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What is needed to eradicate bovine tuberculosis successfully: an Irish perspective

Bovine tuberculosis is a notifiable disease in Northern Ireland with the national eradication programme of compulsory testing and slaughter of reactor animals costing approximately £40 million per year. Backward tracing, known as Backward Check Tests (BCTs), of reactor animals is used to identify previous herds where the bTB positive animal has resided. The aim of this study was to quantify the bovine tuberculosis (bTB) risk posed by inconclusive reactors (ICs) at BCTs at both the individual animal and the herd level. ICs to the Comparative Intradermal Tuberculin Test (CITT) at a BCT, in which no reactors were found, were matched with CITT negative animals, based on age, sex, test ID and follow up period, in Northern Ireland between 1st January 2008 and 31st December 2017 (inclusive). A retrospective matched cohort study design was used with the outcome of interest being the bTB status of each animal and subsequent bTB herd breakdowns. After adjusting for herd size, IC animals at a BCT had 16 times the odds (95% confidence interval: 7.75 to 38.28, p < 0.001) of becoming bTB positive compared to CITT negative animals. The percentage population attributable risk was 0.0001%. The majority 75% (n = 71) of ICs that became bTB positive were identified at the 42 day retest. Of those that were not disclosed at the 42 day retest (n = 24), almost a third (29%) had moved to an unrestricted herd. However, after adjusting for herd size and type, herds that had ICs only identified at a BCT did not have an increased odds of a subsequent bTB herd breakdown compared to herds that had a CITT negative BCT. Given the increased risk posed by ICs at a BCT, it may be justifiable to remove them from the herd immediately or place them under lifetime movement restrictions to the herd where they were detected. However, further action regarding the herd of origin does not appear to be justified.

Bovine tuberculosis (bTB) is an important zoonotic disease which has serious and sometimes fatal effects on both human and non-human animals. In many countries it is endemic in the cattle population and has a considerable economic impact through losses in productivity and impacts on trade. The incidence rate in Ireland varies by herd and location and it is hoped that statistical disease-mapping models accounting for both spatio-temporal correlation and covariates might contribute towards explaining this variation.

Ireland was divided into equally sized hexagons for computational efficiency (n = 997). Different spatio-temporal random-effects models (e.g. negative binomial Besag-York-Mollié) were explored, using comprehensive data from the national bTB eradication programme to examine the association between covariates and the number of bTB cattle. Leveraging a Bayesian framework, model parameter estimates were obtained using the integrated nested Laplace approximation (INLA) approach. Exceedance probabilities were calculated to identify spatial clusters of cases.

Models accounting for spatial correlation significantly improved model fit in comparison to non-spatial versions where independence between regions was assumed. In our final model at hexagon level, the number of cattle (IR = 1.142, CrI: 1.108 – 1.177 per 1000), the capture of badgers (IR = 5.951, CrI: 4.482 – 7.912), percentage of forest cover (IR = 1.031, CrI: 1.020 – 1.042) and number of farm fragments (IR = 1.012, CrI: 1.009 – 1.015 per 10 fragments) were all associated with an increased incidence of bTB. Habitat suitability for badgers, percentage of dairy herds and the number of cattle movements into the herd were not. As an epidemiological tool and to suggest future work, an interactive online dashboard was developed to monitor disease progression and disseminate results to the general public.

Accounting for spatial correlation is an important consideration in disease mapping applications and is often ignored in statistical models examining bTB risk factors. Over time, the same regions in Ireland generally show highest incidences of bTB and allocation of more resources to these areas may be needed to combat the disease. This study highlights national bTB incidence rates. Shifting from national level analysis to smaller geographical regions may help identify localised high-risk areas.

There has been a national bovine tuberculosis (bTB) eradication programme (BTBEP) in Ireland for many years. All cattle herds are tested at least annually using the Single Intradermal Comparative Tuberculin Test (SICTT). Further, abattoir surveillance is conducted on all animals at the time of slaughter. In the Irish BTBEP, a substantial number of confirmed bTB lesions are detected in non-reactor animals, to SICTT, from Officially Tuberculosis Free (OTF) herds at slaughter. In this study we investigate risk factors for non-reactor animals from OTF herds presenting with a confirmed bTB lesion at slaughter, but with no evidence of within-herd transmission.

A case-control study was conducted, with animal as the unit of interest. The case animals were all SICTT non-reactor animals slaughtered in 2012, with a confirmed bTB lesion identified during routine abattoir surveillance and with no evidence of within-herd transmission. Control animals were selected from all SICTT non-reactor animals slaughtered in 2012 from OTF herds where no bTB lesion was found. Four controls matched by age (±1 year) and location (county) were randomly selected for each case. A conditional logistic regression model was developed for univariable and multivariable analysis.

