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A coagulase-negative variant of Staphylococcus aureus from bovine mastitis milk

Published online by Cambridge University Press:  01 December 2010

Ömer Akineden*
Affiliation:
Food Science, Institute of Veterinary Food Science, Justus-Liebig-University Giessen, Frankfurter Strasse 92, D-35392 Giessen, Germany
Abdulwahed Ahmed Hassan
Affiliation:
GD Animal Health Service, Department of Bacteriology and Parasitology, Postbus 9, 7400 AA Deventer, The Netherlands
Elisabeth Schneider
Affiliation:
Dairy Sciences, Institute of Veterinary Food Science, Justus-Liebig-University Giessen, Ludwigstrasse 21, D-35390 Giessen, Germany
Ewald Usleber
Affiliation:
Dairy Sciences, Institute of Veterinary Food Science, Justus-Liebig-University Giessen, Ludwigstrasse 21, D-35390 Giessen, Germany
*

Abstract

Bacteriological analysis of milk samples from quarters of a dairy cow suffering from subclinical mastitis yielded two isolates of Staphylococcus aureus which gave a negative reaction in the standard coagulase test. Both isolates were also clumping factor and thermonuclease negative, and gave a negative reaction in the Staphaurex® test. The isolates were identified by using commercial biochemical systems, and by PCR analysis of different staphylococcal cell surface protein and exoprotein genes. Further molecular identification of the isolates, which included sequencing of the 16S rRNA gene and RT-PCR of coagulase (coa), clumping-factor (clfA) and thermonuclease (nuc) genes, was consistent with the diagnosis phenotypically ‘coagulase-negative variant of Staph. aureus’. The fact that coagulase-negative Staph. aureus variants can occur in the context of intramammary infections in cattle may result in the incorrect diagnosis ‘coagulase-negative staphylococci (CNS)’ in routine mastitis diagnostic, at least in rare cases. To fully ensure correct species diagnosis, sequencing of the 16S rRNA gene and amplification of specific genes such as coa is necessary in these cases.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2010

