Tuberculosis in cattle herds are sentinels for Mycobacterium bovis infection in European badgers (Meles meles): the Irish Greenfield Study

In Ireland badgers are removed in response to tuberculosis (TB) breakdowns in cattle herds (focal culling). Prevalence studies, conducted using a detailed post mortem and bacteriological examination, showed that 36-50% of badgers were infected with Mycobacterium bovis. Focal culling forms part of the medium term national strategy for the control of bovine TB in cattle and is based on the premise that badgers in areas with herd breakdowns have a higher prevalence of infection than the badger population at large. However, the hypothesis that cattle can be used as sentinels for infection in the badger population has never been formally tested. In this study we tested the hypothesis by determining the infection prevalence in badgers in areas where there had been historically, a consistently low prevalence of infection in cattle. Low cattle TB prevalence areas were defined as those herds with ≤ 2 standard reactors in the annual round of skin testing over the preceding 5 years (Greenfield sites). Using GIS, and adjusting for variation in land use, previous culling and cattle density, 198 Greenfield sites were identified and surveyed, and 138 areas with badger setts or signs of badger activity were identified. A single badger was removed from 87 sites and all were examined using detailed post mortem and bacteriological procedures. A prevalence of M. bovis infection of 14.9% was found in the Greenfield site badgers. This prevalence was significantly lower (P<0.001) than in badgers removed during focal culling (36.6%). The results validate the use of cattle as sentinels for TB in badgers and support the medium term national strategy for the control of bovine TB. The geographic variation in M. bovis infection prevalence in the Irish badger populations will be used when devising strategies for the incorporation of badger vaccination into the long term bovine TB control programme.     

Quantifying badger exposure and the risk of bovine tuberculosis for cattle herds in county Kilkenny, Ireland

The objectives of the study were to quantify the levels of badger exposure for cattle and to test the hypothesis that increased badger exposure does not increase the risk of bovine tuberculosis (BTB) in a herd. Information that became available from the targeted removal of badgers over the study period, and from a badger-removal project in county Kilkenny, during 1996-1999 was used. The specific location of cattle within each farm, and the length of time that cattle spent in each farm field during the grazing season, and in the barnyard during winter, was used to build an exposure coefficient to quantify the amount of badger exposure that cattle encountered either on pasture or in the barn. The study design was a matched case-control study in which the control herds were selected using incidence density sampling. During the 4-year study period, 543 badgers were removed and of these 96 badgers were classified as tuberculosis positive; 96 BTB herd breakdowns occurred. There was a significant association between case herds and having a higher badger sett exposure coefficient during 1996-1998. No significant association between case herds and having a higher exposure coefficient based on the number of badgers, or the number of tuberculous badgers, during September 1997-December 1999 was found.     

Advances and prospects for management of TB transmission between badgers and cattle

Bovine tuberculosis (bTB) is the most serious endemic disease facing the livestock industry in the United Kingdom (UK) and Republic of Ireland (RoI), where its management has been confounded by the presence of persistent infection in the Eurasian badger (Meles meles). Field evidence suggests that the social structure of badger populations can have an important influence on disease dynamics, and on the outcome of management interventions. Recent, large-scale badger culling experiments in the UK and RoI had complex epidemiological outcomes. In the UK, proactive culling led to reduced bTB incidence in cattle herds inside culled areas, but a temporary increase in adjacent areas. Reactive culling in response to herd breakdowns was associated with an increase in the incidence of bTB in cattle. In contrast, badger culling in RoI was reported to have only beneficial effects on bTB incidence in cattle. The reasons for these differences are not clear. The complexity of the evidence base for culling is highlighted by the different management approaches currently being adopted by the different authorities of the UK and RoI. It is generally accepted that a holistic approach to bTB management, which targets both cattle and wildlife, is necessary. Consequently recent research activities have also focussed on cattle and badger vaccines, and biosecurity on farms. This paper describes recent advances in our understanding of the epidemiology of bTB in badgers and the consequences of culling, and current research to develop approaches for the vaccination of badgers, and methods of managing the risks of contact between badgers and cattle in farm buildings.     

