Survey of Zoonotic Bacterial Pathogens in Native Foxes in Central Chile: First Record of Brucella canis Exposure
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Detection of Antibodies against B. abortus, B. canis, and Pathogenic Leptospira
2.3. Bacteriological Detection of B. abortus and B. canis
2.4. Molecular Identification of B. abortus and B. canis Colonies
2.5. Molecular Identification of B. abortus, B. canis, and Pathogenic Leptospira from Blood
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Patz, J.A.; Graczyk, T.K.; Geller, N.; Vittor, A.Y. Effects of environmental change on emerging parasitic diseases. Int. J. Parasitol. 2000, 30, 1395–1405. [Google Scholar] [CrossRef] [Green Version]
- Carr, A.N.; Milleson, M.P.; Hernández, F.A.; Merrill, H.R.; Avery, M.L.; Wisely, S.M. Wildlife management practices associated with pathogen exposure in non-native wild pigs in Florida, U.S. Viruses 2018, 11, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mwachui, M.A.; Crump, L.; Hartskeerl, R.; Zinsstag, J.; Hattendorf, J. Environmental and behavioural determinants of leptospirosis transmission: A systematic review. PLoS Negl. Trop. Dis. 2015, 9, e0003843. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Godfroid, J. Brucellosis in livestock and wildlife: Zoonotic diseases without pandemic potential in need of innovative One Health approaches. Arch. Public Health 2017, 75, 34. [Google Scholar] [CrossRef] [PubMed]
- Vieira, A.S.; Pinto, P.S.; Lilenbaum, W. A Systematic review of leptospirosis on wild animals in Latin America. Trop. Anim. Health Prod. 2018, 50, 229–238. [Google Scholar] [CrossRef]
- Essack, S.Y. Environment: The neglected component of the One Health triad. Lancet Planet. Health 2018, 2, e238–e239. [Google Scholar] [CrossRef]
- Alvarado, R. Apuntes sobre los zorros culpeo y chilla en Chile. La Chiricoca 2011, 13, 51–55. Available online: http://www.lachiricoca.cl/wp-content/uploads/2018/03/La-Chiricoca-13_part6_c.pdf (accessed on 15 April 2021).
- Lucherini, M. Lycalopex griseus. IUCN Red List of Threatened Species 2016: E.T6927A111975602. 2016. Available online: https://www.iucnredlist.org/species/6927/111975602 (accessed on 15 April 2021). [CrossRef]
- Lucherini, M. Lycalopex culpaeus. IUCN Red List of Threatened Species 2016: E.T6929A85324366. 2016. Available online: https://www.iucnredlist.org/species/6929/85324366 (accessed on 15 April 2021). [CrossRef]
- Veintimilla, N. Presencia de enfermedades parasitarias e infecciosas (leptospirosis, distemper y brucelosis) en zorros andinos (Lycalopex culpaeus) que habitan en los páramos de la Hacienda Antisanilla (Pintag-Ecuador). Bachelor’s Thesis, Universidad San Francisco de Quito, Quito, Ecuador, 2015. [Google Scholar]
- Ministerio del Medio Ambiente (MMA). Inventario Nacional de Especies de Chile. Available online: http://especies.mma.gob.cl/CNMWeb/Web/WebCiudadana/webCiudadana_busquedaGrilla.aspx?cx=010884267946229321636%3Aoo8i2-smaa4&cof=FORID%3A10&q=zorro (accessed on 15 April 2021).
