Skip to main content

Effect of milk temperature and flow on the adherence of Staphylococcus epidermidis to stainless steel in amounts capable of biofilm formation

Abstract

The adherence of microorganisms to surfaces is a critical precondition for biofilm development. In this study, we evaluated the adherence (in amounts capable of biofilm formation) of Staphylococcus epidermidis in milk to stainless steel. During a 6-h time frame, the effect of milk temperature and laminar flow on adherence was analysed. In amounts capable of biofilm formation, the cells adhered within 0.5 h; however, at the milk temperatures promoting cell growth (25 and 28 °C), the cells proceeded to detach from the surface when bacteria started to grow (after 2 h), but only during the milk flow. When the temperatures were below the growth limit (6 and 22 °C) or under static conditions, the cells remained attached during the whole monitoring period. This study showed that temperatures which are suboptimal for growth and static conditions support the adhesion S. epidermidis in amounts capable of biofilm formation. On the contrary, at temperatures allowing the growth, adhered cells of S. epidermidis can easily be washed away from the stainless steel surface when bacteria begin to grow.

温度和流速对表皮葡萄球菌在不锈钢表面上的粘附以及对生物膜形成的影响

摘要 微生物在表面上粘合是形成生物膜的前提。本文研究了表皮葡萄球菌在不锈钢表面上的粘附作用 (也就是形成生物膜的量)。分析了乳在板框中停留 6h 内乳的温度和层流速度对粘附作用的影响。在 0.5h 内就能发生了细胞粘附和形成生物膜, 然而随着温度升高到 25°C 和 28°C, 微生物的生长速度加快, 2h 后由于细菌的大量繁殖使得细胞随着流动的奶开始从表面上脱附下来。但是当乳的温度低于微生物的生长限 (6°C 和 22°C) 或者是在静态条件下, 在整个检测时间内, 细胞粘附于表面。研究结果表明在不利于微生物生长的温度和静态条件下会导致表皮葡萄球菌的粘附和形成生物膜, 相反, 在有利于微生物生长的温度下, 微生物的大量繁殖则使得粘附的细胞很容易从不锈钢表面上脱附下来。

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Becker K, Bierbaum G, von Eiff C, Engelmann S, Gotz F, Hacker J, Hecker M, Peters G, Rosenstein R, Ziebuhr W (2007) Understanding the physiology and adaptation of staphylococci: a post-genomic approach. Int J Med Microbiol 297:483–501

    Article  CAS  Google Scholar 

  2. Boles BR, Horswill AR (2008) agr – mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:1–13

    Article  Google Scholar 

  3. de Araujo GL, Coelho LR, de Carvalho CB, Maciel RM, Coronado AZ, Rozenbaum R, Ferreira-Carvalho BT, Sa Figueiredo AM, Teixeira LA (2006) Commensal isolates of methicillin-resistant Staphylococcus epidermidis are also well equipped to produce biofilm on polystyrene surfaces. J Antimicrob Chemother 57:855–864

    Article  Google Scholar 

  4. Flint SH, Bremer PJ, Brooks JD (1997) Biofilms in dairy manufacturing plant—description, current concerns and methods of control. Biofouling 11:81–97

    Article  CAS  Google Scholar 

  5. Frank JF (2001) Microbial attachment to food and food contact surfaces. Adv Food Nutr Res 43:319–370

    Article  CAS  Google Scholar 

  6. Genigeorgis CA (2004) Reducing the role of contact materials in the contamination of foods of animal origin. In: Smulders FJM, Collins JD (eds) Safety assurance during food processing: food safety assurance and veterinary public health, vol 2. Wageningen Academic Publishers, Wageningen, pp 279–315

    Google Scholar 

  7. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM (2005) 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

    Article  CAS  Google Scholar 

  8. Gotz F (2002) Staphylococcus and biofilms. Mol Microbiol 43:1367–1378

    Article  CAS  Google Scholar 

  9. Grubbs F (1969) Procedures for detecting outlying observations in samples. Technometrics 11:1–21

    Article  Google Scholar 

  10. Heilmann C, Gerke C, Perdreau-Remington F, Gotz F (1996a) Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 64:277–282

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Hilbert LR, Bagge-Ravn D, Kold J, Gram L (2003) Influence of surface roughness of stainless steel on microbial adhesion and corrosion resistance. Int Biodeterior Biodegrad 52:175–185

    Article  CAS  Google Scholar 

  13. Hood SK, Zottola EA (1997) Adherence to stainless steel by foodborne microorganisms during growth in model food systems. Int J Food Microbiol 37:145–153

    Article  CAS  Google Scholar 

  14. Jaglic Z, Michu M, Holasova M, Vlkova H, Babak V, Kolar M, Bardon J, Schlegelova J (2010) Epidemiology and characterization of Staphylococcus epidermidis isolates from humans, raw bovine milk and a dairy plant. Epidemiol Infect 138:772–782

