Subtle Variations in Surface Properties of Black Silicon Surfaces Influence the Degree of Bactericidal Efficiency
Corresponding Author: Elena P. Ivanova
Nano-Micro Letters,
Vol. 10 No. 2 (2018), Article Number: 36
Abstract
One of the major challenges faced by the biomedical industry is the development of robust synthetic surfaces that can resist bacterial colonization. Much inspiration has been drawn recently from naturally occurring mechano-bactericidal surfaces such as the wings of cicada (Psaltoda claripennis) and dragonfly (Diplacodes bipunctata) species in fabricating their synthetic analogs. However, the bactericidal activity of nanostructured surfaces is observed in a particular range of parameters reflecting the geometry of nanostructures and surface wettability. Here, several of the nanometer-scale characteristics of black silicon (bSi) surfaces including the density and height of the nanopillars that have the potential to influence the bactericidal efficiency of these nanostructured surfaces have been investigated. The results provide important evidence that minor variations in the nanoarchitecture of substrata can substantially alter their performance as bactericidal surfaces.
Highlights:
1 Three types of black silicon (bSi) surface were successfully fabricated using deep reactive ion etching with pillar heights (652.7–1063.2 nm) and density (8–11 tips per µm2).
2 Less bactericidal bSi surfaces were found to contain nanopillars of heights reaching 1000 nm that were not always well separated, lower pillar density (8 tips per µm2), and aspect ratios of 8.8.
Keywords
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- E.P. Ivanova, J. Hasan, H.K. Webb, G. Gervinskas, S. Juodkazis et al., Bactericidal activity of black silicon. Nat. Commun. 4, 2838 (2013). https://doi.org/10.1038/ncomms3838
- D.E. Mainwaring, S.H. Nguyen, H. Webb, T. Jakubov, M. Tobin et al., The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale 8(12), 6527–6534 (2016). https://doi.org/10.1039/C5NR08542J
- S. Kelleher, O. Habimana, J. Lawler, B. O’Reilly, S. Daniels, E. Casey, A. Cowley, Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl. Mater. Interfaces 8(24), 14966–14974 (2016). https://doi.org/10.1021/acsami.5b08309
- A. Elbourne, R.J. Crawford, E.P. Ivanova, Nano-structured antimicrobial surfaces: from nature to synthetic analogues. J. Colloid Interface Sci. 508, 603–616 (2017). https://doi.org/10.1016/j.jcis.2017.07.021
- E.P. Ivanova, J. Hasan, H.K. Webb, V.K. Truong, G.S. Watson et al., Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. Small 8(16), 2489–2494 (2012). https://doi.org/10.1002/smll.201200528
- S. Pogodin, J. Hasan, V.A. Baulin, H.K. Webb, V.K. Truong et al., Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys. J. 104(4), 835–840 (2013). https://doi.org/10.1016/j.bpj.2012.12.046
- C.M. Bhadra, V. Khanh Truong, V.T.H. Pham, M. Al Kobaisi, G. Seniutinas, J.Y. Wang, S. Juodkazis, R.J. Crawford, E.P. Ivanova, Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci. Rep. 5, 16817 (2015). https://doi.org/10.1038/srep16817
- Y.Q. Li, B. Zhu, Y. Li, W.R. Leow, R. Goh, B. Ma, E. Fong, M. Tang, X. Chen, A synergistic capture strategy for enhanced detection and elimination of bacteria. Angew. Chem. Int. Ed. 53(23), 5837–5841 (2014). https://doi.org/10.1002/anie.201310135
- T. Diu, N. Faruqui, T. Sjöström, B. Lamarre, H.F. Jenkinson, B. Su, M.G. Ryadnov, Cicada-inspired cell-instructive nanopatterned arrays. Sci. Rep. 4, 7122 (2014). https://doi.org/10.1038/srep07122
