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Many pathogens of concern regarding the protection of human and domestic animal health can also infect wildlife. Infection may be sustained in a wildlife ‘reservoir’, with occasional ‘spillover’ to people and livestock (Dobson & Meagher 1996; Gordon et al. 2004), but transmission can also occur in the opposite direction, with domestic animals themselves contributing to the persistence of infection (Rhodes et al. 1998). The relative importance of transmission to and from wildlife is very difficult to assess without experimental manipulation (Haydon et al. 2002).
Mycobacterium bovis, the causative agent of bovine tuberculosis (TB), has a wide host range including cattle, humans and multiple wildlife species (Morris, Pfeiffer & Jackson 1994). Regular testing of cattle, with slaughter of those testing positive, has successfully controlled the infection across much of the developed world. However, control has not been achieved where wildlife populations have become persistently infected (Morris, Pfeiffer & Jackson 1994). In Britain, failure to control TB in cattle has been linked to persistent infection in populations of badgers Meles meles L., a widespread, although protected, wildlife species that thrives in landscapes where cattle are farmed (Neal & Cheeseman 1996).
Policies to control bovine TB in Britain have been based on the assumption that cattle acquire infection both from badgers and from other cattle. Control measures include restrictions on the movement of cattle from herds confirmed infected, and testing of cattle on farms that either adjoin the affected farm or have recently received animals originating from the restricted herd. Since 1974, these measures have been supplemented by various forms of badger culling on, and sometimes around, farms that have experienced recent TB outbreaks in cattle (Zuckerman 1980; Dunnet, Jones & McInerney 1986; Krebs et al. 1997).
Control strategies involving localized badger culling are based on the assumption that infections in cattle and badgers are associated, and that cattle may therefore act as a sentinel for infection in badgers. If this assumption is correct, then removing badgers that are spatially associated with infected cattle herds would be expected to reduce the risks of future badger-related outbreaks in the same herd, and also in neighbouring herds likely to be in contact with the same badgers. Despite this plausible logic, the only experimental test of localized badger culling showed that this was not associated with any reduction in the incidence of TB in cattle over the time-scale studied (Donnelly et al. 2003).
There is evidence to suggest that M. bovis infection is spatially clustered in both cattle (Krebs et al. 1997) and badger populations (Cheeseman, Wilesmith & Stuart 1989; Delahay et al. 2000; Olea-Popelka et al. 2003), at regional scales (e.g. counties) as well as at a more localized level (e.g. a few farms or badger territories). Regional clusters (sometimes termed hotspots) are geographically associated in the two species (Krebs et al. 1997). Moreover, at a regional level the prevalence of M. bovis infection has been found to be higher among badgers culled in association with cattle TB incidents than among those killed in road traffic accidents (Krebs et al. 1997), suggesting a local association between infections in the two species. However, detailed spatial comparisons have not been attempted.
Spatial associations between infection in cattle and badgers provide no information on whether transmission occurs from badgers to cattle, from cattle to badgers, from some other host (or hosts) to both species or some combination of these scenarios. Experimental studies of badger culling suggest that badgers do play a role in transmitting infection to cattle (Donnelly et al. 2003; Griffin et al. 2005), but other transmission scenarios have not been tested experimentally in the field. Hence, their potential importance, if any, to the maintenance of infection cannot be determined.
We investigated geographical associations between M. bovis infection in badgers and cattle, and evaluated indirect evidence for badger-to-cattle and cattle-to-badger transmission, using data from an ongoing large-scale study of bovine TB dynamics and control.
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In summary, our data provide clear evidence of an association between M. bovis infection in cattle and badgers. Not only are patterns of infection in the two species spatially correlated, there are also close linkages in the distribution of M. bovis strain types in the two species. Our data do not, however, allow an assessment of the relative importance of badger-to-cattle and cattle-to-badger transmission.
The pattern of M. bovis infection prevalence in different age and sex classes of badgers is likewise similar to that observed in other studies (Cheeseman et al. 1988). We found no association between M. bovis prevalence and tooth wear; this is somewhat surprising as the cumulative probability of infection would be expected to increase with age. We observed substantial variation in prevalence between trial areas and between cubs sampled at different times of year. However, because each trial area was sampled only once (at the initial proactive cull), it is impossible to attribute these findings to regional variation, seasonal differences or changes in prevalence over time as the trial areas were recruited.
Our data reveal evidence of spatial clustering of M. bovis infection within badger populations at a scale of a few kilometres. This is consistent with patterns observed on smaller scale culls, which have found that prevalence may be high in particular social groups while groups in neighbouring territories show no evidence of infection (Cheeseman et al. 1981). Longitudinal studies suggest that these clusters may persist for many years if left undisturbed (Delahay et al. 2000).
We also found clear evidence of clustering of infection within the cattle population, even when analyses excluded any tests that might have been prompted by detection of TB in a contiguous herd. Such clustering has been recognized for a long time, and is the reason why contiguous tests are carried out, as well as being the justification for determining cattle TB-testing regimes at a local (parish) rather than a regional (e.g. county) level.