Risk of tuberculosis cattle herd breakdowns in Ireland: effects of badger culling effort,density and historic large-scale interventions

Bovine tuberculosis (bTB) continues to be a problem in cattle herds in Ireland and Britain. It has been suggested that failure to eradicate this disease is related to the presence of a wildlife reservoir (the badger). A large-scale project was undertaken in the Republic of Ireland during 1997–2002 to assess whether badger removal could contribute to reducing risk of cattle herd breakdowns in four areas. During the period of that “four area” study, there was a significant decrease in risk in intensively culled (removal) areas relative to reference areas. In the present study, we revisit these areas to assess if there were any residual area effects of this former intervention a decade on (2007–2012). Over the study period there was an overall declining trend in bTB breakdown risk to cattle herds. Cattle herds within former removal areas experienced significantly reduced risk of breakdown relative to herds within former reference areas or herds within non-treatment areas (OR: 0.53; P < 0.001). Increased herd breakdown risk was associated with increasing herd size (OR: 1.92-2.03; P < 0.001) and herd bTB history (OR: 2.25-2.40; P < 0.001). There was increased risk of herd breakdowns in areas with higher badger densities, but this association was only significant early in the study (PD*YEAR interaction; P < 0.001). Badgers were culled in areas with higher cattle bTB risk (targeted culling). Risk tended to decline with cumulative culling effort only in three counties, but increased in the fourth (Donegal). Culling badgers is not seen as a viable long-term strategy. However, mixed policy options with biosecurity and badger vaccination, may help in managing cattle breakdown risk.

Electronic supplementary material

The online version of this article (doi:10.1186/s13567-014-0109-4) contains supplementary material, which is available to authorized users.     

Trial design to estimate the effect of vaccination on tuberculosis incidence in badgers

The principal wildlife reservoir of Mycobacterium bovis in Ireland is the European badger. Studies in the Republic of Ireland (RoI) have shown that badgers culled in association with cattle herd tuberculosis breakdowns (focal culling) have a higher prevalence of infection than the badger population at large. This observation is one rationale for the medium term national strategy of focal badger culling. A vaccination strategy for the control of bovine tuberculosis (bTB) in badgers is a preferred long-term option. The Bacillus Calmette-Guérin (BCG) vaccine has been shown to decrease disease severity in captive badgers under controlled conditions. As the vaccine has been tested in a controlled environment with precise information on infection pressure, it cannot be assumed a priori that the effects of vaccination are similar in the wild, where other environmental and/or ecological factors prevail. For this reason we have designed a vaccine field trial to assess the impact of vaccination on the incidence of TB infection in a wild badger population. The selected study area for the vaccine trial (approximately 755 square kilometers) is divided into three zones each of which has similar characteristics in terms of size, number of main badger setts, cattle herds, cattle and land classification type. Three vaccination levels (100%, 50% and 0%) will be allocated to the three zones in a way that a gradient of vaccination coverage North to South is achieved. The middle zone (zone B) will be vaccinated at a 50% coverage but zone A and C will be randomly allocated with 100% or 0% vaccination coverage. Vaccination within zone B will be done randomly at individual badger level. The objective of this paper is to describe the design of a field tuberculosis vaccination trial for badgers, the epidemiological methods that were used to design the trial and the subsequent data analysis. The analysis will enable us to quantify the magnitude of the observed vaccination effect on M. bovis transmission in badgers under field conditions and to improve our knowledge of the biological effects of vaccination on susceptibility and infectiousness.     

The Northern Ireland programme for the control and eradication of Mycobacterium bovis

Bovine tuberculosis is endemic in Northern Ireland and a comprehensive eradication scheme has been in operation since 1959. The current programme involves annual testing, extensive computerized tracing, short-interval testing of herds contiguous to outbreaks and compulsory slaughter of positive cattle. Despite initial reductions in disease prevalence, eradication has proved elusive and potential explanatory factors include high cattle density and potential for between-herd contact, the impact of exotic diseases on resource priorities, and significant levels of bovine tuberculosis in a wildlife reservoir, the European badger (Meles meles). Both the role of the infected bovine and that of the badger in spreading disease have to be addressed to ensure progress towards eradication. Current measures are described and future options for enhancing the programme are outlined.     

Efficacy of trapping during the initial proactive culls in the randomised badger culling trial

The randomised badger culling trial (RBCT) has shown that widespread badger culling in predefined areas of approximately 100 km2 led to a reduction in the number of cattle herds testing positive for bovine tuberculosis (TB) ('herd breakdowns'), but was associated with an increase in cattle tb in surrounding areas. This study has tried to estimate the trapping efficacy and the level of reduction of the badger population during the initial proactive culls in the RBCT. For seven triplets trapping efficacy was estimated between 71 per cent and 85 per cent, and for three triplets between 35 per cent and 46 per cent. Two of the latter triplets had trapping coinciding with harsh climatic conditions. Badger population removal was estimated at 64 per cent to 77 per cent in the former and 32 per cent to 39 per cent in the latter triplets. In most of the treatment areas there was therefore a consistent and substantial reduction in the number of badgers at the end of the initial cull. All the proactive treatment areas were subjected to further culls, and it is therefore likely that greater reductions would have occurred by the end of 2005, when the analysis of cattle herd breakdowns took place.     

