Virulência, grupos agr, resistência a antimicrobianos e epidemiologia de isolados de Staphylococcus aureus obtidos de vacas com mastite

Autores

DOI:

https://doi.org/10.11606/issn.1678-4456.bjvras.2021.186701

Palavras-chave:

MSSA, MIONSA, Accessory gene regulator (agr), Mastite bovina

Resumo

Cinquenta e dois isolados de Staphylococcus aureus obtidos de amostras colhidas do óstio papilar, do leite de vacas com mastite subclínica e do ambiente de ordenha em três fazendas de rebanhos leiteiros localizadas no sudeste do Brasil foram identificados por PCR para o gene da termonuclease (nuc). Todos os isolados foram testados para sensibilidade a antimicrobianos e foram investigados os sequence types (STs), grupos agr (I-IV) e genes de virulência que codificam Microbial Surface Components Recognizing Adhesive Matrix Molecules (MSCRAMMs), proteínas associadas a biofilme, toxinas bi-componentes, toxinas pirogênicas com propriedades de superantígenos e enterotoxinas. Triagem para detecção de resistência à oxacilina (2-6 μg/ml oxacilina), ensaios de atividade de enzimas beta-lactamases e PCR para os genes mecA/mecC detectaram 26 estirpes de S. aureus sensíveis à meticilina (methicillin-susceptible S. aureus, MSSA) e 26 estirpes de S. aureus mec-negativas não sensíveis à meticilina (mec-independent oxacillin-nonsusceptible S. aureus, MIONSA). Enquanto os isolados MSSA foram sensíveis a todos os agentes antimicrobianos testados, ou apenas resistentes à penicilina e ampicilina, os isolados MIONSA foram multirresistentes. MSSA ST126-agr grupo II foram prevalentes no leite (n= 14) e apresentaram um amplo conjunto de genes de virulência (clfA, clfB, eno, fnbA, fiB, icaA, icaD, lukED, hla e hlb), assim como o isolado MIONSA ST126-agr grupo II proveniente de um insuflador (n= 1), o qual também apresentou o gene eta. MIONSA ST1-agr grupo III (n= 4) foram identificados no óstio papilar e leite, mas a maioria dos isolados MIONSA (n= 21), encontrados em óstios papilares e insufladores, foram agr-negativos e pertenceram ao ST126. As linhagens agr-negativas e agr grupo III apresentaram baixo potencial de virulência. Estudos sobre a caracterização de MSSA/MIONSA associados a bovinos são essenciais para a redução da mastite causada por S. aureus e de perdas econômicas na produção leiteira e, também, para o monitoramento do potencial zoonótico desses patógenos associados a infecções invasivas e falhas de tratamento em ambientes hospitalares.

Downloads

Os dados de download ainda não estão disponíveis.

Referências

Abdelhady W, Chen L, Bayer AS, Seidl K, Yeaman MR, Kreiswirth BN, Xiong YQ. Early agr activation correlates with vancomycin treatment failure in multi-clonotype MRSA endovascular infections. J Antimicrob Chemother. 2015;70(5):1443-52. http://doi.org/10.1093/jac/dku547. PMid:25564565.

Altman DR, Sullivan MJ, Chacko KI, Balasubramanian D, Pak TR, Sause WE, Kumar K, Sebra R, Deikus G, Attie O, Rose H, Lewis M, Fulmer Y, Bashir A, Kasarskis A, Schadt EE, Richardson AR, Torres VJ, Shopsin B, van Bakel H. Genome Plasticity of agr-Defective Staphylococcus aureus during Clinical Infection. Infect Immun. 2018;86(10):e00331-18. http://doi.org/10.1128/IAI.00331-18. PMid:30061376.

Barkema HW, Schukken YH, Zadoks RN. Invited Review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci. 2006;89(6):1877-95. http://doi.org/10.3168/jds.S0022-0302(06)72256-1. PMid:16702252.

Becker K, Skov RL, von Eiff C. Staphylococcus, micrococcus, and other catalase-positive cocci. In: Jorgensen JH, Carroll KC, Funke G, Pfaller MA, Landry ML, Richter SS, Warnock DW, editors. Manual of clinical microbiology. Hoboken: John Wiley & Sons, Ltd; 2015. p. 354-82. http://doi.org/10.1128/9781555817381.ch21.

Benito Y, Kolb FA, Romby P, Lina G, Etienne J, Vandenesch F. Probing the structure of RNAIII, the Staphylococcus aureus agr regulatory RNA, and identification of the RNA domain involved in repression of protein A expression. RNA. 2000;6(5):668-79. http://doi.org/10.1017/S1355838200992550. PMid:10836788.

