Association between coa gene and enterotoxin gene in S. aureus from dairy cattle in Brazil

Autores

  • Mylena Karoline VALMORBIDA Universidade Estadual Paulista “Júlio de Mesquita Filho”, Postgraduate Program in Agricultural Microbiology, Faculty of Agricultural and Veterinary Sciences, Department of Veterinary Pathology, Jaboticabal, SP, Brazil. https://orcid.org/0000-0002-8154-2420
  • Marita Vedovelli CARDOZO Universidade do Estado de Minas Gerais, Department of Biomedical Sciences and Health, Passos, MG, Brazil. https://orcid.org/0000-0003-3972-0198
  • Camila Chioda de ALMEIDA Universidade Estadual Paulista “Júlio de Mesquita Filho”, Postgraduate Program in Agricultural Microbiology, Faculty of Agricultural and Veterinary Sciences, Department of Veterinary Pathology, Jaboticabal, SP, Brazil. https://orcid.org/0000-0001-5454-5426
  • Natália PEREIRA Universidade Estadual Paulista “Júlio de Mesquita Filho”, Postgraduate Program in Agricultural Microbiology, Faculty of Agricultural and Veterinary Sciences, Department of Veterinary Pathology, Jaboticabal, SP, Brazil. https://orcid.org/0000-0001-5914-084X
  • Diogenes DEZEN Instituto Federal Catarinense, Veterinary Microbiology Laboratory, Concórdia, SC, Brazil. https://orcid.org/0000-0002-0941-9954
  • Marcella Zampoli de ASSIS Instituto Federal Catarinense, Veterinary Microbiology Laboratory, Concórdia, SC, Brazil. https://orcid.org/0000-0001-8860-4914
  • Newton Valério VERBISCK Empresa Brasileira de Pesquisa Agropecuária, Embrapa beef cattle, Campo Grande, MS, Brazil. https://orcid.org/0000-0001-9817-7223
  • Eliete GRIEBELER Instituto Federal Catarinense, Veterinary Microbiology Laboratory, Concórdia, SC, Brazil. https://orcid.org/0000-0002-5198-6805
  • Lucas José Luduverio PIZAURO Universidade Estadual de Santa Cruz, Department of Agricultural and Environmental Sciences, Ilhéus, BA, Brazil. https://orcid.org/0000-0002-1071-8740
  • Fernando Antônio de ÁVILA Universidade Estadual Paulista “Júlio de Mesquita Filho”, Faculty of Agricultural and Veterinary Sciences, Department of Preventive Veterinary Medicine and Animal Reproduction, Jaboticabal, SP, Brazil. https://orcid.org/0000-0002-9779-2213

DOI:

https://doi.org/10.5327/fst.16222

Palavras-chave:

mastitis, toxins, resistance, pulsed-field gel electrophoresis, dairy

Resumo

Staphylococcus aureus is an important agent in bovine mastitis, and some specific virulence factors may be implicated in this disease. Therefore, this study aimed to investigate the importance of the presence of coagulase, superantigens, genotypic and phenotypic resistance, and pulsotypes in 65 S. aureus isolates from bovine clinical and subclinical mastitis in the Southeast of Brazil. A high correlation was observed between the genes coa and see, as well as between the sei and the see and seh. High resistance rates were observed for penicillin (95.4%), tetracycline (89.2%), cefoxitin (86.1%), oxacillin (84.6%), erythromycin (84.6%), clindamycin (84.6%), chloramphenicol (81.5%), ceftriaxone (80.0%), and ampicillin (80.0%). Analysis of antimicrobial resistance profiles showed that 89.2% of isolates were multi-drug-resistant. No mecA-positive S. aureus isolates were detected. It was observed that seven isolates were resistant to all the β-lactam tested while being susceptible to cefoxitin, which could be indicative of borderline methicillin resistance in S. aureus⁠. High genetic diversity with no specific virulence profile being predominant was observed. Thus, this study observed a high correlation between the coa and enterotoxins genes, and demonstrates that there is no predominant pulsotype causing intramammary infection and that there is a high rate of antibiotic resistance in S. aureus isolates from dairy farms in the southeast regions of Brazil.

Downloads

Não há dados estatísticos.