- World Organization for Animal Health (OIE). Bovine brucellosis (NB: Version adopted in May 2009). In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals; OIE: Paris, France, 2013. [Google Scholar]
- McDermott, J.; Grace, D.; Zinsstag, J. Economics of brucellosis impact and control in low-income countries. Rev. Sci. Tech. 2013, 32, 249–261. [Google Scholar] [CrossRef] [Green Version]
- Whatmore, A.M. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect. Genet. Evol. 2009, 9, 1168–1184. [Google Scholar] [CrossRef]
- Moreno, E. Retrospective and prospective perspectives on zoonotic brucellosis. Front. Microbiol. 2014, 5, 213. [Google Scholar] [CrossRef] [Green Version]
- Cosford, K.L. Brucella canis: An update on research and clinical management. Can. Vet. J. 2018, 59, 74–81. [Google Scholar]
- Holst, B.S.; Löfqvist, K.; Ernholm, L.; Eld, K.; Cedersmyg, M.; Hallgren, G. The first case of Brucella canis in Sweden: Background, case report and recommendations from a northern European perspective. Acta Vet. Scand. 2012, 54, 18. [Google Scholar] [CrossRef] [Green Version]
- Olsen, S.C.; Bellaire, B.H.; Roop, R.M.; Thoen, C.O. Brucella. In Pathogenesis of Bacterial Infections in Animals; John Wiley & Sons Ltd.: Hoboken, NJ, USA, 2010; pp. 429–441. ISBN 978-0-470-95820-9. [Google Scholar]
- Díaz Aparicio, E. Epidemiology of brucellosis in domestic animals caused by Brucella melitensis, Brucella suis and Brucella abortus. Rev. Sci. Tech. 2013, 32, 43–51. [Google Scholar] [CrossRef]
- European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union One Health 2018 zoonoses report. EFSA J. 2019, 17, e05926. [Google Scholar] [CrossRef] [Green Version]
- Cárdenas, L.; Awada, L.; Tizzani, P.; Cáceres, P.; Casal, J. Characterization and evolution of countries affected by bovine brucellosis (1996–2014). Transbound. Emerg. Dis. 2019, 66, 1280–1290. [Google Scholar] [CrossRef]
- Hensel, M.E.; Negron, M.; Arenas-Gamboa, A.M. Brucellosis in dogs and public health risk. Emerg. Infect. Dis. 2018, 24, 1401–1406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buhmann, G.; Paul, F.; Herbst, W.; Melzer, F.; Wolf, G.; Hartmann, K.; Fischer, A. Canine brucellosis: Insights into the epidemiologic situation in Europe. Front. Vet. Sci. 2019, 6, 151. [Google Scholar] [CrossRef] [PubMed]
- Servicio Agrícola y Ganadero de Chile (SAG). Informe de Sanidad Animal. 2019. Available online: https://www.sag.gob.cl/sites/default/files/informe_situacion_sanitaria_animal-2019.pdf (accessed on 15 April 2021).
- Nielsen, K.; Duncan, J.R. Animal Brucellosis; CRC Press: Boca Raton, FL, USA, 1990; ISBN 978-0-8493-5878-4. [Google Scholar]
- Shin, S.; Carmichael, L.E. Canine brucellosis caused by Brucella canis (23 November 1999). In Recent Advances in Canine Infectious Diseases; International Veterinary Information Service: Ithaca, NY, USA, 2005. [Google Scholar]
- Hull, N.C.; Schumaker, B.A. Comparisons of brucellosis between human and veterinary medicine. Infect. Ecol. Epidemiol. 2018, 8, 1500846. [Google Scholar] [CrossRef]
- Adler, B.; de la Peña Moctezuma, A. Leptospira and leptospirosis. Vet. Microbiol. 2010, 140, 287–296. [Google Scholar] [CrossRef]
- Żmudzki, J.; Arent, Z.; Jabłoński, A.; Nowak, A.; Zębek, S.; Stolarek, A.; Bocian, Ł.; Brzana, A.; Pejsak, Z. Seroprevalence of 12 Serovars of pathogenic Leptospira in red foxes (Vulpes vulpes) in Poland. Acta Vet. Scand. 2018, 60, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ellis, W.A. Animal leptospirosis. Curr. Top. Microbiol. Immunol. 2015, 387, 99–137. [Google Scholar] [CrossRef]