Chambers HF. Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev. 1997;10(4):781-91. http://doi.org/10.1128/CMR.10.4.781. PMid:9336672.

Cifrian E, Guidry AJ, Bramley AJ, Norcross NL, Bastida-Corcuera FD, Marquardt WW. Effect of staphylococcal beta toxin on the cytotoxicity, proliferation and adherence of Staphylococcus aureus to bovine mammary epithelial cells. Vet Microbiol. 1996;48(3-4):187-98. http://doi.org/10.1016/0378-1135(95)00159-X. PMid:9054116.

Clinical and Laboratory Standards Institute – CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 4th ed. Wayne, PA: CLSI; 2018. CLSI supplement VET08.

Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penadés JR. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol. 2001;183(9):2888-96. http://doi.org/10.1128/JB.183.9.2888-2896.2001. PMid:11292810.

Dohoo IR, Smith J, Andersen S, Kelton DF, Godden S. Diagnosing intramammary infections: evaluation of definitions based on a single milk sample. J Dairy Sci. 2011;94(1):250-61. http://doi.org/10.3168/jds.2010-3559. PMid:21183035.

Endo Y, Yamada T, Matsunaga K, Hayakawa Y, Kaidoh T, Takeuchi S. Phage conversion of exfoliative toxin A in Staphylococcus aureus isolated from cows with mastitis. Vet Microbiol. 2003;96(1):81-90. http://doi.org/10.1016/S0378-1135(03)00205-0. PMid:14516710.

Fitzgerald JR. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat. Trends Microbiol. 2012;20(4):192-8. http://doi.org/10.1016/j.tim.2012.01.006. PMid:22386364.

Foster TJ, Geoghegan JA, Ganesh VK, Höök M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol. 2014;12(1):49-62. http://doi.org/10.1038/nrmicro3161. PMid:24336184.

García-Álvarez L, Holden MTG, Lindsay H, Webb CR, Brown DFJ, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RLR, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11(8):595-603. http://doi.org/10.1016/S1473-3099(11)70126-8. PMid:21641281.

Geoghegan JA, Ganesh VK, Smeds E, Liang X, Höök M, Foster TJ. Molecular characterization of the interaction of staphylococcal microbial surface components recognizing adhesive matrix molecules (MSCRAMM) ClfA and Fbl with fibrinogen. J Biol Chem. 2010;285(9):6208-16. http://doi.org/10.1074/jbc.M109.062208. PMid:20007717.

Gilot P, Lina G, Cochard T, Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 2002;40(11):4060-7. http://doi.org/10.1128/JCM.40.11.4060-4067.2002. PMid:12409375.

Giulieri SG, Guérillot R, Kwong JC, Monk IR, Hayes AS, Daniel D, Baines S, Sherry NL, Holmes NE, Ward P, Gao W, Seemann T, Stinear TP, Howden BP. Comprehensive Genomic investigation of adaptive mutations driving the low-level oxacillin resistance phenotype in Staphylococcus aureus. MBio. 2020;11(6):e02882-20. http://doi.org/10.1128/mBio.02882-20. PMid:33293382.

Herman-Bausier P, Labate C, Towell AM, Derclaye S, Geoghegan JA, Dufrêne YF. Staphylococcus aureus clumping factor A is a force-sensitive molecular switch that activates bacterial adhesion. Proc Natl Acad Sci USA. 2018;115(21):5564-9. http://doi.org/10.1073/pnas.1718104115. PMid:29735708.

Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70(2):631-41. http://doi.org/10.1128/IAI.70.2.631-641.2002. PMid:11796592.

Ji G, Beavis R, Novick RP. Bacterial interference caused by autoinducing peptide variants. Science. 1997;276(5321):2027-30. http://doi.org/10.1126/science.276.5321.2027. PMid:9197262.

Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124. http://doi.org/10.12688/wellcomeopenres.14826.1. PMid:30345391.

Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother. 2007;51(1):264-74. http://doi.org/10.1128/AAC.00165-06. PMid:17043114.

Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-81. http://doi.org/10.1111/j.1469-0691.2011.03570.x. PMid:21793988.

National Mastitis Council. Microbiological Procedures for use in the diagnosis of bovine udder infection and determination of milk quality. 4th ed. Verona, WI: National Mastitis Council; 2004.

