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Outbreak of tuberculosis caused by Mycobacterium bovis in golden Guernsey goats in Great Britain
  1. R. Daniel, BVSc, BSc, MRCVS1,
  2. H. Evans, MA, BSc, VetMB, MRCVS2,
  3. S. Rolfe, BVetMed, MRCVS3,
  4. R. de la Rua-Domenech, DVM, PhD, DipECVPH, MRCVS4,
  5. T. Crawshaw, BVetMed, MRCVS5,
  6. R. J. Higgins, BVM&S, MSc, MRCVS,
  7. A. Schock, PhD, FRCPath, MRCVS6 and
  8. R. Clifton-Hadley, MA, VetMB, PhD, MSc, MRCVS7
  1. 1 Veterinary Laboratories Agency (VLA) — Carmarthen, Job's Well Road, Johnstown, Carmarthen SA31 3EZ
  2. 2 Animal Health, Ty Merlin, Parc Pensarn, Carmarthen SA31 2NF
  3. 3 TB Team, Office of the Chief Veterinary Officer, Welsh Assembly Government, Cathays Park, Cardiff CF10 3NQ
  4. 4 TB Programme, Defra, Nobel House, 17 Smith Square, London SW1P 3JR
  5. 5 VLA — Starcross, Staplake Mount, Starcross, Exeter EX6 8PE
  6. 6 VLA — Lasswade, Pentlands Science Park, Bush Loan, Penicuik, Midlothian EH26 0PZ
  7. 7 VLA — Weybridge, Woodham Lane, New Haw, Addlestone, Surrey KT15 3NB
  1. r.g.daniel@vla.defra.gsi.gov.uk

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BOVINE tuberculosis (TB), caused by Mycobacterium bovis, is a serious animal health problem in Great Britain. Both the incidence and geographical spread have increased since the mid-1980s, despite a longstanding test and slaughter policy recently enhanced by premovement testing, and interferon-γ (IFN-γ) blood testing (Anon 2008a, Defra 2009).

M bovis has a broad host range, and almost all mammalian species, including human beings, are susceptible to natural infection to varying degrees (O'Reilly and Daborn 1995, Cousins 2001). Although M bovis is maintained primarily in cattle, the Eurasian badger (Meles meles) has long been identified as a significant additional maintenance host that has hampered bovine TB eradication efforts in large tracts of the British Isles (Donnelly and others 2007). Consequently, there is potential for exposure to M bovis in domestic mammals sharing the same environment with the cattle and badger reservoirs. Indeed, a low number of M bovis infections are diagnosed each year in companion and farm animals kept in areas of high bovine TB incidence (Anon 2008a, Monies and others 2006, Twomey and others 2007). Goats, cats, pigs, camelids and sheep have long been recognised as incidental 'spillover' hosts of M bovis (Cousins 2001, Morris and others 1994). Although caprine TB is relatively common in some countries, it became extremely rare in Great Britain following the introduction of the first mandatory bovine TB eradication scheme in the 1950s (O'Reilly and Daborn 1995). Only five caprine isolates of M bovis from four different goat premises were recorded between 1971 and 2008 on the Veterinary Laboratories Agency (VLA) TB Culture Database (Anon 2008a; T. Crawshaw, unpublished observations).

This paper describes an outbreak of caprine TB due to M bovis infection that affected several linked goat herds in Wales and England, which was briefly reported in a letter by Crawshaw and others (2008). It includes descriptions of detailed epidemiological investigations, results of antemortem and postmortem diagnostic tests, and the measures adopted to bring the disease under control. The implications for goat herds reared in areas of endemic M bovis infection and the national goat industry in Great Britain are discussed.

Materials and methods

Tuberculin skin testing

Goats were screened for caprine TB by the single intradermal comparative cervical tuberculin (SICCT) test using Weybridge avian and bovine purified protein derivative (PPD) tuberculin (25,000 iu/ml). The technique was similar to that commonly used in Great Britain on young calves, and in accordance with Annex B to Council Directive 64/432/EEC (Anon 2008b). Avian tuberculin (0·1 ml) was injected into a clean clipped area of skin in the middle of the left side of the neck, and the same volume of bovine tuberculin was administered on the right side. SICCT test results were read after 72 hours, and any difference in skin fold thickness was initially assessed under standard interpretation, pending laboratory culture results to confirm the presence of M bovis. Tested goats were deemed to be positive reactors if they gave a skin response to bovine PPD of more than 4 mm greater than the avian PPD reaction. Repeat testing of individual test-negative goats in infected herds, where required, was carried out at 60-day intervals and using a more severe interpretation of the SICCT test, whereby an animal was classed as a reactor if the bovine PPD response exceeded the avian PPD response by more than 2 mm.

