Part III: Mycobacterium bovis, the English bovine tuberculosis outbreak, badgers and the culling debate.
Critical to the entire culling controversy as a control measure for M. bovis is what the exact role of the Eurasian badger (Meles meles) in the spread of bovine tuberculosis. If badgers are the principal source of bovine tuberculosis, then a cull would make sense and would have the maximum effect on reducing breakdowns (a case of bovine tuberculosis in a cattle herd). If badgers are not the principal source of bovine tuberculosis, or alternatively they are but cannot spread bovine tuberculosis to cattle, then a cull is just going to be a needless waste of time with ultimately no effect as several conservationists have argued. So what does the scientific literature actually say?
Are badgers actually infected with bovine tuberculosis and if so, can they secrete Mycobacterium bovis?
One of the most recent studies relevant to this question is from Chambers et al., (2002) and investigated the current serological tests for identifying badgers that shed Mycobacterium bovis. This study compared two methods, notably ELISA (Enzyme Linked ImmunoSorbent Assay) and Western blotting against direct culture of M. bovis for accurately identifying infected badgers. Importantly, this study was set up to determine if these techniques could accurately determine if a badger was secreting M. bovis. Essentially, the scientists picked an area that had endemic infection with M. bovis among cattle herds and captured 128 badgers. Of these sampled badgers, 44 were confirmed to have secreted M. bovis at some point in their life as confirmed by the ELISA, Western blot and culture detection methods.
With the use of all three methods concordantly it makes it virtually impossible that the result is incorrect or outside factors such as other environmental mycobacteria (Primm et al., 2004) are responsible and as such, the study clearly implicates badgers as a host for M. bovis. Of course, science does not stand simply by itself but rather through the work that others have done in the past and what studies have followed afterwards. Here the consensus is overwhelming. For instance, a previous study from Gallagher and Clifton Hadley (2000) shows that badgers had M. bovis infection in both lung tissue and in their urine from post-mortem examination. Other studies from Costello et al., (1999) and Olea-Popelka et al., (2005) have found that badgers are infected with M. bovis and most importantly, the same strains of M. bovis tend to be shared between cattle and badgers in the same area (this is an important point, more on this later however).
Further, the two key ‘trials’ conducted on the effects of badger culling by Donnelly et al., (2002, 2006) in England and the “Four counties” trial in Ireland by Griffin et al., (2005). Both of these studies have found that bovine tuberculosis is present among badgers around farming areas. Typical prevalence of infected badgers tends to fluctuate widely, with some researchers finding infection rates around 20% and others up to 50% (Corner L.A.L., 2006). In short, numerous studies have all universally been able to find badgers that have been infected with M. bovis. The question remains as to if infected badgers secrete M. bovis that can infect cattle?
In order to spread efficiently from badgers to cattle it’s important to realize that several factors need to occur for any chance of transmission:
1) Badgers need to come into contact with cattle or alternatively, cattle come into contact with feces and other excretions of badgers.
2) Infected badgers must be able to secrete M. bovis to cattle through excretions such as sputum and urine.
3) M. bovis in badger excretions must have some mechanism to survive the passage from a badger to cattle.
We should also expect if these three things are found and that if badgers are transmitting M. bovis to cattle (somehow), then we’d also expect to see the same spoligotypes in cattle and local badgers. So once again, what does the literature say on these three issues?
Possible means of transmission of cattle to badgers.
Several studies have identified that badgers are not afraid to come into contact with cattle, although the circumstances in which badgers come into contact differ. Phillips et al., (2003) and Corner L.A.L. (2006), both report that cattle will typically avoid badgers if at all possible. Interestingly, both papers note that heavily infected badgers tend to behave aberrantly and that cattle will frequently investigate by licking, sniffing and biting. This matches similar observations of cattle in
Additionally cattle are also highly likely to come into contact with the excretions of badgers such as urine, feces and sputum. As badgers excrete copious amounts of infectious bacteria in their sputum (coughed up fluid), urine and from infected bite wounds this does pose a possible risk for cattle grazing in fields visited by badgers (Krebs et al., 1998; Phillips et al., 2003; Scantlebury et al., 2004 and Young et al., 2005). Additionally, badgers are also capable of surviving with tuberculosis for months or even years and may be infectious for long periods of time, until they eventually succumb to infection (Phillips et al., 2003; Scantlebury et al., 2004 and Corner L.A.L., 2006).
Finally, it is also the case that cattle will graze areas that have been used as latrines or ‘crossing points’, essentially places badgers tend to go over often when moving from field to field, which poses a potential risk of ingesting M. bovis. Interestingly the main means of infection in cattle is from aerosolized particles and not from ingestion. This is supported by the fact infected lesions and bacteria from infected cattle are typically isolated from around the head region more so than GALT* (Phillips et al., 2003).
Scantlebury et al., (2004) noted that intensively farmed cattle tended to graze badger latrines and crossing points immediately due to sward (grass) competition. Conversely, cattle farmed in less dense numbers tended to scratch and sniff latrines or badger urine (crossing points) but ultimately avoid these areas. Rates and reasons for cattle investigation or consummation of swards infected with badger excretions should deserve further analysis.
