Keywords
How to Cite
Abstract
Antimicrobial resistance is a natural mechanism in microorganisms, making the treatment of infections more complex in human and veterinary medicine. Global exotic and ornamental bird markets have significantly increased, and the close relationship between pets and humans makes exploring the potential role of these birds as vectors for the spread of antimicrobial-resistant bacteria imperative. This study aimed to use culture-dependent methods to investigate cloacal bacteria and the presence of antibiotic-resistant bacteria in four breeding stocks of ornamental birds. Cloacal swab samples were collected from 53 birds (canaries = 32, cockatiels = 17, and budgies = 4) and used for culturing and isolating facultative anaerobic and/or obligatory aerobic Gram-positive and Gram-negative bacteria. The antimicrobial susceptibility profile of each isolate was determined by the disk diffusion method. Thirty-four isolates were obtained, most of which belonged to the Staphylococcus genus. Bacterial richness was higher in canaries and in one of the breeding stockings, where Gram-negative bacteria were more abundant than in the others. In addition, canaries exhibited a predominance of resistant isolates, particularly multidrug-resistant strains, probably due to prophylactic antimicrobial usage. Most Gram-negative bacteria were resistant to at least one drug tested. A vancomycin-resistant Enterococcus faecalis strain was isolated. Most Staphylococcus strains were resistant to gentamycin, followed by penicillin. Eight strains were cefoxitin-resistant, including oxacillin-resistant S. epidermidis, in which the mecA gene was detected. Understanding the prevalence of resistance in avian species is crucial in the collaborative pursuit of maintaining antibiotic effectiveness and strengthening public health defense against emerging infectious risks.
References
Ahmed, M. O., & Baptiste, K. E. (2018). Vancomycin-resistant Enterococci: A review of antimicrobial resistance mechanisms and perspectives of human and animal health. Microbial Drug Resistance (Larchmont, N.Y.), 24(5), 590-606. http://doi.org/10.1089/mdr.2017.0147. PMid:29058560.
Algammal, A. M., Hetta, H. F., Elkelish, A., Alkhalifah, D. H. H., Hozzein, W. N., Batiha, G. E., Nahhas, N. E., & Mabrok, M. A. (2020). Methicillin-Resistant Staphylococcus aureus (MRSA): One Health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infection and Drug Resistance, 13, 3255-3265. http://doi.org/10.2147/IDR.S272733. PMid:33061472.
Alghamdi, B. A., Al-Johani, I., Al-Shamrani, J. M., Alshamrani, H. M., Al-Otaibi, B. G., Almazmomi, K., & Yusof, Y. (2023). Antimicrobial resistance in methicillin-resistant Staphylococcus aureus. Saudi Journal of Biological Sciences, 30(4), 103604. http://doi.org/10.1016/j.sjbs.2023.103604. PMid:36936699.
Amberpet, R., Sistla, S., Parija, S. C., & Thabah, M. M. (2016). Screening for intestinal colonization with vancomycin resistant enterococci and associated risk factors among patients admitted to an adult intensive care unit of a large teaching hospital. Journal of Clinical and Diagnostic Research : JCDR, 10(9), DC06-DC09. http://doi.org/10.7860/JCDR/2016/20562.8418. PMid:27790430.
Brooke, J. S. (2021). Advances in the Microbiology of Stenotrophomonas maltophilia. Clinical Microbiology Reviews, 34(3), e00030-19. http://doi.org/10.1128/CMR.00030-19. PMid:34043457.
Botoni, L. S., Scherer, C. B., Silva, R. O., Coura, F. M., Heinemann, M. B., Paes-Leme, F. O., & Costa-Val, A. P. (2016). Prevalence and in vitro susceptibility of methicillin-resistant Staphylococcus pseudintermedius (MRSP) from skin and nostrils of dogs with superficial pyoderma. Pesquisa Veterinária Brasileira, 36(12), 1178-1180. http://doi.org/10.1590/s0100-736x2016001200006.
Brazil. (1998). Portaria IBAMA Nº 93, de 7 de julho de 1998. https://www.ibama.gov.br/component/legislacao/? view=legislacao&legislacao=102740.
Brazil. (2019). Portaria IBAMA Nº 2489, de 09 de julho de 2019. https://www.ibama.gov.br/component/legislac ao/?view=legislacao&force=1&legislacao=138522.
Chang, Y. T., Lin, C. Y., Chen, Y. H., & Hsueh, P. R. (2015). Update on infections caused by Stenotrophomonas maltophilia with particular attention to resistance mechanisms and therapeutic options. Frontiers in Microbiology, 6, 893. http://doi.org/10.3389/fmicb.2015.00893. PMid:26388847.
Clinical and Laboratory Research Institute. (2022). Supplement M100. Clinical and Laboratory Standards Institute.
Dutka-Malen, S., Evers, S., & Courvalin, P. (1995). Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. Journal of Clinical Microbiology, 33(1), 24-27. http://doi.org/10.1128/jcm.33.1.24-27.1995. PMid:7699051.
Gaeta, N. C., Hellmeister, A., Possebon, F. S., Araujo, J. P., & Heinemann, M. B. (2022). Genomic analysis of a multidrug methicillin-resistant Staphylococcus epidermidis recovered from the urine of a guinea pig (Cavia porcellus) with suspected pyelonephritis. Veterinary Research Communications, 3. http://doi.org/10.1007/ s11259-022-10006-9. PMid:36323834.
Gil-Gil, T., Martínez, J. L., & Blanco, P. (2020). Mechanisms of antimicrobial resistance in Stenotrophomonas maltophilia: A review of current knowledge. Expert Review of Anti-Infective Therapy, 18(4), 335-347. http://doi.org/10.1080/14787210.2020.1730178. PMid:32052662.
