Tuberculosis in alpaca (Lama pacos) on a farm in Ireland. 1. A clinical report
© The Author(s) 2008
Published: 1 August 2008
This case report describes tuberculosis (TB) due to infection with Mycobacterium bovis (M. bovis) in alpaca (Lama pacos) on a farm in Ireland. Two severely debilitated alpaca were presented to the University Veterinary Hospital, University College Dublin in November 2004. Bloods were taken, and haematology and biochemistry results were indicative of chronic infection. Radiological examination showed evidence of diffuse granulomatous pneumonia suggestive of tuberculosis. On necropsy there were granulomatous lesions present throughout many body organs including lung, liver, kidney, intestine as well on peritoneum and mesentery. Culture of acid-fast bacilli from lesions led to a diagnosis of tuberculosis due to M. bovis. The use of intradermal skin testing proved inefficient and unreliable for ante mortem diagnosis of tuberculosis in alpaca. Infection due to M. bovis should be considered among the differential diagnoses of debilitating diseases in alpaca, particularly those farmed in areas known to be traditional black spots for tuberculosis in cattle.
This case report describes tuberculosis (TB) due to infection with Mycobacterium bovis in alpaca (Lama pacos) on a farm in Ireland.
The alpaca herd was established in Ireland following the importation of 16 foundation stock (15 adults and one juvenile male) from Peru and Chile in 2000, nine from Northern Ireland in 2002 and four from Australia in 2003. The imported animals had all passed through quarantine (which included tuberculin testing using the single intradermal comparative cervical test, SICCT) in Belgium or Northern Ireland, en route to Ireland. They were farmed on newly reclaimed, double-fenced land, contiguous to cattle herds, in an area populated by badgers and wild goats. An eclectic range of health problems was noted from the outset, resulting in some deaths, including: skin disease, strongylosis, weight loss, fascioliasis, rickets, cardiomyopathy, trauma and 'chill'. Some alpacas died unexpectedly. The local veterinary practitioner was requested to investigate some of these deaths. However, few losses were examined post mortem, mainly due to legislative and commercial factors inhibiting on-farm post mortem examination and also due to distance of the alpaca farm from diagnostic laboratories. In October 2004, following the earlier death of three alpaca (A, B and C), the owner sought assistance with three ill alpaca.
Investigation: on-farm and ARVL
Key clinical and clinicopathological findings associated with TB in alpaca during this investigation
Severe weight loss
Harsh lung sounds
Chronic ill thrift
Albumin:globulin ratio less than one
Investigation: University Veterinary Hospital
Post mortem examination
On post mortem examination, animal D showed tuberculous lesions throughout the lungs and in the liver and hepatic, bronchial, mediastinal and mesenteric lymph nodes. Acid-fast bacteria typical of mycobacteria were detected in smears from these organs and in tracheal secretions. Disseminated miliary TB was noted. Following euthanasia of E, miliary TB was also confirmed on post mortem examination. Pulmonary involvement was less pronounced (that is, less lung tissue was affected), but abdominal lesions were more extensive. Granulomatouslike lesions were widespread within the peritoneum, mesentery and also present in the liver, kidneys, intestines and mesenteric lymph nodes. Presumed infected, the two cohort animals were later euthanased but no gross pathological evidence of TB was detected.
Bacteriology for M. bovis was carried out at the Central Veterinary Research Laboratory. Tissues from D and E were submitted for decontamination and culturing [5, 6], and isolates were identified based on colony morphology, growth rate, pigmentation and cording characteristics  and by AccuProbe (Gen-Probe Inc., San Diego, California, USA) and GenoType MTBC (Hain Diagnostika, Nehren, Germany). M. bovis was isolated from tuberculous tissue from both animals.
In many countries, TB in animals, generally due to infection with M. bovis, is of significant economic and zoonotic importance [15, 7, 17]. Cases of TB in South American camelids (llama, alpaca, vicuña and guanaco) in their natural habitat are believed to be rare, even though TB is endemic in local cattle, sheep and humans . However, there are reports of infection in South American camelids held in close association with other infected animals, and grazing near infected cattle and badgers in the UK [2, 18]. TB in camelids is not due solely to M. bovis; M. microti  and M. kansasii  have also been reported. The predominant clinical sign seen in this herd was weight loss. Harsh lung sounds were also present, but only in advanced cases. There was no evidence or history of diarrhoea. At the initial farm visit, differential diagnoses were considered, including type 2 ostertagiosis, Johne's disease and hypocuprosis/trace element deficiencies (selenium/vitamin E), as ill-thrift and weight loss is a feature of each of these conditions, whereas diarrhoea is not common with ostertagiosis type 2 or hypocuprosis. Diarrhoea is a feature of Johne's disease in cattle, but not sheep . There was no evidence of these conditions from the laboratory tests performed. TB has not been reported as a major health problem of camelids, either in their natural habitat in South America or when kept under farmed conditions in other countries. Regardless, Buick  notes that TB should be considered in the differential diagnosis in all cases of ill-thrift in this species, with or without respiratory signs. In the outbreak reported here, clinical suspicion of TB was confirmed using post mortem examination, with confirmatory bacteriology and histopathology. Nonetheless, differential diagnoses will require investigation, especially if post mortem investigations cannot be carried out.