- P.K. Sahoo, R. Janissen, M.P. Monteiro, A. Cavalli, D.M. Murillo et al., Nanowire arrays as cell force sensors to investigate adhesin-enhanced holdfast of single cell bacteria and biofilm stability. Nano Lett. 16(7), 4656–4664 (2016). https://doi.org/10.1021/acs.nanolett.6b01998
- M.N. Dickson, E.I. Liang, L.A. Rodriguez, N. Vollereaux, A.F. Yee, Nanopatterned polymer surfaces with bactericidal properties. Biointerphases 10(2), 021010 (2015). https://doi.org/10.1116/1.4922157
- L.E. Fisher, Y. Yang, M.F. Yuen, W. Zhang, A.H. Nobbs, B. Su, Bactericidal activity of biomimetic diamond nanocone surfaces. Biointerphases 11(1), 011014 (2016). https://doi.org/10.1116/1.4944062
- D.P. Linklater, H.K.D. Nguyen, C.M. Bhadra, S. Juodkazis, E.P. Ivanova, Influence of nanoscale topology on bactericidal efficiency of black silicon surfaces. Nanotechnology 28(24), 245301 (2017). https://doi.org/10.1088/1361-6528/aa700e
- E.P. Ivanova, S.H. Nguyen, Y. Guo, V.A. Baulin, H.K. Webb et al., Bactericidal activity of self-assembled palmitic and stearic fatty acid crystals on highly ordered pyrolytic graphite. Acta Biomater. 59, 148–157 (2017). https://doi.org/10.1016/j.actbio.2017.07.004
- K. Nowlin, A. Boseman, A. Covell, D. LaJeunesse, Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces. J. R. Soc. Interface 12(102), 20140999 (2015). https://doi.org/10.1098/rsif.2014.0999
- X. Li, Bactericidal mechanism of nanopatterned surfaces. Phys. Chem. Chem. Phys. 18(2), 1311–1316 (2016). https://doi.org/10.1039/c5cp05646b
- X. Liu, P.R. Coxon, M. Peters, B. Hoex, J.M. Cole, D.J. Fray, Black silicon: fabrication methods, properties and solar energy applications. Energy Environ. Sci. 7(10), 3223–3263 (2014). https://doi.org/10.1039/c4ee01152j
- P. Zhang, S. Li, C. Liu, X. Wei, Z. Wu, Y. Jiang, Z. Chen, Near-infrared optical absorption enhanced in black silicon via Ag nanoparticle-induced localized surface plasmon. Nanoscale Res. Lett. 9(1), 519 (2014). https://doi.org/10.1186/1556-276X-9-519
- H. Jansen, M. De Boer, R. Legtenberg, M. Elwenspoek, The black silicon method: a universal method for determining the parameter setting of a fluorine-based reactive ion etcher in deep silicon trench etching with profile control. J. Micromech. Microeng. 5(2), 115–120 (1995). https://doi.org/10.1088/0960-1317/5/2/015
- L.L. Ma, Y.C. Zhou, N. Jiang, X. Lu, J. Shao, W. Lu, J. Ge, X.M. Ding, X.Y. Hou, Wide-band “black silicon” based on porous silicon. Appl. Phys. Lett. 88(17), 171907 (2006). https://doi.org/10.1063/1.2199593
- A. Žukauskas, M. Malinauskas, A. Kadys, G. Gervinskas, G. Seniutinas, S. Kandasamy, S. Juodkazis, Black silicon: substrate for laser 3D micro/nano-polymerization. Opt. Express 21(6), 6901–6909 (2013). https://doi.org/10.1364/OE.21.006901
- V.K. Truong, R. Lapovok, Y.S. Estrin, S. Rundell, J.Y. Wang, C.J. Fluke, R.J. Crawford, E.P. Ivanova, The influence of nanoscale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31(13), 3674–3683 (2010). https://doi.org/10.1016/j.biomaterials.2010.01.071
- Z. Yoshimitsu, A. Nakajima, T. Watanabe, K. Hashimoto, Effects of surface structure on the hydrophobicity and sliding behavior of water droplets. Langmuir 18(15), 5818–5822 (2002). https://doi.org/10.1021/la020088p
- A.K. Epstein, A.I. Hochbaum, P. Kim, J. Aizenberg, Control of bacterial biofilm growth on surfaces by nanostructural mechanics and geometry. Nanotechnology 22(49), 494007 (2011). https://doi.org/10.1088/0957-4484/22/49/494007
- S. Sasaoka, K. Saito, K. Higashi, W. Limwikrant, K. Moribe, S. Suzuki, K. Yamamoto, Design of one-dimensional power spectrum using two-dimensional fast Fourier transform for discrimination of paper-based kraft tapes. Forensic Sci. Int. 257, 329–336 (2015). https://doi.org/10.1016/j.forsciint.2015.09.016
