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.
Similar content being viewed by others
References
J.W. Costerton, P.S. Stewart, and E.P. Greenberg: Bacterial biofilms: a common cause of persistent infections. Science 284, 1318 (1999).
S. Miquel, R. Lagrafeuille, B. Souweine, and C. Forestier: Anti-biofilm activity as a health issue. Front Microbiol. 7, 592 (2016).
W.E. Stamm and S.R. Norrby: Urinary tract infections: disease panorama and challenges. J. Infect. Dis. 183, S1 (2001).
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).
W.E. Stamm and T.M. Hooton: Management of urinary tract infections in adults. N. Engl. J. Med. 329, 1328 (1993).
T. Shunmugaperumal: Biofilm eradication and prevention: a pharmaceutical approach to medical device infections (John Wiley & Sons, New Jersey, 2010).
S. Nir and M. Reches: Bio-inspired antifouling approaches: the quest towards non-toxic and non-biocidal materials. Curr. Opin. Biotechnol. 39, 48 (2016).
C.M. Kirschner and A.B. Brennan: Bio-inspired antifouling strategies. Annu. Rev. Mater. Res. 42, 211 (2012).
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).
B. Li, and B.E. Logan: Bacterial adhesion to glass and metal-oxide surfaces. Colloids Surf. B 36, 81 (2004).
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).
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).
R.G. Nuzzo: Biomaterials: stable antifouling surfaces. Nat. Mater. 2, 207 (2003).
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).
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).
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).
C. Liu and Q. Zhao: Influence of surface-energy components of Ni-P-TiO2-PTFE nanocomposite coatings on bacterial adhesion. Langmuir 27, 9512 (2011).
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).
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).
Y.L. Ong, A. Razatos, G. Georgiou, and M.M. Sharma: Adhesion Forces between E. coli bacteria and biomaterial surfaces. Langmuir 15, 2719 (1999).
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).
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).
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).
H.J. Busscher and H.C. van der Mei: Microbial adhesion in flow displacement systems. Clin. Microbiol. Rev. 19, 127 (2006).
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).
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).
N.H. Hwang, V.T. Turitto, and M.R. Yen: Advances in cardiovascular engineering (Springer Science & Business Media, New York, 2013).
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).
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).
H.G. Tompkins and W.A. McGahan: Spectroscopic Ellipsometry and Reflectometry: A User’s Guide (Wiley, New York, 1999).
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).
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).
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).
F.C. Neidhardt: Motility and chemotaxis. In Escherichia coli and Salmonella Typhimurium: Cellular and Molecular biology (ASM Press, Washington, DC, 1987), p. 732.
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).
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).
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).
C. Van Oss: Hydrophobicity of biosurfaces—origin, quantitative determination and interaction energies. Colloids Surf. B 5, 91 (1995).
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).
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).
C.J. Van Oss: Interfacial Forces in Aqueous Media (CRC press, New York, 2006).
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).
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).
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).
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).
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).
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).
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).
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.
Author information
Authors and Affiliations
Corresponding authors
Appendices
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.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1557/mrc.2018.160