Difficulty in the ante mortem diagnosis of TB
The ante mortem diagnosis of TB in these cases was problematic. On this farm, the five cases were negative to all tuberculin tests. According to Buick , the SICCT test offers reasonable sensitivity and specificity in alpaca, and is the official test in the UK for imported camelids. However, in the authors' experience, the SICCT (and particularly the intradermal injection of PPD) was difficult to perform consistently, due to the fine skin of the alpacas tested. It is for this reason that the authors also conducted the SICAT test (using the skin of the axilla rather than the cervical skin), as internationally advocated by some veterinary services and the llama/alpaca industry . Because each of these cases had advanced pathology, it is possible that they were anergic to these tests . Although animal E was 'positive' to the LTA, the reaction was indicative of infection with M. avium rather than M. bovis, and it is worth noting that the LTA has not been validated for use in alpaca. According to Buick , the IFN-γ test (BovigamR) is also not a valid test for the diagnosis of TB in camelids and therefore was not used. Furthermore, there is little evidence that detection of humoral antibody (using methods such as the ELISA) would be a useful indicator of field infection . Among a broad range of other laboratory tests, only the A:G ratio proved useful. This finding is suggestive of a non-specific response to a long-term immune challenge, such as infection with M. bovis. In this herd, a low A:G ratio (specifically less than 1.0) was suggestive of infection risk. Indeed, the lower the A:G ratio, the higher the risk of disease being established. The absence of a reliable ante mortem test prohibited early identification of infected individuals.
Post mortem examination
Post mortem examination of alpacas was a significant part of the investigation permitting definitive diagnosis of TB heretofore presumptively diagnosed by clinical and clinicopathological means. Five alpaca showed well-established and extensive TB lesions confirmed by histopathology and bacteriology. The finding of so-called 'open TB', characterised by leakage of caseo-necrotic material into the bronchial tree, may have increased the risk of transmission of infectious aerosols to herd mates, to cattle in contiguous herds, to wildlife and to human contacts, with the alpaca herd acting as a propagating source. In the absence of a reliable ante mortem test, it was not possible to reliably identify individual alpaca as infected or diseased. Consequently, the whole flock had to be treated as one infected unit.
The infection load within the herd was likely to have been high. Infection had established in at least five animals, and there may have been further infected animals prior to the on-farm investigation. The TB status of these latter animals was unknown as post mortem examinations had not been carried out. Against this, the two healthy cohorts sent to UVH with animals D and E, although presumed infected by contact, showed no gross lesions of TB on post mortem examination. It was also noted that the juvenile alpaca, which presented ill on November 8, and which had shown weight loss along with a low A:G ratio, had recovered uneventfully. Despite these latter considerations, there appeared to be a significant risk of animal-to-animal and animal-to-human transmission within this herd. Primarily as a precautionary health and safety principle, total herd depopulation was recommended. However, this recommendation was rejected by the herd owners on financial grounds. In the absence of depopulation, protective measures were put in place, including isolation of diseased animals, euthanasia of cases with respiratory symptoms should they occur, improved animal hygiene measures and personal protective measures, e.g., using disposable gloves, masks, aprons, rubber boots, and disinfectant.
In retrospect, the diagnosis of TB in farmed alpaca in Ireland is not surprising. A range of risk factors are present, including: the presence of M. bovis in both South America and Ireland; the possible introduction of latent TB infection in imported alpacas; probable direct or indirect contact of alpacas with TB reactor cattle; and the uncontrolled movement of the badger, a TB reservoir species. However, at the time of diagnosis, a range of questions had not been answered, including the TB infection risk for alpaca farmed in areas where TB is endemic, the origin of the infection, the potential for alpaca-to-alpaca transmission and appropriate control measures, including the efficacy of predictor tests. These questions have been examined in a subsequent epidemiological investigation, and are presented separately .
The authors thank Hester McAllister for expert radiological assistance.
