Advertisement

Engineering Approaches to Create Antibacterial Surfaces on Biomedical Implants and Devices

  • Ruwen Tan
  • Jin Yoo
  • Yeongseon JangEmail author
Chapter

Abstract

Bacterial adhesion and biofilm formation on biomedical surfaces remain the annoying problems in global public health, causing severe infectious diseases and increasing health care costs. Moreover, the continued increase in the number of multidrug-resistant bacteria and their fast evolution induce a serious concern with the lack of development of new antimicrobials. These problems have initiated numerous research efforts to develop more effective antimicrobial surfaces through different engineering approaches to prohibit bacterial adhesion and subsequent biofilm formation. In this review, we summarize the engineering technologies for constructing antibacterial surfaces from the conventional to the cutting-edge strategies. Most of the traditional methods are based on the antifouling coatings and the release of toxic biocides from the chemically modified substrates. Antimicrobial nanoparticles can actively inhibit biofilm formation or other essential processes in the drug resistance mechanisms of bacteria. Thus, the combined use of bactericidal nanoparticles and antifouling polymers for functionalized organic–inorganic platforms has been investigated to enhance antibacterial performance. In recent years, unique surface topographies of antibacterial, natural surfaces have been discovered and studied with the increased understanding of the interaction between bacteria and substrates. We introduce various natural surfaces and artificial implantable biomaterials, which present the bactericidal surface topographies, along with their bactericidal mechanisms and efficiency. The use of biomimetic, nanotextured surfaces is a promising approach to overcome the current challenges for the treatment of multidrug-resistant bacteria.

Keywords

Antimicrobial Antifouling Bactericidal Implant Coating Surface engineering Functional surface Nanotechnology Nanostructure 

Notes

Acknowledgments

This work is partially supported by Dr. Jang’s startup funds provided from Department of Chemical Engineering and Herbert Wertheim College of Engineering at the University of Florida. The authors also gratefully acknowledge the helpful comments and suggestions of the reviewers, which have improved the presentation.

References

  1. 1.
    Arsiwala A, Desai P, Patravale V (2014) Recent advances in micro/nanoscale biomedical implants. J Control Release 189:25–45.  https://doi.org/10.1016/j.jconrel.2014.06.021CrossRefPubMedGoogle Scholar
  2. 2.
    Cloutier M, Mantovani D, Rosei F (2015) Antibacterial coatings: challenges, perspectives, and opportunities. Trends Biotechnol 33:637–652.  https://doi.org/10.1016/j.tibtech.2015.09.002CrossRefPubMedGoogle Scholar
  3. 3.
    Tuson HH, Weibel DB (2013) Bacteria-surface interactions. Soft Matter 9:4368–4380.  https://doi.org/10.1039/c3sm27705dCrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Jang Y, Park S, Char K (2011) Functionalization of polymer multilayer thin films for novel biomedical applications. Kor J Chem Eng 28:1149–1160.  https://doi.org/10.1007/s11814-010-0434-xCrossRefGoogle Scholar
  5. 5.
    Son H, Jang Y, Koo J, Lee JS, Theato P, Char K (2016) Penetration and exchange kinetics of primary alkyl amines applied to reactive poly(pentafluorophenyl acrylate) thin films. Polym J 48:487–495.  https://doi.org/10.1038/pj.2016.6CrossRefGoogle Scholar
  6. 6.
    Yoo J, Birke A, Kim J, Jang Y, Song SY, Ryu S, Kim BS, Kim BG, Barz M, Char K (2018) Cooperative catechol-functionalized polypept(o)ide brushes and Ag nanoparticles for combination of protein resistance and antimicrobial activity on metal oxide surfaces. Biomacromolecules 19:1602–1613.  https://doi.org/10.1021/acs.biomac.8b00135CrossRefPubMedGoogle Scholar
  7. 7.
    Xie Y, Tang C, Wang Z, Xu Y, Zhao W, Sun S, Zhao C (2017) Co-deposition towards mussel-inspired antifouling and antibacterial membranes by using zwitterionic polymers and silver nanoparticles. J Mater Chem B 5:7186–7193.  https://doi.org/10.1039/c7tb01516jCrossRefGoogle Scholar
  8. 8.