Unlike previous studies, our data allowed us to detect a spatial association between M. bovis infection in badgers and cattle, again at a scale of 1–2 kilometres. At the start of the trial, badger home range sizes were likely to be on the order of 1 km2 (Woodroffe & Macdonald 1993) and average cattle herd density was approximately 0·75 herds km−2; hence the scale at which associations were detected is similar to the scale at which badgers and cattle could be expected to move and, potentially, to interact. It is difficult to be more precise about the scale at which the association occurs, as both badger and cattle locations were, for the purposes of analysis, necessarily represented as point locations. In reality, badgers move around their home ranges and cattle move within farms that may comprise multiple parcels of land (Johnston et al. 2005). Thus, each point location can be regarded as an approximation of reality measured with error. Such errors, assuming they are random, will have the effect of diminishing the estimated spatial associations, biasing the results toward the null hypothesis of no association. Detecting a spatial association with such imprecise location data supports the hypothesis that M. bovis infections in cattle and badgers are linked.
Spatial associations between cattle and badgers infected with the same spoligotype of M. bovis provide further evidence of a link between infections in the two host species. Simple spatial associations between infections in the two species might be generated by localized environmental conditions that predispose both host species to intraspecific transmission (e.g. microclimatic or micronutrient effects on susceptibility). However, our finding that badgers and cattle are infected with the same spoligotypes at a very localized scale suggests that, to the contrary, transmission is likely to occur between the species. The observation that some spoligotypes were detected only in one or other host species within a trial area (Table 2) might reflect the existence of transmission occurring solely within the cattle or badger population. However, it is also possible that these spoligotypes were undetected because not every infected animal, of either host species, was sampled in these cross-sectional datasets.
Clustering of infection within host populations, and associations between infection in cattle and badgers, were both detected across multiple trial areas. While the strength of the effects appeared to vary between trial areas, there was no consistent pattern in which areas showed particularly strong or weak effects (Figs 2, 3 and 4). In particular, there was no consistent difference in patterns observed in trial areas recruited before and after the FMD epidemic, suggesting that the temporary disruptions to cattle controls had no obvious effect on the associations we describe.
Tests for associations between the distribution of lesioned animals of one host species, and patterns of infection in the other species, provide only very limited information on the direction of transmission. Infected badgers were more closely associated with infected cattle that had tuberculous lesions than with cattle confirmed to be infected, but with no visible lesions. This association might be interpreted as indicating that cattle are involved in transmitting infection to badgers. However, the evidence is indirect and based on an assumption (that lesioned cattle are more infectious) that may be incorrect (Neill, Bryson & Pollock 2001). Moreover, the analysis is based on observational rather than experimental data, so it is impossible to exclude alternative explanations (e.g. that cattle infections acquired from badgers result in more severe pathology than infections acquired from other cattle). Experimental manipulations would be the only way to demonstrate cattle-to-badger transmission under field conditions, and to estimate the relative importance of such transmission. We found no significant differences between the patterns of cattle infections in the vicinity of lesioned badgers relative to infected badgers without visible lesions. However, as the relationships between lesion status and infectiousness are unknown, and are likely to vary between host species, these findings provide no insights into the relative importance of badger-to-cattle vs. cattle-to-badger transmission.
Our findings of clustered infection within both badger and cattle populations, and close spatial associations between M. bovis infections in cattle and badgers, suggest that control measures based on localized removal of badgers in the vicinity of cattle TB incidents, such as the ‘clean ring’ and ‘interim’ strategies, and the RBCT reactive treatment (Dunnet, Jones & McInerney 1986; Krebs et al. 1997) could have been expected to prove effective. However, the reactive strategy was not associated with any reduction in cattle TB incidence over the time-scale on which it was tested (Donnelly et al. 2003) and, while the other strategies were never tested experimentally, national TB incidence rose during the period when they were part of TB control policy (Krebs et al. 1997). Empirical experimental approaches, such as that taken in the RBCT, are required to estimate the potential value (or otherwise) of any culling strategy, despite the strong spatial associations observed between M. bovis infections in cattle and badgers.
One possible explanation for the failure of the reactive strategy to reduce cattle TB incidence is that, in addition to reducing badger density, culling disrupted clusters of infection within badger populations, potentially spreading infection to larger numbers of cattle herds. Comparisons of clustering on these initial culls, with patterns seen on subsequent ‘follow-up’ culls, will allow us to evaluate this hypothesis in future. We note, however, that evidence of clustering was equally strong, and patterns of association with cattle were equally close, in trial areas with varying histories of prior culling, ranging from no culling before the RBCT (trial area G), limited culling (e.g. trial areas D and H) and persistent culling over two decades (e.g. trial areas B and F).
Our finding that cattle might be involved in transmitting infection to badgers, as well as vice versa, would also have relevance to TB control policy if substantiated by further studies. This possibility suggests that aggressive control of TB within cattle populations (e.g. by improved testing regimes and movement restrictions) might help to reduce the risks of developing persistent infection in local badger populations. Such measures would be a particularly high priority in areas with little previous history of TB infection in cattle, where infection may not yet be established in badger populations.