- Amundson, T.E.; Yuill, T.M. Prevalence of selected pathogenic microbial agents in the red fox (Vulpes fulva) and gray fox (Urocyon cinereoargenteus) of southwestern Wisconsin. J. Wildl. Dis. 1981, 17, 17–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akerstedt, J.; Lillehaug, A.; Larsen, I.-L.; Eide, N.E.; Arnemo, J.M.; Handeland, K. Serosurvey for canine distemper virus, canine adenovirus, Leptospira interrogans, and Toxoplasma gondii in free-ranging canids in Scandinavia and Svalbard. J. Wildl. Dis. 2010, 46, 474–480. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moya, S.; Oettinger, S.; Borie, C.; Flores, R.; Abalos, P.; Briceño, C. Serologic survey of Brucella canis and Leptospira spp. in free-ranging wild and domestic canids from Tierra Del Fuego, Chile. J. Wildl. Dis. 2019, 55, 713–716. [Google Scholar] [CrossRef]
- Llanos-Soto, S.; Najle, M.I.; Salgado, M.; González-Acuña, D. Evidence of pathogenic Leptospira infection in a free-ranging andean fox (Lycalopex culpaeus) from Central Chile. J. Wildl. Dis. 2019, 55, 958–960. [Google Scholar] [CrossRef]
- Williams, J.D.; Heck, F.C.; Davis, D.S.; Adams, L.G. Comparison of results from five serologic methods used for detecting Brucella abortus antibody activity in coyote sera. Vet. Immunol. Immunopathol. 1991, 29, 79–87. [Google Scholar] [CrossRef]
- Neiland, K.A. Rangiferine brucellosis in Alaskan Canids. J. Wildl. Dis. 1970, 6, 136–139. [Google Scholar] [CrossRef] [PubMed]
- Sachs, R.; Staak, C.; Groocock, C.M. Serological investigation of brucellosis in game animals in Tanzania. Bull. Epizoot. Dis. Afr. 1968, 16, 93–100. [Google Scholar] [PubMed]
- Morton, J.K. Brucella suis Type 4 in Foxes and Their Role as Reservoirs/Vectors among Reindeer. Ph.D. Thesis, University of Alaska Fairbanks, Fairbanks, AK, USA, 1989. [Google Scholar]
- Olivares, R.; Riveros, V.; Pinochet, L. Brucelosis: Estudio serológico en animales de un zoológico. Arch. Med. Vet. 1993, 25, 101–105. [Google Scholar]
- Borie, C.; Cepeda, R.; Villarroel, M.; De Los Reyes, M. Descripción de características reproductivas en tres perros seropositivos a Brucella canis. Arch. Med. Vet. 2002, 34, 111–116. [Google Scholar] [CrossRef]
- Sotomayor, M. Diagnóstico de brucelosis canina: Utilización de un antígeno proteico citosólico de Brucella abortus cepa RB51 en perros infectados experimentalmente. Bachelor’s Thesis, Universidad de Chile, Santiago, Chile, 2001. [Google Scholar]
- Servicio Agrícola y Ganadero de Chile (SAG). Instructivo Técnico Para El Análisis de Rosa de Bengala. Cod: IT-LAB-06-V1. 2006. Available online: https://www.sag.gob.cl/sites/default/files/it_diagnostico_bb_pruebas_serologicas_d-gf-cgp-pt-021.pdf (accessed on 15 April 2021).
- Alton, G.G.; Jones, L.M.; Pietz, D.E.; World Health Organization; Food and Agriculture Organization of the United Nations (FAO). Las Técnicas de Laboratorios En La Brucelosis; Organización Mundial de la Salud: Ginebra, Switzerland, 1976; ISBN 978-92-4-340055-6. [Google Scholar]
- Keid, L.B.; Soares, R.M.; Vasconcellos, S.A.; Megid, J.; Salgado, V.R.; Richtzenhain, L.J. Comparison of agar gel immunodiffusion test, rapid slide agglutination test, microbiological culture and PCR for the diagnosis of canine brucellosis. Res. Vet. Sci. 2009, 86, 22–26. [Google Scholar] [CrossRef] [PubMed]
- Borie, C.; Bravo, C.; Dettleff, P.; Galarce, N.; Dorner, J.; Martínez, V. First genome sequence of Chilean Brucella canis SCL strain provides insights on the epidemiology and virulence factors, explaining differences between geographical origins. Electron. J. Biotechnol. 2021, 49, 1–4. [Google Scholar] [CrossRef]