Guedes, C. (2016). Mercado de aves ornamentais cresce 10% ao ano. https://www.canalrural.com.br/programas/ mercado-aves-ornamentais-cresce-ano-63.
Hammerum, P. M. (2012). Enterococci of animal origin and their significance for public health. Clinical Microbiology and Infection, 18(7), 619-625. http://doi.org/10.1111/j.1469-0691.2012.03829.x. PMid:22487203.
Hollenbeck, B. L., & Rice, L. B. (2012). Intrinsic and acquired resistance mechanisms in Enterococcus. Virulence, 3(5), 421-569. http://doi.org/10.4161/viru.21282. PMid:23076243.
Lamb, S., Sobczynski, A., Starks, D., & Sitinas, N. (2014). Bacteria isolated from the skin of Congo African Grey Parrots (Psittacus erithacus), Budgerigars (Melopsittacus undulatus), and Cockatiels (Nymphicus hollandicus). Journal of Avian Medicine and Surgery, 28(4), 275-279. http://doi.org/10.1647/1082-6742-28.4.275. PMid:25843464.
Latham, B., Leishman, A., Martin, J., & Phalen, D. (2017). Establishing normal fecal flora in wild Australian passarine birds by use of the fecak Gram stain. Journal of Zoo and Wildlife Medicine, 48(3), 786-793. http:// doi.org/10.1638/2016-0120.1. PMid:28920776.
Lee, G. (2013). Ciprofloxacin resistance in Enterococcus faecalis strains isolated from male patients with complicated urinary tract infection. Korean Journal of Urology, 54(6), 388-393. http://doi.org/10.4111/kju.2013.54.6.388. PMid:23789048.
Lowy, F. D. (2003). Antimicrobial resistance: The example of Staphylococcus aureus. The Journal of Clinical Investigation, 111(9), 1265-1273. http://doi.org/10.1172/JCI18535. PMid:12727914.
Martineau, F., Picard, F. J., Grenier, L., Roy, P. H., Ouellette, M., & Bergeron, M. G. (2000). Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. The Journal of Antimicrobial Chemotherapy, 46(4), 527-534. http://doi.org/10.1093/ jac/46.4.527. PMid:11020248.
Mehrotra, M., Wang, G., & Johnson, W. M. (2000). Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. Journal of Clinical Microbiology, 38(3), 1032-1035. http://doi.org/10.1128/JCM.38.3.1032-1035.2000. PMid:10698991.
Pasotto, D., Dotto, G., Menandro, M. L., Mondin, A., & Martini, M. (2016). Prevalence and antimicrobial-resistance characterization of vancomycin resistant enterococci (VRE) strains in healthy household dogs in Italy. International Journal of Infectious Diseases, 53, 50. http://doi.org/10.1016/j.ijid.2016.11.129.
Paterson, G. K., Harrison, E. M., & Holmes, M. A. (2014). The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends in Microbiology, 22(1), 42-47. http://doi.org/10.1016/j.tim.2013.11.003. PMid:24331435.
Prestinaci, F., Pezzotti, P., & Pantosti, A. (2015). Antimicrobial resistance: A global multifaceted phenomenon. Pathogens and Global Health, 109(7), 309-318. http://doi.org/10.1179/2047773215Y.0000000030. PMid:26343252.
Rizek, C. F., Jonas, D., Paez, J. I. G., Rosa, J. F., Perdigão Neto, L. V., Martins, R. R., Moreno, L. Z., Rossi Junior, A., Levin, A. S., & Costa, S. F. (2018). Multidrug-resistant Stenotrophomonas maltophilia: Description of new MLST profiles and resistance and virulence genes using whole-genome sequencing. Journal of Global Antimicrobial Resistance, 15, 212-214. http://doi.org/10.1016/j.jgar.2018.07.009. PMid:30036694.
RStudio Team. (2020). RStudio: Integrated Development for R. RStudio. http://www.rstudio.com/.
Schaberg, D. R., Dillon, W. I., Terpenning, M. S., Robinson, K. A., Bradley, S. F., & Kauffman, C. A. (1992). Increasing resistance of enterococci to ciprofloxacin. Antimicrobial Agents and Chemotherapy, 36(11), 2533-2535. http://doi.org/10.1128/AAC.36.11.2533. PMid:1489199.
Scherer, C. B., Botoni, L. S., Coura, F. M., Silva, R. O., Santos, R. D., Heinemann, M. B., & Costa-Val, A. P. (2018). Frequency and antimicrobial susceptibility of Staphylococcus pseudintermedius in dogs with otitis externa. Ciência Rural, 48(4), e20170738-e20170744. http://doi.org/10.1590/0103-8478cr20170738.
Tareen, A. R., & Zahra, R. (2023). Community-acquired methicillin-resistant Staphylococci (CA-MRS) in fecal matter of wild birds – a “One Health” point of concern. Journal of Infection and Public Health, 16(6), 877-883. http://doi.org/10.1016/j.jiph.2023.04.002. PMid:37054501.
Videvall, E., Strandh, M., Engelbrecht, A., Cloete, S., & Cornwallis, C. K. (2018). Measuring the gut microbiome in birds: Comparison of fecal and cloacal sampling. Molecular Ecology Resources, 18(3), 424-434. http://doi. org/10.1111/1755-0998.12744. PMid:29205893.
World Health Organization. (2017). WHO publishes list of bacteria for which new antibiotics are urgently needed. https:// www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed.
World Health Organization. (2021). Antimicrobial resistance. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2024 Bianca da Costa Tavares da Silva, Daniel Ubriaco Oliveira Gonçalves de Carvalho, Victoria Tiemi Sorbello Sakauchi, José Soares Ferreira Neto, Adriana Cortez, Marcos Bryan Heinemann, Natália Carrillo Gaeta