    Lau KHA, Ren C, Park SH, Szleifer I, Messersmith PB (2012) An experimental-theoretical analysis of protein adsorption on peptidomimetic polymer brushes. Langmuir 28:2288–2298.  https://doi.org/10.1021/la203905gCrossRefPubMedGoogle Scholar
  9. 9.
    Rosu C, Jang Y, Jiang L, Champion J (2018) Nature-Inspired and “Water-Skating” Paper and Polyester Substrates Enabled by the Molecular Structure of Poly(γ-stearyl-α, l-glutamate) Homopolypeptide. Biomacromolecules 19:4617–4628.  https://doi.org/10.1021/acs.biomac.8b01312
  10. 10.
    Chen L, Zeng R, Xiang L, Luo Z, Wang Y (2012) Polydopamine-graft-PEG antifouling coating for quantitative analysis of food proteins by CE. Anal Methods 4:2852–2859.  https://doi.org/10.1039/c2ay25129aCrossRefGoogle Scholar
  11. 11.
    Zhang RN, Liu YN, He MR, Su YL, Zhao XT, Elimelech M, Jiang ZY (2016) Antifouling membranes for sustainable water purification: strategies and mechanisms. Chem Soc Rev 45:5888–5924.  https://doi.org/10.1039/c5cs00579eCrossRefPubMedGoogle Scholar
  12. 12.
    Banerjee I, Pangule RC, Kane RS (2011) Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv Mater 23:690–718.  https://doi.org/10.1002/adma.201001215CrossRefPubMedGoogle Scholar
  13. 13.
    Kingshott P, Thissen H, Griesser HJ (2002) Effects of cloud-point grafting, chain length, and density of PEG layers on competitive adsorption of ocular proteins. Biomaterials 23:2043–2056.  https://doi.org/10.1016/S0142-9612(01)00334-9CrossRefPubMedGoogle Scholar
  14. 14.
    Prime KL, Whitesides GM (1993) Adsorption of proteins onto surfaces containing end-attached oligo(ethylene oxide)—a model system using self-assembled monolayers. J Am Chem Soc 115:10714–10721.  https://doi.org/10.1021/ja00076a032CrossRefGoogle Scholar
  15. 15.
    Roosjen A, van der Mei HC, Busscher HJ, Norde W (2004) Microbial adhesion to poly(ethylene oxide) brushes: influence of polymer chain length and temperature. Langmuir 20:10949–10955.  https://doi.org/10.1021/la0484691CrossRefPubMedGoogle Scholar
  16. 16.
    Lau KHA, Sileika TS, Park SH, Sousa AML, Burch P, Szleifer I, Messersmith PB (2015) Molecular design of antifouling polymer brushes using sequence-specific peptoids. Adv Mater Interfaces 2:1400225.  https://doi.org/10.1002/Admi.201400225CrossRefPubMedGoogle Scholar
  17. 17.
    Lee SJ, Heo DN, Lee HR, Lee D, Yu SJ, Park SA, Ko WK, Park SW, Im SG, Moon JH, Kwon IK (2015) Biofunctionalized titanium with anti-fouling resistance by grafting thermo-responsive polymer brushes for the prevention of peri-implantitis. J Mater Chem B 3:5161–5165.  https://doi.org/10.1039/c5tb00611bCrossRefGoogle Scholar
  18. 18.
    Chelmowski R, Koster SD, Kerstan A, Prekelt A, Grunwald C, Winkler T, Metzler-Nolte N, Terfort A, Woll C (2008) Peptide-based SAMs that resist the adsorption of proteins. J Am Chem Soc 130:14952–14953.  https://doi.org/10.1021/ja8065754CrossRefPubMedGoogle Scholar
  19. 19.
    Le NCH, Gubala V, Gandhiraman RP, Daniels S, Williams DE (2011) Evaluation of different nonspecific binding blocking agents deposited inside poly(methyl methacrylate) microfluidic flow-cells. Langmuir 27:9043–9051.  https://doi.org/10.1021/la2011502CrossRefPubMedGoogle Scholar
  20. 20.
    Chuang HF, Smith RC, Hammond PT (2008) Polyelectrolyte multilayers for tunable release of antibiotics. Biomacromolecules 9:1660–1668.  https://doi.org/10.1021/bm800185hCrossRefPubMedGoogle Scholar
  21. 21.
    Nystrom L, Stromstedt AA, Schmidtchen A, Malmsten M (2018) Peptide-loaded microgels as antimicrobial and anti-inflammatory surface coatings. Biomacromolecules 19:3456–3466.  https://doi.org/10.1021/acs.biomac.8b00776CrossRefPubMedGoogle Scholar
  22. 22.
