Shedding of Mycobacterium caprae by wild red deer (Cervus elaphus) in the Bavarian alpine regions, Germany.
Animals
Bacterial Shedding
Cattle
Cattle Diseases
/ epidemiology
Cross-Sectional Studies
Deer
/ microbiology
Disease Reservoirs
/ microbiology
Feces
/ microbiology
Geography
Germany
/ epidemiology
Lymph Nodes
/ microbiology
Mycobacterium bovis
/ classification
Palatine Tonsil
/ microbiology
Polymorphism, Single Nucleotide
Real-Time Polymerase Chain Reaction
/ veterinary
Saliva
/ microbiology
Tuberculosis, Bovine
/ epidemiology
M. caprae
MTC
bovine tuberculosis
faeces
qPCR
wildlife
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Jan 2020
Jan 2020
Historique:
received:
14
05
2019
revised:
09
08
2019
accepted:
30
08
2019
pubmed:
13
9
2019
medline:
27
5
2020
entrez:
13
9
2019
Statut:
ppublish
Résumé
The number of natural infections with Mycobacterium caprae in wildlife and in cattle in the Bavarian and Austrian alpine regions has increased over the last decade. Red deer (Cervus elaphus) have been recognized as maintenance reservoir; however, the transmission routes of M. caprae among and from naturally infected red deer are unknown. The unexpected high prevalence in some hot spot regions might suggest an effective indirect transmission of infection. Therefore, this study was undertaken to diagnose the occurrence of M. caprae in faeces and secretions of red deer in their natural habitat. A total of 2,806 red deer hunted in this region during 2014-2016 were included in this study. After pathological examination, organs (lymph nodes, lung, heart), excretions and secretions (faeces, urine, saliva and tonsil swabs) were further investigated by qPCR specific for Mycobacterium tuberculosis complex (MTC), M. bovis and M. caprae. Samples tested positive by qPCR were processed for culturing of mycobacteria. In total, 55 (2.0%) animals were confirmed positive for M. caprae by pathological examination, PCR and culturing of the affected organ material. With the exception of one sample, all of the secretion and excretion samples were negative for mycobacteria of the Mycobacterium tuberculosis complex (MTC). From one red deer, M. caprae could be isolated from the heart sac as well as from the faeces. Whole-genome sequencing confirmed that both strains were clonally related. This is the first confirmation that M. caprae can be shed with the faeces of a naturally infected red deer. However, further studies focusing on a higher number of infected animals, sample standardization and coordinated multiple sampling are necessary to improve the understanding of transmission routes under natural conditions.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
308-317Subventions
Organisme : Federal Office of Agriculture and Food (BLE), German Federal Ministry of Food and Agriculture (BMEL)
ID : 2814HS009
Organisme : German Federal Ministry of Food and Agriculture (BMEL) through the Federal Office of Agriculture and Food (BLE)
ID : 2814HS009
Informations de copyright
© 2019 The Authors. Transboundary and Emerging Diseases published by Blackwell Verlag GmbH.
Références
Alexander, K. A., Laver, P. N., Michel, A. L., Williams, M., Van Helden, P. D., Warren, R. M., & Gey Van Pittius, N. C. (2010). Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerging Infectious Diseases, 16, 1296-1299.
Aranaz, A., Cousins, D., Mateos, A., & Dominguez, L. (2003). Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov. International Journal of Systematic and Evolutionary Microbiology, 53, 1785-1789.
Barasona, J. A., Vicente, J., Díez-Delgado, I., Aznar, J., Gortázar, C., & Torres, M. J. (2017). Environmental presence of Mycobacterium tuberculosis complex in aggregation points at the wildlife/livestock interface. Transboundary and Emerging Diseases, 64, 1148-1158. https://doi.org/10.1111/tbed.12480
Boenchendorf, J. A. D. (2016). Netzwerkanalyse zur bovinen Tuberkulose im bayerischen Voralpenraum. Dissertation, Ludwig-Maximilians-University Munich. https://edoc.ub.uni-muenchen.de/20614/1/Boenchendorf_Julia.pdf
Bundesgesetzblatt, (2013). Gesetz zur Vorbeugung vor und Bekämpfung von Tierseuchen (Tiergesundheitsgesetz - TierGesG). https://www.gesetze-im-internet.de/tiergesg/BJNR132400013.html. accessed 12 December 2018.
