal, transport it outside TB-endemic areas. Ferrets can also be used as disease sentinels for TB, especially in areas where alternative sentinel species are rare or expensive to survey, and when sampling of possums is not cost-effective.

Prevalence of Mycobacterium bovis infection in feral pigs in the Northern Territory.

The prevalence of Mycobacterium bovis infection in populations of feral pigs from five areas in the Northern Territory was examined. In total 790 pigs were necropsied and positive cultures of M bovis were obtained from two pigs (0.25%) and a mycobacterial granuloma was found in one pig. The observed prevalence of M bovis infection in feral pigs is significantly less (chi 2 = 139.8, df = 1, P < 0.001) than the results of a comparable survey conducted during the early 1970s before the implementation of the Brucellosis and Tuberculosis Eradication Campaign. The prevalence of all types of macroscopic lesions resembling tuberculosis was significantly (chi 2 = 338.7, df = 1, P < 0.001) less than the earlier survey. The results are further support for the hypothesis that in the Northern Territory feral pigs are an end-host for M bovis infection, and that the previous high prevalence of M bovis recorded in feral pigs in the 1970s was caused by the close association between these animals and large populations of M bovis-infected buffalo and cattle.

Surveillance of wildlife for Mycobacterium bovis infection using culture of pooled tissue samples from ferrets (Mustela furo).

AIM: To compare culture results of homogenates of pooled lymph nodes from individual ferrets with and without macroscopic lesions of bovine tuberculosis for the presence of Mycobacterium bovis, and to determine whether homogenates from 10-30 ferrets could be combined and cultured without loss of sensitivity as a possible method for improving cost-effectiveness of surveillance for M. bovis infection in wildlife populations. METHODS: Numbers of colony forming units (cfu) of M. bovis present in cultures of homogenates of pooled lymph nodes from individual ferrets known to be infected and having no visible lesions (NVL) or macroscopic lesions consistent with bovine tuberculosis were determined. Prevalences of M. bovis infection in populations of ferrets in the Marlborough region of the South Island of New Zealand were determined by culturing homogenates of pooled lymph nodes from individual animals. Samples from homogenates from North Canterbury were combined to form pools representing 10, 20 and 30 animals and also cultured for M. bovis. RESULTS: Fewer M. bovis cfu were isolated from ferrets with NVL (mean=0.77 log10) compared with ferrets with macroscopic lesions (mean=3.22 log10; p<0.05). The mean prevalence of infection in eight different surveys involving 427 ferrets from the Marlborough region was 18% (range 8-44%), which included a small number of animals with macroscopic lesions of tuberculosis. Pooling of samples from up to 30 different ferrets with NVL did not reduce the sensitivity of detecting M. bovis infected populations. CONCLUSION: Culturing of pools of lymph node samples detected a significant proportion of M. bovis-infected ferrets that would otherwise have gone unnoticed based on samples that had only macroscopic lesions. Culturing of samples pooled from up to 30 different ferrets could provide significant cost savings in surveys of wildlife for the presence of M. bovis infection without any apparent loss of sensitivity.

Is the spatial distribution of tuberculous possums influenced by den quality?

This study aimed to test whether den sites in a single small area containing a cluster of tuberculous brushtail possums were more exposed to adverse environmental conditions than those in a nearby area where no tuberculous possums had been found. No significant differences were found in the visually assessed quality of dens between the two areas. This suggests either that den quality is relatively unimportant in the epidemiology of bovine tuberculosis in possums, or that the differences in den quality are not large enough or are too spatially localised to be detected with the methods used.

Broad-scale possum and ferret correlates of macroscopic Mycobacterium bovis infection in feral ferret populations.

AIMS: To examine the relationships between the prevalence of macroscopic Mycobacterium bovis infection (bovine tuberculosis) in feral ferrets (Mustela furo), the abundance of ferrets, and the abundance of brushtail possums (Trichosurus vulpecula) . METHODS: Data on the prevalence of macroscopic M. bovis infection in ferrets, abundance of ferrets, and abundance of possums were analysed from 12 comparable independent broad-scale surveys. RESULTS: The prevalence of macroscopic M. bovis infection in ferrets was positively correlated with possum abundance but unrelated to ferret abundance, suggesting that possums are an important source of M. bovis infection in ferrets. The lack of any positive relationship between the prevalence of M. bovis infection in ferrets and ferret abundance does not support the hypothesis that per capita transmission rates, and therefore disease prevalence, should be higher at higher ferret abundance. CONCLUSION: The results support the hypothesis that tuberculous possums are the major underlying source of M. bovis infection for feral ferrets in New Zealand.

