The effects of fluid composition and shear conditions on bacterial adhesion to an antifouling peptide-coated surface

Abstract

Biofilms can damage implants and are difficult to treat. Here, we assessed the performance of a tripeptide that self-assembles into an antifouling coating over a broad range of shear conditions that are relevant to biomedical applications. Adhesion assays were performed using a parallel plate flow chamber. The results show that the coating can reduce Escherichia coli adhesion up to 70% when compared with glass. At a shear rate of 15/s, typical for urinary catheters, the coating reduced the adhesion by more than 50%. These findings suggest critical features that should be considered when developing surfaces for biomedical purposes.

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References

  1. 1.

    J.W. Costerton, P.S. Stewart, and E.P. Greenberg: Bacterial biofilms: a common cause of persistent infections. Science 284, 1318 (1999).

    CAS  Article  Google Scholar 

  2. 2.

    S. Miquel, R. Lagrafeuille, B. Souweine, and C. Forestier: Anti-biofilm activity as a health issue. Front Microbiol. 7, 592 (2016).

    Article  Google Scholar 

  3. 3.

    W.E. Stamm and S.R. Norrby: Urinary tract infections: disease panorama and challenges. J. Infect. Dis. 183, S1 (2001).

    Article  Google Scholar 

  4. 4.

    H. Koseoglu, G. Aslan, N. Esen, B.H. Sen, and H. Coban: Ultrastructural stages of biofilm development of Escherichia coli on urethral catheters and effects of antibiotics on biofilm formation. Urology 68, 942 (2006).

    Article  Google Scholar 

  5. 5.

    W.E. Stamm and T.M. Hooton: Management of urinary tract infections in adults. N. Engl. J. Med. 329, 1328 (1993).

    CAS  Article  Google Scholar 

  6. 6.

    T. Shunmugaperumal: Biofilm eradication and prevention: a pharmaceutical approach to medical device infections (John Wiley & Sons, New Jersey, 2010).

    Google Scholar 

  7. 7.

    S. Nir and M. Reches: Bio-inspired antifouling approaches: the quest towards non-toxic and non-biocidal materials. Curr. Opin. Biotechnol. 39, 48 (2016).

    CAS  Article  Google Scholar 

  8. 8.

    C.M. Kirschner and A.B. Brennan: Bio-inspired antifouling strategies. Annu. Rev. Mater. Res. 42, 211 (2012).

    CAS  Article  Google Scholar 

  9. 9.

    I. Banerjee, R.C. Pangule, and R.S. Kane: Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv. Mater. 23, 690 (2011).

    CAS  Article  Google Scholar 

  10. 10.

    B. Li, and B.E. Logan: Bacterial adhesion to glass and metal-oxide surfaces. Colloids Surf. B 36, 81 (2004).

    CAS  Article  Google Scholar 

  11. 11.

    Y.H. An, and R.J. Friedman: Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J. Biomed. Mater. Res. Part A 43, 338 (1998).

    CAS  Article  Google Scholar 

  12. 12.

    J.M. Moreira, M. Simões, L.F. Melo, and F.J. Mergulhão: Escherichia coli adhesion to surfaces-a thermodynamic assessment. Colloid Polym. Sci. 293, 177 (2015).

    CAS  Article  Google Scholar 

  13. 13.

    R.G. Nuzzo: Biomaterials: stable antifouling surfaces. Nat. Mater. 2, 207 (2003).

    CAS  Article  Google Scholar 

  14. 14.

    S. Maity, S. Nir, T. Zada, and M. Reches: Self-assembly of a tripeptide into a functional coating that resists fouling. Chem. Comm. 50, 11154 (2014).

    CAS  Article  Google Scholar 

  15. 15.

    J. Azeredo, N.F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A.R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, and Z. Jaglic: Critical review on biofilm methods. Crit. Rev. Microbiol. 43, 313 (2017).

    CAS  Article  Google Scholar 

  16. 16.

    D.R. Absolom, F.V. Lamberti, Z. Policova, W. Zingg, C.J. van Oss, and A.W. Neumann: Surface thermodynamics of bacterial adhesion. Appl. Environ. Microbiol. 46, 90 (1983).

    CAS  Article  Google Scholar 

  17. 17.

    C. Liu and Q. Zhao: Influence of surface-energy components of Ni-P-TiO2-PTFE nanocomposite coatings on bacterial adhesion. Langmuir 27, 9512 (2011).

    CAS  Article  Google Scholar 

  18. 18.

    L.C. Gomes, L.N. Silva, M. Simoes, L.F. Melo, and F.J. Mergulhao: Escherichia coli adhesion, biofilm development and antibiotic susceptibility on biomedical materials. J. Biomed. Mater. Res. Part A 103, 1414 (2015).