Büttner, M., Just, F., Neuendorf, E., Hörmansdorfer, S., & Zimmermann, P. (2013). Tuberkulose bei Rind und Rotwild in Bayern. Rundschau für. Fleischhygiene und Lebensmittelüberwachung, 9.
Csivincsik, Á., Rónai, Z., Nagy, G., Svéda, G., & Halász, T. (2016). Surveillance of Mycobacterium caprae infection in a wild boar (Sus scrofa) population in south-western Hungary. Veterinarski Arhiv, 86, 767-775.
de Lisle, G. W., Bengis, R. G., Schmitt, S. M., & O'Brien, D. J. (2002). Tuberculosis in free-ranging wild-life: Detection, diagnosis and management. Revue Scientifique Et Technique (International Office of Epizootics), 21, 317-334.
Delahay, R. J., Smith, G. C., Barlow, A. M., Walker, N., Harris, A., Clifton-Hadley, R. S., & Cheeseman, C. L. (2007). Bovine tuberculosis infection in wild mammals in the South-West region of England: A survey of prevalence and a semi-quantitative assessment of the relative risks to cattle. The Veterinary Journal, 173, 287-301. https://doi.org/10.1016/j.tvjl.2005.11.011
Domogalla, J., Prodinger, W. M., Blum, H., Krebs, S., Gellert, S., Müller, M., … Büttner, M. (2013). Region of difference 4 in alpine Mycobacterium caprae isolates indicates three variants. Journal of Clinical Microbiology, 51, 1381-1388. https://doi.org/10.1128/JCM.02966-12
EMIDA (2013). Emerging and Major Infectious Diseases in Livestock Animals - European Research Area - Net (EMIDA - ERA-NET) over „Tuberculosis in Alpine Wildlife“. https://www.tib.eu/de/suchen/id/TIBKAT%3A779341511/EMIDA-ERA-Net-TB-Alpine-Wildlife-Tuberkulose-bei/ accessed 18 October 2018 .
Fink, M., Schleicher, C., Gonano, M., Prodinger, W. M., Pacciarini, M., Glawischnig, W., … Büttner, M. (2015). Red deer as maintenance host for bovine tuberculosis, Alpine region. Emerging Infectious Diseases, 21, 464-467. https://doi.org/10.3201/eid2103.141119
FLI: Friedrich Loeffler Institut, Bundesforschungsinstitut für Tiergesundheit: Federal Research Institute for Animal Health (2013). Rindertuberkulose, https://www.openagrar.de/servlets/MCRFileNodeServlet/Document_derivate_00001363/FLI-Information_Rindertuberkulose20130902.pdf.
FLI: Friedrich Loeffler Institut (2015). Amtliche Methodensammlung: Tuberkulose der Rinder (Mykobakterium bovis und Mykobakterium caprae). https://www.fli.de/de/publikationen/amtliche-methodensammlung/.
FLI: Friedrich Loeffler Institut. (2018). Tiergesundheitsjahresbericht 2018. https://www.openagrar.de/servlets/MCRFileNodeServlet/openagrar_derivate_00019033/TGJB_2017_K.pdf.
García-Jiménez, W. L., Benítez-Medina, J. M., Fernández-Llario, P., Abecia, J. A., García-Sánchez, A., Martínez, R., … Hermoso de Mendoza, J. (2013). Comparative Pathology of the Natural infections by Mycobacterium bovis and by Mycobacterium caprae in wild boar (Sus scrofa). Transboundary and Emerging Diseases, 60, 102-109.
Guerra-Assunção, J. A., Crampin, A. C., Houben, R., Mzembe, T., Mallard, K., Coll, F., … Glynn, J. R. (2015). Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife, 4, 05166. https://doi.org/10.7554/eLife
Hardstaff, J. L., Marion, G., Hutchings, M. R., & White, P. C. L. (2014). Evaluating the tuberculosis hazard posed to cattle from wildlife across Europe. Research in Veterinary Science, 97, 86-93. https://doi.org/10.1016/j.rvsc.2013.12.002
Hatherell, H.-A., Colijn, C., Stagg, H. R., Jackson, C., Winter, J. R., & Abubakar, I. (2016). Interpreting whole genome sequencing for investigating tuberculosis transmission: A systematic review. BMC Medicine, 14(1), 21. https://doi.org/10.1186/s12916-016-0566-x
Huard, R. C., Fabre, M., De Haas, P., Lazzarini, L. C., Van Soolingen, D., Cousins, D., & Ho, J. L. (2006). Novel genetic polymorphisms that further delineate the phylogeny of the Mycobacterium tuberculosis complex. Journal of Bacteriology, 188, 4271-4287. https://doi.org/10.1128/JB.01783-05
Javed, M. T., Usman, M., Irfan, M., & Cagiola, M. (2006). A study on tuberculosis in buffaloes: Some epidemiological aspects, along with haematological and serum protein changes. Veterinarski Arhiv, 76, 193-206.
