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Study of Staphylococcus aureus collected at slaughter from dairy cows with chronic mastitis

Published online by Cambridge University Press:  28 February 2012

Renata Piccinini ,
Riccardo Tassi ,
Valentina Daprà ,
Rachel Pilla ,
Jackie Fenner ,
Ben Carter  and
Muna F. Anjum
Renata Piccinini*
Affiliation:
Department of Veterinary Pathology, Hygiene and Public Health, Università degli Studi di Milano, Via Celoria 10, 20133 Milano, Italy
Riccardo Tassi
Affiliation:
Department of Veterinary Pathology, Hygiene and Public Health, Università degli Studi di Milano, Via Celoria 10, 20133 Milano, Italy
Valentina Daprà
Affiliation:
Department of Veterinary Pathology, Hygiene and Public Health, Università degli Studi di Milano, Via Celoria 10, 20133 Milano, Italy
Rachel Pilla
Affiliation:
Department of Veterinary Pathology, Hygiene and Public Health, Università degli Studi di Milano, Via Celoria 10, 20133 Milano, Italy
Jackie Fenner
Affiliation:
Department of Bacteriology, Veterinary Laboratories Agency-Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK Technology Transfer Unit, Veterinary Laboratories Agency-Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK
Ben Carter
Affiliation:
Department of Primary Care and Public Health, School of Medicine, Cardiff University, Gwenfro Unit 5, Wrexham Technology Park, Wrexham LL17 7YP, UK
Muna F. Anjum
Affiliation:
Department of Bacteriology, Veterinary Laboratories Agency-Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK Technology Transfer Unit, Veterinary Laboratories Agency-Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK
*
*For correspondence; e-mail: renata.piccinini@unimi.it
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Abstract

Staphylococcus aureus is one of the most important pathogens associated with bovine mastitis. Recent studies have shown that Staph. aureus strains may differ in virulence, and in their ability to disseminate across commercial dairy herds. The goal of this study was to determine whether Staph. aureus isolates differed in their ability to colonize mammary tissue, and whether such differences could be related to molecular characteristics. Quarter milk and mammary tissues of 22 cows from two dairy herds, were collected at slaughter and bacteriological analysis was performed. All Staph. aureus isolates were characterized by Pulsed Field Gel Electrophoresis (PFGE) and microarray. Overall 45 mammary quarters were infected and 20 Staph. aureus isolates were identified. The bacteria were mostly recovered from both milk and tissue of the same quarter in significantly higher numbers from herd A cows compared with herd B. Molecular characterization of the isolates showed distinct PFGE profiles for isolates from each herd. Differences in virulence factors between herds A and B isolates were evidenced The genes for enterotoxin D, J and R were present in herd A, those for G, I, N, M, O and U were shown in herd B, whilst both components of the leukocidin lukD/E genes were only carried by herd A isolates. Furthermore, all herd A isolates showed β-haemolysin activity, which was absent in all but one isolate from herd B. Therefore our data indicate that Staph. aureus isolates showing differences in their ability to disseminate and colonize across quarters, also have significantly different virulence characteristics.

Keywords

Staphylococcus aureusbovine mastitismolecular characteristicsmammary localization
Type
Research Article
Information
Journal of Dairy Research , Volume 79 , Issue 2 , May 2012 , pp. 249 - 255
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