Pathology

Postmortem examinations were performed under standard operating procedures at VLA regional laboratories on 36 goats varying from three months to 10 years of age.

For histological examination, representative samples of gross suspect tuberculous lesions were fixed in an appropriate volume of 10 per cent neutral phosphate-buffered formalin. After trimming to 3 to 5 mm in diameter, the slices were transferred to Gooding and Stewart's decalcifying solution (Callis 2002) for four hours, rinsed in running water and then processed to paraffin wax blocks. Sections were cut at 4 μm and stained by both haematoxylin and eosin and cold Ziehl-Neelsen (ZN) for detection of acid-fast bacilli (Swisher 2002).

Mycobacterial culture method

Fresh tissues posted to the United Kingdom Accreditation Serviceaccredited TB culture laboratory at VLA — Weybridge were processed within five days of receipt. Each tissue was finely chopped and approximately 20 g was ground to a paste with sterile sand in a pestle and mortar; 30 ml of 5 per cent oxalic acid was then added and the mixture was transferred to a universal bottle. The homogenate was centrifuged twice for 10 minutes at 1100 g and resuspended in sterile 0·85 per cent saline; 300 μl of this suspension was inoculated on to each of three modified 7H11 slopes, two Lowenstein-Jensen base slopes, two Lowenstein-Jensen base plus pyruvate slopes, 2 Lowenstein-Jensen base plus glycerol slopes, three Stonebrink slopes, three Dubos slopes without mycobactin, three Dubos slopes with mycobactin, one 7H9 broth and one double-strength Dubos broth. Slopes were incubated at 37°C and examined initially at six weeks, then weekly for a total of 12 weeks. Organisms characteristic of mycobacteria were subsequently identified by spoligotyping (Kamerbeek and others 1997) and variable number tandem repeat (VNTR) typing (Smith and others 2006).

Epidemiological investigations

Detailed tracings were carried out based on movement records of the various herds implicated in the outbreak.

Results

Details of outbreak in herd A

On June 10, 2008, the carcase of a euthanased 4·5-year-old female golden Guernsey goat (A1) was submitted to VLA — Carmarthen for postmortem examination, as part of the VLA's small ruminant disease scanning surveillance programme. The goat had shown progressive condition loss, inappetence, intermittent coughing, and had not responded to symptomatic treatment by a private veterinary surgeon. Postmortem examination revealed two large encapsulated foci of necrosis containing yellow pus located in the left and right caudal lung lobes, and a number of smaller nodular lesions scattered through the rest of the lung lobes. ZN-stained smears from the lung lesions revealed acid-fast bacilli consistent with mycobacterial infection. The local Animal Health office was immediately notified of these suspicions and a farm investigation of the herd of origin in south-west Wales, herd A, was instigated.

Herd A comprised 20 golden Guernsey goats kept in three management groups: 16 females and youngstock (which had included the index case A1); two females purchased in February 2007; and two male yearlings (one of which had been purchased from herd B). The three distinct groups were housed and grazed separately.

On June 13, 2008 all 20 animals in herd A were screened by the SICCT test. Thirteen animals in the largest group were subsequently classed as positive reactors, with the remaining three animals testing negative. All 16 animals in this group (that is, 13 reactors and 3 incontacts), and the male animal sourced from herd B, were culled and submitted for postmortem examination. Twelve of the 13 reactors had gross lesions suggestive of mycobacterial infection. Culture proved positive for M bovis in all of these animals, as well as the one goat with no gross lesions (A2). There was no pathological or cultural evidence of M bovis infection in the four SICCT-negative animals slaughtered at the same time. Detailed individual SICCT test, postmortem examination and culture results are summarised in Table 1. The three remaining SICCT-negative animals in herd A gave negative results when re-tested in August and October 2008. TB movement restrictions were lifted in November 2008.