    Kaur R, Liu S (2016) Antibacterial surface design—contact kill. Prog Surf Sci 91:136–153.  https://doi.org/10.1016/j.progsurf.2016.09.001CrossRefGoogle Scholar
  23. 23.
    Tiller JC, Liao C-J, Lewis K, Klibanov AM (2001) Designing surfaces that kill bacteria on contact. Proc Natl Acad Sci 98:5981–5985.  https://doi.org/10.1073/pnas.111143098CrossRefPubMedGoogle Scholar
  24. 24.
    Tiller JC, Lee SB, Lewis K, Klibanov AM (2002) Polymer surfaces derivatized with poly(vinyl-N-hexylpyridinium) kill airborne and waterborne bacteria. Biotechnol Bioeng 79:465–471.  https://doi.org/10.1002/bit.10299CrossRefPubMedGoogle Scholar
  25. 25.
    Wang J, Vermerris W (2016) Antimicrobial nanomaterials derived from natural products—a review. Materials (Basel) 9:255.  https://doi.org/10.3390/ma9040255CrossRefGoogle Scholar
  26. 26.
    Correia VG, Ferraria AM, Pinho MG, Aguiar-Ricardo A (2015) Antimicrobial contact-active oligo(2-oxazoline)s-grafted surfaces for fast water disinfection at the point-of-use. Biomacromolecules 16:3904–3915.  https://doi.org/10.1021/acs.biomac.5b01243CrossRefPubMedGoogle Scholar
  27. 27.
    Rabea EI, Badawy MET, Stevens CV, Smagghe G, Steurbaut W (2003) Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457–1465.  https://doi.org/10.1021/bm034130mCrossRefPubMedGoogle Scholar
  28. 28.
    Ohkawa K, Minato KI, Kumagai G, Hayashi S, Yamamoto H (2006) Chitosan nanofiber. Biomacromolecules 7:3291–3294.  https://doi.org/10.1021/bm0604395CrossRefPubMedGoogle Scholar
  29. 29.
    Elsabee MZ, Naguib HF, Morsi RE (2012) Chitosan based nanofibers, review. Mater Sci Eng C 32:1711–1726.  https://doi.org/10.1016/j.msec.2012.05.009CrossRefGoogle Scholar
  30. 30.
    Torres-Giner S, Ocio MJ, Lagaron JM (2008) Development of active antimicrobial fiber based chitosan polysaccharide nanostructures using electrospinning. Eng Life Sci 8:303–314.  https://doi.org/10.1002/elsc.200700066CrossRefGoogle Scholar
  31. 31.
    Fernandes SCM, Sadocco P, Alonso-Varona A, Palomares T, Eceiza A, Silvestre AJD, Aki Mondragon I, Freire CSR (2013) Bioinspired antimicrobial and biocompatible bacterial cellulose membranes obtained by surface functionalization with aminoalkyl groups. ACS Appl Mater Interfaces 5:3290–3297.  https://doi.org/10.1021/am400338nCrossRefPubMedGoogle Scholar
  32. 32.
    Roemhild K, Wiegand C, Hipler U, Heinze T (2013) Novel bioactive amino-functionalized cellulose nanofibers. Macromol Rapid Commun 34:1767–1771.  https://doi.org/10.1002/marc.201300588CrossRefPubMedGoogle Scholar
  33. 33.
    Roy D, Knapp JS, Guthrie JT, Perrier S (2008) Antibacterial cellulose fiber via RAFT surface graft polymerization. Biomacromolecules 9:91–99.  https://doi.org/10.1021/bm700849jCrossRefPubMedGoogle Scholar
  34. 34.
    Heunis T, Bshena O, Klumperman B, Dicks L (2011) Release of bacteriocins from nanofibers prepared with combinations of poly(D,L-lactide) (PDLLA) and poly(ethylene oxide) (PEO). Int J Mol Sci 12:2158–2173.  https://doi.org/10.3390/ijms12042158CrossRefPubMedGoogle Scholar
  35. 35.
    Viana JFC, Carrijo J, Freitas CG, Paul A, Alcaraz J, Lacorte CC, Migliolo L, Andrade CA, Falcão R, Santos NC, Gonçalves S, Otero-González AJ, Khademhosseini A, Dias SC, Franco OL (2015) Antifungal nanofibers made by controlled release of sea animal derived peptide. Nanoscale 7:6238–6246.  https://doi.org/10.1039/c5nr00767dCrossRefPubMedGoogle Scholar
  36. 36.