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References

Aarestrup, FM, Larsen, HD, Eriksen, NH & Elsberg, CS 1999 Frequency of alpha- and beta-haemolysin in Staphylococcus aureus of bovine and human origin. A comparison between pheno- and genotype and variation in phenotypic expression. Acta Pathologica, Microbiologica et Immunologica Scandinavica 107 425–430Google Scholar
Almeida, RA, Matthews, KR, Cifrian, E, Guidry, AJ & Oliver, SP 1996 Staphylococcus aureus invasion of bovine mammary epithelial cells. Journal of Dairy Science 79 1021–1026CrossRefGoogle ScholarPubMed
Anderson, JC & Chandler, RL 1975 Experimental Staphylococcal mastitis in the mouse. Histological, ultrastructural and bacteriological changes caused by a virulent strain of Staphylococcus aureus. Journal of Comparative Pathology 85 499–510CrossRefGoogle ScholarPubMed
Argudín, MA, Mendoza, MC, Méndez, FJ, Martín, MC, Guerra, B & Rodicio, MR 2011 Clonal complexes and diversity of exotoxin gene profiles in methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from patients in a Spanish hospital. Journal of Clinical Microbiology 47 2097–2105CrossRefGoogle Scholar
Bonura, C, Plano, MRA, Di Carlo, P, Calà, C, Cipolla, D, Corsello, G, Mammina, C & EPI-MRSA Working Group 2010 MRSA ST22-IVa (EMRSA-15 clone) in Palermo, Italy. Journal of Infection and Public Health 3 188–191CrossRefGoogle ScholarPubMed
Bystron, J, Podkowik, M, Korzekwa, K, Lis, E, Molenda, J & Bania, J 2010 Characterization of borderline oxacillin-resistant Staphylococcus aureus isolated from food of animal origin. Journal of Food Protection 73 1325–1327Google Scholar
Chandler, RL & Reid, IM 1973 Ultrastructural and associated observations on clinical cases of mastitis in cattle. Journal of Comparative Pathology 83 233–241CrossRefGoogle ScholarPubMed
Chandler, RL, Reid, IM, Harrison, R & France, BR 1974 Ultrastructural, morphometric and associated observations on experimental mastitis in cattle. Journal of Comparative Pathology 84 517–531Google Scholar
Cheung, AL, Bayer, AS, Zhang, G, Gresham, H & Xiong, YQ 2004 Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunology and Medical Microbiology 40 1–9Google Scholar
Chung, M, de Lencastre, H, Matthews, P, Tomasz, A, Adamsson, I, Aires de Sousa, M, Camou, T, Cocuzza, C, Corso, A, Couto, I, Dominguez, A, Gniadkowski, M, Goering, R, Gomes, A, Kikuchi, K, Marchese, A, Mato, R, Melter, O, Oliveira, D, Palacio, R, Sa-Leao, R, Santos Sanches, I, Song, JH, Tassios, PT & Villari, P 2000 Molecular typing of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis: comparison of results obtained in a multilaboratory effort using identical protocols and MRSA strains. Microbial Drug Resistance 6 189–198CrossRefGoogle Scholar
Clinical and Laboratory Standards Institute 2008 Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standards (M31-A3). Clinical and Laboratory Standards Institute, Wayne, PA, USAGoogle Scholar
Dego, OK, Van Dijk, JE & Nederbragt, H 2002 Factors involved in the early pathogenesis of bovine Staphylococcus aureus mastitis with emphasis on bacterial adhesion and invasion. Veterinary Quarterly 24 181–198CrossRefGoogle Scholar
Fleiss, JL 1981 Statistical Methods for Rates and Proportions, 2nd edn.New York, NY, USA: John WileyGoogle Scholar
Fournier, C, Kuhnert, P, Frey, J, Miserez, R, Kirchhofer, M, Kaufmann, T, Steiner, A & Graber, HU 2008 Bovine Staphylococcus aureus: association of virulence genes, genotypes and clinical outcome. Research in Veterinary Science 85 439–448Google Scholar
Graber, HU, Naskova, L, Studer, E, Kaufmann, T, Kirchhofer, M, Brechbühl, M, Schaeren, W, Steiner, A & Fournier, C 2009 Mastitis-related subtypes of bovine Staphylococcus aureus are characterized by different clinical properties. Journal of Dairy Science 92 1442–1451Google Scholar
