Badgers and bTB – New Background Research

In view of the continuing controversy on badger culling and the costs affecting farmers, I found the following report which I have heavily edited to make it shorter without hopefully changing its inferences!  For the full version go to:  https://www.frontiersin.org/articles/10.3389/fvets.2018.00109/full

Bovine Tuberculosis in Britain and Ireland – A Perfect Storm? the Confluence of Potential Ecological and Epidemiological Impediments to Controlling a Chronic Infectious Disease.

By A. R. Allen, A. Skuce and A. W. Byrne. Published in “Frontiers In Veterinary Science,” 05 June 2018.

Introduction. Bovine tuberculosis (bTB) caused by Mycobacterium bovis is a zoonotic disease, primarily affecting livestock, which is of economic importance to the European Union (EU) due to its impact on trade. Indeed, at the inception of the European project, as the European Economic Community (EEC), the first legal initiatives were taken to combat the disease in 1964 with the drafting of council directive 64/432/EEC. The legislation also defined the goal of the EEC to be disease eradication as opposed to control. Further legislation followed which enshrined the need for member states of the EEC to fund and facilitate test and slaughter schemes for the purposes of bTB eradication. In many member states, eradication programmes proceeded effectively, resulting in the granting of “officially tuberculosis free” (OTF) status to Denmark 1980, the Netherlands 1995, Germany and Luxembourg 1997, Austria 1999, France 2001 and Belgium 2002. Other states were granted OTF status upon joining the EU – Finland and Sweden 1995 and Czech Republic 2004. In 2009, Poland, Slovenia also attained OTF status, whilst non-member state Norway was recognised as meeting EU standards.

Against this backdrop of successful eradication is the contrasting situation observed in the islands at the western fringe of the European continent – Britain and Ireland. Despite dramatic initial success in controlling bTB, England, Wales and Northern Ireland have suffered increasing incidence since the late 1980’s. Scotland is the notable exception, having been granted OTF status in 2009. Data from 2009 indicated that 5–6% of herds from both islands tested positive for the presence of M. bovis. A contributing factor to the rise in herd incidence in England and Wales can be attributed to the suspension of bTB testing during the 2001 outbreak of foot and mouth disease [F&M]. However it has been recognised that even before the F & M epidemic, bTB herd incidence was on the rise and F & M disease merely exacerbated an already existing problem consistent with an upward trend in incidence since 1986. Indeed, data from DEFRA indicates that since 2003 the total number of new bTB breakdowns identified (every quarter) in GB has been doubling at a rate of every 10 years. Prior to the F & M disease epidemic of 2001, the doubling rate was every 5.2 years. More recently, England, Wales and Northern Ireland have exhibited a rise in herd incidence whilst the Republic of Ireland has experienced a fall. Whilst mainland Europe still has a substantial bTB problem in the Iberian peninsula (Spain herd incidence 1.4% in 2009), this pales in comparison to the problems observed in the UK and Republic of Ireland.

Despite standardisation, there remain differences in application of skin tests and in the programs they support across the EU. We address an overview of these: tuberculin potency for use in all skin tests used in Europe is tightly regulated by EU Council Directive 64/432. It is however recognised that changes in manufacturing and production procedures can result in batch to batch variation in potency. Indeed, even with strict regulation, tuberculins of lower potency have been released before. Such batch to batch variation and low potency would affect sensitivity of the skin test by reducing the DTH response / skin swelling that underpins diagnosis. Could such heterogeneity underpin the divergent outcomes in Britain and Ireland’s TB control programmes compared to mainland Europe?

Wildlife Hosts Are a Significant Impediment to Eradication. The presence of wildlife hosts of bTB has been found to be a major impediment to eradication in a number of countries worldwide [e.g., Michigan, USA, New Zealand, UK and Ireland. In Michigan the wildlife host is the white tailed deer, while in New Zealand there is a multi-host problem with the most significant reservoir being the non-native brushtail possum. In continental Europe, recent research has suggested that wild boar may act as a reservoir of infection, causing increased risk to cattle herds in parts of France and Spain. Deer may be a widespread, but relatively localised, problem in a number of countries across Europe. It has been suggested that European badgers may also play a role in the epidemiology of bTB in cattle in Spain and France, however, it is only in Britain and Ireland where there is strong evidence of their impact on the control of bTB in cattle.