Koboldt, D. C., Chen, K., Wylie, T., Larson, D. E., McLellan, M. D., Mardis, E. R., … Ding, L. (2009). VarScan: Variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics, 25, 2283-2285. https://doi.org/10.1093/bioinformatics/btp373
Krzysiak, M. K., Jabłoński, A., Iwaniak, W., Krajewska, M., Kęsik-Maliszewska, J., & Larska, M. (2018). Seroprevalence and risk factors for selected respiratory and reproductive tract pathogen exposure in European bison (Bison bonasus) in Poland. Veterinary Microbiology, 215, 57-65. https://doi.org/10.1016/j.vetmic.2018.01.005
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Lopez-Olvera, J. R., Fernandez-De-Mera, I. G., Serrano, E., Vidal, D., Vicente, J., Fierro, Y., & Gortazar, C. (2013). Sex-related differences in body condition and serum biochemical parameters in red deer (Cervus elaphus) naturally infected with Mycobacterium bovis. The Veterinary Journal, 198, 702-706. https://doi.org/10.1016/j.tvjl.2013.10.002
Matos, A. C., Figueira, L., Martins, M. H., Pinto, M. L., Matos, M., & Coelho, A. C. (2014). New insights into Mycobacterium bovis prevalence in wild mammals in Portugal. Transboundary and Emerging Diseases, 63, e313-e322. https://doi.org/10.1111/tbed.12306
McCorry, T., Whelan, A. O., Welsh, M. D., McNair, J., Walton, E., Bryson, D. G., … Pollock, J. M. (2005). Shedding of Mycobacterium bovis in the nasal mucus of cattle infected experimentally with tuberculosis by the intranasal and intratracheal routes. Veterinary Record, 157, 613-618. https://doi.org/10.1136/vr.157.20.613
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., … DePristo, M. A. (2010). The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297-1303. https://doi.org/10.1101/gr.107524.110
Michelet, L., De Cruz, K., Hénault, S., Tambosco, J., Richomme, C., Réveillaud, É., … Boschiroli, M. L. (2018). Mycobacterium bovis infection of red fox, France. Emerging Infectious Diseases, 24, 1151-1153. https://doi.org/10.3201/eid2406.180094
Muller, B., Durr, S., Alonso, S., Hattendorf, J., Laisse, C. J., Parsons, S. D., … Zinsstag, J. (2013). Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerging Infectious Diseases, 19, 899-908.
Müller, M., Hafner-Marx, A., Ehrlein, J., Ewringmann, T., Ebert, U., Weber, B. K., … Schick, M. (2014). Pathomorphologische Veränderungen bei der Tuberkulose des Rotwildes verursacht durch Mycobacterium caprae. Amtstierärztlicher Dienst und Lebensmittelkontrolle 21. Jahrgang, 4, 251-258.
Nugent, G. (2011). Maintenance, spillover and spillback transmission of bovine tuberculosis in multi-host wildlife complexes: A New Zealand case study. Veterinary Microbiology, 151, 34-42. https://doi.org/10.1016/j.vetmic.2011.02.023
O'Brien, D. J., Schmitt, S. M., Rudolph, B. A., & Nugent, G. (2011). Recent advances in the management of bovine tuberculosis in free-ranging wildlife. Veterinary Microbiology, 151, 23-33. https://doi.org/10.1016/j.vetmic.2011.02.022
OIE (2013). OIE-Listed diseases, infections and infestations in force in 2013. http://www.oie.int/animal-health-in-the-world/oie-listed-diseases-2013/ accessed 08 October 2013.
