Northern Ireland farm-level management factors for recurrent bovine tuberculosis herd breakdowns.

Bovine tuberculosis (bTB) is a chronic, infectious and zoonotic disease of domestic and wild animals caused mainly by Mycobacterium bovis. This study investigated farm management factors associated with recurrent bTB herd breakdowns (n = 2935) disclosed in the period 23 May 2016 to 21 May 2018 and is a follow-up to our 2020 paper which looked at long duration bTB herd breakdowns. A case control study design was used to construct an explanatory set of farm-level management factors associated with recurrent bTB herd breakdowns. In Northern Ireland, a Department of Agriculture Environment and Rural Affairs (DAERA) Veterinarian investigates bTB herd breakdowns using standardised guidelines to allocate a disease source. In this study, source was strongly linked to carryover of infection, suggesting that the diagnostic tests had failed to clear herd infection during the breakdown period. Other results from this study associated with recurrent bTB herd breakdowns were herd size and type (dairy herds 43% of cases), with both these variables intrinsically linked. Other associated risk factors were time of application of slurry, badger access to silage clamps, badger setts in the locality, cattle grazing silage fields immediately post-harvest, number of parcels of land the farmer associated with bTB, number of land parcels used for grazing and region of the country.

Are major roads effective barriers for badger (Meles meles) movements?

As part of a bovine tuberculosis (bTB) control related Test and Vaccinate or Remove (TVR) badger research study in Northern Ireland, a project was launched evaluating whether badgers cross major roads (in this case the A1 dual carriageway linking Belfast/Newry/Dublin). This road formed the western boundary of the TVR study area and it was chosen to discourage badger movements in and out of the area. This was important in order to ensure that the badger study population was as stable as possible and also to get a better understanding of the risk of any spill over of bTB infection from the study area to the buffer area. Five badgers trapped close to the A1 were fitted with a Global Positioning System (GPS) collar in October 2017, which were set to record the badger location every 20 min between 19.20 and 03.00 h during a maximum of 84 days. Based on 4313 location points recorded, only 2 (0.05%) location points were located on the western side of the A1. Although this was a small sample, it can be concluded that generally badgers avoid crossing dual carriageways which is supported by evidence from other studies. This finding is important for informing on development of future badger intervention areas where major roads could be considered as strong borders. Furthermore, it adds to the body of knowledge in trying to understand drivers and barriers for badger dispersal behaviour.

Effect of selective removal of badgers (Meles meles) on ranging behaviour during a 'Test and Vaccinate or Remove' intervention in Northern Ireland.

The role of the Eurasian badger (Meles meles) as a wildlife host has complicated the management of bovine tuberculosis (bTB) in cattle. Badger ranging behaviour has previously been found to be altered by culling of badgers and has been suggested to increase the transmission of bTB either among badgers or between badgers and cattle. In 2014, a five-year bTB intervention research project in a 100 km2 area in Northern Ireland was initiated involving selective removal of dual path platform (DPP) VetTB (immunoassay) test positive badgers and vaccination followed by release of DPP test negative badgers ('Test and Vaccinate or Remove'). Home range sizes, based on position data obtained from global positioning system collared badgers, were compared between the first year of the project, where no DPP test positive badgers were removed, and follow-up years 2-4 when DPP test positive badgers were removed. A total of 105 individual badgers were followed over 21 200 collar tracking nights. Using multivariable analyses, neither annual nor monthly home ranges differed significantly in size between years, suggesting they were not significantly altered by the bTB intervention that was applied in the study area.

Northern Ireland farm-level management factors for prolonged bovine tuberculosis herd breakdowns.

This study determined farm management factors associated with long-duration bovine tuberculosis (bTB) breakdowns disclosed in the period 23 May 2016 to 21 May 2018; a study area not previously subject to investigation in Northern Ireland. A farm-level epidemiological investigation (n = 2935) was completed when one or more Single Intradermal Comparative Cervical Test (SICCT) reactors or when one or more confirmed (positive histological and/or bacteriological result) lesion at routine slaughter were disclosed. A case-control study design was used to construct an explanatory set of management factors associated with long-duration bTB herd breakdowns; with a case (n = 191) defined as an investigation into a breakdown of 365 days or longer. Purchase of infected animal(s) had the strongest association as the most likely source of infection for long-duration bTB herd breakdowns followed by badgers and then cattle-to-cattle contiguous herd spread. However, 73.5% (95% CI 61.1-85.9%) of the herd type contributing to the purchase of infection source were defined as beef fattening herds. This result demonstrates two subpopulations of prolonged bTB breakdowns, the first being beef fattening herds with main source continuous purchase of infected animals and a second group of primary production herds (dairy, beef cows and mixed) with risk from multiple sources.