    Gatti JW, Smithgall MC, Paranjape SM, Rolfes RJ, Paranjape M (2013) Using electrospun poly(ethylene-oxide) nanofibers for improved retention and efficacy of bacteriolytic antibiotics. Biomed Microdevices 15:887–893.  https://doi.org/10.1007/s10544-013-9777-5CrossRefPubMedGoogle Scholar
  37. 37.
    Baptista PV, McCusker MP, Carvalho A, Ferreira DA, Mohan NM, Martins M, Fernandes AR (2018) Nano-strategies to fight multidrug resistant bacteria—“A Battle of the Titans”. Front Microbiol 9:1441.  https://doi.org/10.3389/fmicb.2018.01441CrossRefPubMedGoogle Scholar
  38. 38.
    Wang L, Hu C, Shoa L (2017) The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomed 12:1227–1249.  https://doi.org/10.2147/IJN.S121956CrossRefGoogle Scholar
  39. 39.
    Le Ouay B, Stellacci F (2015) Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10:339–354.  https://doi.org/10.1016/j.nantod.2015.04.002CrossRefGoogle Scholar
  40. 40.
    Ramalingam B, Parandhaman T, Das SK (2016) Antibacterial effects of biosynthesized silver nanoparticles on surface ultrastructure and nanomechanical properties of gram-negative bacteria viz Escherichia coli and Pseudomonas aeruginosa. ACS Appl Mater Interfaces 8:4963–4976.  https://doi.org/10.1021/acsami.6b00161CrossRefPubMedGoogle Scholar
  41. 41.
    Duran N, Marcato PD, De Conti R, Alves OL, Costa FTM, Brocchi M (2010) Potential use of silver nanoparticles on pathogenic bacteria, their toxicity and possible mechanisms of action. J Braz Chem Soc 21:949–959.  https://doi.org/10.1590/S0103-50532010000600002CrossRefGoogle Scholar
  42. 42.
    Salem W, Leitner DR, Zingl FG, Schratter G, Prassl R, Goessler W, Reidl J, Schild S (2015) Antibacterial activity of silver and zinc nanoparticles against Vibrio cholerae and enterotoxic Escherichia coli. Int J Med Microbiol 305:85–95.  https://doi.org/10.1016/j.ijmm.2014.11.005CrossRefPubMedGoogle Scholar
  43. 43.
    Hemeg HA (2017) Nanomaterials for alternative antibacterial therapy. Int J Nanomedicine 12:8211–8225.  https://doi.org/10.2147/Ijn.S132163CrossRefPubMedGoogle Scholar
  44. 44.
    Slavin YN, Asnis J, Hafeli UO, Bach H (2017) Metal nanoparticles: understanding the mechanisms behind antibacterial activity. J Nanobiotechnol 15:56.  https://doi.org/10.1186/s12951-017-0308-zCrossRefGoogle Scholar
  45. 45.
    Cui Y, Zhao YY, Tian Y, Zhang W, Lu XY, Jiang XY (2012) The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli. Biomaterials 33:2327–2333.  https://doi.org/10.1016/j.biomaterials.2011.11.057CrossRefPubMedGoogle Scholar
  46. 46.
    Shamaila S, Zafar N, Riaz S, Sharif R, Nazir J, Naseem S (2016) Gold nanoparticles: an efficient antimicrobial agent against enteric bacterial human pathogen. Nanomaterials 6:71.  https://doi.org/10.3390/nano6040071CrossRefGoogle Scholar
  47. 47.
    Rastogi L, Kora AJ, Arunachalam J (2012) Highly stable, protein capped gold nanoparticles as effective drug delivery vehicles for amino-glycosidic antibiotics. Materials Science and Engineering: C 32(6):1571–1577.  https://doi.org/10.1016/J.MSEC.2012.04.044
  48. 48.
    Roshmi T, Soumya KR, Jyothis M, Radhakrishnan EK (2015) Effect of biofabricated gold nanoparticle-based antibiotic conjugates on minimum inhibitory concentration of bacterial isolates of clinical origin. Gold Bulletin 48(1–2):63–71.  https://doi.org/10.1007/s13404-015-0162-4
  49. 49.