    CAS  Article  Google Scholar 

  19. 19.

    L. Gomes, J. Moreira, J. Teodósio, J. Araújo, J. Miranda, M. Simões, L. Melo, and F. Mergulhão: 96-well microtiter plates for biofouling simulation in biomedical settings. Biofouling 30, 535 (2014).

    CAS  Article  Google Scholar 

  20. 20.

    Y.L. Ong, A. Razatos, G. Georgiou, and M.M. Sharma: Adhesion Forces between E. coli bacteria and biomaterial surfaces. Langmuir 15, 2719 (1999).

    CAS  Article  Google Scholar 

  21. 21.

    A.M. Gallardo-Moreno, M.L. Navarro-Pérez, V. Vadillo-Rodríguez, J.M. Bruque, and M.L. González-Martín: Insights into bacterial contact angles: difficulties in defining hydrophobicity and surface Gibbs energy. Colloids Surf. B 88, 373 (2011).

    CAS  Article  Google Scholar 

  22. 22.

    R. Baier, A. Meyer, J. Natiella, R. Natiella, and J. Carter: Surface properties determine bioadhesive outcomes: methods and results. J. Biomed. Mater. Res. Part A 18, 337 (1984).

    CAS  Article  Google Scholar 

  23. 23.

    J. Moreira, J. Araújo, J.M. Miranda, M. Simões, L. Melo, and F. Mergulhão: The effects of surface properties on Escherichia coli adhesion are modulated by shear stress. Colloids Surf. B 123, 1 (2014).

    CAS  Article  Google Scholar 

  24. 24.

    H.J. Busscher and H.C. van der Mei: Microbial adhesion in flow displacement systems. Clin. Microbiol. Rev. 19, 127 (2006).

    Article  Google Scholar 

  25. 25.

    D. Bakker, A. Van der Plaats, G. Verkerke, H. Busscher, and H. Van der Mei: Comparison of velocity profiles for different flow chamber designs used in studies of microbial adhesion to surfaces. Appl. Environ. Microbiol. 69, 6280 (2003).

    CAS  Article  Google Scholar 

  26. 26.

    M.M. Velraeds, H.C. Van Der Mei, G. Reid, and H.J. Busscher: Inhibition of initial adhesion of uropathogenic Enterococcus faecalis to solid substrata by an adsorbed biosurfactant layer from Lactobacillus acidophilus. Urology 49, 790 (1997).

    CAS  Article  Google Scholar 

  27. 27.

    N.H. Hwang, V.T. Turitto, and M.R. Yen: Advances in cardiovascular engineering (Springer Science & Business Media, New York, 2013).

    Google Scholar 

  28. 28.

    W. Inauen, H.R. Baumgartner, T. Bombeli, A. Haeberli, and P.W. Straub: Dose-and shear rate-dependent effects of heparin on thrombogenesis induced by rabbit aorta subendothelium exposed to flowing human blood. Arterioscler. Thromb. Vasc. Biol. 10, 607 (1990).

    CAS  Google Scholar 

  29. 29.

    K.A. Marx: Quartz crystal microbalance: a useful tool for studying thin polymer films and complex biomolecular systems at the solution − surface interface. Biomacromolecules 4, 1099 (2003).

    CAS  Article  Google Scholar 

  30. 30.

    H.G. Tompkins and W.A. McGahan: Spectroscopic Ellipsometry and Reflectometry: A User’s Guide (Wiley, New York, 1999).

    Google Scholar 

  31. 31.

    J. Moreira, J. Ponmozhi, J. Campos, J.M. Miranda, and F. Mergulhão: Micro-and macro-flow systems to study Escherichia coli adhesion to biomedical materials. Chem. Eng. Sci. 126, 440 (2015).

    CAS  Article  Google Scholar 

  32. 32.

    J. Teodósio, M. Simões, L. Melo, and F. Mergulhão: Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 27, 1 (2011).

    Article  CAS  Google Scholar 

  33. 33.

    J. Teodósio, M. Simões, and F. Mergulhão: The influence of nonconjugative Escherichia coli plasmids on biofilm formation and resistance. J. Appl. Microbiol. 113, 373 (2012).

    Article  CAS  Google Scholar 

  34. 34.

    F.C. Neidhardt: Motility and chemotaxis. In Escherichia coli and Salmonella Typhimurium: Cellular and Molecular biology (ASM Press, Washington, DC, 1987), p. 732.

    Google Scholar 

  35. 35.

    J. Moreira, R. Fulgêncio, P. Alves, I. Machado, I. Bialuch, L. Melo, M. Simões, and F. Mergulhão: Evaluation of SICAN performance for biofouling mitigation in the food industry. Food Control 62, 201 (2016).