Habitat-related prevalence of macroscopic Mycobacterium bovis infection in brushtail possums (Trichosurus vulpecula), Hohonu Range, Westland, New Zealand.

AIM: To identify broadscale habitat factors influencing the prevalence of macroscopic Mycobacterium bovis infection in brushtail possums (Trichosurus vulpecula) at a site in Westland, New Zealand. METHODS: During 1973/74, 1989/90 and 1997, we undertook repeated cross-sectional surveys of M. bovis infection in a possum population on the Hohonu Range , Westland. Data were analysed to determine the influence of site-specific habitat characteristics (land form, aspect, slope, altitude), distance from forest-pasture margin and time since infection on the spatial and temporal prevalence of macroscopic M. bovis infection. RESULTS: The prevalence of M. bovis infection was highest in 1973/74 (13.4%), compared with 1989/90 (3.1%) and 1997 (9.4%). The prevalence of macroscopic M. bovis infection was significantly influenced by habitat, as indexed by altitude and slope in this study site. Every 100 m increase in elevation was associated with a 29% decrease in the odds of infection, and every 10 degrees increase in slope was associated with a 20% decrease in the odds of infection. For possums caught in the lowland podocarp forest (altitude 100-200 m, average slope=5.7 degrees ), the odds of infection were nearly 30-fold higher than those for possums caught in high-altitude hardwood forest near the tree line (altitude 900-1000 m, average slope=28 degrees ). Whilst the prevalence of disease fluctuated markedly between surveys, its broadscale spatial distribution changed little over time. Proximity to the forest-pasture margin had no significant influence on the prevalence of disease, once the effect of habitat was taken into account. CONCLUSION: The prevalence of macroscopic M. bovis infection in possums was strongly influenced by habitat type, being highest in habitats that supported the highest density of possums, and lowest in habitats where population density was low. There was no evidence of progressive spread of M. bovis infection in possums into forest away from pasture-forest margins over the 24-year period of these surveys.

The relationship between prevalence of Mycobacterium bovis infection in feral ferrets and possum abundance.

AIM: To determine the relationship between the prevalence of macroscopic Mycobacterium bovis infection in feral ferrets (Mustela furo) and the abundance of brushtail possums (Trichosurus vulpecula). METHODS: The predictive power of a previously reported positive association between the prevalence of macroscopic M. bovis infection in ferrets and possum abundance was examined by undertaking surveys of M. bovis infection in ferrets at sites of low and high possum abundance. The association was then tested by a manipulative experiment that measured changes in the prevalence of macroscopic M. bovis infection in feral ferrets after reducing possum abundance. RESULTS: The positive relationship between the prevalence of macroscopic M. bovis infection in ferrets and possum abundance remained valid for new survey data, although the goodness of fit of the relationship was reduced. Experimentally reducing possum abundance reduced the odds of macroscopic M. bovis infection in ferrets by 80% in the years immediately following possum control (Odds Ratio=0.23, p=0.003). CONCLUSIONS: There is a causal link between possum abundance and the prevalence of macroscopic M. bovis infection in feral ferrets in areas in which M. bovis infection is known to occur in ferret populations. This suggests that possum-to-ferret transmission of disease occurs and accounts for most of the disease evident in ferret populations, though does not determine whether ferrets are spillover or maintenance hosts of M. bovis. Management to reduce the prevalence of M. bovis infection in ferrets should consider reducing possum abundance as a control tactic.

Epidemiology of Mycobacterium bovis infection in feral ferrets (Mustela furo) in New Zealand: I. Pathology and diagnosis.