Evidence That Badgers Are Implicated in the Epidemiology of bTB in Cattle. Badgers are a host species for M. bovis, and have been implicated in the epidemiology of cattle bTB in UK and Ireland. Culling trials have demonstrated significant reduction in risk to cattle herds in areas where badger densities were significantly reduced. The magnitude of this effect has been shown to be larger in the ROI [Rep of Ireland] than in (Randomised badger cull) trials in GB. In GB, badger culling was associated with a temporarily increased risk also to herds found at the periphery of cull sites. This was hypothesised (the “perturbation effect” hypothesis) to be as a result of increasing transmission amongst badger populations, causing increased spill back infection to cattle herds. This suggests that badgers can play a significant role in spilling back infection to cattle over short duration. However, this peripheral increased risk was transient [<2 years post-cull] and was not demonstrated during badger cull trials or government-led culling operations in ROI. The apparent beneficial effects of proactive culling to farms in cull areas have been maintained for up to 5–11 years after GB cull trials.

Britain and Ireland Have Higher Average Badger Densities. The islands of Britain and Ireland have the highest average recorded density of badgers compared to any other country in Europe. Median badger densities across badger study sites suggest a median density of 4.3–5.4 badger sq/km for the British Isles, while studies from across Europe suggest that median badger densities are 0.29–0.55 badger sq/km. Furthermore, in England and Wales there has been a significant increase in badger social group and population densities in recent decades. These figures mask the wide variation in density at landscape scale – for example, badger densities in Spain can vary from <0.3 to 3.4 badgers sq/km across habitat types. Similarly, badger densities in Ireland can vary from 0.7 badgers sq/km in poor upland habitat; in ideal conditions on a wooded island, densities up to 37 badgers sq/km have been recorded. However, what is important is that badgers benefit from a benign temperate climate in the British Isles, and have thrived in areas where woodland and pasture abound. These habitats can maintain badgers at mean densities of 3–5 badgers sq/km in Britain and Ireland and are also the contact point for potential direct and indirect interaction between badgers and grazing cattle. While badger density per se may not be related directly to risk in studies have found significant and positive associations between badger density and increased bTB herd breakdown risk.

There is considerable variation in the societal attitudes to the management of wildlife across Europe and this results in significant variation in the actual management practices implemented across Europe. This may relate to the apparent conflict between conservation, animal welfare, and management goals, as well as cultural differences in the acceptability of pursuits such as hunting. Hunting is more common, and arguably more socially acceptable in many continental European countries than it is in the UK and Ireland. Badger hunting is widespread and relatively intense in a number of countries across continental Europe, despite the badger being listed under the Bern Convention. In Germany, the annual recorded hunting bag for badgers has been between 50–70,000 per annum, within an increasing trend in the hunt bag in recent years – for example, the bag for 2016 was 71,168, a 11.98% increase from 2015. Similarly, in Finland 8,600–14,000 badgers have been reported in the national hunting records per annum and an increasing trend is reported in Poland where recent game bags are in excess of 4,000 badgers. Badger hunting is common and widespread in France, though there are limited available data on the national badger status, but hunters have been used recently in bTB outbreaks to sample badgers. In Britain and Ireland, the badger has been protected by legislation since the 1970’s. It is likely that this protection status has had beneficial effects on population size and may have influenced the considerable variation in the estimated densities of badgers across European countries, and between the British Isles. Furthermore, this broader issue of the “palatability” of wildlife management within society, and the relationship between this effect and the interventions undertaken may have been a significant factor in the bTB epi-system within the UK and Ireland.

Badgers Exhibit Significant TB Prevalence. Recent investigations indicate that more detailed post-mortem examinations result in the detection of microscopic lesions that would otherwise evade detection by standard procedures. Badgers killed in road traffic accidents (RTA) have proven to be a useful source of data in attempting to determine badger TB prevalence at a county-wide scale. The ISG reported that standard post mortem examination revealed that 15% of GB RTA badgers had TB. The ISG cautioned, however, that at a localised level below county size, owing to reduced availability of RTA badgers, this method may not be sufficient for surveillance. Similar RTA data collected in NI indicated that ~15% of badgers were infected. In GB, the ISG reported that in proactive cull regions, 16.6% of badgers were tuberculous whilst in reactive cull regions this figure was 14.9%.

Similarly, in the ROI, more detailed post-mortem examination of culled badgers from across the country revealed a prevalence of 36.3%. However, other studies found higher prevalence up to 43%, indicating the variation in estimates depending on sampling and laboratory methods. Using cage trapping, anaesthesia and live sampling of badgers Drewe et al. sensitivity of diagnostic testing was estimated at ~93% and badger TB prevalence was estimated subsequently as 20.8% in Woodchester Park, Gloucester. Regardless of “true” prevalence, these studies indicate that a significant component of the badger population across the UK and Republic of Ireland is infected with M. bovis, where bTB is also prevalent in cattle.