    Zeng Q, Zhu Y, Yu B, Sun Y, Ding X, Xu C, Wu YW, Tang Z, Xu FJ (2018) Antimicrobial and antifouling polymeric agents for surface functionalization of medical implants. Biomacromolecules 9:2805–2811.  https://doi.org/10.1021/acs.biomac.8b00399CrossRefGoogle Scholar
  50. 50.
    Qayyum S, Oves M, Khan AU (2017) Obliteration of bacterial growth and biofilm through ROS generation by facilely synthesized green silver nanoparticles. PLoS One 12:e0181363.  https://doi.org/10.1371/journal.pone.0181363CrossRefPubMedGoogle Scholar
  51. 51.
    Jankauskaite V, Lazauskas A, Griskonis E, Lisauskaite A, Zukiene K (2017) UV-curable aliphatic silicone acrylate organic-inorganic hybrid coatings with antibacterial activity. Molecules 22:964.  https://doi.org/10.3390/molecules22060964CrossRefGoogle Scholar
  52. 52.
    Xu DQ, Su YL, Zhao LL, Meng FC, Liu C, Guan YY, Zhang JY, Luo JB (2017) Antibacterial and antifouling properties of a polyurethane surface modified with perfluoroalkyl and silver nanoparticles. J Biomed Mater Res Pt A 105:531–538.  https://doi.org/10.1002/jbm.a.35929CrossRefGoogle Scholar
  53. 53.
    Prasannaraj G, Venkatachalam P (2017) Enhanced antibacterial, anti-biofilm and antioxidant (ROS) activities of biomolecules engineered silver nanoparticles against clinically isolated gram positive and gram negative microbial pathogens. J Clust Sci 28:645–664.  https://doi.org/10.1007/s10876-017-1160-xCrossRefGoogle Scholar
  54. 54.
    Gupta K, Barua S, Hazarika SN, Manhar AK, Nath D, Karak N, Namsa ND, Mukhopadhyay R, Kalia VC, Mandal M (2014) Green silver nanoparticles: enhanced antimicrobial and antibiofilm activity with effects on DNA replication and cell cytotoxicity. RSC Adv 4:52845–52855.  https://doi.org/10.1039/c4ra08791gCrossRefGoogle Scholar
  55. 55.
    Wooh S, Butt HJ (2017) A photocatalytically active lubricant-impregnated surface. Angew Chem Int Ed 56:4965–4969.  https://doi.org/10.1002/anie.201611277CrossRefGoogle Scholar
  56. 56.
    Shankar S, Teng XN, Li GB, Rhim JW (2015) Preparation, characterization, and antimicrobial activity of gelatin/ZnO nanocomposite films. Food Hydrocoll 45:264–271.  https://doi.org/10.1016/j.foodhyd.2014.12.001CrossRefGoogle Scholar
  57. 57.
    Solga A, Cerman Z, Striffler BF, Spaeth M, Barthlott W (2007) The dream of staying clean: lotus and biomimetic surfaces. Bioinspir Biomim 2:S126–S134.  https://doi.org/10.1088/1748-3182/2/4/S02CrossRefPubMedGoogle Scholar
  58. 58.
    Watson GS, Green DW, Schwarzkopf L, Li X, Cribb BW, Myhra S, Watson JA (2015) A gecko skin micro/nano structure—a low adhesion, superhydrophobic, anti-wetting, self-cleaning, biocompatible, antibacterial surface. Acta Biomater 21:109–122.  https://doi.org/10.1016/j.actbio.2015.03.007CrossRefPubMedGoogle Scholar
  59. 59.
    Bixler GD, Bhushan B (2013) Fluid drag reduction with shark-skin riblet inspired microstructured surfaces. Adv Funct Mater 23:4507–4528.  https://doi.org/10.1002/adfm.201203683CrossRefGoogle Scholar
  60. 60.
    Watson GS, Cribb BW, Watson JA (2010) How micro/nanoarchitecture facilitates anti-wetting: an elegant hierarchical design on the termite wing. ACS Nano 4:129–136.  https://doi.org/10.1021/nn900869bCrossRefPubMedGoogle Scholar
  61. 61.
    Wagner T, Neinhuis C, Barthlott W (1996) Wettability and contaminability of insect wings as a function of their surface sculptures. Acta Zool 77:213–225.  https://doi.org/10.1111/j.1463-6395.1996.tb01265.xCrossRefGoogle Scholar
  62. 62.