Necropsies from 228 ferrets captured from eight areas in the North and South Islands provided material for an investigation into the epidemiology of tuberculosis in feral ferrets. Mycobacterial culture of pooled lymph nodes (retropharyngeal, respiratory and jejunal) identified the prevalence of infection to be much higher than that estimated from gross lesions only. Seventy-three of the 228 animals examined (32%) were diagnosed as tuberculous. Fifty-three culture-positive ferrets and 18 seemingly uninfected animals were subjected to detailed histopathological examination. The outcomes of these investigations, including the characteristics of the disease, distribution of lesions and aids to diagnosis, are presented. Of the feral carnivores found in New Zealand, the disease persists at high prevalence only in ferrets, and is probably the maintained principally by ingestion of tuberculous carrion. The course of the disease may be prolonged in some ferrets, but tuberculosis eventually causes death of many infected animals. Microscopic hepatic granulomas may be considered pathognomonic of the disease, and have potential to be used as a rapid diagnostic tool in ferrets with no gross lesions.

Epidemiology of Mycobacterium bovis infection in feral ferrets (Mustela furo) in New Zealand: II. Routes of infection and excretion.

Detailed necropsies of 228 ferrets captured from eight areas in the North and South Islands provided material for an investigation into the epidemiology of tuberculosis in wild ferrets. Seventy-three of the 228 (32%) animals examined were diagnosed as tuberculous, by culture of pooled lymph nodes and detailed histopathological examination. The prevalence of bovine tuberculosis was 96% in 24 ferrets taken from areas in which tuberculous possums were common. None of 35 animals under 4 months of age were found to be infected, and the prevalence of infection was shown to rise with age, such that for each 6 month age increment there was a 2.8 times greater risk of becoming infected. The most common route of infection appeared to be via the alimentary tract, as 79% of 38 animals, in which the initial lesions could be reasonably determined, had these lesions associated with the digestive tract. Samples from potential sites of excretion from infected ferrets were submitted for culturing. The most common route of excretion was via the oral cavity, with M. bovis recovered from 15 of 64 (23%) oral swabs. Mycobacterium bovis was also isolated from four of 64 (6%) tracheobronchial lavage samples, ten of 63 (16%) faecal samples, two of 29 (7%) urine samples and one of 8 (12.5%) mammary glands. The disease in ferrets appears to be principally maintained by ingestion of tuberculous carrion. Although a moderate number of ferrets excrete M. bovis orally, there appears to be only minor intraspecific transmission by bite wounding. The findings provided no evidence to support the occurrence of pseudo-vertical transmission.

Effects of sustained control of brushtail possums on levels of Mycobacterium bovis infection in cattle and brushtail possum populations from Hohotaka, New Zealand.

AIMS: To examine the effect of reducing the abundance of brushtail possums (Trichosurus vulpecula) on the distribution and prevalence of bovine tuberculosis (Mycobacterium bovis, Tb) in possums and the incidence of Tb in domestic cattle on a group of farms in the central North Island, New Zealand. METHODS: The cumulative yearly incidence of Tb infection from 12 cattle herds was estimated from annual tuberculin testing and abattoir inspection data over the period 1983-98. Intensive control of possum populations began for six of the herds in 1988, five herds in 1994 and the remaining herd in 1996. The prevalence and distribution of macroscopic M. bovis infection in possums and an index of possum abundance was estimated during yearly cross-sectional surveys from 1988 to 1998. This enabled formal testing of the link between the abundance of tuberculous possums and the incidence of Tb in cattle. RESULTS: Before possum control, infected possums were clustered in foci on or adjacent to the farms with the highest annual incidence of tuberculosis in cattle, and had an overall prevalence of macroscopic M. bovis infection of 2.3%. The prevalence of disease declined to zero with ongoing possum control, although infected possums continued to be found during the first 5 years of control. Maintaining the possum population at an average of 22.1% of its pre-control density significantly reduced the odds of the cumulative yearly incidence of Tb in cattle by 77% during the first 5 years of possum control and a further 65% in the second 5-year period. Nine of 11 tuberculous possums identified since the start of possum control were found within the areas where infected possums were clustered during the pre-control survey, suggesting that the persistence of infection within these clusters rather than infected immigrants was the source of ongoing disease. Annual estimates of the prevalence of tuberculous possums broadly followed the predictions of Barlow's possum-Tb model for a controlled possum population. CONCLUSION: The results support the hypothesis that tuberculous possums transmit bovine tuberculosis to domestic cattle, and therefore that reducing the abundance of tuberculous possums reduces the incidence of Tb in cattle. If the level of possum culling is sufficient, it appears that M. bovis infection may be eradicated from possum populations. Better information on population density, rate of increase and annual culling rates would have been needed for a truly independent examination of the Barlow possum-Tb model.