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Bovine tuberculosis, culling and agriculture: The Eurasian badger as a source of conflict in the UK



Since the inception of widespread agriculture, thought to have proliferated across the globe from around 11,000 years ago during the Neolithic revolution (Diamond and Bellwood, 2003) man has encountered biological pests, responsible for reductions in agricultural yields. Animal pests particularly have been documented in a wide range of taxa that cause damage through direct means – often through feeding on crops or livestock, or indirect means – through the transference and propagation of agriculturally damaging pathogens and diseases. Damage caused by pests historically has led to conflict arising between them and farmers (Headley, 1972), and hosts of novel wildlife control methods have been adopted in the pursuit of damage limitation.

Throughout Britain, the Eurasian badger (Meles meles) has acquired a reputation as a pest, in small part by direct agricultural damage caused towards crops, livestock and infrastructure (Honda, 2018; Johanna et al., 2017; Moore et al., 1999). More prevalently, however, the Eurasian badger has been labelled in this manner due to its perceived role as a considerable wildlife vector and transmitter of bovine tuberculosis to agricultural livestock, most notably cattle (Godfray et al., 2013; Lodge and Matus, 2014). Where countries within the UK are not distinct in having a wildlife reservoir for the disease or having currently implemented culling policies adopted to limit wildlife induced spread, for example, the brushtail possum, in New Zealand (Ryan et al., 2006), the white-tailed deer in the USA (Carstensen et al., 2011) and the wild boar in Spain (García-Jiménez et al., 2013), the disproportionate levels of controversy surrounding the Eurasian badger's role in Bovine tuberculosis spread and culling as an appropriate wildlife control method here are unprecedented (Enticott, 2015).



What is bovine tuberculosis and why is it a problem?

Bovine Tuberculosis is a zoonotic, bacterial disease characterised through the development of tubercles or lesions in the respiratory tract, lymph nodes or lung tissue of the host (Ayele et al., 2004; Banos et al., 2017). Cattle are recognised as true hosts for the disease; however, humans, a host of wildlife including foxes, mice, deer (Delahay et al., 2007) and agriculturally or otherwise domesticated animals including sheep, goats, pigs, cats and dogs are vulnerable to infection (Ayele et al., 2004). The M. Bovis bacterium is thought to most frequently transmit through aerosol following direct contact between an infected and healthy individual, but can also pass indirectly, through urine, faecal matter, via the placenta, via the environment and also through unpasteurised milk or infected meat (O'Mahony, 2014).

In the UK, around 85 years ago, 40% of cows were thought to be infected with M.bovis (Sharp, 2006) and 50,000 new human cases of the disease were recorded annually, resulting in fatality rates of one in twenty (Reynolds, 2006). Where the risks to human health are now considered slight in the UK (Davidson et al., 2017), likely due to advancements in meat hygiene regulations and mandatory milk pasteurisation procedures, the existence of the disease remains an economic complication in agriculture. The infection of a cow within a herd not only directly decreases the value of the animal itself - in the majority of developed countries slaughter of an infected individual is mandatory, but also leads to additional local movement and trade restrictions, leading to considerable indirect losses for the farmer (Godfray et al., 2013). On top of this, international trade regulations sanctioned by the EU deem any cattle product infected with BTB unfit for international trade (Enticott, 2015).



A History of the disease in Europe

Throughout Europe, the first legal initiatives to combat the spread of bovine tuberculosis occurred

In 1964, as its existence was recognised to be unsustainable, owing to its potential for extensive economic losses (Reviriego Gordejo and Vermeersch, 2006). Since these first legal initiatives came to fruition and control methods underwent, many European nations earned OTF (officially tuberculosis free) status – where the percentage of herds confirmed as infected within a country does not exceed 0.1% for six consecutive years (Reviriego Gordejo and Vermeersch, 2006). Examples of the countries declared OTF since 1964 include Denmark, The Netherlands, Germany, Austria, Belgium and Scotland, amongst others (Allen et al., 2018). Where these nations have been able to eradicate BTB to a degree deserving of this OTF label, Ireland, England and Wales have struggled more distinctly.