Orłowska, B., Augustynowicz-Kopeć, E., Krajewska, M., Zabost, A., Welz, M., Kaczor, S., & Anusz, K. (2017). Mycobacterium caprae transmission to free-living grey wolves (Canis lupus) in the Bieszczady Mountains in Southern Poland. European Journal of Wildlife Research, 63, 1-5. https://doi.org/10.1007/s10344-017-1079-4
Palmer, M. V. (2013). Mycobacterium bovis: Characteristics of wildlife reservoir hosts. Transboundary and Emerging Diseases, 60, 1-13. https://doi.org/10.1111/tbed.12115
Pate, M., Svara, T., Gombac, M., Paller, T., Zolnir-Dovc, M., Emersic, I., … Ocepek, M. (2006). Outbreak of tuberculosis caused by Mycobacterium caprae in a zoological garden. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 53, 387-392. https://doi.org/10.1111/j.1439-0450.2006.01000.x
Santos, N., Almeida, V., Gortázar, C., & Correia-Neves, M. (2015a). Patterns of Mycobacterium tuberculosis-complex excretion and characterization of super-shedders in naturally infected wild boar and red deer. Veterinary Research, 46, 129. https://doi.org/10.1186/s13567-015-0270-4
Santos, N., Santos, C., Valente, T., Gortázar, C., Almeida, V., & Correia-Neves, M. (2015b). Widespread environmental contamination with Mycobacterium tuberculosis complex revealed by a molecular detection protocol. PLoS ONE, 10(11), e0142079. https://doi.org/10.1371/journal.pone.0142079
Schoepf, K., Prodinger, W. M., Glawischnig, W., Hofer, E., Revilla-Fernandez, S., Hofrichter, J., … Schmoll, F. (2012). A two-years' survey on the prevalence of tuberculosis caused by Mycobacterium caprae in red deer (Cervus elaphus) in the Tyrol. Austria: ISRN Veterinary Science. https://doi.org/10.5402/2012/245138
Sweeney, F. P., Courtenay, O., Hibberd, V., Hewinson, R. G., Reilly, L. A., Gaze, W. H., & Wellington, E. M. H. (2007). Environmental monitoring of Mycobacterium bovis in badger feces and badger sett soil by real-time PCR, as confirmed by immunofluorescence, immunocapture, and cultivation. Applied and Environmental Microbiology, 73, 7471-7473. https://doi.org/10.1128/AEM.00978-07
Thorvaldsdóttir, H., Robinson, J. T., & Mesirov, J. P. (2013). Integrative Genomics Viewer (IGV): High-performance genomics data visualization and exploration. Briefings in Bioinformatics, 14, 178-192. https://doi.org/10.1093/bib/bbs017
Tomlinson, A. J., Chambers, M. A., Mcdonald, R. A., & Delahay, R. J. (2015). Association of quantitative interferon-gamma responses with the progression of naturally acquired Mycobacterium bovis infection in wild European badgers (Meles meles). Immunology, 144, 263-270.
Torres-Gonzalez, P., Soberanis-Ramos, O., Martinez-Gamboa, A., Chavez-Mazari, B., Barrios-Herrera, M. T., Torres-Rojas, M., … Bobadilla-Del-Valle, M. (2013). Prevalence of latent and active tuberculosis among dairy farm workers exposed to cattle infected by Mycobacterium bovis. PLOS Neglected Tropical Diseases, 7, e2177. https://doi.org/10.1371/journal.pntd.0002177
Wilson, G., Broughan, J., Chambers, M., Clifton-Hadley, R., Crawshaw, T., De La Fuente, J., … Hewinson, G. (2009). Scientific review on tuberculosis in wildlife in the EU. http://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/12e.pdf.
Yoshida, S., Suga, S., Ishikawa, S., Mukai, Y., Tsuyuguchi, K., Inoue, Y., … Wada, T. (2018). Mycobacterium caprae infection in captive Borneo elephant, Japan. Emerging Infectious Disease, 24, 1937-1940.
Zanella, G., Durand, B., Hars, J., Moutou, F., Garin-Bastuji, B., Duvauchelle, A., … Boschiroli, M. L. (2008). Mycobacterium bovis in wildlife in France. Journal of Wildlife Diseases, 44, 99-108. https://doi.org/10.7589/0090-3558-44.1.99