Spatial relationship between Mycobacterium bovis strains in cattle and badgers in four areas in Ireland

We investigated whether strains (restriction fragment length polymorphism, RFLP-types) of Mycobacterium bovis isolated from badgers and from cattle clustered among and within four areas in Ireland. The spatial scan test and nearest-neighbor analysis were used as the spatial cluster-detection techniques. In addition, for each of the major strains, associations between the distance to badger setts and the "centroid" of the cattle farm were assessed in a logistic model. Overall, between September 1997 and May 2000, 316 and 287 M. bovis samples, from badgers and cattle, respectively, were strain-typed. The distribution of strains in badgers, and separately in cattle, differed among areas. Within each of the four large areas, badgers and cattle tended to have similar strains; this is consistent with the sharing of M. bovis strains within an area. In more detailed within-area analyses, some spatial clusters of M. bovis strains were detected, separately, in both cattle and badgers. Almost half of the infected badger setts with a specific strain were located outside of the "detected" clusters. There was no association between the number of infected badgers with a specific M. bovis strain within 2 or 5 km distances to cattle herds, and the risk of the same strain in cattle. We speculate about the dynamic nature of badger movements, as an explanation for the absence of more clusters of most of the strains of M. bovis isolated from badgers, and its impact on trying to study transmission of M. bovis between cattle and badger.     

The transmission of Mycobacterium bovis infection to cattle

The prevalence of Mycobacterium bovis infection in cattle is increasing rapidly in some countries, including the UK and Ireland. The organism infects a wide range of mammalian hosts, and eradication of the disease is difficult if there is an extensive reservoir in the wildlife population. Existing evidence suggests that wildlife vectors include the European badger in the UK and Ireland, the brush-tailed possum and ferret in New Zealand and ungulates in some other countries. Cattle grazing field boundaries or short swards are at particularly high risk, since the chance of contact with the intermediate host or their excreta is increased. There is evidence that the transmission of the disease between cattle following movement accounts for 10-15% of outbreaks in the British Isles and that transmission can occur across farm boundaries. The prevalence the prevalence of single reactors in herds suggested that within-herd transmission was not common. In herds with infected cattle, spreading slurry is a risk factor, which can be minimised by prolonged storage of the slurry, by spreading it on fields not used for grazing or by soil injection. M. bovis also survives in water and may enter the respiratory tract during drinking. It is concluded that M. bovis infection in cattle can be transmitted by a number of routes, some of which can be controlled by appropriate husbandry, but that circumstantial evidence suggests that the existence of a widespread intermediate host is the greatest contributor to infection in cattle.     

Vaccinating badgers (Meles meles) against Mycobacterium bovis: the ecological considerations

Bovine tuberculosis (TB) is a serious zoonotic disease, which despite a largely successful test and slaughter programme has persisted in cattle herds in parts of the UK. The badger (Meles meles) is widely considered to represent a significant wildlife reservoir for the transmission of Mycobacterium bovis to cattle, and has been the subject of a variety of culling strategies since the mid 1970s. Nevertheless, the incidence of herd breakdowns has continued to rise, and the efficacy of culling is currently the subject of a large-scale field trial. One potential alternative tool for the management of disease in wildlife populations is vaccination. However, the successful development of an effective vaccine and a strategy for its delivery will require careful consideration of the practical constraints imposed by ecological factors. In the current paper, we discuss relevant ecological and epidemiological characteristics of badger populations and practical aspects of vaccine delivery in the field.     

A case-control study on the association of selected risk factors with the occurrence of bovine tuberculosis in the Republic of Ireland

We did a case-control study on the association between the occurrence of bovine tuberculosis in herds in the East Offaly area and a number of possible risk factors: herd size, the purchasing of cattle, the herd history, the status of contiguous herds, distance to the nearest badger sett, and animal factors such as age, breed and animal type. The characteristics of 100 herds that had a confirmed outbreak of tuberculosis at a herd test in 1988 were compared with those from an equal number of herds that passed at least one tuberculin test during that year. The study base consisted of 1379 herds mainly from the eastern part of County Offaly. The data were analysed at both herd and animal levels. Factors that were associated with an increased risk of tuberculosis breakdowns at the herd level were (i) the total number of animals in the herd and (ii) the restriction of a contiguous herd for tuberculosis within a period of 6 months prior to or following the herd under study. A number of factors were associated with an animal having an increased risk of failing a tuberculin test. After adjusting for all other variables in the model, cows, heifers and bullocks were 10.3, 14.8 and 8.0 times, respectively, more likely to fail a tuberculin test than calves. Cattle that had teen purchased since the previous herd test were less likely to fail a tuberculin test compared with cattle that had been present at the time of the preceding herd test.     

