MRSA and enterobacteria of one health concern in wild animals undergoing rehabilitation

Authors

DOI:

https://doi.org/10.33448/rsd-v10i1.11809

Keywords:

Biofilm; Birds; Campylobacter; Mammals; Reptiles; Salmonella; Staphylococcus aureus; Yersinia enterocolitica.

Abstract

The presence of contaminated animals in wildlife rehabilitation centers poses a threat for both animals and humans that come into contact with them or the contaminated environment. The aim of this study was to assess the presence of Staphylococcus aureus, including methicillin-resistant S. aureus (MRSA), as well as studying the biofilm formation capacity of these isolates, Yersinia enterocolitica, Salmonella enterica and Campylobacter spp. in wild animals from a rehabilitation center. During a two-year period, feces were collected from animals that were admitted to a wildlife rehabilitation center (n=324 samples). The pathogens were isolated from 51 (15.7%) animals of different species of mammals, birds and reptiles. Forty isolates (12.3%) were identified as S. aureus, of these, 32 (9.9%) were identified as MRSA and 72.5% were able to form biofilm. Y. enterocolitica was found in five mammals (5.1%), three reptiles (21.43%) and two birds (0.94%). Salmonella and Campylobacter were isolated from one bird each (0.67% and 0.67%, respectively). A wide diversity of animal species in rehabilitation centers, including birds, mammals and reptiles, can carry MRSA and enterobacteria of one health concern and eliminate in the feces. The presence of these pathogens in the gastrointestinal tract of wild animals admitted to a wildlife rehabilitation center shows the importance of microbiological monitoring of animals at the time of their admission and reinforces the need for specific hygienic-sanitary care.

References

Andrews, W. H., Andrew, J. & Hammack, T. (2014). Salmonella. U.S. Food and Drug Administration, Bacteriological analytical manual (BAM), Chap. 5, 2014. Retrieved from http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm

Archer, N. K., Mazaitis, M. J., Costerton, J. W., Leid, J. G., Powers, M. E. & Shirtliff, M. E. (2011). Staphylococcus aureus biofilms: Properties, regulation, and roles in human disease. Virulence, 2(5), 445–459.

Billerman, S. M., Keeney, B. K., Rodewald, P. G. & Schulenberg, T. S. (2020). Birds of the World. Cornell Laboratory of Ornithology, Ithaca, NY, USA. Retrieved from https://birdsoftheworld.org/bow/home

Castro-Silva, M. A., Manoel, F. C., Krueger, J., Barreiros, M. A. B. & Branco, J. O. (2011). Identificação de bactérias potencialmente patogênicas a humanos presentes em Sula leucogaster (Suliformes: Sulidae), no litoral de Santa Catarina, Brasil. Revista Brasileira de Ornitologia, 19(4), 520-524.

Catry, B., Van Duijkeren, E., Pomba, M. C., Greko, C., Moreno, M. A., Pyörälä, S., Ruz Auskas, M., Sanders, P., Threlfall, E. J., Ungemach, F., Torneke, K., munoz-madero, C. & Törneke, K. (2010). Reflection paper on MRSA in food-producing and companion animals: epidemiology and control options for human and animal health. Epidemiology and Infection, 138(5), 626-644.

Centers for Desease Control and Prevention – CDC. 2017. Morbidity and Mortality Weekly Report – MMWR. Notifiable Diseases and Mortality Tables. Retrieved from https://www.cdc.gov/mmwr/volumes/66/wr/mm6650md.htm?s_cid=mm6650md_w

Chambers, H. F. (2001). The changing epidemiology of Staphylococcus aureus? Emerging Infectious Diseases, 7(2), 178.

Chen, L., Tang, Z. Y., Cui, S. Y., Ma, Z. B., Deng, H., Kong, W. L., Yang, L. W., Lin, C., Xiong, W. G. & Zeng, Z. L. (2020). Biofilm Production Ability, Virulence and Antimicrobial Resistance Genes in Staphylococcus aureus from Various Veterinary Hospitals. Pathogens, 9(4), 264.

CLSI. (2015). Performance Standards for Antimicrobial Susceptibility Testing. Twenty Fourth Informational Supplement. CLSI document M100-S24. Wayne: Clinical and Laboratory Standards Institute.

Costa, H. C. & Bérnils, R. S. (2015). Répteis brasileiros: lista de espécies 2015. Herpetologia Brasileira, 4(3), 75-93.

