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.     

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.     

Cattle-to-cattle transmission of bovine tuberculosis

In developed countries, Mycobacterium bovis infection in cattle is now mostly confined to the respiratory system, which reflects transmission and establishment of infection mainly by this route. A single bacillus transported within a droplet nucleus is probably sufficient to establish infection within the bovine lung. Infected cattle should always be considered as potential sources of infection, since studies have demonstrated that a significant proportion of tuberculous cattle excrete M. bovis.In general, the dynamics of M. bovis transmission are poorly understood and the conditions under which a tuberculous animal becomes an effective disseminator of infection are currently not defined although environmental contamination appears to be a less effective method of disease transmission. Field studies indicate a wide spectrum of transmission rates but generally the spread of M. bovis infection is still considered to be a relatively slow process. Slaughter of diseased cattle detected by tuberculin testing and at meat plant inspection has been shown to be an effective policy for tuberculosis eradication, provided there are no other reservoirs of infection and all involved in the cattle industry are committed to a policy of eradication. Epidemiological approaches, particularly case-control studies, seem to provide the best method for quantifying the relative importance of the various sources of M. bovis transmission to cattle and modelling techniques can be used to assist in the design of cost-effective control measures that may lead to tuberculosis eradication.     

Effects of farm management practices on cattle grazing behaviour and the potential for transmission of bovine tuberculosis from badgers to cattle

Despite the large body of circumstantial evidence to suggest a link, the means by which bovine tuberculosis is passed from badgers to cattle remains unclear; pasture contamination with the urine, faeces and/or sputum of infectious badgers is believed to be the main route of transmission. Therefore the behaviour of grazing cattle was studied to determine whether they avoided investigating and/or grazing pasture contaminated with badger excreta, and whether different farm management practices enhanced the potential for disease transmission. Active latrines were avoided by most cattle until the sward length in the rest of the field was reduced, after which there was an increasing likelihood that active badger latrines would be grazed. Most of the cattle grazed active badger latrines, but cattle of low rank within the herd grazed latrines more heavily. Farm management practices that reduced the availability of long swards shortened the period of investigative behaviour and greatly enhanced the risk that cattle would graze active badger latrines. Cattle were more likely to graze pasture away from latrines that was contaminated either with badger urine or single faeces. Because bacilli remain viable in the soil for up to 2 years, there is the potential for bacilli to accumulate at active badger latrines, and these could pose a significant risk to cattle, even when the latrine is no longer being used by badgers. Cattle readily grazed the lush sward at disused latrines, during which they could ingest contaminated soil; the amount of soil ingested increases as sward length decreases.     

Tuberculosis in cattle: strategic planning for the future

In the later stages of eradication of tuberculosis in cattle there is a need to take account of the fact that Mycobacterium bovis infection in cattle presents, not as cases of clinical disease but most commonly as apparently healthy animals showing an immunological response to tuberculin. This is an entirely different scenario to that seen when national eradication programmes were first devised, at a time when the protection of public health rather than animal health was the prime motivation. In countries with active programmes to eradicate bovine tuberculosis, it is critical for the programme's success that account is taken of this redefinition of tuberculosis, side by side with changes in modern animal production systems and their impact on the transmission of M. bovis. This paper highlights factors critical to the success of a national eradication programme, including a clear identification of the goals, of the policies that guide actions, and of the sequences of actions that are required within the programme to accomplish these goals. Experience has illustrated the adverse effects of compromise on outcome when the application of fundamental principles of disease control such as sound animal management, removal of known sources of infection, early diagnosis, quarantine, movement control and environmental hygiene are less than enthusiastically promoted and applied. The reality is that where these principles are applied in a sustained manner, the outcome is more likely to be successful. Therein lies the challenge for the risk manager.     