    Neinhuis C, Barthlott W (1997) Characterization and distribution of water-repellent, self-cleaning plant surfaces. Ann Bot 79:667–677.  https://doi.org/10.1006/ANBO.1997.0400CrossRefGoogle Scholar
  63. 63.
    Li X, Cheung GS, Watson GS, Watson JA, Lin S, Schwarzkopf L, Green DW (2016) The nanotipped hairs of gecko skin and biotemplated replicas impair and/or kill pathogenic bacteria with high efficiency. Nanoscale 8:18860–18869.  https://doi.org/10.1039/c6nr05046hCrossRefPubMedGoogle Scholar
  64. 64.
    Ivanova EP, Hasan J, Webb HK, Truong VK, Watson GS, Watson JA, Baulin VA, Pogodin S, Wang JY, Tobin MJ, Löbbe C, Crawford RJ (2012) Natural bactericidal surfaces: mechanical rupture of pseudomonas aeruginosa cells by cicada wings. Small 8:2489–2494.  https://doi.org/10.1002/smll.201200528CrossRefPubMedGoogle Scholar
  65. 65.
    Ivanova EP, Hasan J, Webb HK, Gervinskas G, Juodkazis S, Truong VK, Wu AHF, Lamb RN, Baulin VA, Watson GS, Watson JA, Mainwaring DE, Crawford RJ (2013) Bactericidal activity of black silicon. Nat Commun 4:2838.  https://doi.org/10.1038/ncomms3838CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Jaggessar A, Shahali H, Mathew A, Yarlagadda PKDV (2017) Bio-mimicking nano and micro-structured surface fabrication for antibacterial properties in medical implants. J Nanobiotechnol 15:64.  https://doi.org/10.1186/s12951-017-0306-1CrossRefGoogle Scholar
  67. 67.
    Ma J, Sun Y, Gleichauf K, Lou J, Li Q (2011) Nanostructure on Taro Leaves Resists Fouling by Colloids and Bacteria under Submerged Conditions. Langmuir 27 (16):10035–10040Google Scholar
  68. 68.
    Guo Z, Liu W (2007) Biomimic from the superhydrophobic plant leaves in nature: binary structure and unitary structure. Plant Sci 172:1103–1112.  https://doi.org/10.1016/j.plantsci.2007.03.005CrossRefGoogle Scholar
  69. 69.
    Feng L, Li S, Li Y, Li H, Zhang L, Zhai J, Song Y, Liu B, Jiang L, Zhu D (2002) Super-hydrophobic surfaces: from natural to artificial. Adv Mater 14:1857–1860.  https://doi.org/10.1002/adma.200290020CrossRefGoogle Scholar
  70. 70.
    Cassie ABD, Baxter S (1944) Wettability of porous surfaces. Trans Faraday Soc 40:546–551.  https://doi.org/10.1039/tf9444000546CrossRefGoogle Scholar
  71. 71.
    Dundar Arisoy F, Kolewe KW, Homyak B, Kurtz IS, Schiffman JD, Watkins JJ (2018) Bioinspired photocatalytic shark-skin surfaces with antibacterial and antifouling activity via nanoimprint lithography. ACS Appl Mater Interfaces 10:20055–20063.  https://doi.org/10.1021/acsami.8b05066CrossRefPubMedGoogle Scholar
  72. 72.
    Bixler GD, Bhushan B (2015) Rice and butterfly wing effect inspired low drag and antifouling surfaces: a review. Crit Rev Solid State Mater Sci 40:1–37.  https://doi.org/10.1080/10408436.2014.917368CrossRefGoogle Scholar
  73. 73.
    Bixler GD, Bhushan B (2012) Bioinspired rice leaf and butterfly wing surface structures combining shark skin and lotus effects. Soft Matter 8:11271–11284.  https://doi.org/10.1039/c2sm26655eCrossRefGoogle Scholar
  74. 74.
    Pogodin S, Hasan J, Baulin VA, Webb HK, Truong VK, Phong Nguyen TH, Boshkovikj V, Fluke CJ, Watson GS, Watson JA, Crawford RJ, Ivanova EP (2013) Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J 104:835–840.  https://doi.org/10.1016/j.bpj.2012.12.046CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Hasan J, Webb HK, Truong VK, Pogodin S, Baulin VA, Watson GS, Watson JA, Crawford RJ, Ivanova EP (2013) Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol 97:9257–9262.  https://doi.org/10.1007/s00253-012-4628-5CrossRefPubMedGoogle Scholar
  76. 76.