Herd A tracings

Herd A had been established with the purchase of a nanny and kid in April 2006, followed by three further female animals in June 2006, all sourced from herd Z in south-west Wales. A further three female animals were purchased in May 2007 from herd Z. One of these animals died within two weeks of arrival and was diagnosed with Clostridium perfringens type D enterotoxaemia, following postmortem examination at VLA — Carmarthen. A second animal died in October 2007, following a period of inappetence, weight loss, reduced milk yield and intermittent coughing. The remaining animal in this group was euthanased in May 2008, having shown chronic respiratory signs since autumn 2007. The latter two animals had been clinically examined by the private veterinary surgeon, but postmortem examinations were not undertaken.

During 2007, further goats had been sourced from herds in north-east Wales and southern England. Although clinical signs suggestive of caprine TB were never observed in these animals, some subsequently reacted positively to the SICCT test in June 2008. Because of these findings both source herds were investigated. Neither had a history suggestive of caprine TB and all the animals in these herds tested negative by the SICCT.

In March 2008, one of the goats purchased from herd Z in 2006 died after a six-week period of inappetence, weight loss and coughing, but a postmortem examination was not performed. A second animal from the same cohort was euthanased in June 2008, again after a period of inappetence, reduced milk yield and coughing. This animal was identified as the index case (A1) following postmortem examination at VLA — Carmarthen. Because circumstantial evidence pointed towards the introduction of M bovis infection to herd A by the cohort sourced from herd Z in May 2007, Animal Health extended its investigations to this herd.

Investigation of the source herd Z

The dispersal of animals from herd Z had begun with the sale of five goats to herd A in the spring of 2006, followed by further sales to herd A in the spring and early summer of 2007. All remaining stock within herd Z were dispersed to a number of premises during winter 2007/08, so that by April 2008 no goats remained on the premises. Difficulties in accessing movement records hampered the tracing exercise.

Although the owners had first kept goats in 1996, the nucleus of this golden Guernsey herd was established in 1997 with the purchase of four animals from two unrelated herds. The only reported subsequent additions had been male animals. Two female goatlings were retained each year as future breeding replacements. Surplus kids were sent for slaughter for meat. Herd numbers averaged 15 to 20 adult goats.

Adult females and kids were housed in a single purpose-built shed. Adult and weaned male kids were kept in a stable block. These two distinct groups grazed separately. All stock were penned overnight but were loose during the day, either within their respective buildings or at grass. The 10 ha farm also held five sheep, but no cattle. Secure farm boundaries prevented direct contact between resident goats and livestock on neighbouring farms, and adjacent common land primarily grazed by sheep. The farm was situated in an annual TB testing parish, and the wider area had experienced several bovine TB breakdowns in recent years.

Health problems were first reported in September 2007, when a nanny became inappetent and treatment with oxytetracycline was unsuccessful. In October 2007, the goat developed a cough and was examined by a private veterinary surgeon, who prescribed an anthelmintic and further antibiotics. The goat continued to deteriorate and died on October 14, 2007, but was not examined postmortem.

Three further animals showed clinical signs between December 2007 and April 2008, with the owner reporting a consistent history of in appetence accompanied by coughing. Despite intervention by a private veterinary surgeon, all the goats eventually died, and no postmortem examinations were carried out.

Herd Z tracings

All animals dispersed from herd Z since January 1, 2007 are believed to have been traced, involving nine goat premises in Wales and 10 in England. In addition, all herds understood to have had any contact with goats from herd Z, either through attendance at agricultural shows, or temporary visitations of females for natural service, were also contacted and any in-contact goats were skin tested.

Tuberculin skin test

SICCT-positive reactor goats were identified in a total of 10 herds, including the 13 reactors found in herd A. The ensuing tracing and TB testing exercise in all the herds that had received goats from herd Z resulted in the disclosure of a further 17 reactors in five smallholdings in south-west Wales (herds B to F) and four premises in England (herds G to J). All reactors were slaughtered, examined postmortem and subjected to mycobacterial culture (Table 1). In almost every case, M bovis infection was associated with the introduction of an animal reared in the adult female group of herd Z. The only exceptions were a nanny goat (G6) sent to herd Z from October 15 to November 16, 2007, for mating, and an adult male (J1), which had direct contact with infected females during attendance at two agricultural shows in 2007, and when mated with a homebred nanny in October 2007. Infection was not detected in other herds that had sent goats to the same shows as herd Z. There was evidence of dissemination of M bovis infection from the traced goats to resident animals in the index herd A and in herds G and H (Table 2). In the other herds, infected reactors were limited to the goats purchased from herd Z.