Evaluating the application of the dual path platform VetTB test for badgers (Meles meles) in the test and vaccinate or remove (TVR) wildlife research intervention project in Northern Ireland.

European badgers (Meles meles) are accepted as a wildlife reservoir host for Mycobacterium bovis, which causes bovine tuberculosis (bTB) in the British Isles. The objective of this study was to evaluate the use of Dual Path Platform (DPP) VetTB test (Chembio Diagnostic Systems Inc., Medford, NY, USA) within a Test and Vaccinate or Remove (TVR) wildlife research intervention project. Blood samples were collected from 456 individual badgers, trapped in 2015 and 2016, and tested in the field with DPP VetTB test using whole blood. Additionally, whole blood and serum samples were taken to the laboratory for further DPP VetTB testing and for gamma interferon (IFN-γ) testing. Swabs were taken from the oropharynx and trachea and submitted for bacteriological culture as were swabs from wounds, if present. Field DPP VetTB test positive badgers were euthanised and underwent post-mortem examination and bTB confirmatory testing. The results demonstrated that the test performed as well in the field using whole blood as DPP Vet TB tests in the laboratory using sera or whole blood, and as well as other established tests for M. bovis. Visual assessment of the DPP VetTB test using serum under laboratory conditions showed a high degree of consistency between raters. Using a relative gold standard (parallel interpretation of IFN-γ assay and oropharyngeal/tracheal sample/culture), sensitivity estimates for the DPP VetTB test using sera and whole blood were 0.5 (95%CI 0.34-0.66) and 0.42 (95%CI 0.24-0.66), respectively. Specificity estimates were 0.95 (95%CI 0.93-0.97) for sera and 0.89 (95%CI 0.86-0.92) for whole blood. Parallel interpretation of Band 1 (MPB83) and Band 2 (CFP-10/ESAT-6) of the DPP VetTB test was not superior to interpretation of Band 1 only. The results give confidence in the reliability and reproducibility of the DPP VetTB test for badgers under field conditions and therefore it is considered appropriate for use in a badger bTB control campaign.

Test characteristics of the tuberculin skin test and post-mortem examination for bovine tuberculosis diagnosis in cattle in Northern Ireland estimated by Bayesian latent class analysis with adjustments for covariates.

The single intradermal comparative cervical tuberculin (SICCT) test and post-mortem examination are the main diagnostic tools for bovine tuberculosis (bTB) in cattle in the British Isles. Latent class modelling is often used to estimate the bTB test characteristics due to the absence of a gold standard. However, the reported sensitivity of especially the SICCT test has shown a lot of variation. We applied both the Hui-Walter latent class model under the Bayesian framework and the Bayesian model specified at the animal level, including various risk factors as predictors, to estimate the SICCT test and post-mortem test characteristics. Data were collected from all cattle slaughtered in abattoirs in Northern Ireland in 2015. Both models showed comparable posterior median estimation for the sensitivity of the SICCT test (88.61% and 90.56%, respectively) using standard interpretation and for post-mortem examination (53.65% and 53.79%, respectively). Both models showed almost identical posterior median estimates for the specificity (99.99% vs. 99.80% for SICCT test at standard interpretation and 99.66% vs. 99.86% for post-mortem examination). The animal-level model showed slightly narrower posterior 95% credible intervals. Notably, this study was carried out in slaughtered cattle which may not be representative for the general cattle population.

Bayesian latent class estimation of sensitivity and specificity parameters of diagnostic tests for bovine tuberculosis in chronically infected herds in Northern Ireland.

