Humans as source of Mycobacterium tuberculosis infection in cattle, Spain.
Recent studies have reported isolation of M. tuberculosis in cattle with prevalences of 4.7%-30.8% in African and Asian countries (1-3). In cattle, this infection occurs in countries with the highest incidence of human tuberculosis in the world. In Europe, only 14 cases of M. tuberculosis infection have been described in 3 eastern countries since implementation of eradication programs (4,5). The only reported cases of M. tuberculosis in cattle in western Europe were described in Great Britain and date back to the 1950s (6).
During 2007-2009, three cases of tuberculosis caused by M. tuberculosis were detected in 3 unrelated cattle farms, 2 of them free of tuberculosis (farms 1 and 2). As part of the surveillance system of bovine tuberculosis, a pool of tissue samples from each cow (respiratory lymph nodes and lung) were homogenized with sterile distilled water, and culture was carried out by the BACTEC mycobacteria growth indicator tube 960 system (Beckton Dickinson, Madrid, Spain). Members of the M. tuberculosis complex were identified and genotyped by direct variable repeat spacer olig-nucleotide typing and mycobacterial interspersed repetitive unit-variable number tandem repeat (MIRU-VNTR) typing (7).
The 3 M. tuberculosis-infected animals were <9 months of age (Table). As described (6), the possibility of infection in young animals could be more probable than infection in older cows.
M. tuberculosis-infected animals from farms 1 and 3 were detected by the intradermal tuberculin test (Table). The animal without immunologic response (farm 2) was detected because an M. bovis infection was confirmed in the herd, and all animals were slaughtered. Confirmation of infection by culture without immunologic response is rare, although the high sensitivity of the mycobacteria growth indicator tube system could detect a low bacterial load in the initial stages of infection. Recent implementation of liquid systems in animal health laboratories has enabled detection of M. tuberculosis when it is compared with results using only conventional methods. Moreover, no tuberculosis-compatible lesions were observed in the 3 animals, similar to previous studies (6). On the basis of these facts, M. tuberculosis transmission was not detected among cattle in the following intradermal tuberculin tests.
Co-infection with other mycobacteria (M. avium subsp. hominissuis) was found in the same animal from farm 1 (Table). This co-infection suggested the immunocompromised status of the animal and hence a high susceptibility to M. tuberculosis infection. Moreover, M. bovis was isolated from 52% (16/31) of all animals from farm 2 that showed a positive reaction to the intradermal tuberculin skin test, making remarkable the absence of co-infection with M. bovis in the M. tuberculosis-infected animal. Therefore, the lack of M. tuberculosis transmission within this herd contrasts with the M. bovis dissemination.
The veterinary services reported these findings to the National Public Health System, and an epidemiologic investigation was conducted on the cattle farms to determine the source of infection. In all cases, staff of the farms had active tuberculosis (Table). Three different strains were characterized: SIT2537 (octal code 777617777720771), 253533233433236252211423 (farm 1); SIT1564, 3'5233423245545725121 3423 (farm 2); and SIT58, 254343 243232325262213423 (farm 3) (Table). The MIRU-VNTR pattern and spoligotype are shared by Spanish human and cattle isolates from farm 1; SIT2537 is an uncommon profile that has been detected in Brazil and Spain (according to the SITVIT2 database). The human strain showed multidrug resistance to isoniazid, rifampin, and ethionamide. In cattle and human isolates, genes associated with isoniazid and rifampin resistance were studied (8) and rpoB analysis confirmed rifampin resistance (Ser531Leu). In farm 2, the origin of the farm worker was eastern Europe and the cattle isolate showed an SIT1564 profile, which is found only in 6 human isolates in the SpolDB4 database, all from Poland, Bulgaria, and Russia. On farm 3, human and cattle isolates from Spain shared identical spoligotype and MIRU-VNTR patterns. The profile SIT58 is frequent in Spain (9) and other countries with historical links to Spain, mainly the south American countries (79/114 according to Spol DB4).
A well-designed program for eradicating bovine tuberculosis helps to detect M. tuberculosis infection by immune response or by bacteriologic culture. The use of liquid systems and results of epidemiologic studies (Spanish Database of Animal Mycobacteriosis, mycoDB.es) (S. Rodriguez, unpub. data) are recommended for prompt confirmation of the M. tuberculosis complex infection and for enhancing the sensitivity of culture. In addition, the Spanish Ministry of Environment, Rural and Marine Affairs has reinforced the need to improve cooperation between human and animal health systems to minimize the risk for M. tuberculosis complex transmission from animals to humans or vice versa and to control infection in all susceptible animal species (10).
doi: http://dx.doi.org/ 10.3201/eid1712.101476
We thank L. Carbajo, J. Carpintero, E. Fernandez, and L.M. Alvarez for their continuous encouragement; F. Lozano, N. Moya, A. Gutierrez, J. Gimeno, A. Penedo, A. Menendez, C. Martinez, and J.A. Anguiano for technical help; R. Daza and M.S. Jimenez for providing the human strains and related data; Nalin Rastogi for comparison of spoligotyping results with the SITVIT2 proprietary database; and M. Gilmour for careful revision of the manuscript.