Following the initial suspicion of disease in goat A1, postmortem examinations were carried out on a total of 35 other golden Guernsey goats. SICCT test results, the distribution of gross lesions and mycobacterial culture results are presented in Table 1. In the tracing to herd J, goat J1 subsequently became a reactor at its second SICCT test, 60 days after the first SICCT test, and showed gross lesions at postmortem examination.

All animals with suspicious lesions had been previously identified as positive reactors using the standard SICCT test interpretation except for one kid in herd B, which was considered as a reactor only under the severe test interpretation. Because of the extensive lesions found at postmortem examination of the other reactors in herd A, a decision was made to immediately cull this animal (B1), which was subsequently shown to have gross tubercular lesions.

Pathology

At postmortem examination, lesions suspicious of mycobacterial infection were observed in 29 of 35 goats (Table 1) following the postmortem examination of the index case (A1). Eleven of the goats with lesions were between three and four months old. Necrotising lymphadenitis was detected in the thoracic lymph nodes of these 29 goats. Lesions in grossly affected lymph nodes were typically caseous, varying in size from pinpoint foci (Fig 1) to larger, focally mineralised lesions occupying most of the lymph node with a diameter of 0·5 to 2 cm (Fig 2). Similar multifocal to coalescent lesions were occasionally seen in tonsil and retropharyngeal and submandibular lymph nodes.

FIG 1

Multifocal necrotising mesenteric lymphadenitis in a 10-month-old goat (A3), caused by Mycobacterium bovis. Subcapsular pinpoint lesions can be seen on the cut surface of the mesenteric lymph node

FIG 2

Severe chronic extensive necrotising bronchial lymphadenitis with mineralisation in a three-month-old goat (A6), caused by Mycobacterium bovis. There is almost complete loss of architecture associated with copious amounts of caseous, gritty material on the cut surface of the bronchial lymph node

Following postmortem examination of the index case, chronic necrotising pneumonia was recorded in 21 of the 29 goats with lesions of the thoracic lymph nodes. Pulmonary lesions varied from 2 to 5 cm in diameter with larger cavitated lesions containing yellow pus (Fig 3). There was a predilection for the caudal lung lobes, but occasionally there was a more miliary distribution throughout the lungs. Chronic pleuritis was detected in one goat (A7).

FIG 3

Severe, chronic, focally extensive necrotising pneumonia in a goat (A6), caused by Mycobacterium bovis. A moderately well-encapsulated irregularly shaped focus of necrosis containing pus can be seen in the right dorsal lung

Extrathoracic lesions suggestive of a mycobacterial infection were recorded in 12 goats, all of which showed thoracic lymphadenitis and/or pneumonia. Mesenteric lymphadenitis was the most frequently observed non-respiratory lesion (11 animals), and in one instance it was associated with granulomatous ileitis (A6). Multifocal hepatitis was observed in five animals (Fig 4) and splenitis in one animal (E1). It was notable that many of the infected goats were still in good body condition when presented for postmortem examination, with reasonable fat reserves despite extensive pathological changes.

FIG 4

Chronic, multifocal necrotising hepatitis in a three-year-old goat (E1) caused by Mycobacterium bovis. There are multiple, randomly distributed, irregularly shaped, soft white foci on the external and cut surfaces

Histopathological examination of lesions in all affected tissues showed typical features of granulomatous inflammation, with central caseous necrosis and mineralisation surrounded by a mantle of macrophage and Langhans-type multinucleate giant cells, with variable numbers of lymphocytes and plasma cells surrounded by a partial or complete fibrous capsule. Acid-fast bacilli varying in numbers from sparse to numerous were usually detected in macrophages and giant cells or free within the coagulum. In some lesions, clusters of neutrophils and degenerate leucocytes were present at the interface between viable and non-viable tissue. Only very occasionally were acid-fast bacilli not found in lesions after a thorough search of the ZN-stained section. Suspicious focal lesions in the mammary glands of two goats were associated with chronic interstitial mastitis, with no evidence of mycobacterial infection.

There was a strong correlation between a positive SICCT test and mycobacterial culture results (Table 3).