- Borie, C.; Galarce, N. Brucella canis. Rev. Chilena Infectol. 2015, 32, 219–220. [Google Scholar] [CrossRef] [Green Version]
- Lorca, V.C.; Borie, C.F.; Navarro, C.O. Differential detection of Brucella canis by means a conventional polymerase chain reaction. Vet. Sci. Med. 2018, 1, 5. [Google Scholar]
- Galarce, N.; Escobar, B.; Martínez, E.; Alvarado, N.; Peralta, G.; Dettleff, P.; Dorner, J.; Martínez, V.; Borie, C. Prevalence and genomic characterization of Brucella canis strains isolated from kennels, household, and stray dogs in Chile. Animals 2020, 10, 2073. [Google Scholar] [CrossRef]
- Bustin, S.A.; Benes, V.; Garson, J.A.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M.W.; Shipley, G.L.; et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55, 611–622. [Google Scholar] [CrossRef] [Green Version]
- Bourhy, P.; Bremont, S.; Zinini, F.; Giry, C.; Picardeau, M. Comparison of real-time PCR assays for detection of pathogenic Leptospira spp. in blood and identification of variations in target sequences. J. Clin. Microbiol. 2011, 49, 2154–2160. [Google Scholar] [CrossRef] [Green Version]
- Karesh, W.B.; Dobson, A.; Lloyd-Smith, J.O.; Lubroth, J.; Dixon, M.A.; Bennett, M.; Aldrich, S.; Harrington, T.; Formenty, P.; Loh, E.H.; et al. Ecology of zoonoses: Natural and unnatural histories. Lancet 2012, 380, 1936–1945. [Google Scholar] [CrossRef]
- Jones, B.A.; Grace, D.; Kock, R.; Alonso, S.; Rushton, J.; Said, M.Y.; McKeever, D.; Mutua, F.; Young, J.; McDermott, J.; et al. Zoonosis emergence linked to agricultural intensification and environmental change. Proc. Natl. Acad. Sci. USA 2013, 110, 8399–8404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alamian, S.; Esmaelizad, M.; Zahraei, T.; Etemadi, A.; Mohammadi, M.; Afshar, D.; Ghaderi, S. A novel PCR assay for detecting Brucella abortus and Brucella melitensis. Osong. Public Health Res. Perspect. 2017, 8, 65–70. [Google Scholar] [CrossRef]
- Millán, J.; Candela, M.G.; López-Bao, J.V.; Pereira, M.; Jiménez, M.A.; León-Vizcaíno, L. Leptospirosis in wild and domestic carnivores in natural areas in Andalusia, Spain. Vector Borne Zoonotic Dis. 2009, 9, 549–554. [Google Scholar] [CrossRef] [PubMed]
- Borie, C.; Pinochet, L. Brucelosis canina: Conceptos generales y estudios realizados en el país. Monogr. Med. Vet. 1987, 9. [Google Scholar]
- Borie, C. Situación actual de la brucelosis canina en Latinoamérica. In II Simposio Latinoamericano de Reproducción Animal; Fac. Cs. Veterinarias y Pecuarias: Santiago, Chile, 2014. [Google Scholar]
- Alvarado, N. Brucelosis canina en la Región Metropolitana: Estudio de corte transversal para determinar la presencia de Brucella canis en perros con dueño. Bachelor’s Thesis, Universidad de Chile, Santiago, Chile, 2019. [Google Scholar]
- The Center for Food Security & Public Health (CFSPH). Brucellosis: Brucella canis. Available online: https://www.cfsph.iastate.edu/Factsheets/pdfs/brucellosis_canis.pdf (accessed on 15 April 2021).
- Bischof, R.; Rogers, D.G. Serologic survey of select infectious diseases in coyotes and raccoons in Nebraska. J. Wildl. Dis. 2005, 41, 787–791. [Google Scholar] [CrossRef] [Green Version]
- Kosoy, M.; Goodrich, I. Comparative ecology of Bartonella and Brucella infections in wild carnivores. Front. Vet. Sci. 2019, 5, 322. [Google Scholar] [CrossRef] [Green Version]
- Aguiar, D.M.D.; Cavalcante, G.T.; Vasconcellos, S.A.; Megid, J.; Salgado, V.R.; Cruz, T.F.; Labruna, M.B.; Pinter, A.; Silva, J.C.R.D.; Moraes, Z.M.; et al. Anti-Brucella abortus and anti-Brucella canis antibodies occurrence in rural and urban dogs from Monte Negro County, Rondônia, Brazil. Ciência Rural 2005, 35, 1216–1219. [Google Scholar] [CrossRef]
