A retrospective cohort study was conducted to determine the risk of bovine tuberculosis (TB) among animals sold out from herds that were free to trade animals during the year 2005 according to their bovine TB testing history during the year 2005. The present study sample comprised of 338,960 animals, of which 124,360 animals were sold out from herds that were restricted from trading at some stage during 2005 (bovine TB ‘exposed’) and 214,600 animals that were sold from herds which did not have their trading status withdrawn in 2005 (bovine TB ‘non-exposed’). The overall risk of a diagnosis of bovine TB during the two-year period after the animals were sold out was 0.69 per cent. The odds of bovine TB were 1.91 higher for animals sold out from bovine TB ‘exposed’ herds compared with animals sold out from bovine TB ‘non-exposed’ herds (OR 95 per cent CI: 1.76 to 2.07, P < 0.0001). Ten per cent of animals identified during field surveillance with bovine TB did so less than two months after being sold out in 2005, and similarly, 10 per cent of the animals classified as bovine TB positive by finding a bovine TB lesion at slaughter did so within 25 days (or less) of being sold out in 2005.
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Mycobacterium bovis is the agent that causes bovine tuberculosis (TB), a chronic infectious-contagious disease of cattle. Although bovine TB was once distributed worldwide, control programmes have successfully eradicated the disease from domesticated animals in many developed countries. In countries such as the Republic of Ireland, where the disease persists despite bovine TB control programmes that are in place, the later stage pathology of the disease is rarely observed at postmortem meat inspection due to the early and constant removal of infected animals. Thus, animals infected with M bovis in Ireland present most commonly as outwardly healthy, showing an immunological response to the tuberculin test (Collins 2006).
The Irish national bovine TB eradication programme is a comprehensive disease surveillance strategy and consists of compulsory annual farm-based tuberculin skin testing of all cattle using the Single Intradermal Comparative Cervical Test (SICCT) combined with veterinary inspection at slaughter plants of all bovine carcasses presented for human consumption (Good 2006). The detection at slaughter of gross lesions (factory surveillance) in cattle from attested herds, that is cattle from herds considered bovine TB free on the basis of annual skin testing, is an additional and important method for detecting infected herds as part of the national programme (Frankena and others 2007). Despite the early success of the programme, bovine TB persists within the Irish national herd. Approximately 0.3 per cent or approximately 20,000 reactors are identified annually from the national herd of nearly 6.5 million.
The national programme is supported by a long-term research programme, to identify and address constraints to eradication. As described previously, key constraints can be broadly grouped into those relating to wildlife (due to ongoing spillback of infection from badgers to cattle), to ongoing infection within the cattle population and to programme governance (More 2009). A range of Irish studies have highlighted ongoing difficulties with control of infection in cattle, including concerns with residual infection (inapparent infection in cattle, despite annual testing) (Olea-Popelka and others 2008, Wolfe and others 2009, Clegg and others 2011 b,c, Good and others 2011, Kelly and More, 2011). Similar conclusions have also been drawn from the UK (Carrique-Mas and others 2008, Karolemeas and others 2011). These problems generally present as difficulties in clearing infected herds, although the movement of infected cattle to previously clear herds is also of concern. Approximately 7 per cent and 16 per cent of breakdowns each year can be attributed to the introduction of infected cattle in Ireland (Clegg and others 2008) and Great Britain (Green and others 2008), respectively.
The national bovine TB control programme is primarily herd-based, and most actions (including most relating to surveillance and control) are focused on the herd rather than the individual animals. This is appropriate, as the herd is the epidemiological unit of interest. Further, there are substantial difficulties associated with animal-level bovine TB diagnosis (de la Rua-Domenech and others 2006). Understandably, most studies in Ireland have focused on the herd, with few being conducted to assess the risk of bovine TB at the animal level. However, epidemiological studies at the animal level are essential to the quantification of the risk posed by animals introduced into herds, particularly by movements of infected animals.
The current study seeks to provide new information of the role of animal movements in future disease risk at the animal level. The study objectives were several-fold, including 1) to quantify the risk of bovine TB among animals sold out from attested Irish herds in 2005, 2) to compare the risk of bovine TB among animals sold out from herds with different bovine TB history and 3) to describe temporal patterns associated to animals sold out from herds during 2005 and their association with bovine TB identification within a two years window from the time they left a herd in 2005.
Materials and methods
A retrospective cohort study was conducted to quantify the risk of bovine TB among animals sold out from attested herds during the year 2005. Herds from which the animals were sold out were classified as ‘exposed’ and ‘non-exposed’ to bovine TB according to their bovine TB history during 2005. Herds that experienced a bovine TB breakdown (at least one bovine TB-positive animal was identified within a herd) in 2005 were classified as ‘exposed’. Herds that did not experience a bovine TB breakdown (no bovine TB-positive animals were identified within the herd) in 2005 were classified as ‘non-exposed.’