This research was funded by project TB-STEP FP7-KBBE-2007-212414 of the European Union and by the Spanish Ministry of the Environment, and Rural and Marine Affairs and partially by Fondo de Investigaciones Sanitarias (FIS S09/02205). B.R. received a research contract funded by Comunidad de Madrid (IV regional framework program of research and technological innovation 2005-2008).
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Beatriz Romero, Sabrina Rodriguez, Javier Bezos, Rosa Diaz, M. Francisca Copano, Isabel Merediz, Olga Minguez, Sergio Marques, Juan J. Palacios, Dario Garcia de Viedma, Jose Luis Saez, Ana Mateos, Alicia Aranaz, Lucas Dominguez, and Lucia de Juan
Author affiliations: Universidad Complutense, Madrid, Spain (B. Romero, S. Rodriguez, J. Bezos, A. Mateos, A. Aranaz, L. Dominguez, L. de Juan); Consejeria de Medio Ambiente, Vivienda y Ordenacion del Territorio, Madrid (R. Diaz); Laboratorio de Sanidad Animal de Jove, Gijon, Spain (M.F. Copano, I. Merediz); Consejeria de Agricultura y Ganaderia, Valladolid, Spain (O. Minguez, S. Marques); Hospital Universitario Central de Asturias, Oviedo, Spain (J.J. Palacios); Hospital General Universitario Gregorio Maranon, Madrid, and Centro de Investigacion Biomedica en Red Enfermedades Respiratorias Enfermedades Respiratorias, Madrid (D. Garcia de Viedma); and Ministerio de Medio Ambiente, y Medio Rural y Marino, Madrid (J.L. Saez)
Address for correspondence: Lucia de Juan, VISAVET Health Surveillance Centre and Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain; email: dejuan@ visavet.ucm.es
Table. Relevant information about Mycobacterium tuberculosis infection in 3 cattle farms in Spain * Variable Farm 1 Cattle herd No. animals 6 Production Beef Previous status TB free No. reactors 1 M. tuberculosis infection in cattle Year of isolation 2007 Age, mo 9 IDTB/interferon-Y Pos/not determined TB-compatible lesion No Spoligotyping profile SIT2537 MIRU-VNTR profile ([dagger]) 25353323343323 '6252211423 Co-infection with Yes other mycobacteria (M. avium subsp. hominissuis) ([double dagger]) M. tuberculosis infection in human Active tuberculosis Yes Spoligotyping profile SIT2537 MIRU-VNTR profile ([dagger]) 25353323343 3236252211423 Origin Spain Variable Farm 2 Cattle herd No. animals 54 Production Beef Previous status TB-free No. reactors 31 M. tuberculosis infection in cattle Year of isolation 2008 Age, mo 4 IDTB/interferon-Y Neg/neg TB-compatible lesion No Spoligotyping profile SIT1564 MIRU-VNTR profile ([dagger]) 3'5233423245 5457251213423 Co-infection with Yes other mycobacteria (M. bovis) M. tuberculosis infection in human Active tuberculosis Yes Spoligotyping profile Not available MIRU-VNTR profile ([dagger]) 3'523342324 55457251213423 Origin Eastern Europe Variable Farm 3 Cattle herd No. animals >200 Production Dairy Previous status Non-TB free No. reactors 12 M. tuberculosis infection in cattle Year of isolation 2009 Age, mo 3 IDTB/interferon-Y Pos/not determined TB-compatible lesion No Spoligotyping profile SIT58 MIRU-VNTR profile ([dagger]) 254343243232 325262213423 Co-infection with No other mycobacteria M. tuberculosis infection in human Active tuberculosis Yes Spoligotyping profile SIT58 MIRU-VNTR profile ([dagger]) 254343243232 325262213423 Origin Spain * TB, tuberculosis; IDTB, intradermal tuberculin tested according to the European Council Directive 64/432/EEC; pos, positive; neg, negative; MIRU- VNTR, mycobacterial interspersed repetitive unit-variable number tandem repeat. ([dagger]) MIRU-VNTR profile on the basis of the 24 MIRU-VNTR loci (7). ([double dagger]) Co-infection in the same animal.
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|Author:||Romero, Beatriz; Rodriguez, Sabrina; Bezos, Javier; Diaz, Rosa; Copano, M. Francisca; Merediz, Isabe|
|Publication:||Emerging Infectious Diseases|
|Article Type:||Letter to the editor|
|Date:||Dec 1, 2011|
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