Survey of badger access to farm buildings and facilities in relation to contact with cattle

Thirty-six farms in parishes in western England that had recently experienced herd breakdowns of bovine tuberculosis were surveyed for signs of badger activity and for husbandry practices relating to the access of badgers to the farm buildings and facilities. Signs of activity were detected within the farmyards and buildings of 14 of the farms and were associated with water troughs at pasture on two of them. Few of the farmers implemented practices to reduce contact between badgers and cattle. Stored cattle feed was freely accessible to wild animals in 88 per cent of the feed stores. Two badger carcases, and two of 66 samples of badger droppings, cultured positive for Mycobacterium bovis. Signs of badgers within farmyards were significantly positively associated with the number of badger setts and latrines in the immediate vicinity, but were not related to any recorded farm husbandry procedures.     

A cost-benefit analysis of culling badgers to control bovine tuberculosis

Bovine tuberculosis (TB) is an important economic problem. The incidence of TB in cattle herds has steadily risen in the UK, and badgers are strongly implicated in spreading disease. Since the mid-1970s the UK government has adopted a number of badger culling strategies to attempt to reduce infection in cattle. In this report, an established model has been used to simulate TB in badgers, transmission to cattle, and control by badger culling. Costs were supplied by the UK Government's Department for Environment Food and Rural Affairs (Defra) for badger trapping and gassing. Regardless of culling intensity or area simulated, an overall reduction in the herd breakdown rate was seen. With a high culling efficacy and no social perturbation, the mean Net Present Value of a few simulated culling strategies in an "ideal world" was positive, meaning the economic benefits outweighed the costs. Further work is required before these results could be considered definitive, as it is necessary to evaluate uncertainties and simulate less than perfect conditions.     

Factors influencing the incidence and scale of bovine tuberculosis in cattle in southwest England

Bovine tuberculosis (TB) in cattle is a major economic problem in Britain. In the past 25 years, the infection has been concentrated in the southwest region of England. We investigated the effects of agricultural and farm-management characteristics on the occurrence and scale of TB in cattle in the region (1988-1996) using logistic and linear regression. Factors relating to the existence of previous infection in cattle and the management of cattle and badgers are all linked to the incidence of the infection--but those related specifically to the management of cattle are of overriding importance in determining the scale of the problem. Although our analysis was conducted at a large spatial scale, the results suggest that improvements to the procedure for testing and managing TB in cattle, reductions in cattle stocking density, a greater human input in herd management and more-carefully targeted badger culling all might contribute to reducing the incidence and/or number of herd breakdowns.     

Detection of Mycobacterium bovis infection and production of interleukin-2 by in vitro stimulation of badger lymphocytes

The Eurasian badger (Meles meles) is considered to be an important wildlife reservoir for Mycobacterium bovis infection of cattle in Ireland and in GB. However, rapid diagnosis of tuberculosis in live badgers has been constrained through a lack of suitable immuno-diagnostic reagents for detection of M. bovis-infected animals. To date, there have been no reports of cytokine activity in badgers that might be associated with specific immune responses to M. bovis infection. In this study, nine badgers were removed from an area with a persistent tuberculosis problem in cattle herds and tuberculosis was confirmed in four of the animals by "post-mortem" examination and M. bovis culture. In preliminary investigations of interleukin-2 (IL-2) activity, we were able to demonstrate that lymphoblasts prepared from badger peripheral blood mononuclear cells (PBMCs) proliferated when cultured in the presence of human recombinant IL-2 (HrIL-2). Supernatants derived from purified protein derivative of tuberculin (PPD-bovine) stimulated PBMC cultures also induced blastogenesis of badger-derived lymphoblasts. The results demonstrate that badger lymphocytes are responsive to HrIL-2 and that PPD-bovine stimulation of badger PBMC results in production of bio-active IL-2.     