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References

Aarestrup, FM, Larsen, HD, Eriksen, NH, Elsberg, CS & Jensen, NE 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 425430CrossRefGoogle ScholarPubMed
Akineden, Ö, Annemüller, C, Hassan, AA, Lämmler, C, Wolter, W & Zschöck, M 2001 Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clinical and Diagnostic Laboratory Immunology 8 959964CrossRefGoogle Scholar
Akineden, Ö, Hassan, AA, Schneider, E & Usleber, E 2008 Enterotoxigenic properties of Staphylococcus aureus isolated from goats’ milk cheese. International Journal of Food Microbiology 124 211216CrossRefGoogle ScholarPubMed
Al Obaid, AI, Udo, EE, Jacob, LE & Johny, M 1999 Isolation and characterization of cogulase-negative methicillin-resistant Staphylococcus aureus from patients in an intensive care unit. Medical Principles and Practice 8 230236CrossRefGoogle Scholar
Anonymous 2009 [Guidelines for the collection of milk samples under antiseptic conditions and for identification of mastitis pathogens. Expert committee on subclinical mastitis] Deutsche Veterinärmedizinische Gesellschaft (DVG), GießenGoogle Scholar
Brakstad, OG, Aasbakk, K & Maeland, JA 1992 Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. Journal of Clinical Microbiology 30 16541660CrossRefGoogle ScholarPubMed
Bodén, MK & Flock, JI 1989 Fibrinogen-binding protein/clumping factor from Staphylococcus aureus. Infection and Immunity 57 23582363CrossRefGoogle ScholarPubMed
Boerlin, P, Kuhnert, P, Hussy, D & Schaellibaum, M 2003 Methods for identification of Staphylococcus aureus isolates in cases of bovine mastitis. Journal of Clinical Microbiology 41 767771CrossRefGoogle ScholarPubMed
Forsman, P, Tilsala-Timisjärvi, A & Alatossava, T 1997 Identification of staphylococcal and streptococcal causes of bovine mastitis using 16S-23S rRNA spacer regions. Microbiology 143 34913500CrossRefGoogle ScholarPubMed
Fox, LK & Gay, JM 1993 Contagious mastitis. Veterinary Clinics of North America Food Animal Practice 9 475487CrossRefGoogle ScholarPubMed
Garbacz, K, Piechowicz, L, Wisniewska, K & Galinski, J 2002 Characteristics of defective strains of methicillin resistance Staphylococcus aureus that do not produce coagulase or CF. Medycyna Doswiadczalna i Mikrobiologia 54 18Google ScholarPubMed
Golledge, C & Gordon, A 1989 Slide coagulase positive, tube coagulase negative Staphylococcus aureus. Journal of Clinical Pathology 42 443CrossRefGoogle ScholarPubMed
Heltberg, O & Bruun, B 1984 Recognition of coagulase-negative Staphylococcus aureus strains by primary polymyxin susceptibility testing. Acta Pathologica et Microbiologica Scandinavica 92 115118CrossRefGoogle ScholarPubMed
Kloos, WE & Schleifer, KH 1975 Simplified scheme for routine identification of human Staphylococcus species. Journal of Clinical Microbiology 1 8288CrossRefGoogle ScholarPubMed
Kuhnert, P, Capaul, SE, Nicolet, J & Frey, J 1996 Phylogenetic positions of Clostridium chauvoei and Clostridium septicum based on 16S rRNA gene sequences. International Journal of Systematic Bacteriology 46 11741176CrossRefGoogle ScholarPubMed
Laevens, H, Devriese, LA, Deluyker, H, Hommez, J & de Kruif, A 1996 An atypical Staphylococcus aureus intramammary infection in a dairy herd. Veterinary Microbiology 52 271275CrossRefGoogle Scholar
Lam, TJ, Pengov, A, Schukken, A, Smit, YH & Brand, A 1995 The differentiation of Staphylococcus aureus from other Micrococcaceae isolated from bovine mammary glands. Journal of Applied Bacteriology 79 6972CrossRefGoogle ScholarPubMed
Lange, C, Cardoso, M, Senczek, D & Schwarz, S 1999 Molecular subtyping of Staphylococcus aureus isolates from cases of bovine mastitis in Brazil. Veterinary Microbiology 67 127141CrossRefGoogle ScholarPubMed
Luijendijk, A, van Belkum, A, Verbrugh, H & Kluytmans, J 1996 Comparison of five tests for identification of Staphylococcus aureus from clinical samples. Journal of Clinical Microbiology 34 22672269CrossRefGoogle ScholarPubMed
Mackay, AD, Quick, A, Gillespie, SH & Kibbler, CC 1993 Coagulase-negative methicillin-resistant Staphylococcus aureus infection. Lancet 342 492CrossRefGoogle ScholarPubMed
Malinowski, E, Lassa, H, Klossowska, A, Smulski, S & Kaczmarowski, M 2009 Atypical Staphylococcus aureus as an aetiological agent of mastitis in cows. Bulletin of the Veterinary Institute in Pulawy 53 383387Google Scholar
Martineau, F, Picard, FJ, Roy, PH, Ouellette, M & Bergeron, MG 1998 Species-specific and ubiquitous-DNA based assays for rapid identification of Staphylococcus aureus. Journal of Clinical Microbiology 36 618623CrossRefGoogle ScholarPubMed