- Q. Zheng, B.K. Milthorpe, A.S. Jones, Direct neural network application for automated cell recognition. Cytom. Part A 57(1), 1–9 (2004). https://doi.org/10.1002/cyto.a.10106
- D. Campoccia, L. Montanaro, C.R. Arciola, The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27(11), 2331–2339 (2006). https://doi.org/10.1016/j.biomaterials.2005.11.044
- L. Boulos, M. Prévost, B. Barbeau, J. Coallier, R. Desjardins, LIVE/DEAD® BacLight™: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37(1), 77–86 (1999). https://doi.org/10.1016/S0167-7012(99)00048-2
- J.R. Postgate, Chapter XVIII viable counts and viability. Methods Microbiol. 1, 611–628 (1969). https://doi.org/10.1016/S0580-9517(08)70149-1
References
E.P. Ivanova, J. Hasan, H.K. Webb, G. Gervinskas, S. Juodkazis et al., Bactericidal activity of black silicon. Nat. Commun. 4, 2838 (2013). https://doi.org/10.1038/ncomms3838
D.E. Mainwaring, S.H. Nguyen, H. Webb, T. Jakubov, M. Tobin et al., The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale 8(12), 6527–6534 (2016). https://doi.org/10.1039/C5NR08542J
S. Kelleher, O. Habimana, J. Lawler, B. O’Reilly, S. Daniels, E. Casey, A. Cowley, Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl. Mater. Interfaces 8(24), 14966–14974 (2016). https://doi.org/10.1021/acsami.5b08309
A. Elbourne, R.J. Crawford, E.P. Ivanova, Nano-structured antimicrobial surfaces: from nature to synthetic analogues. J. Colloid Interface Sci. 508, 603–616 (2017). https://doi.org/10.1016/j.jcis.2017.07.021
E.P. Ivanova, J. Hasan, H.K. Webb, V.K. Truong, G.S. Watson et al., Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. Small 8(16), 2489–2494 (2012). https://doi.org/10.1002/smll.201200528
S. Pogodin, J. Hasan, V.A. Baulin, H.K. Webb, V.K. Truong et al., Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys. J. 104(4), 835–840 (2013). https://doi.org/10.1016/j.bpj.2012.12.046
C.M. Bhadra, V. Khanh Truong, V.T.H. Pham, M. Al Kobaisi, G. Seniutinas, J.Y. Wang, S. Juodkazis, R.J. Crawford, E.P. Ivanova, Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci. Rep. 5, 16817 (2015). https://doi.org/10.1038/srep16817
Y.Q. Li, B. Zhu, Y. Li, W.R. Leow, R. Goh, B. Ma, E. Fong, M. Tang, X. Chen, A synergistic capture strategy for enhanced detection and elimination of bacteria. Angew. Chem. Int. Ed. 53(23), 5837–5841 (2014). https://doi.org/10.1002/anie.201310135
T. Diu, N. Faruqui, T. Sjöström, B. Lamarre, H.F. Jenkinson, B. Su, M.G. Ryadnov, Cicada-inspired cell-instructive nanopatterned arrays. Sci. Rep. 4, 7122 (2014). https://doi.org/10.1038/srep07122
P.K. Sahoo, R. Janissen, M.P. Monteiro, A. Cavalli, D.M. Murillo et al., Nanowire arrays as cell force sensors to investigate adhesin-enhanced holdfast of single cell bacteria and biofilm stability. Nano Lett. 16(7), 4656–4664 (2016). https://doi.org/10.1021/acs.nanolett.6b01998
M.N. Dickson, E.I. Liang, L.A. Rodriguez, N. Vollereaux, A.F. Yee, Nanopatterned polymer surfaces with bactericidal properties. Biointerphases 10(2), 021010 (2015). https://doi.org/10.1116/1.4922157
L.E. Fisher, Y. Yang, M.F. Yuen, W. Zhang, A.H. Nobbs, B. Su, Bactericidal activity of biomimetic diamond nanocone surfaces. Biointerphases 11(1), 011014 (2016). https://doi.org/10.1116/1.4944062
D.P. Linklater, H.K.D. Nguyen, C.M. Bhadra, S. Juodkazis, E.P. Ivanova, Influence of nanoscale topology on bactericidal efficiency of black silicon surfaces. Nanotechnology 28(24), 245301 (2017). https://doi.org/10.1088/1361-6528/aa700e