- Miceli, G.S.; Pérez Meyer, L.N.; Peralta, L.M.; Mórtola, E.C. Detección de anticuerpos contra Brucella abortus en perros en contacto con zona rural: Aspectos zoonóticos de la infección. Analecta Vet. 2019, 39, 8–14. [Google Scholar] [CrossRef]
- Fuchs, L.; Baldone, V.; Fort, M.; del Carmen Rojas, M.; Samartino, L.; Giménez, H. Brucelosis en el zorro gris pampeano (Pseudalopex gymnocercus) en la provincia de La Pampa (Argentina). Acta Bioquímica Clínica Latinoam. 2009, 43, 227–231. [Google Scholar]
- Scanlan, C.M.; Pidgeon, G.L.; Swango, L.J.; Hannon, S.S.; Galik, P.A. Experimental infection of gray foxes (Urocyon cinereoargenteus) with Brucella abortus. J. Wildl. Dis. 1984, 20, 27–30. [Google Scholar] [CrossRef] [Green Version]
- Simpson, G.; Thompson, P.N.; Saegerman, C.; Marcotty, T.; Letesson, J.-J.; de Bolle, X.; Godfroid, J. Brucellosis in wildlife in Africa: A systematic review and meta-analysis. Sci. Rep. 2021, 11, 5960. [Google Scholar] [CrossRef]
- Davis, D.S.; Heck, F.C.; Williams, J.D.; Simpson, T.R.; Adams, L.G. Interspecific transmission of Brucella abortus from experimentally infected coyotes (Canis latrans) to parturient cattle. J. Wildl. Dis. 1988, 24, 533–537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tessaro, S.V.; Forbes, L.B. Experimental Brucella abortus infection in wolves. J. Wildl. Dis. 2004, 40, 60–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levett, P.N. Leptospirosis. Clin. Microbiol. Rev. 2001, 14, 296–326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scialfa, E.; Brihuega, B.; Venzano, A.; Morris, W.E.; Bolpe, J.; Schettino, M. First isolation of Leptospira interrogans from Lycalopex griseus (South American gray fox) in Argentina shows new MLVA genotype. J. Wildl. Dis. 2013, 49, 168–172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zamora, J.; Riedemann, S. Animales silvestres como reservorios de leptospirosis en Chile: Una revisión de los estudios efectuados en el país. Arch. Med. Vet. 1999, 31, 151–156. [Google Scholar] [CrossRef]
- Benacer, D.; Thong, K.L.; Verasahib, K.B.; Galloway, R.L.; Hartskeerl, R.A.; Lewis, J.W.; Mohd Zain, S.N. Human leptospirosis in Malaysia: Reviewing the challenges after 8 decades (1925–2012). Asia Pac. J. Public Health 2016, 28, 290–302. [Google Scholar] [CrossRef] [PubMed]
- Ambily, R.; Mini, M.; Joseph, S.; Krishna, S.; Abhinay, G. Canine leptospirosis—A seroprevalence study from Kerala, India. Vet. World 2013, 6, 42. [Google Scholar] [CrossRef]
- Jara, M.; Escobar, L.E.; Rodriges, R.O.; Frias-De-Diego, A.; Sanhueza, J.; Machado, G. Spatial distribution and spread potential of sixteen Leptospira serovars in a subtropical region of Brazil. Transbound. Emerg. Dis. 2019, 66, 2482–2495. [Google Scholar] [CrossRef] [PubMed]
- Lilenbaum, W.; Martins, G. Leptospirosis in cattle: A challenging scenario for the understanding of the epidemiology. Transbound. Emerg. Dis. 2014, 61 (Suppl. S1), 63–68. [Google Scholar] [CrossRef]
- Reilly, J.R. The susceptibility of five species of wild animals to experimental infection with Leptospira Grippotyphosa. J. Wildl. Dis. 1970, 6, 289–294. [Google Scholar] [CrossRef] [Green Version]
- Limmathurotsakul, D.; Turner, E.L.; Wuthiekanun, V.; Thaipadungpanit, J.; Suputtamongkol, Y.; Chierakul, W.; Smythe, L.D.; Day, N.P.J.; Cooper, B.; Peacock, S.J. Fool’s gold: Why imperfect reference tests are undermining the evaluation of novel diagnostics: A reevaluation of 5 diagnostic tests for leptospirosis. Clin. Infect. Dis. 2012, 55, 322–331. [Google Scholar] [CrossRef]