Matthews, KR, Roberson, J, Gillespie, BE, Luther, DA, Oliver, SP 1997 Identification and differentiation of coagulase-negative Staphylococcus aureus by polymerase chain reaction. Jounal of Food Protection 60 686688CrossRefGoogle ScholarPubMed
Menzies, ER 1977 Comparison of coagulase, deoxyribonuclease (DNase), and heat-stable nuclease tests for identification of Staphylococcus aureus. Journal of Clinical Pathology 30 606608CrossRefGoogle ScholarPubMed
Mlynarczyk, G, Kochman, M, Lawrynowicz, M, Fordymacki, P, Mlynarczyk, A & Jeljaszewicz, J 1998 Coagulase-negative variants of methicillin-resistant Staphylococcus aureus subsp. aureus strains isolated from hospital specimens. Zentralblatt für Bakteriologie 288 373381CrossRefGoogle ScholarPubMed
Neville, LO, Billington, OJ, Kibbler, CC & Gillespie, SH 1991 Methicillin resistant Staphylococcus aureus without clumping factor, protein A, and DNAse. Lancet 338 518CrossRefGoogle ScholarPubMed
Notarnicola, SM, Zamarchi, GR & Onderdonk, AB 1985 Misidentification of mucoid variants of Staphylococcus aureus by standard laboratory techniques. Journal of Clinical Microbiology 22 459461CrossRefGoogle ScholarPubMed
Ruane, PJ, Morgan, MA, Citron, DM & Mulligan, ME 1986 Failure of rapid agglutination methods to detect oxacillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 24 490492CrossRefGoogle ScholarPubMed
Personne, P, Bes, M, Lina, G, Vandenesch, F, Brun, Y & Etienne, J 1997 Comparative performances of six agglutination kits assessed by using typical and atypical strains of Staphylococcus aureus. Journal of Clinical Microbiology 35 11381140CrossRefGoogle ScholarPubMed
Smole, SC, Aronson, E, Durbin, A, Brecher, SM & Arbeit, RD 1998 Sensitivity and specificity of an improved rapid latex agglutination test for identification of methicillin-sensitive and -resistant Staphylococcus aureus isolates. Journal of Clinical Microbiology 36 11091112CrossRefGoogle ScholarPubMed
Smyth, EG, Wright, ED & Marples, RR 1988 New type of staphylococcal enteriditis. Journal of Clinical Pathology 41 809810CrossRefGoogle Scholar
Stephan, R, Annemüller, C, Hassan, AA & Lämmler, C 2000 Characterization of enterotoxigenic Staphylococcus aureus strains isolated from bovine mastitis in north-east Switzerland. Veterinary Microbiology 78 373382CrossRefGoogle Scholar
Straub, JA, Hertel, C & Hammes, WP 1999 A 23S rRNA-targeted polymerase chain reaction-based system for detection of Staphylococcus aureus in meat starter cultures and dairy products. Journal of Food Protection 62 11501156CrossRefGoogle Scholar
Van Griethuysen, A, Bes, M, Etienne, J, Zbinden, R & Kluytmans, J 2001 International multicenter evaluation of latex agglutination tests for identification of Staphylococcus aureus. Journal of Clinical Microbiology 39 8689CrossRefGoogle ScholarPubMed
Vandenesch, F, Lebeau, C, Bes, M, McDevitt, D, Greenland, T, Novick, RP & Etienne, J 1994a Coagulase deficiency in clinical isolates of Staphylococcus aureus involves both transcriptional and post-transcriptional defects. Journal of Medical Microbiology 40 344349CrossRefGoogle ScholarPubMed
Vandenesch, F, Lebeau, C, Bes, M, Lina, G, Lina, B, Greenland, T, Benito, Y, Brun, Y, Fleurette, J & Etienne, J 1994b Clotting activity in Staphylococcus schleiferi subspecies from human patients. Journal of Clinical Microbiology 32 388392CrossRefGoogle ScholarPubMed
Vandenesch, F, Bes, M, Lebeau, C, Greenland, T, Brun, Y & Etienne, J 1993 Coagulase-negative Staphylococcus aureus. Lancet 342 994995CrossRefGoogle ScholarPubMed
Varshney, JP, Kapur, MP & Sharma, A 1993 Studies on some biochemical characteristics of Staphylococcus aureus of buffalo mammary origin. Comparative Immunology Microbiology and Infectious Diseases 16 317321CrossRefGoogle ScholarPubMed
Wanger, AR, Morris, SL, Ericsson, C, Singh, KV & LaRocco, MT 1992 Latex agglutination-negative methicillin-resistant Staphylococcus aureus recovered from neonates: epidemiologic features and comparison of typing methods. Journal of Clinical Microbiology 30 25832588CrossRefGoogle ScholarPubMed
Wilkerson, M, McAllister, S, Miller, JM, Heiter, BJ & Bourbeau, PP 1997 Comparison of five agglutination tests for identification of Staphylococcus aureus. Journal of Clinical Microbiology 35 148151CrossRefGoogle ScholarPubMed
Woo, PC, Leung, AS, Leung, KW & Yuen, KY 2001 Identification of slide coagulase positive, tube coagulase negative Staphylococcus aureus by 16S ribosomal RNA gene sequencing. Molecular Pathology 54 2442447CrossRefGoogle ScholarPubMed