The authors analysed movement records from animals sold out from exposed and non-exposed herds during the year 2005, and the bovine TB testing history of these animals up to the end of year 2007 was used in our study to identify bovine TB positive animals. The outcome of interest in this study was bovine TB status at the animal level from the time that the animal was sold in 2005 until the end of the year 2007. An animal was considered bovine TB positive if it was deemed a SICTT reactor (during field surveillance, using a ‘standard’ interpretation) or if it disclosed a bovine TB-like lesion at slaughter (during abattoir surveillance) that was subsequently confirmed as M bovis by histopathology and/or bacterial culture. During standard interpretation, an animal is considered a reactor when the bovine reaction is more than 4 mm greater than the avian reaction, or if local clinical signs such as oedema, exudation, necrosis or pain are present at the bovine site. Routine factory surveillance, conducted in Ireland by veterinarians employed as temporary veterinary inspectors, is based on the palpation, incision and inspection of a defined range of lymph nodes, including the parotid, mandibular, lateral and medial retropharyngeal nodes in the head, the cranial and medial tracheobronchial nodes, and the cranial, middle and caudal mediastinal nodes in the pleura (Costello and others 1998). Because bovine TB lesions generally cannot be distinguished on gross inspection from non-tuberculous granulomas, suspect bovine TB lesions from animals from attested herds are further examined in the laboratory.
The risk of bovine TB was compared between animals sold out from herds with different bovine TB exposure status. A descriptive analysis was conducted in order to identify the distribution of the interval between animals leaving herds in 2005 and being identified as bovine TB positive (during either field or abattoir surveillance) during the next two years.
Three (Irish) national databases were used in this study: (1) The Animal Health Computer System (AHCS), with tuberculin testing data from all herds in Ireland including all bovine TB reactor animals since 1989. (2) The Cattle Movement and Monitoring System (CMMS), an animal identification system which is used to record all calf births/registrations, all cattle movements (farm-to-farm, via a market and to the slaughter plant) and all on-farm deaths in Ireland since January 1, 2000 and (3) A database of laboratory testing results (available since 2000) from the national slaughter plant surveillance programme (histopathology and culture results from all animals with a suspect lesion detected at slaughter).
The Irish national cattle herd is comprised of approximately 6.5 million animals. The study population was drawn from all animals on the official register present in Ireland in the year 2005. All animals sold out from bovine TB ‘exposed’ herds during 2005 were identified and included in the study, and a random representative sample of all animals sold out from bovine TB ‘non-exposed’ herds during 2005 was selected and included in this study (10 per cent of the population, was randomly selected using computer software).
The study sample included 338,960 animals, of which 124,360 animals were sold out from ‘exposed’ herds during 2005 and 214,600 animals were sold out during 2005 from ‘non-exposed’ herds.
SAS v 9.2 was used for data manipulation, descriptive analysis and comparison of the risk among different groups. A descriptive analysis was carried out to assess the subsequent risk of bovine TB at the animal level based on the herd of origin's bovine TB exposure status. For all bovine TB positive animals, the authors also calculated the distribution of the interval (days) between out-movement and bovine TB disclosure for animals sold from attested herds during 2005, by method of bovine TB disclosure (either field or abattoir surveillance). The bovine TB-positive animals originating from ‘exposed’ herds were further investigated using data available pertaining to the herd bovine TB episode duration in 2005. Restriction and clearance dates were used to determine whether animals were moved from the ‘exposed’ herds before the bovine TB episode or after clearance of the bovine TB was achieved at the herd level in 2005. Logistic regression analysis was used to obtain the odds ratios with their corresponding 95 per cent CI and P values when comparing the risk of TB between different exposure groups. Statistical significance was declared at P < 0.05.
The overall risk of bovine TB for animals sold out in 2005 from attested herds until the end of the year 2007 was 0.69 per cent (2330 bovine TB-positive animals). Of the 2330 animals classified as bovine TB-positive, 1740 (74.7 per cent) were identified as SICCT reactors, and 590 animals (25.3 per cent) had lesions indicative of bovine TB during slaughter surveillance that subsequently were confirmed as M bovis at the laboratory by histopathology and/or culture (Table 1).
Table 1 describes the risk of bovine TB at the animal level based on the herd of origin's bovine TB exposure during 2005 (stratified by method of bovine TB disclosure, either field or abattoir surveillance). Overall, animals sold out from ‘exposed’ herds had an overall higher risk of bovine TB compared with animals sold out from ‘non-exposed’ herds (0.98 per cent v 0.52 per cent; OR = 1.91, 95 per cent CI = 1.76 to 2.07; P < 0.0001).