De Sá, M. I. & Ferreira, C. (2007). Importância das zoonoses na segurança alimentar. Retrieved from http://www.infoqualidade.net/SEQUALI/PDF-SEQUALI-02/n02-14-17.pdf

Dias, P. A., Wilsmann, D. E., Heinen, J. G., Corsini, D. F., Calabuig, C. & Timm, C. D. (2014). Primeiro relato de Salmonella enterica e Campylobacter spp. isolados de Garibaldi (Chrysomus ruficapillus) e Canário-da-terra (Sicalis flaveola) silvestres. Revista do Instituto Adolfo Lutz, 73, 368-71.

Dias, P. A. (2015). Campylobacter spp., Salmonella enterica e Yersinia enterocolitica em aves silvestres e frangos de corte. 55f. Pelotas – RS. Tese (Doutorado em Veterinária) – Programa de Pós-graduação em Veterinária, Universidade Federal de Pelotas.

Dias, P. A., Moraes, T. P., Wilsmann, D. E., Ferrasso, M. M., Marinheiro, M. F., Heinen, J. G., Calabuig, C. I. P. & Timm, C. D. (2019). Ocorrência de Campylobacter e Enterobacteriaceae em aves silvestres e frangos de corte. Arquivo Brasileiro de Medicina Vetetrinária e Zootecnia, 71(1), 225-231.

Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nature Reviews Drug Discovery, 2(2), 114-122.

Donlan, R. M. & Costerton, J. M. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15(2), 167-193.

Espinosa-Gongora, C., Chrobak, D., Moodley, A., Bertelsen, M. F. & Guardabassi, L. (2012). Occurrence and distribution of Staphylococcus aureus lineages among zoo animals. Veterinary Microbiology, 158(1-2), 228-231.

Falcão, J. P., Falcão, D. P., Pitondo-Silva, A., Malaspina, A. C. & Brocchi, M. (2006). Molecular typing and virulence markers of Yersinia enterocolitica strains from human, animal and food origins isolated between 1968 and 2000 in Brazil. Journal of Medical Microbiology, 55(11), 1539-1548.

Febler, A. T., Thomas, P., Mühldorfer, K., Grobbel, M., Brombach, J., Eichhorn, I., Monecke, S., Ehricht, R. & Schwarz, S. (2018). Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from zoo and wild animals. Veterinary Microbiology, 218, 98-103.

Felten, A., Grandry, B., Lagrange, P. H. & Casin, I. (2002). Evaluation of three techniques for detection of low-level methicillin-resistant Staphylococcus aureus (MRSA): a disk diffusion method with cefoxitin and moxalactam, the Vitek 2 system, and the MRSA-screen latex agglutination test. Journal of Clinical Microbiology, 40(8), 2766-2771.

Freeman, D. J., Falkiner, F. R. & Keane, C. T. (1989). New method for detecting slime production by coagulase negative staphylococci. Journal of Clinical Pathology, 42(8), 872-874.

Friedriczewski, A. B., Gandra, E. Á., Cereser, N. D., Moreira, L. M. & Timm, C. D. (2018). Biofilm Formation by Coagulase-Positive Staphylococcus aureus Isolated from Mozzarella Cheese Elaborated with Buffalo Milk and its Effect on Sensitivity to Sanitizers. Acta Scientiae Veterinariae, 46(1), 1-6.

Gomes, C. M. B., Batista K. S., Oliveira, S. A. & Bezerra L. M. (2011). Determinação de enterobactérias de mamíferos silvestres em criadouro conservacionista. Revista de Biologia e Ciências da Terra, 11(2), 74-80.

Gomes, S., De Macedo, M. R. P., Pesenti, T., Pereira, D. I. B., Cirne, M. P. & Müller, G. (2015). Isolamento de Salmonella enterica subsp. diarizonae em Calidris fuscicollis (Aves: Scolopacidade) no Rio Grande do Sul, Brasil. Ornithologia, 8(1), 43-45.

Handeland, K., Refsum, T., Johansen, B. S., Holstad, G., Knutsen, G., Solberg, I., Schulze, J. & Kapperud, G. (2002). Prevalence of Salmonella Typhimurium infection in Norwegian hedgehog populations associated with two human disease outbreaks. Epidemiology and Infection, 128(3), 523-7.

Hart, J. A. (2020). Ruddy Ground Dove (Columbina talpacoti), version 1.0. In Birds of the World. T. S. Schulenberg, Editor. Ithaca: Cornell Lab of Ornithology.

Hicks, C. L., Napier, J. E., Armstrong, D. L., Gladney, L. M., Tarr, C. L., Freeman, M. M. & Iwen, P. C. (2020). Clonal spread of Yersinia enterocolitica 1B/O: 8 in multiple zoo species. Journal of Zoo and Wildlife Medicine, 51(1), 170-176.