Figure 1 - BTB incidence throughout Britain according to the last quarterly review (released on the16th Sept, 2020) from DEFRA (The Department for Environment Food & Rural Affairs) (1).



Current policies adopted throughout the UK

Throughout the UK, a range of policies have been adopted to reduce the spread of BTB. Firstly, a range of initiatives have been adopted to influence farming practices and agriculture, mostly to prevent cattle to cattle transmission. Among these Initiatives are the surveillance testing of cattle annually or six-monthly depending on the level of disease incidence in the area, pre-movement testing of herds, movement restrictions on infected herds, Increased biosecurity on farms and the slaughter of infected animals (Enticott, 2018a; Gwenllian et al., 2017).

In addition to these agriculturally directed policies, in recognition of the badger as a potential disease transmission source, ongoing culling and vaccination initiatives are in place across the UK (Enticott, 2018a). Though both wildlife control methods see implementation within England, Ireland and Wales, each country carries out these policies in varying degrees. Generally speaking, throughout Wales vaccination is the more comprehensive and preferred approach and the threshold for culling here is higher than in England and Ireland (in Wales, culling is carried out ‘only where evidence suggests badgers to be contributing towards the persistence of Bovine TB in chronic breakdown herds’). In England, although vaccination is used, culling has been adopted more substantially, and the English ‘blanket cull’ approach currently adopted exceeds the Welsh scope in range, number and selectivity threshold. Culling in Ireland compared with Wales requires a lower threshold to be fulfilled: culling is approved where badgers are considered the ‘probable cause’ for disease spread to cattle herds (Byrne et al., 2015), compared to England however, the scope of this culling is lower.

Stances adopted by the UK governments have generated conflict, not only between farmers and badgers but between farmers and the government, scientists, charities, independent organisations and the general public whose opinions on the level to which badgers are involved in disease transmission and opinions on future routes that should be adopted to limit disease spread do not align (Price, 2017).



Sources of conflict

For many farmers in the UK, the existence of infection within badger populations is a more significant cause of disease spread than current efforts defined through legislature might suggest (Cassidy, 2012). These opinions might source from scientific research, where BTB is suggested to transmit from badgers to cattle in levels of significant abundance.


Firstly, evidence suggestive of badgers’ influence over disease spread to cattle has been shown through strain typing analysis conducted on M. Bovis strains across the UK and Ireland within the same regions. Results found strains in badgers and cattle sharing similar geographic clusters to exhibit high levels of genetic similarity indicative of transmission between the two animals (Goodchild et al., 2012; Skuce et al., 2010). This said, the transmission direction has proven hard to determine in these studies, the blame might be directed more heavily towards the badger due to the magnitude of damage farmers experience as a result of transmission from badgers to cattle (rather than vice versa) due to the test and slaughter approach adopted for infected individuals.


Secondly, a range of post-mortem examinations have suggested the level of infection within badger populations as high. In Great Britain, prevalence recently has been estimated to sit at around 15% subject to regional variations (Bourne et al., 2007), similar estimations in badger BTB prevalence were made at 12.1% in Ireland (Murphy et al., 2010). On top of this, the abundance of badgers throughout England, Wales and Ireland is a considerable number. In England and Wales alone this abundance is estimated to sit between 391,000-581,000, and is thought to be rising (Johanna et al., 2017). These two points: high levels of infection and high abundance are suggestive of a vast pool of infection with great transmission potential. On a similar note, large scale studies on the epidemiology of BTB not only in Great Britain but in the Republic of Ireland and Northern Ireland have reported significant associations between badger density and the likelihood of a breakdown in cattle herds (Bessell et al., 2012; Byrne et al., 2014; Wright et al., 2015). Britain and Ireland are currently thought to have the highest densities of badgers across Europe (Byrne et al., 2012), and are also the regions within Europe that have some of the highest BTB incidences (Allen et al., 2018).


Under the current protection of badger’s act of 1992, it is illegal to wilfully kill, harm or recklessly damage or destroy any part of a badger sett in the absence of a pardon (Rollin, 2017). This level of protection afforded to the badger is unique for a wild animal not considered to be rare (Macdonald and Newman, 2002) and is blamed by some farmers as the reason for badger populations being ‘out of control’ and ‘out of balance’ (Maye et al., 2014).