    CAS  Article  Google Scholar 

  36. 36.

    J. Moreira, L. Gomes, M. Simões, L. Melo, and F. Mergulhão: The impact of material properties, nutrient load and shear stress on biofouling in food industries. Food Bioprod. Process. 95, 228 (2015).

    Article  Google Scholar 

  37. 37.

    J. Frias, F. Ribas, and F. Lucena: Effects of different nutrients on bacterial growth in a pilot distribution system. Antonie Van Leeuwenhoek 80, 129 (2001).

    CAS  Article  Google Scholar 

  38. 38.

    C. Van Oss: Hydrophobicity of biosurfaces—origin, quantitative determination and interaction energies. Colloids Surf. B 5, 91 (1995).

    Article  Google Scholar 

  39. 39.

    C.J. Van Oss, R.J. Good, and M.K. Chaudhury: Additive and nonadditive surface tension components and the interpretation of contact angles. Langmuir 4, 884 (1988).

    Article  Google Scholar 

  40. 40.

    B. Janczuk, E. Chibowski, J. Bruque, M. Kerkeb, and F.G. Caballero: On the consistency of surface free energy components as calculated from contact angles of different liquids: an application to the cholesterol surface. J. Colloid Interface Sci. 159, 421 (1993).

    CAS  Article  Google Scholar 

  41. 41.

    C.J. Van Oss: Interfacial Forces in Aqueous Media (CRC press, New York, 2006).

    Google Scholar 

  42. 42.

    M.I. Ojovan: Glass formation in amorphous SiO2 as a percolation phase transition in a system of network defects. J. Exp. Theor. Phys. 79, 632 (2004).

    CAS  Article  Google Scholar 

  43. 43.

    J.S. Teodósio, F.C. Silva, J.M. Moreira, M. Simões, L.F. Melo, M.A. Alves, and F.J. Mergulhão: Flow cells as quasi-ideal systems for biofouling simulation of industrial piping systems. Biofouling 29, 953 (2013).

    Article  Google Scholar 

  44. 44.

    M. Fletcher and G. Loeb: Influence of substratum characteristics on the attachment of a marine pseudomonad to solid surfaces. Appl. Environ. Microbiol. 37, 67 (1979).

    CAS  Article  Google Scholar 

  45. 45.

    N. Cerca, G.B. Pier, M. Vilanova, R. Oliveira, and J. Azeredo: Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res. Microbiol. 156, 506 (2005).

    CAS  Article  Google Scholar 

  46. 46.

    K. Oliveira, T. Oliveira, P. Teixeira, J. Azeredo, M. Henriques, and R. Oliveira: Comparison of the adhesion ability of different Salmonella enteritidis serotypes to materials used in kitchens. J. Food Protect 69, 2352 (2006).

    Article  Google Scholar 

  47. 47.

    R. Bos, H.C. Van der Mei, and H.J. Busscher: Physico-chemistry of initial microbial adhesive interactions-its mechanisms and methods for study. FEMS Microbiol. Rev. 23, 179 (1999).

    CAS  Article  Google Scholar 

  48. 48.

    M.V. Graham, A.P. Mosier, T.R. Kiehl, A.E. Kaloyeros, and N.C. Cady: Development of antifouling surfaces to reduce bacterial attachment. Soft Matter 9, 6235 (2013).

    CAS  Article  Google Scholar 

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Acknowledgments

This work was supported by project NORTE-01-0145-FEDER-000005–LEPABE-2-ECO-INNOVATION from NORTE 2020, under the Portugal 2020 Partnership Agreement, through the European Regional Development Fund (ERDF) and by the Rosetrees Trust. Patricia Alves acknowledges the receipt of a Ph.D. grant from the Portuguese Foundation from Science and Technology (FCT) (PD/BD/114317/2016). Sivan Nir acknowledges the support of the Israeli Water Authority. The authors also acknowledge support from the EU COST Action iPROMEDAI TD1305.

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Correspondence to Meital Reches or Filipe Mergulhão.

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Supplementary material

The supplementary material for this article can be found at {rs|https://doi.org/10.1557/mrc.2018.160|url|}.

Authors’ contributions

Reches M and Mergulhao F conceptualized and designed the study. Alves P performed all the adhesion assays and the surface hydrophobicity analysis. Nir S characterized the peptide coating and surface. All authors contributed to the data interpretation. All the authors reviewed the manuscript and approved the final manuscript.

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Alves, P., Nir, S., Reches, M. et al. The effects of fluid composition and shear conditions on bacterial adhesion to an antifouling peptide-coated surface. MRS Communications 8, 938–946 (2018). https://doi.org/10.1557/mrc.2018.160

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