Referências

Ameen, F., Reda, S. A., El-Shatoury, S. A., Riad, E. M., Enany, M. E., & Alarfaj, A. A. (2019). Prevalence of antibiotic resistant mastitis pathogens in dairy cows in Egypt and potential biological control agents produced from plant endophytic actinobacteria. Saudi Journal of Biological Sciences, 26(7), 1492-1498. https://doi.org/10.1016/j.sjbs.2019.09.008

Baba, T., Bae, T., Schneewind, O., Takeuchi, F., & Hiramatsu, K. (2008). Genome sequence of Staphylococcus aureus strain newman and comparative analysis of staphylococcal genomes: Polymorphism and evolution of two major pathogenicity islands. Journal of Bacteriology, 190(1), 300-310. https://doi.org/10.1128/JB.01000-07

Bauer, A. W., Kirby, W. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4), 493-496. https://doi.org/10.1093/ajcp/45.4_ts.493

Clinical and Laboratory Standards Institute (CLSI) (2018). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals (2nd ed.). CLSI.

Dan, M., Yehui, W., Qingling, M., Jun, Q., Xingxing, Z., Shuai, M., Kuojun, C., Jinsheng, Z., Zibing, C., Zaichao, Z., & Xuepeng, C. (2019). Antimicrobial resistance, virulence gene profile and molecular typing of Staphylococcus aureus isolates from dairy cows in Xinjiang Province, northwest China. Journal of Global Antimicrobial Resistance, 16, 98-104. https://doi.org/10.1016/j.jgar.2018.08.024

De Almeida, C. C., Pizauro, L. J. L., Soltes, G. A., Slavic, D., De Ávila, F. A., Pizauro, J. M., & MacInnes, J. I. (2018). Some coagulase negative Staphylococcus spp. isolated from buffalo can be misidentified as Staphylococcus aureus by phenotypic and Sa442 PCR methods. BMC Research Notes, 11(1), 346. https://doi.org/10.1186/s13104-018-3449-8

Duran, N., Ozer, B., Duran, G. G., Onlen, Y., & Demir, C. (2012). Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian Journal of Medical Research, 135(3), 389-396.

Fang, R., Cui, J., Cui, T., Guo, H., Ono, H. K., Park, C. H., Okamura, M., Nakane, A., & Hu, D. L. (2019). Staphylococcal enterotoxin C is an important virulence factor for mastitis. Toxins, 11(3), 141. https://doi.org/10.3390/toxins11030141

Freitas, C. H., Mendes, J. F., Villarreal, P. V., Santos, P. R., Gonçalves, C. L., Gonzales, H. L., & Nascente, P. S. (2018). Identification and antimicrobial suceptibility profile of bacteria causing bovine mastitis from dairy farms in Pelotas, Rio Grande do Sul. Brazilian Journal of Biology, 78(4), 661-666. https://doi.org/10.1590/1519-6984.170727

Fursova, K. K., Shchannikova, M. P., Loskutova, I. V., Shepelyakovskaya, A. O., Laman, A. G., Boutanaev, A. M., Sokolov, S. L., Artem’eva, O. A., Nikanova, D. A., Zinovieva, N. A., & Brovko, F. A. (2018). Exotoxin diversity of Staphylococcus aureus isolated from milk of cows with subclinical mastitis in Central Russia. Journal of Dairy Science, 101(5), 4325-4331. https://doi.org/10.3168/jds.2017-14074

Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontoligia Electronica, 4(1), 1-9.

Heikkilä, A. M., Nousiainen, J. I., & Pyörälä, S. (2012). Costs of clinical mastitis with special reference to premature culling. Journal of Dairy Science, 95(1), 139-150. https://doi.org/10.3168/jds.2011-4321

Hryniewicz, M. M., & Garbacz, K. (2017). Borderline oxacillin-resistant staphylococcus aureus (BORSA) - a more common problem than expected? Journal of Medical Microbiology, 66(10), 1367-1373. https://doi.org/10.1099/jmm.0.000585

Hunter, J. D. (2007). Matplotlib: A 2D graphics environment. Computing in Science and Engineering, 9(3), 90-95. https://doi.org/10.1109/MCSE.2007.55

Javid, F., Taku, A., Bhat, M. A., Badroo, G. A., Mudasir, M., & Sofi, T. A. (2018). Molecular typing of Staphylococcus aureus based on coagulase gene. Veterinary World, 11(4), 423-430. https://doi.org/10.14202/vetworld.2018.423-430

