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The biofilm-positive Staphylococcus epidermidis isolates in raw materials, foodstuffs and on contact surfaces in processing plants

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Abstract

Isolates from the “farm to fork” samples (182 isolates from 2779 samples) were examined genotypically (icaAB genes) and phenotypically (in vitro biofilm formation, typical growth on Congo red agar; CRA) with the aim to assess the risk of penetration of virulent strains of Staphylococcus epidermidis into the food chain. The contamination of meat and milk products was significantly higher in comparison with raw materials. Contamination of contact surfaces in the meat-processing plants was significantly lower than that of contact surfaces in the dairy plants. The ica genes (which precondition the biofilm formation) were concurrently detected in 20 isolates that also showed a typical growth on CRA. Two ica operon-negative isolates produced biofilm in vitro but perhaps by an ica-independent mechanism. The surfaces in the dairy plants and the milk products were more frequently contaminated with ica operon-positive strains (2.3 and 1.2 % samples) than the other sample types (0–0.6 % samples).

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Abbreviations

BF:

biofilm formation

CRA:

Congo red agar

PFGE:

pulsed field gel electrophoresis

PIA:

polysaccharidic intercellular adhesin

References

  • Arciola C.R., Baldassarri L., Montanaro L.: Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J.Clin.Microbiol.39, 2151–2156 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Asao T., Kumeda Y., Kawai T., Shibata T., Oda H., Haruki K., Nakazawa H., Kozaki S.: An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol.Infect.130, 33–40 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Chmielewski R., Frank J.F.: Biofilm formation and control in food processing facilities. Comp.Rev.Food Sci.Food Safety2, 22–32 (2003).

    Article  CAS  Google Scholar 

  • Conlon K.M., Humphreys H., O’GARA J.P.: icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J.Bacteriol184, 4400–4408 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Cramton S.E., Gerke C., Götz F.: In vitro methods to study staphylococcal biofilm formation. Meth.Enzymol.336, 239–255 (2001a).

    Article  PubMed  CAS  Google Scholar 

  • Cramton S.E., Ulrich M., Götz F., Döring G.: Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect.Immun.69, 4079–4085 (2001b).

    Article  PubMed  CAS  Google Scholar 

  • Cucarella C., Solano C., Valle J., Amorena B., Lasa I., Penades J.R.: Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J.Bacteriol.183, 2888–2896 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Donlan R.M., Costerton J.W.: Biofilms: survival mechanisms of clinically relevant microorganisms. Clin.Microbiol.Rev.15, 167–193 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Von Eiff C., Peters G., Heilmann C.: Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect.Dis.2, 677–685 (2002).

    Article  Google Scholar 

  • Fitzpatrick F., Humphreys H., Smyth E., Kennedy C.A., O’gara J.P.: Environmental regulation of biofilm formation in intensive care unit isolates of Staphylococcus epidermidis. J.Hosp.Infect. 52, 212–218(2002).

    Article  PubMed  CAS  Google Scholar 

  • Frebourg N.B., Lefebvre S., Baert S., Lemeland J.F.: PCR-based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J.Clin.Microbiol.38, 877–880 (2000).

    PubMed  CAS  Google Scholar 

  • Gill S.R., Fouts D.E., Archer G.L., Mongodin E.F., Deboy R.T., Ravel J., Paulsen I.T., Kolonay J.F., Brinkac L., Beanan M., Dodson R.J., Daugherty S.C., Madupu R., Angiuoli S.V., Durkin A.S., Haft D.H., Vamathevan J., Khouri H., Utterback T., Lee C., Dimitrov G., Jiang L.X., Qin H.Y., Weidman J., Tran K., Kang K., Hance I.R., Nelson K.E., Fraser C.M.: Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J.Bacteriol.187, 2426–2438 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Götz F.: Staphylococcus and biofilms. Mol.Microbiol.43, 1367–1378 (2002).

    Article  PubMed  Google Scholar 

  • Heilmann C., Schweitzer O., Gerke C., Vanittanakom N., Mack D., Götz F.: Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol.Microbiol.20, 1083–1091 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Knobloch J.K., Jäger S., Horstkotte M.A., Rohde H., Mack D.: RsbU-dependent regulation of Staphylococcus epidermidis biofilm formation is mediated via the alternative sigma factor σB by repression of the negative regulator gene icaR. Infect. Immun.72, 3838–3848 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Malíková L., Sedláček I., Nováková D., Němec M.: Ribotyping and biotyping of Staphylococcus epidermidis isolated from hospital environment. Folia Microbiol.52, 375–380 (2007).