In the European Union, the recommended ante-mortem diagnostic methods for bovine tuberculosis (bTB) include the single intradermal cervical comparative tuberculin (SICCT) test and the interferon-gamma (IFN-γ) test as an ancillary test. The SICCT test has a moderate sensitivity (Se) and high specificity (Sp), while the IFN-γ test has good Se, but a lower Sp than the SICCT test. A retrospective Bayesian latent class analysis was conducted on 71,185 cattle from 806 herds chronically infected with bTB distributed across Northern Ireland (NI) to estimate the Se and Sp of the common ante-mortem tests and meat inspection. Analyses were also performed on data stratified by farming type and herd location to explore possible differences in test performance given the heterogeneity in the population. The mean estimates in chronically infected herds were: (1) 'standard' SICCT: Se 40.5-57.7%, Sp 96.3-99.7%; (2) 'severe' SICCT: Se 49.0%-60.6%, Sp 94.4-99.4%; (3) IFN-γ(bovine-avian) using a NI optical density (OD) cut-off difference of 0.05: IFN-γ(B-A)NI: Se 85.8-93.0%, Sp 75.6-96.2%; (4) IFN-γ(bovine-avian) using a standard 'commercial' OD cut-off difference of 0.1: IFN-γ(B-A)0.1: Se 83.1-92.1%, Sp 83.1-97.3%; and (5) meat inspection: Se 49.0-57.1% Se, Sp 99.1-100%. Se estimates were lower in cattle from dairy farms than from beef farms. There were no notable differences in estimates by location of herds. Certain population characteristics, such as production type, might influence the ability of bTB tests to disclose truly infected cases.

The impact of the number of tuberculin skin test reactors and infection confirmation on the risk of future bovine tuberculosis incidents; a Northern Ireland perspective.

Currently policies enabling cattle herds to regain Official Tuberculosis Free (OTF) status after a bovine tuberculosis (bTB) herd incident vary between individual parts of the British Isles from requiring only one negative single comparative intradermal tuberculin test (SCITT) herd test when bTB infection is not confirmed to needing two consecutively negative SCITT herd tests after disclosure of two or more reactors, irrespective of bTB confirmation. This study used Kaplan-Meier curves and univariable and multivariable Cox Proportional Hazard models to evaluate the effect of the number of SCITT reactors and bTB confirmation on the risk of future bTB herd incident utilising data extracted from the national animal health database in Northern Ireland. Based on multivariable analyses the risk of a future bTB herd incident was positively associated with the number of SCITT reactors identified during the incident period (hazard ratio = 1.861 in incidents >5 SCITT reactors compared to incidents with only one SCITT reactor; P < 0.001), but not with bTB confirmation. These findings suggest that the probability of residual bTB infection in a herd increases with an increasing number of SCITT reactors disclosed during a bTB herd incident. It was concluded that bTB herd incidents with multiple SCITT reactors should be subjected to stricter control measures irrespective of bTB infection confirmation status.

Bovine tuberculosis in Northern Ireland: quantification of the population disease-level effect from cattle leaving herds detected as a source of infection.

Determination of the proportion of bovine tuberculosis (bTB) breakdowns attributed to a herd purchasing infected animals has not been previously quantified using data from the Animal and Public Health Information System (APHIS) database in Northern Ireland. We used a case-control study design to account for the infection process occurring in the disclosing bTB breakdown herds. Cases (N = 6926) were cattle moving to a future confirmed bTB breakdown where they would disclose as a confirmed bTB reactor or a Lesion at Routine Slaughter (LRS). Controls (N = 303 499) were cattle moving to a future confirmed bTB breakdown where they did not become a bTB reactor or LRS. Our study showed that the cattle leaving herds which disclosed bTB within 450 days had an increased odds of becoming a confirmed bTB reactor or LRS compared with the cattle which left herds that remained free for 450 days (odds ratio (OR) = 2·09: 95% CI 1·96-2·22). Of the 12 060 confirmed bTB breakdowns included in our study (2007-2015 inclusive), 31% (95% CI 29·8-31·5) contained a confirmed bTB reactor(s) or LRS(s) at the disclosing test which entered the herd within the previous 450 days. After controlling for the infection process occurring in the disclosing bTB breakdown herd, our study showed that 6·4% (95% CI 5·9-6·8) of bTB breakdowns in Northern Ireland were directly attributable to the movement of infected animals.

Efficiency of slaughterhouse surveillance for the detection of bovine tuberculosis in cattle in Northern Ireland.