Finally M. bovis is more than capable of surviving outside of the host once it has been excreted. As mentioned in part II, mycobacteria are particularly hardy organisms and have a wide metabolism. M. bovis in soil samples has been demonstrated to be viable for months by culture and may even be viable for years (Young et al., 2005). This is because although previous studies that have failed to culture M. bovis after long periods of time, molecular methods for the detection of RNA have indicated the organism could still be present but non-culturable (Young et al., 2005). In a similar manner to other microbes, it is possible for a viable organism to exist in the environment that cannot be cultured for whatever reason (Colwell and Grimes, 2000).
The final link in the chain.
Generally infected badgers tend to be found in clusters, with the surrounding cattle farms also infected with the same strains of M. bovis (Costello et al., 1999; Smith et al., 2003; Griffin et al., 2005 and Olea-Popelka et al., 2005, 2006). Additionally, many studies have indicated that badgers may roam relatively widely and have varying levels of contact with cattle, see for examples Griffin et al., 2005 and Olea-Popelka et al., 2006. As mentioned earlier, this concordance between the general spoligotypes in an area being the same between those found in infected cattle and nearby infected badger setts resolves the issue. It’s almost certain that badgers are to some degree responsible for spreading M. bovis to cattle, even if the exact mechanism is unknown and has yet to be illucidated (Olea-Popelka et al., 2006).
It’s very clear that badgers can be infected by M. bovis, excrete the organism in their sputum and urine due to chronic infection of the lungs and kidneys and that the same strains of M. bovis that infect badgers are found in cattle. Also importantly, the proactive culling portions of the Donnelly et al., (2003, 2006) study and the Griffin et al., (2005) “four counties” trial have shown considerable drops in the prevalence of herd breakdowns**. Finally however, if you’re the sort of person who requires a more ‘visual’ aid, then I would propose having a look at this poor badger (Horrific image! Do NOT click it unless you like copious amounts of pus!), which has died of tuberculosis and believe me, it’s not a pretty sight.
However, despite the strength of the evidence presented from the literature supporting a link between badgers and bovine tuberculosis, it’s insufficient to resolve the issue mentioned in the opening paragraph. Even if badgers are responsible for spreading tuberculosis, the role of cattle will also need to be determined as it may be possible that badgers are only a symptom, and not the cause of the high prevalence of BTB in the
*GALT=Gastrointestinal Associated Lymphoid Tissue.
**I will point out before someone else does, that I’m aware the reactive culling part of the Donnelly studies have shown an increase in herd breakdowns. I’m not deliberately ignoring this point as I intend to cover this later in the series.
References
Chambers M.A., W.A. Pressling, C.L. Cheeseman, R.S.
Colwell R.R. and Grimes D.J. (2000). Nonculturable microorganisms in the environment. ASM press Washington D.C.
Corner L.A.L. (2006). The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: How to assess the risk. Veterinary microbiology, 112:303-312.
Costello E., D. O’Grady, O. Flynn, R. O’Brien, M. Rogers, F. Quigly, J. Egan and J. Griffin (1999). Study of restriction fragment length polymorphism analysis and spoliogotyping for epidemiological investigation of Mycobacterium bovis infection. The Journal of Clinical Microbiology, 37:3217-3222.
Donnelly C.A., R. Woodroffe, D.R. Cox, J. Bourne, G. Gettinby, A.M. Le Fevre, J.P. McInerney and W.I. Morrison (2003). Impact of localized badger culling on tuberculosis incidence in British cattle. Nature, 426:834-837.
Donnelly C.A., R. Woodroffe, D.R. Cox, F.J. Bourne, C.L. Cheeseman, R.S. Clifton-Hadley, G. Wei, G. Gettinby, P. Gilks, H. Jenkins, W.T. Johnston, A.M. Le Fevre, J.P. McInerney and W.I. Morrison (2006). Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature, 439:843-846.
Gallagher J. and R.S.
Krebs J.R., R.M. Anderson, T. Clutton-Brock,
Olea-Popelka F.J., O. Flynn, E. Costello, G. McGrath, J.D. Collings, J. O’Keeffe, D.F. Kelton, O. Berke and S.W. Marin (2005). Spatial relationship between Mycobacterium bovis strains in cattle and badgers in four areas in
Olea-Popelka F.J., J. Phelan, P.W. White, G. McGrath, J.D. Collins, J. O’Keeffe, M. Duggan, D.M. Collins, D.F. Kelton, O. Berke, S.J. More and S.W. Martin (2006). Quantifying badger exposure and the risk of bovine tuberculosis for cattle herds in
Phillips C.J.C., C.R.W. Foster, P.A. Morris and R. Teverson (2003).The transmission of Mycobacterium bovis infection to cattle. Research in Veterinary Science, 74:1-15.
Primm P.,
Scantlebury M., M.R. Hutchings, D.J. Allcroft and S. Harris (2004). Risk of disease from wildlife reservoirs: Badgers, cattle and bovine tuberculosis. Journal of Dairy Science, 87:330-339.
Young J.S., E. Gormley and E.M.H. Wellington (2005). Molecular detection of Mycobacterium bovis and Mycobacterium bovis BCG in soil. Applied and Environmental Microbiology, 1946-1952.