Mariana, N. S., Salman, S. A., Neela, V. & Zamberi, S. (2009). Evaluation of modified Congo red agar for detection of biofilm produced by clinical isolates of methicillin resistance Staphylococcus aureus. African Journal of Microbiology Research, 3(6), 330-338.

Monecke, S., Gavier-Widén, D., Hotzel, H., Peters, M., Guenther, S., Lazaris, A., Loncaric, I., Müller, E. & Reissig, A. (2016). Diversity of Staphylococcus aureus isolates in European wildlife. Plos One, 11(12), e0168433.

Morgan, M. (2008). Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis? Journal of Antimicrobial Chemotherapy, 62(6), 1181–1187.

Nunes, H., Rocha, F. L. & Cordeiro-Estrela, P. (2017). Bats in urban areas of Brazil: roosts, food resources and parasites in disturbed environments. Urban Ecosystems, 20(4), 953-969.

Oliveira, S. D., Rodenbusch, C. R., Cé, M. C., Rocha, S. L. S. & Canal, C. W. (2003). Evaluation of selective and nonselective enrichment PCR procedures for Salmonella detection. Letters in Applied Microbiology, 36(4), 217–221.

Paglia, A. P., Fonseca, G. A. B., Rylands, A. B., Herrmann, G., Aguiar, L. M. S., Chiarello, A. G., Leite, Y. L. R., Costa, L. P., Siciliano, S., Kierulff, M. C. M., Mendes, S. L., Tavares, V. C., Mittermeier, R. A. & Patton, J. L. (2012). Lista Anotada dos Mamíferos do Brasil. Occasional Papers in Conservation Biology nº 6. 2°ed. Conservation International: Arlington, 76p.

Pereira, A. S., Shitsuka, D. M., Parreira, F. J., & Shitsuka, R. (2018). Metodologia da pesquisa científica.[e-book]. Santa Maria. Ed. UAB/NTE/UFSM. Retrieved from https://repositorio. ufsm. br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica. pdf.

Piacentini, V. Q., Aleixo, A., Agne, C. E., Maurício, G. N., Pacheco, J. F., Bravo, G. A., Brito, G. R. R., Naka, L. N., Olmos, F., Posso, S., Silveira, L. F., Betini, G. S., Carrano, E., Franz, I., Lees, A. C., Lima, L. M., Pioli, D., Schunck, F., Amaral, F. R., Bencke, G. A., Cohn-Haft, M., Figueiredo, L. F., Straube, F. C. & Cesari, E. (2015). Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia, 23(2), 91-298.

Polícia Civil do Estado do Rio Grande do Sul. 2019. Operação Bad Hunters investiga crimes de caça ilegal de animais silvestres no norte gaúcho. Retrieved from https://www.pc.rs.gov.br/operacao-bad-hunters-investiga-crimes-de-caca-ilegal-de-animais-silvestres-no-norte-gaucho

Porrero, M. C., Mentaberre, G., Sánchez, S., Fernández-Llario, P., Gómez-Barrero, S. Navarro-Gonzalez, N., Serrano, E., Casas-Díaz, E., Marco, I., Fernández-Garayzabal, J. F., Mateos, A., Vidal, D., Lavín, S. & Domínguez, L. (2013). Methicillin resistant Staphylococcus aureus (MRSA) carriage in different free-living wild animal species in Spain. The Veterinary Journal, 198(1), 127-130.

Rabsch, W., Andrews, H. L., Kingsley, R. A., Prager, R., Tschäpe, H., Adams, L. G. & Bäumler, A. J. (2002). Salmonella enterica serotype Typhimurium and its host-adapted variants. Infection and Immunity, 70(5), 2249- 55.

Rubini, S., Ravaioli, C., Previato, S., D’Incau, M., Tassinari, M., Guidi, E. & Bergamini, M. (2016). Prevalence of Salmonella strains in wild animals from a highly populated area of north-eastern Italy. Annali dell'Istituto Superiore di Sanità, 52(2), 277-280.

Sá, I. V. A. D., & Solari, C. A. (2001). Salmonella in Brazilian and imported pet reptiles. Brazilian Journal of Microbiology, 32(4), 293-297.

Sambrook, J. & Russel, D. W. (2001). Molecular Cloning: A Laboratory Manual. 3°ed. Nova York: Cold Spring Harbor Laboratory Press, 999 p.

Sasaki, T., Tsubakishita, S., Tanaka, Y., Sakusabe, A., Ohtsuka, M., Hirotaki, S., Kawakami, T., Fukata, T. & Hiramatsu, K. (2010). Multiplex-PCR method for species indentification of coagulase-positive Staphylococci. Journal of Clinical Microbiology, 48(3), 765-769.