Oliveira L, Hulland C, Ruegg PL. Characterization of clinical mastitis occurring in cows on 50 large dairy herds in Wisconsin. J Dairy Sci. 2013;96(12):7538-49. http://doi.org/10.3168/jds.2012-6078. PMid:24119795.

Omoe K, Ishikawa M, Shimoda Y, Hu D-L, Ueda S, Shinagawa K. Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates Harboring seg, seh, or sei genes. J Clin Microbiol. 2002;40(3):857-62. http://doi.org/10.1128/JCM.40.3.857-862.2002. PMid:11880405.

Painter KL, Krishna A, Wigneshweraraj S, Edwards AM. What role does the quorum-sensing accessory gene regulator system play during Staphylococcus aureus bacteremia? Trends Microbiol. 2014;22(12):676-85. http://doi.org/10.1016/j.tim.2014.09.002. PMid:25300477.

Pyörälä S. Indicators of inflammation in the diagnosis of mastitis. Vet Res. 2003;34(5):565-78. http://doi.org/10.1051/vetres:2003026. PMid:14556695.

Reyes-Robles T, Alonzo F 3rd, Kozhaya L, Lacy DB, Unutmaz D, Torres VJ. Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promote infection. Cell Host Microbe. 2013;14(4):453-9. http://doi.org/10.1016/j.chom.2013.09.005. PMid:24139401.

Schalm OW, Noorlander DO. Experiments and observations leading to development of the California mastitis test. J Am Vet Med Assoc. 1957;130(5):199-204. PMid:13416088.

Schukken YH, Wilson DJ, Welcome F, Garrison-Tikofsky L, Gonzalez RN. Monitoring udder health and milk quality using somatic cell counts. Vet Res. 2003;34(5):579-96. http://doi.org/10.1051/vetres:2003028. PMid:14556696.

Seidl K, Chen L, Bayer AS, Hady WA, Kreiswirth BN, Xiong YQ. Relationship of agr expression and function with virulence and vancomycin treatment outcomes in experimental endocarditis due to methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2011;55(12):5631-9. http://doi.org/10.1128/AAC.05251-11. PMid:21968365.

Shopsin B, Drlica-Wagner A, Mathema B, Adhikari RP, Kreiswirth BN, Novick RP. Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J Infect Dis. 2008;198(8):1171-4. http://doi.org/10.1086/592051. PMid:18752431.

Smith EM, Green LE, Medley GF, Bird HE, Fox LK, Schukken YH, Kruze JV, Bradley AJ, Zadoks RN, Dowson CG. Multilocus sequence typing of intercontinental bovine Staphylococcus aureus isolates. J Clin Microbiol. 2005;43(9):4737-43. http://doi.org/10.1128/JCM.43.9.4737-4743.2005. PMid:16145135.

Takeuchi S, Maeda T, Hashimoto N, Imaizumi K, Kaidoh T, Hayakawa Y. Variation of the agr locus in Staphylococcus aureus isolates from cows with mastitis. Vet Microbiol. 2001;79(3):267-74. http://doi.org/10.1016/S0378-1135(00)00354-0. PMid:11240104.

Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol. 2003;41(9):4465-7. http://doi.org/10.1128/JCM.41.9.4465-4467.2003. PMid:12958296.

van den Borne BHP, van Schaik G, Lam TJGM, Nielen M, Frankena K. Intramammary antimicrobial treatment of subclinical mastitis and cow performance later in lactation. J Dairy Sci. 2019;102(5):4441-51. http://doi.org/10.3168/jds.2019-16254. PMid:30827563.

Vasudevan P, Nair MKM, Annamalai T, Venkitanarayanan KS. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol. 2003;92(1-2):179-85. http://doi.org/10.1016/S0378-1135(02)00360-7. PMid:12488081.

Yarwood JM, Schlievert PM. Quorum sensing in Staphylococcus infections. J Clin Invest. 2003;112(11):1620-5. http://doi.org/10.1172/JCI200320442. PMid:14660735.

Downloads

Publicado

2021-12-01

Edição

Seção

ARTIGO COMPLETO

Dados de financiamento

Como Citar

1.
Zorzi FM, Zafalon LF, Santos FB, Borges AF, Nascimento TG, Basílio-Júnior ID, et al. Virulência, grupos agr, resistência a antimicrobianos e epidemiologia de isolados de Staphylococcus aureus obtidos de vacas com mastite. Braz. J. Vet. Res. Anim. Sci. [Internet]. 1º de dezembro de 2021 [citado 19º de maio de 2024];58:e186701. Disponível em: https://www.periodicos.usp.br/bjvras/article/view/186701