- Silva, R.F.; Riedemann, S. Seroprevalencia de leptospirosis canina en perros atendidos en clínicas veterinarias, mediante aglutinación microscópica y comparación con las técnicas de aislamiento e inmunofluorescencia indirecta. Arch. Med. Vet. 2007, 39, 269–274. [Google Scholar] [CrossRef] [Green Version]
- Morales, A.C. Prevalencia de leptospirosis en perros y gatos de predios lecheros del sur de Chile. Bachelor’s Thesis, Universidad Austral de Valdivia, Valdivia, Chile, 2012. [Google Scholar]
- Lelu, M.; Muñoz-Zanzi, C.; Higgins, B.; Galloway, R. Seroepidemiology of leptospirosis in dogs from rural and slum communities of Los Ríos Region, Chile. BMC Vet. Res. 2015, 11, 31. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Serovar | Species | Strain |
---|---|---|
Andamana | L. biflexa | CH11 |
Australis | L. interrogans | Ballico |
Autumnalis | L. interrogans | Akiyami A |
Ballum | L. borgepetersenii | Mus 125 |
Bataviae | L. interrogans | Van Tienen |
Canicola | L. interrogans | Hond Utrecht IV |
Celledoni | L. weilii | Celledoni |
Cynopteri | L. kischneri | 3522 C |
Djasiman | L. interrogans | Djasiman |
Grippotyphosa | L. interrogans | Moskva V |
Borincana | L. santarosai | HS 622 |
Icterohaemorragiae | L. interrogans | RGA |
Javanica | L. borgepetersenii | Veldrat Batavia 46 |
Georgia | L. santarosai | LT117 |
Pomona | L. interrogans | Pomona |
Pyriogenes | L. interrogans | Salinem |
Canicola | L. interrogans | Reubush |
Copenhageni | L. interrogans | M20 |
Hardjo | L. interrogans | Hardjoprajitno |
Species | Forward | Reverse | Tm | Source |
---|---|---|---|---|
B. canis | ACGAACACAAGGGCCAATAC | GGACGGCTACAAGATCGAAG | 62 | [47] |
B. abortus | CGCTCGCTGCTAAAGACATA | TAGGATCGACCTCGACAATACA | 62 | This study |
Pathogenic Leptospira | AAGCATTACCGCTTGTGGTG | GAACTCCCATTTCAGCGATT | 62 | [50] |
Animal ID | Animal Species | Center of Origin | Age Class | Sex |
---|---|---|---|---|
LC-10 | L. culpaeus * | Exhibition 1 | Adult | Female |
LC-18 | L. culpaeus | Rehabilitation 3 | Juvenile | Female |
LC-21 | L. culpaeus | Rehabilitation 2 | Juvenile | Female |
LC-23 | L. culpaeus | Rehabilitation 1 | Adult | Male |
LC-49 | L. culpaeus | Rehabilitation 1 | Adult | Female |
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Galarce, N.; de la Fuente, S.; Escobar, B.; Dettleff, P.; Abalos, P.; Hormazábal, J.C.; Flores, R.; Sallaberry-Pincheira, N.; Martínez, V. Survey of Zoonotic Bacterial Pathogens in Native Foxes in Central Chile: First Record of Brucella canis Exposure. Animals 2021, 11, 1980. https://doi.org/10.3390/ani11071980
Galarce N, de la Fuente S, Escobar B, Dettleff P, Abalos P, Hormazábal JC, Flores R, Sallaberry-Pincheira N, Martínez V. Survey of Zoonotic Bacterial Pathogens in Native Foxes in Central Chile: First Record of Brucella canis Exposure. Animals. 2021; 11(7):1980. https://doi.org/10.3390/ani11071980
Chicago/Turabian StyleGalarce, Nicolás, Sebastián de la Fuente, Beatriz Escobar, Phillip Dettleff, Pedro Abalos, Juan Carlos Hormazábal, Roberto Flores, Nicole Sallaberry-Pincheira, and Víctor Martínez. 2021. "Survey of Zoonotic Bacterial Pathogens in Native Foxes in Central Chile: First Record of Brucella canis Exposure" Animals 11, no. 7: 1980. https://doi.org/10.3390/ani11071980
APA StyleGalarce, N., de la Fuente, S., Escobar, B., Dettleff, P., Abalos, P., Hormazábal, J. C., Flores, R., Sallaberry-Pincheira, N., & Martínez, V. (2021). Survey of Zoonotic Bacterial Pathogens in Native Foxes in Central Chile: First Record of Brucella canis Exposure. Animals, 11(7), 1980. https://doi.org/10.3390/ani11071980