Post-mortem examination continues to play an important surveillance role in the bovine tuberculosis (bTB) eradication programme in Northern Ireland. It is estimated that 18-28% of new bTB herd breakdowns are disclosed by the detection of bTB lesions in animals routinely slaughtered. The purpose of this study was to compare the performance of different slaughterhouses in Northern Ireland in detecting bTB-lesioned animals at routine slaughter (LRS) and to apply the findings to maximize the sensitivity of bTB slaughterhouse surveillance. Univariate statistical analysis on cattle slaughtered in Northern Ireland during 2011-2013 revealed that the risk of LRS disclosure varied between slaughterhouses, ranging from 0·08% to 0·54%. Furthermore, the risk of confirmation of these LRS as bTB varied between slaughterhouses, ranging from 57·9% to 72·4%. Logistic regression modelling of selected risk factors found that the risk of LRS disclosure increased with age, and was higher in purchased animals, during winter months, in animals coming from high bTB incidence areas and in animals slaughtered from herds with a bTB restriction in the last 2-3 years. Adjusting for these selected factors, the risk of LRS disclosure and bTB confirmation changed very little from the univariable analysis, suggesting that differences in disclosure risks between slaughterhouses were likely to be due to factors related to the slaughterhouses, rather than to the risk status of the animals presented. Examination of procedures within these slaughterhouses is recommended to identify ways that could increase the sensitivity of their bTB surveillance.

Bovine tuberculosis in Northern Ireland: Risk factors associated with duration and recurrence of chronic herd breakdowns.

This study investigated 8058 bovine tuberculosis (bTB) confirmed breakdowns occurring in Northern Ireland during the period 2005-2010 inclusive. The methodology used two case-control studies; one determined the risk factors associated with long duration bTB breakdowns and the other with recurrent bTB breakdowns. The analyses were implemented using a generalized linear mixed model analysis with variables relating to repeated measures on herds, locality and year of breakdown included as random effects. The case definition for long duration breakdowns (n=679) was any confirmed bTB disclosure with duration greater than one year. The case definition for recurrent breakdowns (n=657) was any confirmed bTB disclosure with duration less than one year, followed by two or more bTB breakdowns within 2 years from the end of the initial bTB breakdown. In the multivariable model based on duration of bTB breakdowns, significant factors were local area bTB prevalence, number of associated cattle herds, total years restricted in the previous five years, total number of bTB reactors during the breakdown and the presence of a bTB lesion at routine slaughter (LRS). The number of bTB reactors at the disclosing test was also significant; with increased numbers associated to reduced odds of a long duration breakdown. In the second analysis based on recurrence of bTB breakdowns, high local area prevalence, movement intensity into the herd, total years restricted in the previous five years, herd size, total number of TB reactors during the restricted breakdown and presence of a LRS were all statistically significant.

Bovine tuberculosis trends in the UK and the Republic of Ireland, 1995-2010.

Selected demographic features and trends in bovine tuberculosis (BTB) from 1995 to 2010 are described for the countries of the UK and the Republic of Ireland, using standardised definitions and measures. All countries experienced a reduction in the number of cattle and herds and in the proportion of dairy herds, while average herd size increased. In general, the trends indicate a stable situation of very low BTB prevalence in Scotland and, over most of the period, a rising prevalence in England and Wales. The prevalence in the Republic of Ireland declined while Northern Ireland experienced both a rise and fall. Differences in demography, BTB programme structure and test results were noted, particularly between the island of Ireland and Great Britain. Further investigation of these differences may provide valuable insights into risk factors for BTB and optimisation of existing BTB programmes.

Field trial of six serological tests for bovine brucellosis.

Serum agglutination (SAT), complement fixation (CFT), indirect ELISA (iELISA), competitive ELISA (cELISA), Rose Bengal (RBT) and EDTA-modified agglutination (EDTA) tests were used in parallel on serological samples from 19,935 cattle in 301 herds. The study herds were selected according to putative exposure to Brucellaabortus with cases defined by bacteriological culture or test agreement. No single test identified all infected cattle and, at diagnostic thresholds, relative sensitivity was highest in the iELISA (67.9%) or RBT (78.1%), using bacteriological culture or test agreement, respectively, to define cases. As screening tests, the relative sensitivity of the SAT was highest (75.9% by culture or 84.9% by test agreement), with an optimal threshold of 31 IU. The relative specificity of the diagnostic tests ranged from 99.6% (SAT 31IU) to 100% (iELISA, RBT and CFT). The trial confirmed the value of the SAT as a screening test and the value of parallel testing.

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.

Coxiella burnetii (Q fever) seroprevalence in cattle.