Targeted badger removal and the subsequent risk of bovine tuberculosis in cattle herds in county Laois, Ireland

We investigated the impact of targeted removal of badgers on the subsequent bovine tuberculosis (BTB) risk in cattle herds in county Laois, Ireland. The study period was 1989-2005. For each of 122 targeted badger-removal licenses (permit to remove badgers in the proximity of cattle herds undergoing a serious BTB episode), the herd number (index herd) for which the license was given was obtained. The herds in the proximity of the index herd were identified from another database. The main "exposure" in our study was the geographical location of herds relative to the area in which targeted badger removal was conducted. We categorized herds into five different exposure groups: herds were classified as non-exposed and denoted as group 0 (reference group) if they were located 500 m or more from the edge of any parcel of land of the index herd; group 1, was the index herds, group 2 the immediate (contiguous) neighbors of the index herd, group 3 herds were not immediate neighbors but within 150 m and group 4 herds were between 150 m and 500 m distance from the edge of any parcel of land of the index herd, respectively. We conducted a survival analysis (allowing multiple failures per herd) to compare the hazard of having a BTB episode in any of the four groups of exposed herds vs. the hazard in herds in the reference group. We controlled for other known risk factors as well taking into account a temporal component. Our analysis showed that the hazard ratio for the index herds (group 1) were non-significantly increased, indicating that there was no difference in the hazard of failing a BTB test (after the targeted badger removal was conducted) between index herds and reference herds. For the rest of the herds farther away from badger removal activities the hazards were lower than herds in areas not under badger removal. The hazard in the reference group decreased over the study period.     

An all-island approach to mapping bovine tuberculosis in Ireland

This study used techniques in Geographical Information Systems (GIS) to explore the spatial patterns of bovine tuberculosis (TB) in the whole island of Ireland over an 11-year period. This is the first time that data pertaining to TB from the Republic of Ireland and Northern Ireland have been collated and examined in an all-Ireland context. The analyses were based on 198, 156 point locations representing active farms with cattle in Northern Ireland and the Republic of Ireland between the years 1996 and 2006. The results consist of a series of maps giving a visual representation of cattle populations and associated detected bTB levels on the island of Ireland over this time interval.     

Geographical association between the genotype of bovine tuberculosis in found dead badgers and in cattle herds

In a survey, 457 badgers that had been found dead in Wales were postmortem-examined, and samples were examined by histology and by extended culture (for up to 12 weeks). Mycobacterium bovis was cultured from 55 badgers (12.0 per cent), and the histology typical of M bovis infection was seen in a further six (1.3 per cent). The prevalence in badgers in each of 10 geographical areas varied between 0 and 26 per cent (P<0.001), and was associated with the incidence of confirmed M bovis infection in cattle herds in the same areas (P<0.01). In northern Wales, bTB was rare in both hosts. An infected badger was 12.3 times more likely to be within 5 km of a confirmed cattle bTB breakdown than an uninfected badger. The M bovis isolates from badgers belonged to one of four genotypes defined by spoligotype and variable number tandem repeat type. These genotypes were also found in 290 concurrent confirmed herd breakdowns, and tended to be similar to the genotypes in badgers in the same geographical areas. When badgers and cattle no more than 30 km apart were compared, the genotype diversity was greater in cattle than in badgers (P=0.016), suggesting that the movement of cattle plays a greater part in the spatial distribution of M bovis than the movement of badgers.     

The association of cattle husbandry practices, environmental factors and farmer characteristics with the occurence of chronic bovine tuberculosis in dairy herds in the Republic of Ireland

A matched case-control study was undertaken to provide information on the role of farm management practices, environmental factors and farmer characteristics in the epidemiology of bovine tuberculosis. Eighty dairy herds with chronic tuberculosis were compared with the same number of herds which had been free of the disease for many years. A standardized questionnaire was used to obtain information from the farmers. the study was conducted from August to October 1990, in Counties Cork and Kilkenny, Republic of Ireland.

Factors which were identified as possibly contributing to recurrent outbreaks of tuberculosis outbreaks included nutritional factors, cattle purchases (especially bulls), the presence of badgers, and the spreading of slurry. Overall, the findings suggested that intensively managed dairy herds were at greater risk of bovine tuberculosis outbreaks than were other herds.

The study did not support some of the hypotheses which traditionally have been put forward as contributing to tuberculosis outbreaks. These included contact with neigboring cattle owing to movements to and from fragments or poor boundary fencing, presence of sub-standard cattle housing, movement of equipment or vehicles onto farms, and exposure to water supplies from rivers or streams. In the light of these findings, and in view of the lack of evidence in the scientific literature to support these hypotheses, we suggest that a general re-evaluation of their role in chronic tuberculosis is needed.