Käppeli, N., Morach, M., Corti, S., Eicher, C., Stephan, R., & Johler, S. (2019). Staphylococcus aureus related to bovine mastitis in Switzerland: Clonal diversity, virulence gene profiles, and antimicrobial resistance of isolates collected throughout 2017. Journal of Dairy Science, 102(4), 3274-3281. https://doi.org/10.3168/jds.2018-15317

Kim, N. H., Yun, A. R., & Rhee, M. S. (2011). Prevalence and classification of toxigenic Staphylococcus aureus isolated from refrigerated ready-to-eat foods (sushi, kimbab and California rolls) in Korea. Journal of Applied Microbiology, 111(6), 1456-1464. https://doi.org/10.1111/j.1365-2672.2011.05168.x

Kumar, R., Yadav, B. R., & Singh, R. S. (2010). Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle. Current Microbiology, 60(5), 379-386. https://doi.org/10.1007/s00284-009-9553-1

Kuramae-Izioka, E. E. (1997). A rapid, easy and high yield protocol for total genomic DNA isolation of Colletotrichum gloeosporioides and Fusarium oxysporum. Unimar, 19(3), 683-689.

Liu, H., Li, S., Meng, L., Dong, L., Zhao, S., Lan, X., Wang, J., & Zheng, N. (2017). Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. Journal of Dairy Science, 100(11), 8796-8803. https://doi.org/10.3168/jds.2017-13370

Luo, K., Shao, F., Kamara, K. N., Chen, S., Zhang, R., Duan, G., & Yang, H. (2018). Molecular characteristics of antimicrobial resistance and virulence determinants of Staphylococcus aureus isolates derived from clinical infection and food. Journal of Clinical Laboratory Analysis, 32(7), e22456. https://doi.org/10.1002/jcla.22456

Manukumar, H. M., & Umesha, S. (2017). MALDI-TOF-MS based identification and molecular characterization of food associated methicillin-resistant Staphylococcus aureus. Scientific Reports, 7(1), 11414. https://doi.org/10.1038/s41598-017-11597-z

Markey, B., Leonard, F., Archambault, M., Cullinane, A., & Maguire, D. (2013). Staphylococcus species. In Edinburgh (Ed.), Clinical Veterinary Microbiology (2nd ed., pp. 105-120). Elsevier.

Martineau, F., Picard, F. J., Ke, D., Paradis, S., Roy, P. H., Ouellete, M., & Bergeron, M. G. (2001). Development of a PCR Assay for Identification of Staphylococci at Genus and Species Levels Journal of Clinical Microbiology, 39(7), 2541-2547. https://doi.org/10.1128/jcm.39.7.2541-2547.2001

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. https://doi.org/10.1128/jcm.38.3.1032-1035.2000

Nix, I. D., Idelevich, E. A., Storck, L. M., Sparbier, K., Drews, O., Kostrzewa, M., & Becker, K. (2020). Detection of Methicillin Resistance in Staphylococcus aureus From Agar Cultures and Directly From Positive Blood Cultures Using MALDI-TOF Mass Spectrometry-Based Direct-on-Target Microdroplet Growth Assay. Frontiers in Microbiology, 11, 232. https://doi.org/10.3389/fmicb.2020.00232

Paniagua-Contreras, G., Sáinz-Espuñes, T., Monroy-Pérez, E., Rodríguez-Moctezuma, J. R., Arenas-Aranda, D., Negrete-Abascal, E., & Vaca, S. (2012). Virulence Markers in Staphylococcus aureus Strains Isolated from Hemodialysis Catheters of Mexican Patients. Advances in Microbiology, 2(4), 476-487. https://doi.org/10.4236/aim.2012.24061

Pérez-Sancho, M., Vela, A. I., Horcajo, P., Ugarte-Ruiz, M., Domínguez, L., Fernández-Garayzábal, J. F., & Fuente, R. (2018). Rapid differentiation of Staphylococcus aureus subspecies based on MALDI-TOF MS profiles. Journal of Veterinary Diagnostic Investigation, 30(6), 813-820. https://doi.org/10.1177/1040638718805537

Pizauro, L. J. L., Almeida, C. C., Silva, S. R., MacInnes, J. I., Kropinski, A. M., Zafalon, L. F., Avila, F. A., & Mello Varani, A. (2021). Genomic comparisons and phylogenetic analysis of mastitis-related staphylococci with a focus on adhesion, biofilm, and related regulatory genes. Scientific Reports, 11(1), 17392. https://doi.org/10.1038/s41598-021-96842-2