Mycobacterial culture

M bovis genotype SB0140: 7-5-5-5*-3-2.1 (known in Great Britain as VLA genotype 9:b) was identified in all goats with a positive isolate, with the exception of D1, E1 and H3, in which VNTR analysis failed. These three isolates were nevertheless subsequently classified by spoligotyping as SB0140 (VLA spoligotype 9). The correlation between the SICCT test and mycobacterial culture results is shown in Table 3, which demonstrates a significant correlation between a positive skin test and mycobacterial infection.

Discussion

Caprine TB is usually associated with M bovis infection (O'Reilly and Daborn 1995, Cousins 2001). Goats are also susceptible to Mycobacterium tuberculosis, Mycobacterium avium and Mycobacterium kansasii (Lesslie and others 1960, Bernabé and others 1990-91a, 1990-91b, Acosta and others 1998), but these organisms are considered far less common causes of caprine TB. A goat-adapted strain (ecotype) of the M tuberculosis complex, known as M caprae (Aranaz and others 2003), has recently emerged in central and southern Europe as a genetically and phenotypically distinct agent of TB in goats, cattle, deer, wild boar, exotic ungulates and human beings (Prodinger and others 2002, Kubica and others 2003, Pate and others 2006, Ikonomopoulos and others 2006, Cvetnic and others 2007, Duarte and others 2008).

In the present extended outbreak, M bovis was initially cultured from 13 goats examined postmortem as SICCT test reactors in the disclosing herd A and subsequently identified in 17 other positive reactors from nine different goat herds traced from the dispersed source herd Z. Genotype 9:b, the predominant molecular type of M bovis in southwest Wales, was consistently recovered from these goats. This particular genotype comprised almost 7 per cent of cattle isolates in the VLA Spoligotype Database in 2007. This strain is geographically localised to cattle in south-west Wales (Pembrokeshire, west Carmarthenshire, south Ceredigion and the Gower Peninsula) and is seldom found further afield. Despite extensive tracings, no other caprine source of M bovis infection was identified in this widespread outbreak, suggesting that herd Z was likely to have initially contracted the infection locally. Breeding male goats had been the only purchases in the past 10 years. Cattle had never been kept on the property and direct contact with cattle on neighbouring farms was not possible. A contiguous cattle herd had experienced a bovine TB breakdown with M bovis infection four years earlier. More recently, the same herd had an IFN-γ test reactor, but no lesions were detected at slaughter. Movement restrictions were lifted from this cattle herd in November 2008 following a herd SICCT test with negative results. Other bovine TB herd breakdowns with culturepositive, lesioned reactors had been reported in the same parish during the previous 10 years. Based on the absence of direct contact with infected cattle, the local pattern of bovine TB breakdowns and reported badger activity on an adjacent cattle farm, it is probable that infected local wildlife was the source of M bovis infection for herd Z.

In many countries, caprine TB in both domestic and feral goats occurs as a result of contact with cattle and wildlife reservoirs infected with M bovis, and therefore goats have historically been regarded as an accidental spillover host in areas with endemic bovine TB (Morris and others 1994). Until now, this appears to have been the situation in Great Britain. Goats are not, however, dead-end hosts of M bovis. Infected goats with active pulmonary or udder lesions can spread infection within their cohort and to other in-contact susceptible species, including human beings, thus posing a significant animal and public health risk (O'Reilly and Daborn 1995, Cousins 2001). Furthermore, the role of a given animal species in the transmission of M bovis may change over time, or between geographical regions. Under certain conditions, M bovis infection might therefore be self-sustaining in a defined goat population. There is no evidence at present that caprine TB is established in the wider British goat population, in contrast to some Mediterranean countries where domestic goats, together with cattle, act as maintenance hosts and a reservoir of M bovis infection for other species (Bernabé and others 1990-91a, 1990-91b, Cousins 2001, Aranaz and others 2003, Ikonomopoulos 2006). M bovis was isolated from approximately 100 samples from Spanish goats between 1993 and 1998 (Gutiérrez and others 1998). In regions of Spain where the incidence of bovine TB is relatively high, commercial goat herds are regularly included in the TB eradication programme (Acosta and others 1998, Seva and others 2002, Álvarez and others 2008). M bovis infection in domestic goats has also been reported sporadically in France, Germany, Italy, the USA, Africa, India, Taiwan and Australia (O'Reilly and Daborn 1995, Cousins 2001), and more recently in Portugal (Duarte and others 2008) and Ireland (Anon 2008c), but published reports have provided little accurate information on herd or animal prevalences. In New Zealand, prevalences of up to 31 per cent were reported in feral goats in the 1980s in bovine TB-endemic areas (Sanson 1988). Accurate prevalences of M bovis infection in goats in developing countries are similarly unrecorded, although caprine TB is probably widespread in areas where goats co-graze with cattle herds that are not subject to rigorous TB test and slaughter regimes (O'Reilly and Daborn 1995, Cousins 2001, Ayele and others 2004, Hiko 2005, Nigussie 2005).