    Article  Google Scholar 

  • Martineau F., Picard F.J., Roy P.H., Ouellette M., Bergeron M.G.: Species-specific and ubiquitous DNA-based assays for rapid identification of Staphylococcus epidermidis. J.Clin.Microbiol.34, 2888–2893 (1996).

    PubMed  CAS  Google Scholar 

  • Melchior M.B., Vaarkamp H., Fink-gremmels J.: Biofilms: a role in recurrent mastitis infections? Vet.J.171, 398–407 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Mettler E., Carpentier B.: Variations over time of microbial load and physicochemical properties of floor materials after cleaning in food industry premises. J.Food Prot.61, 57–65 (1998).

    PubMed  CAS  Google Scholar 

  • Projan S.J., Novick R.P.: The molecular basis of pathogenocity, pp. 55–81 in K.B. Crossley, G.L. Archer (Eds): The Staphylococci in Human Disease.Churchill Livingstone, New York 1997.

    Google Scholar 

  • Rohde H., Burdelski C., Bartscht K., Hussain M., Buck F., Horstkotte M.A., Knobloch J.K., Heilmann C., Herrmann M., Mack D.: Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteinases. Mol.Microbiol.55, 1883–1895 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Rùžička F., Holá V., Votava M., Tejkalová R., Horvát R., Heroldová M., Woznicová V.: Biofilm detection and the clinical significance of Staphylococcus epidermidis isolates. Folia Microbiol.49, 596–600 (2004).

    Article  Google Scholar 

  • Sadovskaya I., Vinogradov E., Li J., Jabbouri S.: Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr.Res.339, 1467–1473 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Schlegelová J., Nápravníková E., Dendis M., Horváth R., Benedik J., Babak V., Klímová E., Navrátilová P., Šustáčková A.: Beef carcass contamination in a slaughterhouse and prevalence of resistance to antimicrobial drugs in isolates of selected microbial species. Meat Sci.66, 557–565 (2004).

    Article  CAS  Google Scholar 

  • Sharma M., Anand S.K.: Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol.19, 627–636 (2002).

    Article  CAS  Google Scholar 

  • Somers E.B., Johnson M.E., Wong A.C.: Biofilm formation and contamination of cheese by nonstarter lactic acid bacteria in the dairy environment. J.Dairy Sci.84, 1926–1936 (2001).

    PubMed  CAS  Google Scholar 

  • Tormo M.A., Marti M., Valle J., Manna A.C., Cheung A.L., Lasa I., Penades J.R.: SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J.Bacteriol.187, 2348–2356 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Troller J.A.: Water relations of foodborne bacterial pathogens. An update review. J.Food Prot.49, 656–670 (1986).

    Google Scholar 

  • Vuong C., Gerke C., Somerville G.A., Fischer E.R., Otto M.: Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J.Infect.Dis.188, 706–718 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Walencka E., Sadowska B., Różalska S., Hryniewicz W., Różalska B.: Staphylococcus aureus biofilm as a target for single or repeated doses of oxacillin, vancomycin, linezolid and/or lysostaphin. Folia Microbiol.51, 381–386 (2006).

    Article  CAS  Google Scholar 

  • Wong A.C.: Biofilms in food processing environments. J.Dairy Sci.81, 2765–2770 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Yarwood J.M., Schlievert P.M.: Quorum sensing in staphylococcus infections. J.Clin.Invest.112, 1620–1625 (2003).

    PubMed  CAS  Google Scholar 

  • Zhang Y.Q., Ren S.X., Li H.L., Wang Y.X., Fu G., Yang J., Qin Z.Q., Miao Y.G., Wang W.Y., Chen R.S., Shen Y., Chen Z., Yuan Z.H., Zhao G.P., Qu D., Danchin A., Wen Y.M.: Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol.Microbiol.49, 1577–1593 (2003).

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Veterinary Research Institute, 621 00, Brno, Czech Republic

    J. Schlegelová, V. Babák & M. Holasová

  2. Genex CZ Ltd., 615 00, Brno, Czech Republic

    M. Dendis

Authors
  1. J. Schlegelová
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  2. V. Babák
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  3. M. Holasová
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  4. M. Dendis
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Correspondence to J. Schlegelová.

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Schlegelová, J., Babák, V., Holasová, M. et al. The biofilm-positive Staphylococcus epidermidis isolates in raw materials, foodstuffs and on contact surfaces in processing plants. Folia Microbiol 53, 500–504 (2008). https://doi.org/10.1007/s12223-008-0078-y

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  • DOI: https://doi.org/10.1007/s12223-008-0078-y

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