R Core (2016). R: a Language and Environment for Statistical Computing. Retrieved from: http://www.R-project.org

Ren, Q., Liao, G., Wu, Z., Lv, J., & Chen, W. (2020). Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang, China. Journal of Dairy Science, 103(4), 3368-3380. https://doi.org/10.3168/jds.2019-17420

Ribot, E. M., Fair, M. A., Gautom, R., Cameron, D. N., Hunter, S. B., Swaminathan, B., & Barrett, T. J. (2006). Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathogens and Disease, 3(1), 59–67. https://doi.org/10.1089/fpd.2006.3.59

Rossi, C. C., Pereira, M. F., & Giambiagi-Demarval, M. (2020). Underrated staphylococcus species and their role in antimicrobial resistance spreading. Genetics and Molecular Biology, 43(1 Suppl. 2), 1-10. https://doi.org/10.1590/1678-4685-gmb-2019-0065

Santos, D. C., Lange, C. C., Avellar-Costa, P., Santos, K. R. N., Brito, M. A. V. P., & Giambiagi-deMarval, M. (2016). Staphylococcus chromogenes, a coagulase-negative Staphylococcus species that can clot plasma. Journal of Clinical Microbiology, 54(5), 1372-1375. https://doi.org/10.1128/JCM.03139-15

Schmidt, T., Kock, M. M., & Ehlers, M. M. (2017). Molecular characterization of staphylococcus aureus isolated from bovine mastitis and close human contacts in South African dairy herds: Genetic diversity and inter-species host transmission. Frontiers in Microbiology, 8, 511. https://doi.org/10.3389/fmicb.2017.00511

Silva, E. R., & Silva, N. (2005). Coagulase gene typing of Staphylococcus aureus isolated from cows with mastitis in southeastern Brazil. Canadian Journal of Veterinary Research, 69(4), 260-264.

Szafraniec, G. M., Szeleszczuk, P., & Dolka, B. (2020). A review of current knowledge on staphylococcus agnetis in poultry. Animals, 10(8), 1421. https://doi.org/10.3390/ani10081421

Tam, K., & Torres, V. J. (2019). Staphylococcus aureus Secreted Toxins and Extracellular Enzymes. Gram-Positive Pathogens, 7(2), 640-668. https://doi.org/10.1128/9781683670131.ch40

Van Der Walt, S., Colbert, S. C., & Varoquaux, G. (2011). The NumPy array: A structure for efficient numerical computation. Computing in Science and Engineering, 13(2), 22-30. https://doi.org/10.1109/MCSE.2011.37

Vitale, M., Gaglio, S., Galluzzo, P., Cascone, G., Piraino, C., Di Marco Lo Presti, V., & Alduina, R. (2018). Antibiotic Resistance Profiling, Analysis of Virulence Aspects and Molecular Genotyping of Staphylococcus aureus Isolated in Sicily, Italy. Foodborne Pathogens and Disease, 15(3), 177-185. https://doi.org/10.1089/fpd.2017.2338

Wang, W., Lin, X., Jiang, T., Peng, Z., Xu, J., Yi, L., Li, F., Fanning, S., & Baloch, Z. (2018). Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in Beijing, China. Frontiers in Microbiology, 9, 1123. https://doi.org/10.3389/fmicb.2018.01123

Zhao, S., Tyson, G. H., Chen, Y., Li, C., Mukherjee, S., Young, S., Lam, C., Folster, J. P., Whichard, J. M., & McDermott, P. F. (2016). Whole-genome sequencing analysis accurately predicts antimicrobial resistance phenotypes in Campylobacter spp. Applied and Environmental Microbiology, 82(2), 459-466. https://doi.org/10.1128/AEM.02873-15

Downloads

Publicado

2023-10-05

Como Citar

VALMORBIDA, M. K., CARDOZO, M. V., ALMEIDA, C. C. de, PEREIRA, N., DEZEN, D., ASSIS, M. Z. de, VERBISCK, N. V., GRIEBELER, E., PIZAURO, L. J. L., & ÁVILA, F. A. de. (2023). Association between coa gene and enterotoxin gene in S. aureus from dairy cattle in Brazil. Food Science and Technology, 43. https://doi.org/10.5327/fst.16222

Edição

v. 43 (2023)

Seção

Artigos Originais