Table 2 focuses solely on bovine TB-positive animals, describing the distribution of the interval (days) between out-movement (from attested herds during 2005) and subsequent bovine TB disclosure, by method of bovine TB disclosure (either field or abattoir surveillance). Of the 1740 animals classified as bovine TB positive during field surveillance, the median time from out-movement to bovine TB disclosure was 337 days (Q1 = 153 days, Q3 = 590 days). Ten percent of these animals (174 animals) tested positive to the SICCT within 69 days of the out-movement in 2005. Of the 590 animals classified as bovine TB positive during slaughter surveillance, the median time from out-movement to bovine TB disclosure was 301 days (Q1 = 116 days, Q3 = 522 days). In 10 per cent of these animals (59 animals), the bovine TB lesion was detected at slaughter 25 days or less after been sold out during 2005.
Accurate and complete data for the most-recent bovine TB episode were available for 1127 (92.2 per cent) of the 1223 animals sold from ‘exposed’ herds in 2005. As highlighted in Table 3, animals moved before the herd restriction date had a higher risk of being classified as bovine TB positive than those animals sold out after the clearance date for the 2005 bovine TB episode (OR = 2.40, 95 per cent CI = 2.05 to 2.79, P < 0.0001).
Focusing on the above-mentioned 1127 animals, Table 4 presents the distribution of the interval (days) between out-movement and subsequent bovine TB disclosure for animals sold from ‘exposed’ herds in 2005, by time of animal movement relative to the herd bovine TB restriction in 2005. The mean time between out-movement and subsequent bovine TB disclosure was 126.4 and 354.4 days for animals that moved before and following the herd bovine TB restriction in 2005, respectively.
The focus of the national bovine TB control programme in Ireland targets herds as the epidemiological unit of interest. However, it is important to understand and better evaluate the risk that individual animals pose when moving from one farm to another farm.
The low prevalence of bovine TB in animals sold out from ‘attested’ herds indicates that the Irish national control programme is maintaining the risk of bovine TB at the animal level at low levels (0.69 per cent). However, despite the attested (bovine TB ‘free’) status granted to the source herds of these animals, nearly one percent (0.98 per cent) of animals originating from ‘exposed’ herds were classified as bovine TB-positive in the subsequent two years after being sold out from herds undergoing a bovine TB episode during 2005. Due to the contagious nature of bovine TB and the chronic development of the disease, our results support the hypothesis of a higher risk of bovine TB persisting among animals previously ‘exposed’ to M bovis by being in direct contact with infected (or previously infected) animals.
There is agreement that only certain tuberculous individuals act as effective disseminators, and they likely do so intermittently and only under certain circumstances (Morris and others 1994). It would not be reasonable to assume, nor possible to determine using the available data for this study, that all of the 2330 bovine TB-positive animals in the present study carried out the infection from the herds from which they were sold out during 2005. It could be possible that the cattle acquired infection after being sold out, either by contact with other cattle in the buyer herd or by infected wildlife reservoirs (badgers) in the buying herd (direct or indirect contact). The use of molecular techniques to differentiate strains of M bovis has proved useful in establishing associations in time and space between M bovis isolates from different cattle, and from cattle and badgers, both in Ireland (Roring and others 2004, Olea-Popelka and others 2005, Kelly and More 2011) and the UK (Smith and others 2003, Goodchild and otehrs 2012). However, M bovis strain-typing is not routinely conducted in Ireland, and no relevant data were available for cattle associated with the current study.
The present study confirms that the overall risk of bovine TB from attested (bovine TB ‘free’) herds is low; however, animals sold out from herds with a recent bovine TB episode have nearly twice the risk of developing bovine TB as compared with animals originating from herds without a previous recent bovine TB episode (Table 1).
In Table 2, the time (in days) between the date animals were sold out and the date in which animals were classified as bovine TB-positive indicated that half of the 1740 animals classified as bovine TB positive by the SICCT tested positive in less than a year from being sold out (median = 337 days). Twenty-five (25 per cent) of these animals tested positive within 153 days (approximately 5 months) of being sold out. Furthermore, five per cent of cattle (87 animals) that tested positive for bovine TB by the SICCT did so within 41 days (less than two months) of being sold out. While it cannot be definitively determined, based on the pathology and immunological response of animals to M bovis infection, the shorter the interval between being sold out and being classified as bovine TB positive, the greater the chance animals that animals were infected with TB at the time of movement from the seller herd. The present study results suggest that animals classified bovine TB positive within two months of being sold onward could certainly have brought the infection from the seller herd.
Among the animals identified as bovine TB-positive at slaughter by meat inspection, 25 per cent had tuberculous lesions within 116 days of movement (Table 2). Ten per cent (59 animals) had tuberculous lesions within 25 days of been sold out (less than one month). Based on the time needed for a lesion to develop after exposure and infection with M bovis (Cassidy 2006), these results are highly suggestive that animals identified with a bovine TB lesion at slaughter within 25 days of being sold out also brought the infection from the herds they came from.