O'Reilly and Daborn (1995) comprehensively reviewed M bovis infection in various animal species and human beings, including historic case studies and surveys of caprine TB in Great Britain and other countries. The first recorded case of natural M bovis-associated caprine TB in Great Britain was in 1917, involving a young goat reared on raw cow's milk. Other isolated cases were reported in Great Britain during the first half of the 20th century, at a time when more than 40 per cent of cows in dairy herds were estimated to be infected (Luke 1958). The compulsory Area Eradication Plan for bovine TB (the forerunner of the current cattle TB test and slaughter regime) was launched in 1950. A severe outbreak of caprine TB in an experimental herd of 75 goats in the early 1950s was reported retrospectively by O'Reilly and Daborn (1995). In the past three decades, reports of caprine TB have been extremely rare in Great Britain despite a high incidence of bovine TB in southwest England, the West Midlands and south Wales.

Before the present outbreak, only five goats infected with M bovis on four different farms had been recorded on the VLA's TB Culture Database between 1971 (when the VLA's TB submission records began) and 2008, all of them in bovine TB-endemic localities. The first of these isolates, in 1981, originated in west Wales. The second, in 1996, was from small tubercular lesions found at slaughter of a SICCT-positive reactor goat kept on a cattle farm in south-east Wales experiencing a bovine TB breakdown (J. Montague, personal communication). The third incident, in 2007, involving a female golden Guernsey and a female pygmy goat on a smallholding in north Wiltshire, was associated with the same local strain of M bovis (Anon 2008a). The latest M bovis isolate in April 2008, from a diseased Angora goat co-located with a small herd of infected llamas in south-west Wales, was unrelated to the present outbreak. This list is not necessarily exhaustive as previous preclinical cases of M bovis infection in goats might have gone undetected, and clinical cases might have been misdiagnosed as other chronic conditions. Infected goats in herd A showed inappetence, reduced milk yield and coughing in particular, but no progressive loss of condition that might have alerted the attending private veterinary surgeon to the possibility of caprine TB.

According to the 2008 Annual June Survey of Agriculture and Horti culture in the UK, there are an estimated 96,000 goats in the UK, 82,000 of which are distributed across 6400 holdings in England; however, more than half of the goat population is concentrated in only 79 holdings (Anon 2008d). Approximately half of the English goat population is kept in the south-west and Yorkshire regions (Defra 2004). The size of the goat population in Wales is 7100 animals in 1200 holdings. The UK goat meat industry is small, with approximately 8850 goats slaughtered for meat production in 2008. There is no routine TB testing programme for goat herds in Great Britain, although goats may be privately SICCT tested by prior arrangement between the owner and the local Animal Health office. Nevertheless, if M bovis infection is identified in goats, or if goats happen to be co-located with an infected cattle herd, the animals will be placed under movement restrictions until they have been SICCT tested at the Government's expense and found to be free from infection. Any goats identified as forward or back tracings from an infected goat herd must also undergo skin testing at the Government's expense. Additionally, Animal Health will give consideration to testing any goats that are contiguous to TB-infected cattle herds. Surveillance for caprine TB at present relies on meat inspection of goats slaughtered for human consumption, scanning surveillance of goat carcases submitted to the VLA, and by attending private veterinary surgeons reporting any suspect clinical cases or fatalities. Because statutory notification to Animal Health of any suspect caprine TB lesions detected at postmortem examination has been mandatory only since March 2006, it is likely that the true prevalence of caprine TB in Great Britain has been underestimated. Until scientifically validated statutory or voluntary caprine TB screening programmes are implemented, there is a danger that uncontrolled movement of untested, preclinically infected goats might result in the dissemination of M bovis infection to naive goat herds. It would be of great concern if infection were introduced by goats to cattle in areas with a low prevalence of bovine TB.