Predicted costs and benefits of eradicating BVDV from Ireland

Bovine viral diarrhoea virus (BVDV) causes an economically important endemic disease (BVD) of cattle in Ireland and worldwide. Systematic eradication by detection and removal of infectious (BVDV carrier) cattle has been successful in several regions. We therefore assessed the benefits (disease losses avoided) and costs (testing and culling regime) of a potential eradication programme in Ireland. Published bio-economic models of BVDV spread in beef suckler herds and dairy herds were adapted to estimate potential benefits of eradication in Ireland. A simple model of BVDV spread in beef finisher herds was devised to estimate the benefits of eradication in this sector. A six year eradication programme consisting of 5 inter-related virological and serological testing programmes is outlined and costed. We found that the annualised benefits of BVDV eradication in Ireland exceeded the costs by a factor of 5 in the beef suckler sector and a factor of 14 in the dairy sector. Corresponding payback periods were 1.2 and 0.5 years respectively. These results highlight the significant economic impact of BVDV on the Irish cattle industry and suggest a clear economic benefit to eradication using the proposed approach. This type of cost-benefit analysis is considered an essential prerequisite prior to undertaking an eradication campaign of this magnitude.     

The impact of badger removal on the control of tuberculosis in cattle herds in Ireland

In Ireland, the herd prevalence of bovine tuberculosis has remained stable for several decades, and in common with several other countries, progress towards eradication has stalled. There is evidence in support of the potential role of infected badgers (Meles meles, a protected species) in bovine tuberculosis in Ireland and Britain. However, this evidence on its own has not been sufficient to prove disease causation. Field trials are likely to offer the best opportunity to define this role. Building on the earlier East Offaly project, our objectives were to assess the impact of badger removal on the control of tuberculosis in cattle herds in Ireland.

The study was conducted from September 1997 to August 2002 in matched removal and reference areas (average area of 245.1 km²) in four counties: Cork, Donegal, Kilkenny and Monaghan. Badger removal was intensive and proactive throughout the study period in the removal areas, but reactive (in response to severe tuberculosis outbreaks in cattle) in the reference areas. Removal intensity in the removal and reference areas during the first 2 years of the study averaged 0.57 and 0.07 badgers/km²/year, respectively.

The outcome of interest was restriction of cattle herds due to confirmed tuberculosis, where tuberculous lesions were detected in one or more animals. Data were analysed using logistic regression (modelling the probability of a confirmed herd restriction) and survival analysis (modelling time to a confirmed herd restriction).

During the study period, there was a significant difference between the removal and reference areas in all four counties in both the probability of and the time to a confirmed herd restriction due to tuberculosis. In the final year of the study, the odds of a confirmed herd restriction in the removal (as compared to the reference areas) were 0.25 in Cork, 0.04 in Donegal, 0.26 in Kilkenny and 0.43 in Monaghan. Further, the hazard ratios (removal over reference) ranged from 0.4 to 0.04 (a 60–96% decrease in the rate at which herds were becoming the subject of a confirmed restriction).     

An update on bovine tuberculosis programmes in Latin American and Caribbean countries

Of the approximately 374 million cattle in Latin America and the Caribbean, 70% are held in areas where rates of Mycobacterium bovis infection in cattle are higher than 1%. The remaining 30% are in countries where infection affects less than 1% of cattle, including 62 million in countries where bovine tuberculosis infection is virtually nil. Measures for controlling bovine tuberculosis are partially or extensively applied in most of the countries in the Region. These measures are based on test and slaughter, notification, post-mortem inspection and surveillance in slaughterhouses. A coordinated production, standardization and quality control of purified protein derivatives is urgently required for use in control and eradication campaigns in order to assure reliability of reagents and comparability of data on tuberculin testing within the Region. On the basis of information from Argentina, M. bovis is estimated to cause 2% of all human cases of tuberculosis in the Region. Slaughterhouse and dairy farms workers are most-frequently infected, with infection occurring via the respiratory tract. Various in vitro assays for the diagnosis of bovine tuberculosis have been developed and/or assessed in the Region, and DNA fingerprinting has been applied for a comprehensive understanding of the epidemiology of bovine tuberculosis at the local and regional level.     