- Australian Alpaca Association Inc: Body condition score (BCS) of alpacas. Alpaca Note No 4/03. 2001, Last accessed 11 January 2008, [http://www.alpaca.org.nz/downloads/bcs.pdf]Google Scholar
- Barlow AM, Mitchell KA, Visram KH: Bovine tuberculosis in llama (Lama glama) in the UK. Veterinary Record. 1999, 145: 639-640. 10.1136/vr.145.22.639.View ArticlePubMedGoogle Scholar
- Buick W: TB in domestic species other than cattle and badgers. Government Veterinary Journal. 2006, 16: 87-91.Google Scholar
- Connolly DJ, More SJ, Dwyer PJ, Hayes M, Ryan EG, Costello E, Kilroy A: Tuberculosis in alpaca (Lama pacos) on a farm in Ireland. 2. Results of an epidemiological investigation. Irish Veterinary Journal. 2008, 61 (8): 533-537.PubMed CentralView ArticlePubMedGoogle Scholar
- Collins CH, Grange JM, Yates MD: Tuberculosis bacteriology: organization and practice. 1997, Butterworth-Heinemann, Oxford, SecondGoogle Scholar
- Costello E, Quigley F, Flynn O, Gogarty A, McGurk J, Murphy A, Dolan L: Laboratory examination of suspect tuberculosis lesions detected on abattoir post mortem examination of cattle from nonreactor herds. Irish Veterinary Journal. 1998, 51: 248-250.Google Scholar
- Cousins DV, Dawson DJ: Tuberculosis due to Mycobacterium bovis in the Australian population: cases recorded during 1970-1994. International Journal of Tuberculosis and Lung Disease. 1999, 3: 715-721.PubMedGoogle Scholar
- Cousins DV, Florisson N: A review of tests available for use in the diagnosis of tuberculosis in non-bovine species. Revue scientifique et technique - Office International des Epizooties. 2005, 24: 1039-1059.Google Scholar
- Dalley D, Chambers MA, Cockle P, Pressling W, Gavier-Widén D, Hewinson RG: A lymphocyte transformation assay for the detection of Mycobacterium bovis infection in the Eurasian Badger (Meles meles). Veterinary Immunology and Immunopathology. 1999, 70: 85-94. 10.1016/S0165-2427(99)00072-0.View ArticlePubMedGoogle Scholar
- Fowler ME: Infectious diseases. Medicine and Surgery of South American Camelids (Llama, Alpaca, Vicuña, Guanaco). 1998, Iowa State University Press, Ames, 148-194. SecondGoogle Scholar
- Frost B: Research update on diagnostic tests for tuberculosis in llamas/alpacas. Proceedings of the 102nd Annual Meeting of the United States Animal Health Association, Minneapolis, Minnesota, USA. 3 - 9 October 1999. 1999Google Scholar
- Johnson CT, Winkler CE, Boughton E, Penfold JWF: Mycobacterium kansasii infection in a llama. Veterinary Record. 1993, 133: 243-244. 10.1136/vr.133.10.243.View ArticlePubMedGoogle Scholar
- Lepper AWD, Pearson CW, Corner LA: Anergy to tuberculin in beef cattle. Australian Veterinary Journal. 1977, 53: 214-216. 10.1111/j.1751-0813.1977.tb00188.x.View ArticlePubMedGoogle Scholar
- Oevermann A, Pfyffer GE, Zanolari P, Meylan M, Robert N: Generalized tuberculosis in llamas (Lama glama) due to Mycobacterium microti. Journal of Clinical Microbiology. 2004, 42: 1818-1821. 10.1128/JCM.42.4.1818-1821.2004.PubMed CentralView ArticlePubMedGoogle Scholar
- O'Reilly LM, Daborn CJ: The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tubercle and Lung Disease. 1995, 76 (Supplement 1): 1-46.View ArticlePubMedGoogle Scholar
- Radostits OM, Gay CC, Hinchcliff KW, Constable PD: Veterinary Medicine: a textbook of the diseases of cattle, horses, sheep, pigs and goats. 2007, Saunders Elsevier, EdinburghGoogle Scholar
- Robert J, Boulahbal F, Trystram D, Truffot-Pernot C, de Benoist A-C, Vincent V, Jarlier V, Grosset J: A national survey of human Mycobacterium bovis infection in France. International Journal of Tuberculosis and Lung Disease. 1999, 3: 711-714.PubMedGoogle Scholar
- Twomey DF, Crawshaw TR, Anscombe JE, Farrant L, Evans LJ, McElligott WS, Higgins RJ, Dean G, Vordermeier M, Jahans K, de la Rua-Domenech R: TB in llamas caused by Mycobacterium bovis. Veterinary Record. 2007, 160: 170-10.1136/vr.160.5.170.View ArticlePubMedGoogle Scholar