The final multivariable model included: number of movements, herd type, herd-size, inconclusive reactor status at any previous test, abattoir and time spent in a herd restricted for bTB. The odds of being a case increased with the number of times an animal had moved herds. Animals from suckler herds were significantly more likely to be a case compared to those from beef herds. The odds of being a case decreased with herd-size and increased as the time spent in a restricted herd increased.

There were three key conclusions from this study. Firstly, the main risk factors for animals presenting with a confirmed bTB lesion at slaughter were: previous bTB exposure history, previous inconclusive reactor result at the SICTT, the number of herd movements and herd type/size. Secondly, there was very limited evidence that these animals could have been detected any earlier. Finally, there is a need to reconsider the importance of abattoir surveillance during the latter stages of an eradication campaign. As herd prevalence declines, an increasing proportion of herd restrictions will be triggered by a single bTB-lesioned animal, with no evidence of within-herd transmission.

There is substantial variation in herd risk for bovine tuberculosis (bTB) in Ireland, with most herds playing little to no role in the ongoing endemic. In infected areas, bTB persistence (affecting one or a group of herds) is a key feature of the infection. In this paper, we present our current understanding and management of bTB risk in Ireland, based on a detailed review of research and policy. There is close interaction between science and policy in Ireland, seeking both to understand and effectively manage bTB risk. Detailed research on bTB persistence is presented, including current understanding of the relative importance of different infection sources, which can include residual infection in cattle and/or re-infection, either from local sources or following cattle introduction. In recent years, there have been three primary drivers for policy change, including scientific advances, ongoing improvements to programme supports, and ongoing programme review. In this review, three key future programme challenges are identified. Although good progress is being made, eradication has not yet been achieved. Firstly, a key question concerns the additional effort that will be required, to move towards final eradication. Secondly, a percentage of non-infected animals are falsely positive to current testing methods. This is an ongoing challenge, given the imperfect specificity of test methods but will become more so, as the positive predictive value falls with reducing bTB prevalence. Finally, there is a need to re-engage with the farming community, so that they play a much greater role in programme ownership.

As European dairy farms become larger and diverge between grass-based and fully housed systems, interest in the welfare of the dairy cow and related environmental issues by consumers and legislators is increasing. These pressures mean that good nutrition and management, which underpin much dairy cow welfare, is critical. Despite considerable research into the management and nutrition of the dairy cow from calf to adulthood there is much on-farm variability in its application. While the incidences of many endemic diseases are reduced most are still significant, for example lameness. In addition, trade and climate change are bringing a more diverse range of pathogens, parasites and pests into Northern Europe. Housing aspects are limited in application by economics and in most cases still do not match grazing for welfare in temperate climates. Genomic technologies offer increased opportunities to breed for ‘robustness’ but like ‘precision animal management systems’ have still to be fully exploited.

During the last several decades in Ireland, there has been substantial scientific progress in our understanding and related policy changes in the bovine tuberculosis (bTB) eradication programme. A range of performance measurements are routinely available, each highlighting a steadily improving situation in Ireland. However, recent research has highlighted an on-going problem of residual infection, contributing to recurrent breakdowns. In light of this general improvement, but also cognisant of residual infection, a critical evaluation of changes in effectiveness of managing recurrence is particularly valuable. Therefore, the objective of the study was to compare the herd-level risk of recurrence of bTB in Ireland between 1998 and 2008. A retrospective cohort study was carried out, using a Cox proportional-hazards model, to compare the risk of restriction recurrence in herds derestricted during 1998 and 2008. These herds were observed for up to 3 years from the end of the ‘index restriction’. At the univariable level, 46.4% and 34.8% of study herds derestricted in 1998 and 2008, respectively, had a subsequent breakdown during the study period (χ² = 70.6, P < 0.001). In the multivariable analysis, there has been a significant reduction in bTB recurrence in Ireland, with 2008-derestricted herds being 0.74 times (95% confidence interval: 0.68–0.81) as likely to be restricted during the subsequent study period compared with 1998-derestricted herds. In the final Cox model, the rate of a future breakdown increased with increasing herd size, increasing number of standard reactors in the index restriction, increasing percentage of newly restricted herds within the District Electoral Division (DED) and if the herd had a previous bTB episode in the previous 5 years. The risk varied across herd type. The results from the current study provide further reassurance of an improved national situation, both in terms of limiting the establishment of new infection (bTB incidence) and in effectively clearing infection once detected (recurrence following derestriction). Recurrence of bTB requires effective implementation of multiple control strategies, focusing on identifying and removing residually infected cattle, and limiting environmental sources of infection, which in Ireland primarily relates to badgers.