Reports of successes such as those seen after a four-year cull between 2013 - 2017 in Gloustershire and Somerset, that indicated a reduction of confirmed BTB incidence of 66% and 37% respectively in comparison to areas that were subject to no culling over the same period (Downs et al., 2019), might be seen as evidence for culling efficacy. Additionally, in the Republic of Ireland, in 2005, the ‘Four Areas Trial’ cull found reductions in TB incidence ranging from 51% to 68% over five years in specific locations (Griffin et al., 2005).

Culling successes in these examples have given rise to dubiousness amongst those in contention of the practice due to reports of bad science and cherry-picking of data to push through further legislature (Barkham, 2016; Naylor et al., 2017). This ‘Anti-cull’ demographic, generally comprising of the general public, a host of vociferous charities and independent organisations as well as a handful of scientists (Cassidy, 2012; McCulloch and Reiss, 2017a) have together contributed substantial opposition against badger culling (Jenkins et al., 2010; McCulloch and Reiss, 2017b) and instead prefer further vaccination and agricultural restrictions. Part of this preference might source from scientific evidence pointing away from the efficacy of badger culling (McCulloch and Reiss, 2017a).


Evidence in this regard firstly comes from 1996, where John Krebs, a scientist commissioned by the UK government to review any evidence as to whether badger culling justifies implementation summated findings to be ‘inconclusive’, and stated that further research was necessary before policy adoption (Cassidy, 2012). Secondly, results yielded from randomised culling trials in England between 1998-2008 concluded that the project, which cost the government £50 million failed at being cost-efficient, and that implementation of the project cost more money than it saved through disease spread prevention. After a freedom of information request submitted by the badger trust, the cost of culling one badger was revealed to be around £6775 (McCulloch and Reiss, 2017b), evidence which suggests poor resource management. In addition to financial factors, culling has demonstrated to accentuate disease spread through inducing perturbations in badger roaming ranges (Woodroffe et al., 2006). This phenomenon has been provided additional research-based support in Carter et al., 2007; Weber et al., 2013 and Vicente et al., 2007, where culling was shown to interrupt social stability in badger populations, leading to an expansion in roaming ranges and increasing the likelihood of epidemiological spread to previously unaffected geographic locations.

Where ‘anti-cull’ demographic preferences for vaccination and agricultural restrictions might source from these examples proving culling to be inefficient, these preferences might alternately source from an ethical viewpoint, where these two practices are preferred due to being perceived as less cold-hearted (Rollin, 2017). Views in this respect may have intensified after information revealing trapping and shooting of badgers as part of the English cull failed in meeting the humanness criteria of acceptability (McCulloch and Reiss, 2017a). Additionally, worries regarding local population extinctions might shape these opinions, where some might view killing 70% of the local population as unacceptable (Donnelly and Woodroffe, 2012). Those against culling might view the current efficiency of vaccination as ample evidence justifying its use. The currently used BCG vaccine has been found to significantly reduce the number and severity of lesions caused by bovine tuberculosis in laboratory settings (Chambers et al., 2011) and exhibited up to 79% immunity in certain groups of vaccinated cubs in the wild (Carter et al., 2012).

Figure 2 - A protest in Derbyshire (6th sept, 2020) where anti-cull wildlife lovers demonstrate their anger towards the English government's decision to shoot an estimated 62,000 badgers this autumn to control BTB (2).



Those as part of the ‘anti-cull’ demographic might additionally point towards agricultural restrictions as a more viable method to control disease spread after a host of studies suggested agricultural factors to contribute significantly towards BTB spread. Firstly, research has suggested the size of a herd, as well as the intensity of farming can contribute towards larger BTB breakdown risks (Humblet et al., 2009). Throughout Britain and Ireland in recent years there has been a shift towards agricultural intensification, which involves an overall reduction in the number of farms but an increase in farm size (Brooks-Pollock and Keeling, 2009; Mee John, 2004). Where this phenomenon is not independent to the UK, this shift has led to cattle densities here accelerating beyond those observed in other European countries (Allen et al., 2018). For example, Northern Ireland currently has the highest cattle densities seen in any European country, the Republic of Ireland places third in this list, and England and Wales place sixth and seventh respectively (Hardstaff et al., 2014). Scotland, another country within the UK which was labelled OTF in 2009 (Allen et al., 2018) places 13th in this list. This evidence might be seen to some as farmers not taking responsibility, not acknowledging the shortcomings of the industry they are part of and using the Eurasian badger as a scapegoat (Price, 2017).