Human cases of Q fever appear to be common in Northern Ireland compared to the rest of the British Isles. The purpose of this study was to describe the seroepidemiology of Coxiella burnetii infection in cattle in Northern Ireland in terms of seroprevalence and determinants of infection. A total of 5182 animals (from a stratified systematic random sample of 273 herds) were tested with a commercial C. burnetii phase 2 IgG ELISA. A total of 6.2% of animals and 48.4% of herds tested positively. Results from a multilevel logistic regression model indicated that the odds of cattle being infected with Q fever increased with age, Friesian breed, being from large herds and from dairy herds. Large dairy herd animal prevalence was 12.5% compared to 2.1% for small beef herds. Preliminary seroprevalence in sheep (12.3%), goats (9.3%), pigs (0%) rats (9.7%) and mice (3.2%) using indirect immunofluorescence is reported.

Evidence for transplacental and contact transmission of bluetongue virus in cattle.

This paper presents evidence that a field strain of bluetongue virus serotype 8 (BTV-8) was transmitted transplacentally and that it was also spread by a direct contact route. Twenty pregnant heifers were imported from the Netherlands into Northern Ireland during the midge-free season. Tests before and after the animals were imported showed that eight of them had antibodies to bluetongue virus, but no viral RNA was detected in any of them by reverse transcriptase-PCR (RT-PCR). Two of the seropositive heifers gave birth to three calves that showed evidence of bluetongue virus infection (RT-PCR-positive), and one of the calves was viraemic. Two further viraemic animals (one newly calved Dutch heifer, and one milking cow originally from Scotland) were also found to have been infected with BTV-8 and evidence is presented that these two animals may have been infected by direct contact, possibly through the ingestion of placentas infected with BTV-8.

Campylobacter spp. in conventional broiler flocks in Northern Ireland: epidemiology and risk factors.

Risk factors for Campylobacter infection in conventional broiler flocks in the time period up to the first removal of birds to slaughter were investigated over a maximum of five consecutive production cycles in a cohort of 88 broiler farms in Northern Ireland. Samples for Campylobacter culture, which consisted of 14 cloacal swabs per flock, were collected from one house on each farm prior to the first depopulation of birds. In total 388 flocks were sampled, of which 163 tested positive for Campylobacter spp. (42.0%; 95% CI 35.1-48.9%). Data on farm and flock variables were obtained from questionnaires and random-effects logistic regression modelling used to investigate the association between these and the Campylobacter status of flocks. Six variables, all of which were significant at p<0.05, were included in the final multivariable model. These included a combined variable on the presence of rodents on farms, which showed an increased odds of infection in flocks where the farmer reported having observed rodents during the production cycle (OR=2.1) and/or where rodent droppings were observed at the sampling visit (OR=2.9). Other variables that were significantly associated with an increased odds of infection included the age of the birds at sampling (odds ratio for its linear effect=1.16 for each day of increase in age), season (summer versus other seasons OR=2.0), farms with three or more broiler houses (OR=2.9 compared to those with one house), the frequency of footbath disinfectant changes (OR=2.5 for once weekly and OR=4.0 for less than once weekly compared to twice weekly changes) and a categorical variable on the standard of tidiness and cleanliness of the broiler house ante-room (OR=2.0 and OR=4.9 for flocks from houses with poorer standards). There was no significant evidence of direct carry-over of infection from one production cycle to the next, neither was there evidence of other farm species acting as a source of infection.

Risk associated with animals moved from herds infected with brucellosis in Northern Ireland.

The movement of cattle from herds infected with Brucella abortus was investigated in order to assess the control measures for eradication of brucellosis from the cattle population of Northern Ireland. Using recorded cattle movement data, a historical cohort study was designed and carried out to quantify the risk of seropositivity in bovine animals moved from herds infected with brucellosis. The study found that 3.1% of animals, moved in the 6-month period prior to disclosure of infection in the source herd and subsequently tested, were interpreted as seropositive in their destination herds. The odds of seropositivity were approximately 19 (95% confidence interval: 7.8-46.4) times higher in this cohort compared with animals from herds with no history of infection. A multivariate logistic regression model was constructed to examine factors influencing the risk of seropositivity in the exposed cohort of animals, identifying maternal status (whether the dam had been a brucellosis reactor) and age at leaving the infected herd as the main risk factors.

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.