Animals that were sold out of herds with a bovine TB episode in 2005 (exposed herds) before the bovine TB episode began (before the restriction date) had more than twice the odds of developing bovine TB in the subsequent two years compared the animals that moved out of the herd after the 2005 bovine TB episode cleared (after the clearance date) (Table 3). These animals, which remain within the ‘exposed’ herds, while they have a greater risk of developing bovine TB within the subsequent two years than animals from herds without a bovine TB exposure, have a lower risk of developing bovine TB than those animals that moved from ‘exposed’ herds before the start of the episode. Because herds in Ireland with a ‘reactor’ animal are re-tested at 60 day intervals until the herd has passed two clear herd tests, one can hypothesise that the lower risk of bovine TB to animals moving after the herd clearance is due to the rigorous and effective testing protocol in Ireland due to the removal of infected animals (reactors) during the bovine TB episode in 2005.
The visible lesion risk (number of animals deemed a reactor at a herd test with a tuberculosis lesion detected at postmortem examination) has been progressively falling (from 40 per cent in 1998 to 28.3 per cent in 2004) (Byrne, unpublished observations). While the true prevalence of bovine TB in cattle in Ireland is not known, this decrease in the number of reactor animals identified with bovine TB lesions may serve as an indicator of a true decrease in prevalence of the disease among the cattle population.
With regards to potential misclassification bias in our outcome variable (bovine TB positive), the authors recognise that the SICCT is not a perfect test. As a reasonable guide, the SICCT as administered in Ireland has a specificity (proportion of non-infected cattle that test negatively) of 99.8 to 99.9 per cent and a sensitivity (proportion of infected cattle that test positively) of between 68 per cent and 95 per cent (Monaghan and others 1994). Thus, it is likely that at the herd test, not all animals infected with M bovis are detected. In a study conducted in Australia, Corner (1994) concluded that the routine abattoir inspection had a low sensitivity and detected only 47 per cent of lesions compared with the number detected by the detailed inspection. Further, in Ireland, there is considerable variation between abattoirs in the effectiveness of surveillance to disclose TB lesions in attested Irish cattle (Frankena and others 2007, Olea-Popelka and others 2012). Thus, the authors recognise this limitation in the classification of the outcome in the present study. Nonetheless, the lack of sensitivity both for the SICTT and for slaughter meat inspection should be non-differential with respect to the bovine TB exposure status included in the present study.
The results of the descriptive study are consistent with the presence of residually infected cattle following herd derestriction following a bovine TB episode. Although residually infected cattle are not common, they result in an almost two fold (0.98 v 0.51) overall increase in future bovine TB risk (Table 1). This concern has been highlighted previously (Olea-Popelka and others 2008, Wolfe and others 2009, Clegg and others 2011b,c, Good and others 2011, Kelly and More 2011), and is a constraint in the Irish bovine TB national control programme. Several strategies are currently used to identify and remove residually infected, but SICCT-negative, animals. Following recent findings (Clegg and others 2011 b,c), national policy has changed and animals with an inconclusive SICTT test result are subsequently restricted to the herd of diagnosis until finally consigned to slaughter.
The use of a parallel testing in infected herds, generally using the interferon-γ assay, is being extensively in infected herds in Ireland to identify animals likely to be residually infected. The interferon-γ assay was not routinely used in Ireland at the time of this study, in 2005. The sensitivity of the testing system approaches 97 per cent when the SICCT and interferon-γ test are used in parallel (the animal is deemed positive if either test is positive) (Gormley and others 2003), highlighting the role of this test as an adjunct to the tuberculin test in problem (chronic) herds in particular, where removal of infected animals is a priority. This approach is limited to known infected herds, to limit problems of test specificity (Clegg and others 2011a).
The results from the descriptive study are important since they have identified potential constraints to the goals of the Irish bovine TB national control program. Further work, focusing on bovine TB risk at the animal level, would help to identify factors that are associated with an animal being classified as bovine TB positive. These are likely to include the bovine TB history of a seller herd, the severity and duration of an specific bovine TB episode before de-restriction on a seller herd, the location of the seller herd should be further investigated with regard the risk of bovine TB for animals being sold out. Also, when available in the future (as part of current undergoing work in Ireland), information about the risk posed by badgers in different geographical areas of Ireland should be added when possible into the risk assessment of bovine TB at the animal level. Specifically, as done in Ireland at the herd level by Griffin and others (2005) and Olea-Popelka and others (2009), associations between badger removal activities should be evaluated with regards their impact on the risk of bovine TB at the animal level. A better understanding and control of factors affecting the lack of identification of infected animals, as well the ability to manage and decrease the risk of infected animals leaving herds and carrying out the infection, would enhance current efforts to control bovine TB in cattle in Ireland.
Provenance: not commissioned; externally peer reviewed
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