Bovine viral diarrhea (BVD) eradication in Switzerland--experiences of the first two years

A national eradication programme was designed with the aim of achieving total freedom from bovine viral diarrhea virus (BVDV) infection in the Swiss cattle population. The eradication programme consisted of testing every Swiss bovine for antigen, culling virus-positive animals and applying movement restrictions. Starting in 2008, the campaign achieved the goal of reducing the proportion of newborn calves that were virus-positive from 1.8% to under 0.2% within two years (situation in September 2010). Both good data flow between the parties involved as well as speed and efficiency (e.g. concerning the application of tests, movement restrictions and slaughter) are central to the success of the programme. Since the beginning of the programme 2.85 million cattle have been tested for bovine viral diarrhea virus (BVDV). The BVD-prevalence in cattle at the individual and herd levels following the implementation of the eradication programme was assessed. Using data collected during this campaign a risk factor analysis was conducted in order to identify factors associated with the appearance of virus positive newborn calves in herds where BVD had not previously been detected; these risk factors would allow targeting of future surveillance. Herd size, early death rate (i.e. the number of animals that either die before 15 days of age or are stillborn per number of newborns per year), buying in stock, using communal summer grazing, production type, age structure and management strategy were factors associated with the appearance of new cases of infection. Testing of newborn calves for antigen will continue to be conducted until the end of 2011, this is combined with outbreak investigation of newly infected herds (consisting of re-testing dams of virus-positive calves and if necessary all cattle on or that recently left the farm). This process is done to identify infected animals that may have been missed during prior testing (false negatives), it also serves to identify other factors that may be responsible for the introduction of BVDV onto the farm. Since October 2009, testing of calves for antigen combined with outbreak investigation has led to the detection of 55 infected animals that had tested negative (presumably false negative) during previous rounds of testing.     

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.     

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.     

Bovine tuberculosis in Northern Ireland: a case-control study of herd risk factors

This paper presents the results of the first formal epidemiological study in Northern Ireland of risk factors for bovine tuberculosis (TB) associated with farm boundaries, neighbours and wildlife. The study was designed as a case-control study and 427 dairy herds were investigated between December 1993 and January 1995. The case herds had more than 30 cattle, and herds in which the source of infection had been ascribed to purchased cattle were avoided. Data on the Department of Agriculture Animal Health Computer were used in conjunction with data collected through a questionnaire to examine a range of possible risk factors, including the number and nature of the farm boundaries, the number of neighbours and their TB history, the number of hedgerows, the presence of badger setts, whether badger carcases had been found on the land, and the possible presence of deer. A follow-up telephone survey was conducted to minimise bias. The results highlighted two main associations with TB breakdowns, the presence of badgers, and contiguous neighbours who had had confirmed TB breakdowns. The estimated aetiological fraction for both associations was approximately 40 per cent, suggesting that although infected cattle may have a significant role in the transmission of TB their importance relative to the badger may have been over-estimated in the Northern Ireland TB scheme. The contribution of the badger is possibly one of several main reasons for the lack of significant progress in TB eradication despite strenuous efforts associated with all aspects of the scheme.     

Does reactive badger culling lead to an increase in tuberculosis in cattle?

The conclusion from the randomised badger culling trial was that localised badger culling not only fails to control but can actually increase the incidence of bovine tuberculosis in cattle. Professor Simon More and colleagues from University College Dublin question that conclusion, arguing that the data do not provide sufficient evidence to rule out alternative hypotheses.     

Laboratory study of Mycobacterium bovis infection in badgers and calves

Two experiments with badgers infected with Mycobacterium bovis are described. In the first, badgers were infected by intravenous inoculation of a bovine isolate of M bovis. The course of the disease in these and its spread to healthy badgers and calves was monitored by clinical, immunological and bacteriological means. In the second experiment a group of naturally infected badgers were observed for a period of up to four years. They were found to excrete M bovis in their faeces for periods of between 165 and 1305 days before they died of tuberculosis or were killed. M bovis was also shed in the urine. The badgers in both experiments were examined regularly and blood samples were taken for complement fixation tests. Faeces, urine, pus and sputum were also collected for cultural and biological tests and the badgers were skin tested using Weybridge bovine and avian tuberculin. The skin tests were uniformly negative while the complement fixation test were positive in some infected badgers but gave very variable results. Only the isolation of M bovis gave a definite diagnosis of tuberculosis in the living badger but a number of badgers which were found to have tuberculosis at post mortem were not detected while alive by this method. Environmental samples from the yards, including badger faeces, soil, hay, scrapings from feeding bowls and water were regularly examined for the presence of M bovis but apart from faeces only one water sample was positive, indicating that the organism did not persist for long in the environment. In both experiments calves developed sensitivity to bovine tuberculin after six months' exposure to infected badgers. The experiments further demonstrate the potential of a badger population to become endemically infected with M bovis and to act as a source of infection for cattle.     