Future directions

Moving forward, one area that should receive greater levels of attention is an improvement in the level of communication between the UK governments and cattle farmers. Although farmer’s opinions should not be used as a basis for policymaking, the appeasement of farmers (who are the individuals largely responsible for the implementation of any top-down governmental policies) should be considered as an area of greater importance. Farmers have been observed to rely on their judgements and personal perceptions where evidence provided is not trusted (Palmer et al., 2009), a factor that must be minimised if concise BTB eradication programmes are to yield any future successes.

Though farmers have been found to exhibit distrust in the government and scientists, feelings rooted from both the foot and mouth outbreak of 2001 and currently, the BTB outbreaks (Bickerstaff and Simmons, 2004; Enticott, 2015; Enticott, 2008), greater levels of trust are thought to exist between them and veterinarians. Due to this fact and owing to the veterinarian’s role as a trusted expert, relied heavily upon by farmers for combatting disease (Enticott et al., 2012; Hernández-Jover et al., 2012), the implementation of policy changes and upkeep of existing policies should be communicated through them rather than directly from the government. Despite these higher levels of trust, the expert opinions in disease epidemiology of vets are not thought to be utilised fully in certain scenarios (Richens et al., 2015; Ruston et al., 2016), and so initiatives should be put in place to strengthen this relationship and increase discourse between the two parties. Through the use of this relationship, ambiguity regarding the causal link between policies implemented and how this prevents disease spread explicitly (a factor found to affect a farmer’s decision whether or not to further carry out suggested actions (Alarcon et al., 2014; Garforth et al., 2013)) might be reduced, potentially leading to policies being followed with greater rigidity and enthusiasm (Enticott et al., 2012; Toma et al., 2013).

On a laboratory research related note, and more generally, a better understanding of the bacteria is thought to be necessary if further progress in eradication is to be achieved (Robinson, 2019) and additionally, the question of how to prevent the spread remains a question largely unanswered (Naylor et al., 2017). Ongoing research into methods for disease transmission prevention might partially solve these issues. One such method is an oral vaccination currently being worked on which may prove more effective than the current injections administered. The oral vaccine is effective in an experimental setting for badgers (Murphy et al., 2014) but must in the future demonstrate efficacy in a wild setting as well as demonstrate effective value for money and time-saving capability. Currently, the dose required for oral administration is higher than that of injection due to gut degradation, therefore current research is focusing on maintaining BCG viability up until the point it reaches the intestine (Tompkins et al., 2009) which would make it cost-efficient in the future. Development in this regard to a level where it becomes more efficient than the current cost of the injectable vaccine, which is estimated to be around £2000-£4000 per Km2 (Chambers, 2014) might aid in disease eradication. The development of an oral vaccine for rabies, which was once common throughout Europe and North America was noted as one of the major factors in controlling its spread (Brochier et al., 1991; Slate et al., 2005), development of a BTB oral vaccine might replicate successes seen in this example.

Another method currently being worked on is the development of a new, novel BCG vaccine. The currently used BCG vaccine is not used on cattle throughout the UK due to it being indistinguishable from the actual infection through the most commonly used testing method (Tuberculin skin test (PPD)). Scientists at the University of Surrey have developed a novel vaccine which looks as though it protects cattle but also reveals itself as a harmless strain of M.bovis using PPD testing (Chandran et al., 2019). Though the development is still in its early stages, the progress that is being made looks promising. If this new strain proves effective, it would allow farmers to vaccinate cattle and to accurately identify these protected individuals, thus providing immunity in the long - term and reducing the number of cattle that would need to be slaughtered. This development would reduce

blame on badgers for transmitting the disease and reduce conflict overall.



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Images

1)https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/918098/bovinetb-gb-quarterlyoverview-16sep20.pdf

2) https://greenworld.org.uk/article/fury-badgers-culled-vaccination-zones


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