Britain and Ireland Have Some of the Highest National Cattle Densities in Europe. As has been described above for the European badger, the density of host organism available for infection by the TB causing bacilli seems to be of critical importance to ongoing transmission of disease and persistence. By analogy to bTB, Human tuberculosis, caused by M. bovis’ close relative, Mycobacterium tuberculosis, is typically associated with overcrowding in confined spaces. It is not surprising therefore that as with badgers, cattle densities will probably have an influence on bTB transmission dynamics. The countries that make up the islands of Britain and Ireland have notably high cattle densities in comparison with other European countries. In 2010, out of 27 countries within the EU, Northern Ireland had the highest mean cattle density of any country at 112 cattle per sq km. The Republic of Ireland was third (84 cattle per sq km), with Wales and England ranking 6 and 7th respectively (54 and 40 cattle per sq km). Scotland, who are now officially bTB free, are ranked 13th with a mean density of 22 cattle per sq km. To illustrate the differences amongst countries, the national herds are large relative to their area in Britain and Ireland, for example, both the Republic of Ireland and Spain have approximately 6 million cattle, yet Spain is 7.2 times the size of ROI (504,645 Spain/70,273 ROI sq km). Research suggests that both the size of herds and the intensity of farming  can be associated with increased risk of bTB breakdown in endemic countries. Larger herds may constitute greater risk as it may be more difficult to clear infection, once identified within the herd, due to the poor sensitivity of skin tests. The density of cattle within farms can be a proxy measure for the intensity of agricultural production, and has been associated with increased risk of bTB. At a macro-scale the risk of bTB increases with increasing intensity, primarily due to closer proximity between animals and potential infectious contacts. In Britain and Ireland there has been a move towards intensification, with a trend towards larger farm sizes, yet a decline in the absolute number of farms. Recent changes in dairy production at the EU level may exacerbate this pattern in the future.

Britain and Ireland Farming Characteristics That May Cause Difficulties in Managing Infections. Trade is a significant characteristic of cattle farming in the UK and Ireland, with significant patterns of movement that transcend national boundaries. Indeed, for example, in 2015 significant flows of animals traded over long distances, and also showed that movement metrics were a significant risk factor for bovine TB. While long distance movements occur and can potentially link disparate areas epidemiologically, the majority of trade moves are local. Recent analysis of trade networks in Northern Ireland has demonstrated that farms are extremely well connected, forming a robust network that is resistant to random and targeted node removal.

A crucial question for the viability of this hypothesis is how long can M. bovis persist in the environment? Previously, bacilli in badger urine were observed to survive on pasture for ~3 days in the summer and ~14 days in the winter potentially due to the differing intensity of solar UV radiation, which can kill the bacilli. A number of studies in different countries indicate that the survival of M. bovis in environmental matrices is variable. M. bovis in faeces or faeces-contaminated soil appears to remain viable for up to ~6 months in some studies. Findings indicated that M. bovis persisted for longer (up to 150 days) at cooler temperatures, whilst results for differing soil types were inconclusive.

Current and Future Climate Effects on M. Bovis Persistence in the Environment. Pertinent to this debate is the climate of the UK and Ireland compared to continental Europe. Britain and Ireland inhabit a zone of the globe whose predominant weather tends to be mild and wet without experiencing extremes in temperature. Both territories are islands, surrounded on all sides by the Atlantic Ocean and various seas. Indeed, the North Atlantic Oscillation is the primary driver of the maritime climate niche that Britain and Ireland occupy. Whilst there is variation across Britain and Ireland in climate – a general west to east cline in temperature, precipitation and sunlight is observed  – the general trend (even for south east Britain, which is most like the continent) is that both islands exhibit milder winters and cooler summers than continental neighbours. Indeed, records show that these islands receive less sunshine and more precipitation than other Western European countries. For instance, Britain did not completely eradicate bTB after initial success in reducing prevalence throughout the 1950 and 1960’s. Low level infection in cattle remained a problem with eventual recrudescence through the 1970–2000 s leading to the current impasse. It is plausible that an environmental reservoir may have played a role, alongside other factors, in preventing that final push to complete eradication. With changing climate in the future, the UK and Ireland are predicted to see even milder, wetter weather, with intra-regional variation in exact outcomes. The effect of weather conditions have been correlated with variation in M. bovis risk in cattle, and such weather variation has significant impact on the population dynamics of wild reservoirs also potentially impacting patterns of infection, adding to the complexity.

Conclusions. In this article we have attempted to propose potential reasons why the British and Irish experience in eradicating bovine tuberculosis has been so fraught compared to that of other jurisdictions in recent times. Our suggestions have arisen from a broad comparative approach which contrasts landscape, ecological, animal husbandry and molecular epidemiological characteristics within Britain and Ireland to those primarily observed on the wider European Continent. We note, with caution, that correlation is not causation. However for all proposed factors, we have endeavoured to present a coherent narrative, supported by published evidence, which links each to pertinent aspects of bTB epidemiology. We do not propose that these potential factors are exhaustive, merely that they may be worthy of further investigation, and individually or collectively may constitute novel hypotheses that go some way to explaining the comparative lack of progress in bTB eradication in these islands.