E.P. Ivanova, S.H. Nguyen, Y. Guo, V.A. Baulin, H.K. Webb et al., Bactericidal activity of self-assembled palmitic and stearic fatty acid crystals on highly ordered pyrolytic graphite. Acta Biomater. 59, 148–157 (2017). https://doi.org/10.1016/j.actbio.2017.07.004
K. Nowlin, A. Boseman, A. Covell, D. LaJeunesse, Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces. J. R. Soc. Interface 12(102), 20140999 (2015). https://doi.org/10.1098/rsif.2014.0999
X. Li, Bactericidal mechanism of nanopatterned surfaces. Phys. Chem. Chem. Phys. 18(2), 1311–1316 (2016). https://doi.org/10.1039/c5cp05646b
X. Liu, P.R. Coxon, M. Peters, B. Hoex, J.M. Cole, D.J. Fray, Black silicon: fabrication methods, properties and solar energy applications. Energy Environ. Sci. 7(10), 3223–3263 (2014). https://doi.org/10.1039/c4ee01152j
P. Zhang, S. Li, C. Liu, X. Wei, Z. Wu, Y. Jiang, Z. Chen, Near-infrared optical absorption enhanced in black silicon via Ag nanoparticle-induced localized surface plasmon. Nanoscale Res. Lett. 9(1), 519 (2014). https://doi.org/10.1186/1556-276X-9-519
H. Jansen, M. De Boer, R. Legtenberg, M. Elwenspoek, The black silicon method: a universal method for determining the parameter setting of a fluorine-based reactive ion etcher in deep silicon trench etching with profile control. J. Micromech. Microeng. 5(2), 115–120 (1995). https://doi.org/10.1088/0960-1317/5/2/015
L.L. Ma, Y.C. Zhou, N. Jiang, X. Lu, J. Shao, W. Lu, J. Ge, X.M. Ding, X.Y. Hou, Wide-band “black silicon” based on porous silicon. Appl. Phys. Lett. 88(17), 171907 (2006). https://doi.org/10.1063/1.2199593
A. Žukauskas, M. Malinauskas, A. Kadys, G. Gervinskas, G. Seniutinas, S. Kandasamy, S. Juodkazis, Black silicon: substrate for laser 3D micro/nano-polymerization. Opt. Express 21(6), 6901–6909 (2013). https://doi.org/10.1364/OE.21.006901
V.K. Truong, R. Lapovok, Y.S. Estrin, S. Rundell, J.Y. Wang, C.J. Fluke, R.J. Crawford, E.P. Ivanova, The influence of nanoscale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31(13), 3674–3683 (2010). https://doi.org/10.1016/j.biomaterials.2010.01.071
Z. Yoshimitsu, A. Nakajima, T. Watanabe, K. Hashimoto, Effects of surface structure on the hydrophobicity and sliding behavior of water droplets. Langmuir 18(15), 5818–5822 (2002). https://doi.org/10.1021/la020088p
A.K. Epstein, A.I. Hochbaum, P. Kim, J. Aizenberg, Control of bacterial biofilm growth on surfaces by nanostructural mechanics and geometry. Nanotechnology 22(49), 494007 (2011). https://doi.org/10.1088/0957-4484/22/49/494007
S. Sasaoka, K. Saito, K. Higashi, W. Limwikrant, K. Moribe, S. Suzuki, K. Yamamoto, Design of one-dimensional power spectrum using two-dimensional fast Fourier transform for discrimination of paper-based kraft tapes. Forensic Sci. Int. 257, 329–336 (2015). https://doi.org/10.1016/j.forsciint.2015.09.016
Q. Zheng, B.K. Milthorpe, A.S. Jones, Direct neural network application for automated cell recognition. Cytom. Part A 57(1), 1–9 (2004). https://doi.org/10.1002/cyto.a.10106
D. Campoccia, L. Montanaro, C.R. Arciola, The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27(11), 2331–2339 (2006). https://doi.org/10.1016/j.biomaterials.2005.11.044
L. Boulos, M. Prévost, B. Barbeau, J. Coallier, R. Desjardins, LIVE/DEAD® BacLight™: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37(1), 77–86 (1999). https://doi.org/10.1016/S0167-7012(99)00048-2
J.R. Postgate, Chapter XVIII viable counts and viability. Methods Microbiol. 1, 611–628 (1969). https://doi.org/10.1016/S0580-9517(08)70149-1