Grumann, D, Scharf, SS, Holtfreter, S, Kohler, C, Steil, L, Engelmann, S, Hecker, M, Völker, U & Bröker, BM 2008 Immune cell activation by enterotoxin gene cluster (egc)-encoded and non-egc superantigens from Staphylococcus aureus. Journal of Immunology 181 5054–5061Google Scholar
Gudding, R, McDonald, JS & Cheville, NS 1984 Pathogenesis of Staphylococcus aureus mastitis: bacteriologic, histologic, and ultrastructural pathologic findings. American Journal of Veterinary Research 45 2525–2531Google Scholar
Haveri, M, Roslof, A, Rantala, L & Pyorala, S 2007 Virulence genes of bovine Staphylococcus aureus from persistent and nonpersistent intramammary infections with different clinical characteristics. Journal of Applied Microbiology 103 993–1000CrossRefGoogle ScholarPubMed
Haveri, M, Suominen, S, Rantala, L, Honkanen-Buzalski, T & Pyorala, S 2005 Comparison of phenotypic and genotypic detection of penicillin G resistance of Staphylococcus aureus isolated from bovine intramammary infection. Veterinary Microbiology 106 97–102CrossRefGoogle ScholarPubMed
Hebert, A, Sayasit, K, Senechal, S, Dubreuil, P & Lagace, J 2000 Demonstration of intracellular Staphylococcus aureus in bovine mastitis alveolar cells and macrophages isolated from naturally infected cow milk. FEMS Microbiology Letters 193 57–62Google Scholar
Hensen, SM, Pavicic, MJ, Lohuis, JACM, de Hoog, JAM & Poutrel, B 2000 Location of Staphylococcus aureus within the experimentally infected bovine udder and the expression of capsular polysaccharide type 5 in situ. Journal of Dairy Science 83 1966–1975CrossRefGoogle ScholarPubMed
Hogan, JS, Gonzales, RN, Harmon, RJ, Nickerson, SC, Oliver, SP, Pankey, JW & Smith, KL 1999 Laboratory Handbook on Bovine Mastitis, revised edition, p. 222. Madison, WI: National Mastitis Council Inc.Google Scholar
Holmes, MA & Zadoks, RN 2011 Methicillin resistant S. aureus in human and bovine mastitis. Journal of Mammary Gland Biology and Neoplasia 16 373–382Google Scholar
Kaase, M, Lenga, S, Friedrich, S, Szabados, F, Sakinc, T, Kleine, B & Gatermann, SG 2008 Comparison of phenotypic methods for penicillinase detection in Staphylococcus aureus. Clinical Microbiology and Infection 14 614–616CrossRefGoogle ScholarPubMed
Lammers, A, Nujiten, PJM & Smith, HE 1999 The fibronectin binding proteins of Staphylococcus aureus are required for adhesion and invasion of bovine mammary gland cells. FEMS Microbiology Letters 180 103–109CrossRefGoogle ScholarPubMed
Larsen, HD, Aarestrup, FM & Jensen, NE 2002 Geographical variation in the presence of genes encoding superantigenic exotoxins and β-hemolysin among Staphylococcus aureus isolated from bovine mastitis in Europe and USA. Veterinary Microbiology 85 61–67CrossRefGoogle ScholarPubMed
Lindsay, JA & Holden, MT 2006 Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Functional and Integrative Genomics 6 186–201Google Scholar
Lowy, FD 2000 Is Staphyloccocus aureus an intracellular pathogen? Trends in Microbiology 8 341–343CrossRefGoogle Scholar
Monecke, S & Ehricht, R 2005 Rapid genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolates using miniaturised oligonucleotide arrays. Clinical Microbiology and Infection 11 825–833CrossRefGoogle ScholarPubMed
Monecke, S, Kuhnert, P, Hotzel, H, Slickers, P & Ehricht, R 2007 Microarray-based study on virulence associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Veterinary Microbiology 125 128–140Google Scholar
Moret-Stalder, S, Fournier, C, Miserez, R, Albini, S, Doherr, MG, Reist, M, Schaeren, W, Kirchhofer, M, Graber, HU, Steiner, A & Kaufmann, T 2009 Prevalence study of Staphylococcus aureus in quarter milk samples of dairy cows in the Canton of Bern, Switzerland. Preventive Veterinary Medicine 88 72–76CrossRefGoogle ScholarPubMed