Silva, H. R., Rocha, Á. S. C., Rocha, M. V. S., Veras, D. M., de Sousa, O. M. C., da Costa Sousa, G., Almeida, D. F., Oliveira, A. L. P., Bezerra, G. S. S., Ribeiro, D. A. S., Pereira N. M., Alves, A. K. R., Silva, B. B. L., Nogueira, F. D., Rodrigues, F. L. G. & Pessoa, G. T. (2020). Reflexo do desequilíbrio ambiental na saúde: bactérias multirresistentes em ambiente hospitalar. Research, Society and Development, 9(8), e220985604-e220985604.

Silveira, D. R., Milan, C., Ferrasso, M. M., Dias, P. A., Moraes, T. P., Bandarra, P. M., Minello, L. F. & Timm, C. D. (2018). Campylobacter jejuni, Campylobacter coli, Salmonella spp. e Yersinia enterocolitica isoladas de animais silvestres em um centro de reabilitação. Pesquisa Veterinária Brasileira, 38(9), 1838-1843.

Skov, R., Smyth, R., Clausen, M., Larsen, A. R., Frimodt-Moller, N., Olsson-Lijequist, B. & Kahlmeter, G. (2003). Evaluation of a cefoxitin 30 microg disc on Iso-Sensitest agar for detection of methicillin resistant Staphylococcus aureus. Journal of Antimicrobial Chemotherapy, 52(2), 204-207.

Smyser, C. F. & Snoeyenbos, G. H. (1972). A pigeon host-adapted type of Salmonella typhimurium var. Copenhagen. Avian diseases, 16(2), 270-277.

Söderlund, R., Jernberg, C., Trönnberg, L., Pääjärvi, A., Ågren, E. & Lahti, E. (2019). Linked seasonal outbreaks of Salmonella Typhimurium among passerine birds, domestic cats and humans, Sweden, 2009 to 2016. Eurosurveillance, 24(34), 1-10.

Steele, C. M., Brown, R. N. & Botzler, R. G. (2005). Prevalence of zoonotic bacteria among seabirds in rehabilitation centers along the Pacific Coast of California and Washington, USA. Journal of Wildlife Diseases, 41(4), 735-744.

Timm, C. D., Dias, P. A., Conceição, R. C. S., Lima, H. G., Silveira, D. R. (2016). Manual de técnicas microbiológicas em leite e derivados. Pelotas: Ed. do autor, 88 p.

Timm, C. D. & Timm, V. F. (2016). Aves do extremo sul do Brasil: guia de identificação. Pelotas: Useb. 334 p.

Tompkins, D. M., Carver, S., Jones, M. E., Krkošek, M. & Skerratt, L. F. (2015). Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology, 31(4), 149-159.

Wannet, J. B. W., Reessink, M. & Brunings, H. A. (2001). Detection of pathogenic Yersinia enterocolitica by a rapid and sensitive Duplex PCR assay. Journal of Clinical Microbiology, 39(12), 4483–4486.

Wardyn, S. E., Kauffman, L. K. & Smith, T. C. (2012). Methicillin-resistant Staphylococcus aureus in central Iowa wildlife. Journal of wildlife Diseases, 48(4), 1069-1073.

Weagant, S. D. & Feng, P. (2017). Yersinia enterocolitica. U.S. Food and Drug Administration, Bacteriological analytical manual (BAM), Chap. 8, 2017. Retrieved from URL https://www.fda.gov/food/foodscienceresearch

Weese, J. S. & Van Duijkeren, E. (2010). Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Veterinary Microbiology, 140(3-4), 418-429.

Yabsley, M. J. (2019). The Role of Wildlife Rehabilitation in Wildlife Disease Research and Surveillance. Medical Management of Wildlife Species: A Guide for Practitioners, p. 159-165, 2019.

Downloads

Published

17/01/2021

How to Cite

SILVEIRA, D. R.; MORAES, T. P. de .; KAEFER, K.; BACH, L. G.; BARBOSA, A. de O.; MORETTI, V. D.; MENEZES, P. Q. de .; MEDEIROS, U. S. de .; SILVA, T. T. da .; BANDARRA, P. M.; MINELLO, L. F.; TIMM, C. D. MRSA and enterobacteria of one health concern in wild animals undergoing rehabilitation. Research, Society and Development, [S. l.], v. 10, n. 1, p. e34810111809, 2021. DOI: 10.33448/rsd-v10i1.11809. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/11809. Acesso em: 23 nov. 2024.

Issue

Section

Agrarian and Biological Sciences