    Article  CAS  Google Scholar 

  15. Johnson AP, Clark JB, Osborn MF (1983) Scanning electron microscopy of the interaction between Haemophilus influenza and organ cultures of rat trachea. J Med Microbiol 16:477–482

    Article  CAS  Google Scholar 

  16. Kim H, Ryu JH, Beuchat LR (2006) Attachment of and biofilm formation by Enterobacter sakazakii on stainless steel and enteral feeding tubes. Appl Environ Microbiol 72:5846–5856

    Article  CAS  Google Scholar 

  17. Knight GC, Nicol RS, McMeekin TA (2004) Temperature step changes: a novel approach to control biofilms of Streptococcus thermophilus in a pilot plant-scale cheese-milk pasteurisation plant. Int J Food Microbiol 93:305–318

    Article  CAS  Google Scholar 

  18. Lens P, Moran AP, Mahony T, Stoodley P, O'Flaherty V (2003) Biofilms in medicine, industry and environmental biotechnology. Characteristics, analysis and control, 1st edn. IWA Publishing, London

    Google Scholar 

  19. Mack D, Davies AP, Harris LG, Rohde H, Horstkotte MA, Knobloch JKM (2007) Microbial interactions in Staphylococcus epidermidis biofilms. Anal Bioanal Chem 387:399–408

    Article  CAS  Google Scholar 

  20. Mattila-Sandholm T, Wirtanen G (1992) Biofilm formation in the food industry: a review. Food Rev Int 8:573–603

    Article  CAS  Google Scholar 

  21. Michu E, Cervinkova D, Babak V, Kyrova K, Jaglic Z (2011) Biofilm formation on stainless steel by Staphylococcus epidermidis in milk and influence of glucose and sodium chloride on the development of ica-mediated biofilms. Int Dairy J 21:179-184

    Google Scholar 

  22. Moretro T, Hermansen L, Holck AL, Sidhu MS, Rudi K, Langsrud S (2003) Biofilm formation and the presence of the intercellular adhesion locus ica, among staphylococci from food and food processing environments. Appl Environ Microbiol 69:5648–5655

    Article  CAS  Google Scholar 

  23. Piette A, Verschraegen G (2009) Role of coagulase-negative staphylococci in human disease. Vet Microbiol 134:45–54

    Article  CAS  Google Scholar 

  24. Pompermayer DMC, Gaylarde CC (2000) The influence of temperature on the adhesion of mixed cultures of Staphylococcus aureus and Escherichia coli to polypropylene. Food Microbiol 17:361–365

    Article  CAS  Google Scholar 

  25. Rieu A, Lemaitre JP, Guzzo J, Piveteau P (2008) Interactions in dual species biofilms between Listeria monocytogenes EGD-e and several strains of Staphylococcus aureus. Int J Food Microbiol 126:76–82

    Article  CAS  Google Scholar 

  26. Schlegelova J, Babak V, Holasova M, Konstantinova L, Necidova L, Sisak F, Vlkova H, Roubal P, Jaglic Z (2010) Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants. Czech J Food Sci 28:450–461

    Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Sommer P, Martin-Rouas C, Mettler E (1999) Influence of the adherent population level on biofilm population, structure and resistance to chlorination. Food Microbiol 16:503–515

    Article  CAS  Google Scholar 

  29. Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microbes Infect 4:481–489

    Article  Google Scholar 

  30. Vuong C, Gerke C, Somerville GA, Fischer ER, Otto M (2003) Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J Infect Dis 188:706–718

    Article  CAS  Google Scholar 

  31. Wang C, Li M, Dong D, Wang J, Ren J, Otto M, Gao Q (2007) Role of ClpP in biofilm formation and virulence of Staphylococcus epidermidis. Microbes Infect 9:1376–1383

    Article  CAS  Google Scholar 

  32. Ziebuhr W, Heilmann C, Gotz F, Meyer P, Wilms K, Straube E, Hacker J (1997) Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 65:890–896

    CAS  Google Scholar 

Download references

Acknowledge

The authors thank Mr. Jiri Kudrna (Veterinary Research Institute, Brno, Czech Republic) for preparation of specimens and images from scanning electron microscope, Mgr. Maria Vass, PhD. for English proofreading and Prof. Anping Deng, Ph.D. for Chinese translation of the abstract. Supported by the Ministry of Agriculture of the Czech Republic (project MZe0002716202) and Ministry of Education, Youth and Sports of the Czech Republic (projects 2B08074 and CZ.1.05/2.1.00/01.0006; ED0006/01/01).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Zoran Jaglic.

About this article

Cite this article

Jaglic, Z., Cervinkova, D., Michu, E. et al. Effect of milk temperature and flow on the adherence of Staphylococcus epidermidis to stainless steel in amounts capable of biofilm formation. Dairy Science & Technol. 91, 361–372 (2011). https://doi.org/10.1007/s13594-011-0017-6

Download citation

Keywords

  • Food safety
  • Hygiene
  • Dairy
  • Attachment
  • Detachment

关键词

  • 食品安全
  • 卫生学
  • 吸附
  • 脱附