The cornerstone of TB control is the accurate detection and removal of infected animals before they become infectious to other animals. The limited non-specific clinical signs described so far in goats may not always alert private veterinary surgeons to the possibility of caprine TB. Effective antemortem diagnosis of caprine TB must therefore rely on detecting immunological markers of infection with M bovis. Compared with cattle, however, there is relatively little validated information on the accuracy of TB screening tests for live goats. The performance of the tuberculin skin test, the IFN-γ blood test (Bovigam; Prionics) and some serological assays has been evaluated in goats. Thoen and others (1984) suggested that the SICCT test was a reliable method of screening goats for M bovis infection, a view subsequently supported by Cousins and Florisson) (2005 and by experimental studies (Gomes da Silva and others 2006). Gutiérrez and others (1998) evaluated the diagnostic accuracy of the SICCT test and in vitro TB tests on 63 goats from infected herds, and 13 goats from non-infected herds in Spain that were subsequently subjected to postmortem examination and mycobacterial culture. Because the SICCT test was shown to have a sensitivity of 83·7 per cent and a specificity of 100 per cent the authors suggested that the SICCT test was reliable for the detection of caprine TB in goats in the early and middle stages of an eradication programme, even when herds were co-infected with M avium subspecies paratuberculosis. Sensitivities in excess of 80 per cent have been estimated for the IFN-γ test in goats (Gutiérrez and others 1998, Liébana and others 1998). As with cattle, the greatest diagnostic sensitivity was achieved by using the SICCT and IFN-γ tests in tandem, although this did result in reduced specificity relative to using the SICCT test alone. However, a more recent study conducted in a naturally infected goat herd in Spain has reported lower sensitivities for the SICCT and IFN-γ tests than previously described, and also cautioned that intercurrent paratuberculosis can have a deleterious effect on the sensitivity of the tests (Alvarez and others 2008). The authors' observations from the present investigation revealed a high positive predictive value for SICCT in goats, as every reactor identified subsequently proved positive on culture and all but one had lesions at postmortem examination.

There are no detailed descriptions of histopathological findings in M bovis-associated caprine TB. The authors' observations indicate a similar reaction to that recognised in cattle with bovine TB with extensive caseous necrosis, mineralisation and multinucleate giant cells. A systematic search is, however, essential to ensure detection of the often low number of acid-fast bacilli present in lesions.

The authors' findings suggest that golden Guernsey goats may have a particular susceptibility to M bovis infection, but this hypothesis could not be tested in the absence of other goat breeds within these infected herds. Caswell and Williams (2007) stated that 'the final determinants of the nature and intensity of TB lesions are the magnitude of bacterial infection, the intensity and appropriateness of the immune response and the modifying influence of the structures of the tissues involved'. The often extensive pneumonic lesions, especially those showing liquefactive necrosis, would facilitate the escape of viable mycobacteria into adjacent airways with potential aerosol spread from infected sputum. There may also have been internal dissemination via the intestine and mesenteric lymph notes with likely faecal contamination of the environment. Another notable feature of this outbreak was the number of young goats ages between three and 12 months, dispersed from herd Z, that were found to have lesions at postmortem examination. The majority of these young goats had extensive lesions that would favour aerosol spread of infection in herd Z. Fetal exposure in utero, and/or consumption of infected colostrum and milk, were other possibilities that could not be evaluated, as postmortem examinations were not carried out on the dams in herd Z.

Private veterinary surgeons should be aware of the zoonotic risk when attending goats, of all ages, showing the suggestive clinical signs reported here. The SICCT test, which is a reliable test for caprine TB in live animals, can be performed only by agreement with the local Animal Health office. VLA regional laboratories are able to undertake postmortem examination and mycobacterial culture on suspect tuberculous goats as part of their surveillance activities for TB in domestic animals other than cattle.

Acknowledgements

The authors thank Angela Wheeler-Stimson and Edward Jones, for photography, and all staff at VLA — Carmarthen, VLA — Luddington, VLA — Shrewsbury, VLA — Winchester and VLA — Lasswade for their work during this investigation. They also thank Noel Smith of VLA — Weybridge for genotyping data, and K. Gover, M. Okker and J. Dale for their excellent technical assistance. They acknowledge the staff at Animal Health offices in Carmarthen, Gloucester and Shrewsbury for their assistance during the investigation. The investigations carried out by the VLA were funded by Defra under the small ruminant scanning surveillance contract (ED1100), and the TB in species other than badgers and cattle contract (SB4510).

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