Nickerson, SC & Heald, CW 1981 Histopathologic response of the bovine mammary gland to experimentally induced Staphylococcus aureus infection. American Journal of Veterinary Research 42 1351–1355Google ScholarPubMed
NMC 1999 Laboratory Handbook on Bovine Mastitis. Madison, WI, USA: National Mastitis Council Inc.Google Scholar
Ogawa, SK, Yurberg, ER, Hatcher, VB, Levitt, MA & Lowy, FD 1985 Bacterial adherence to human endothelial cells in vitro. Infection and Immunity 50 218–224CrossRefGoogle ScholarPubMed
Osteras, O, Edge, VL & Martin, SW 1999 Determinants of success or failure in the elimination of major mastitis pathogens in selective dry cow therapy. Journal of Dairy Science 82 1221–1231Google Scholar
Piccinini, R, Borromeo, V & Zecconi, A 2010 Relationship between S. aureus gene pattern and dairy herd mastitis prevalence. Veterinary Microbiology 145 100–105Google Scholar
Piccinini, R, Cesaris, L, Daprà, V, Borromeo, V, Picozzi, C, Secchi, C & Zecconi, A 2009 The role of teat skin contamination in the epidemiology of Staphylococcus aureus intramammary infection. Journal of Dairy Research 76 36–41Google Scholar
Rainard, P, Corrales, JC, Barrio, MB, Cochard, T & Poutrel, B 2003 Leucotoxic activities of Staphylococcus aureus strains isolated from cows, ewes, and goats with mastitis: importance of LukM/LukF-PV Leukotoxin. Clinical and Diagnostic Laboratory Immunology 10 272–277Google Scholar
Rubin, JE, Ball, KR & Chirino-Trejo, M 2011 Antimicrobial susceptibility of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from various animals. Canadian Veterinary Journal 52 153–157Google Scholar
Shopsin, B, Eaton, C, Wasserman, GA, Mathema, B, Adhikari, RP, Agolory, S, Altman, DR, Holzman, RS, Kreiswirth, BN & Novick, RP 2010 Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. Journal of Infectious Diseases 202 1593–1599Google Scholar
Sordillo, LM, Nickerson, SC & Akers, RM 1989 Pathology of Staphylococcus aureus mastitis during lactogenesis: relationship with bovine mammary structure and function. Journal of Dairy Science 72 228–240CrossRefGoogle ScholarPubMed
Tenover, FC, Arbeit, RD, Goering, RV, Mickelsen, PA, Murray, BE, Persing, DH & Swaminathan, B 1995 Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. Journal of Clinical Microbiology 33 2233–2239Google Scholar
Tollersrud, T, Kenny, K, Caugant, DA & Lund, A 2000 Characterisation of isolates of Staphylococcus aureus from acute, chronic and subclinical mastitis in cows in Norway. Acta Pathologica, Microbiologica et Immunologica Scandinavica 108 565–572Google Scholar
Traber, KE, Lee, E, Benson, S, Corrigan, R, Cantera, M, Shopsin, B & Novick, RP 2008 Agr function in clinical Staphylococcus aureus isolates. Microbiology 154 2265–2274CrossRefGoogle ScholarPubMed
Van Wamel, WJB, Rooijakkers, SHM, Ruyken, M, van Kessel, KPM & van Strijp, JAG 2006 The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on β-hemolysin-converting bacteriophages. Journal of Bacteriology 188 1310–1315Google Scholar
Younis, A, Krifucks, O, Fleminger, G, Heller, ED, Gollop, N, Saran, A & Leitner, G 2005 Staphylococcus aureus leucocidin, a virulence factor in bovine mastitis. Journal of Dairy Research 72 188–194Google Scholar
Zecconi, A, Cesaris, L, Liandris, E, Daprà, V & Piccinini, R 2006 Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microbial Pathogenesis 40 177–183Google Scholar
Zecconi, A, Piccinini, R & Fox, KL 2003 Epidemiologic study of intramammary infections with Staphylococcus aureus during a control program in nine commercial dairy herds. Journal of the American Veterinary Medical Association 223 684–688Google Scholar