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.     

Progress in the development of tuberculosis vaccines for cattle and wildlife

Vaccination against bovine tuberculosis is likely to become an important disease control strategy in developing countries, which cannot afford a test and slaughter control programme, or in countries which have a wildlife reservoir of Mycobacterium bovis infection. In the past decade, considerable progress has been made in the development and evaluation of tuberculosis vaccines for cattle and for a range of wildlife maintenance hosts including possums, badgers, deer and African buffaloes. Experimental challenge systems have been established for the different target species and the resulting disease process has mimicked that seen in the field. In cattle, neonatal vaccination with BCG appeared to be more effective than vaccination of 6-month-old calves and in most situations no other vaccine has been shown to be better than BCG. However, prime-boost strategies involving combinations of BCG with a protein or DNA vaccine, to improve on BCG vaccination alone, have produced very encouraging results. Differential diagnostic tests have been developed using mycobacterial antigens that are only present in virulent M. bovis to differentiate between BCG-vaccinated and M. bovis-infected cattle. BCG vaccine has been shown to reduce the spread of tuberculous lesions in a range of wildlife species and a prototype oral bait delivery system has been developed. Prospects for the development of improved vaccines against bovine tuberculosis are promising and vaccination approaches could become very valuable in the control and eradication of bovine tuberculosis.     

Abattoir surveillance: the U.S. experience

Abattoir, or slaughter, surveillance has been an important component of bovine tuberculosis control and eradication programs in the U.S., and has adapted to changes in the livestock market from farm to table, and the threat of bovine tuberculosis from a wildlife reservoir. The purpose of this overview was to describe the current goals of U.S. bovine tuberculosis slaughter surveillance, describe the elements of slaughter surveillance in the U.S., describe enhancements to the slaughter surveillance system, and discuss future challenges for the U.S. bovine tuberculosis surveillance program. Government regulations and the scientific literature were examined to provide information for this paper. The control and eradication of bovine tuberculosis in livestock falls to the United States Department of Agriculture and two agencies within the Department: the Food Safety and Inspection Service (FSIS) and the Animal and Plant Health Inspection Service (APHIS). FSIS conducts routine slaughter surveillance for disease or conditions that render carcasses unsuitable for human consumption, while APHIS is involved in antemortem bovine tuberculosis testing, and necropsy and investigation of bovine tuberculosis cases identified through slaughter surveillance or antemortem testing. Results from the previous 5 years of surveillance are presented. Enhancements have been added to the current surveillance system to improve its performance. An incentive program has been used to increase the numbers of tissues submitted for laboratory examination, the state of Michigan is implementing electronic animal identification under a pilot program, and expansions to the current system are being developed to accommodate new livestock industries. The success of these programs and challenges for the future are discussed.     

A comparison of badger activity in two areas of high and low bovine tuberculosis incidence of Northern Ireland

During 2005, a field survey of badger activity was carried out to evaluate differences between two areas with different levels of bovine tuberculosis (annual herd incidences of 16% and 4%) and to assess the awareness of herd keepers in relation to badgers. A random selection of herd keepers was interviewed and their farm land surveyed for the presence of badgers. The survey end point for each farm was the discovery of an active badger sett. Participation was very high in both areas (>80%). Evidence of badger activity was recorded on a higher proportion of farms in the area with a high tuberculosis herd incidence. However, when the difference in quality of agricultural land within each area was taken into account, a statistically significant association was not demonstrated. This suggests that the quality of agricultural land is a major determinant in the location of active badger setts. Nevertheless, the study did demonstrate the potential for increased exposure of cattle to badgers in the high incidence area. Herd keepers accurately identified the presence of badger setts on their land (positive predictive value=97%) but herd keepers reporting the absence of badger setts/activities on their land were found to be less accurate. Overall, the conclusions from this study tend to reflect the findings observed in other studies.     

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.