    Kelleher SM, Habimana O, Lawler J, O’reilly B, Daniels S, Casey E, Cowley A (2016) Cicada wing surface topography: an investigation into the bactericidal properties of nanostructural features. ACS Appl Mater Interfaces 8:14966–14974.  https://doi.org/10.1021/acsami.5b08309CrossRefPubMedGoogle Scholar
  77. 77.
    Ivanova EP, Nguyen SH, Webb HK, Hasan J, Truong VK, Lamb RN, Duan X, Tobin MJ, Mahon PJ, Crawford RJ (2013) Molecular organization of the nanoscale surface structures of the dragonfly Hemianax papuensis wing epicuticle. PLoS One 8:e67893.  https://doi.org/10.1371/journal.pone.0067893CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Selvakumar R, Karuppanan KK, Pezhinkattil R (2012) Analysis on surface nanostructures present in hindwing of dragon fly (Sympetrum vulgatum) using atomic force microscopy. Micron 43:1299–1303.  https://doi.org/10.1016/J.MICRON.2011.10.017CrossRefPubMedGoogle Scholar
  79. 79.
    Mainwaring DE, Nguyen SH, Webb H, Jakubov T, Tobin M, Lamb RN, Wu AHF, Marchant R, Crawford RJ, Ivanova EP (2016) The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale 8:6527–6534.  https://doi.org/10.1039/c5nr08542jCrossRefPubMedGoogle Scholar
  80. 80.
    Bandara CD, Singh S, Afara IO, Wolff A, Tesfamichael T, Ostrikov K, Oloyede A (2017) Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli. ACS Appl Mater Interfaces 9:6746–6760.  https://doi.org/10.1021/acsami.6b13666CrossRefPubMedGoogle Scholar
  81. 81.
    Linklater DP, Juodkazis S, Rubanov S, Ivanova EP (2017) Comment on “Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli”. ACS Appl Mater Interfaces 9:29387–29393.  https://doi.org/10.1021/acsami.7b05707CrossRefPubMedGoogle Scholar
  82. 82.
    Watson GS, Cribb BW, Schwarzkopf L, Watson JA (2015) Contaminant adhesion (aerial/ground biofouling) on the skin of a gecko. J R Soc Interface 12:20150318.  https://doi.org/10.1098/rsif.2015.0318CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Hayes MJ, Levine TP, Wilson RH (2016) Identification of nanopillars on the cuticle of the aquatic larvae of the drone fly (diptera: Syrphidae). J Insect Sci 16:1–7.  https://doi.org/10.1093/jisesa/iew019CrossRefGoogle Scholar
  84. 84.
    Kayes MI, Galante AJ, Stella NA, Haghanifar S, Shanks RMQ, Leu PW (2018) Stable lotus leaf-inspired hierarchical, fluorinated polypropylene surfaces for reduced bacterial adhesion. React Funct Polym 128:40–46.  https://doi.org/10.1016/J.REACTFUNCTPOLYM.2018.04.013CrossRefGoogle Scholar
  85. 85.
    Wolfe DB, Love JC, Whitesides GM (2004) Nanostructures replicated by polymer molding. Marcel Dekker, New YorkGoogle Scholar
  86. 86.
    Jafari Nodoushan E, Ebrahimi NG, Ayazi M (2017) An anti-bacterial approach to nanoscale roughening of biomimetic rice-like pattern PP by thermal annealing. Appl Surf Sci 423:1054–1061.  https://doi.org/10.1016/J.APSUSC.2017.06.193CrossRefGoogle Scholar
  87. 87.
    Munther M, Palma T, Angeron IA, Salari S, Ghassemi H, Vasefi M, Beheshti A, Davami K (2018) Microfabricated biomimetic placoid scale-inspired surfaces for antifouling applications. Appl Surf Sci 453:166–172.  https://doi.org/10.1016/j.apsusc.2018.05.030CrossRefGoogle Scholar
  88. 88.
    Carman ML, Estes TG, Feinberg AW, Schumacher JF, Wilkerson W, Wilson LH, Callow ME, Callow JA, Brennan AB (2006) Engineered antifouling microtopographies—correlating wettability with cell attachment. Biofouling 22:11–21.  https://doi.org/10.1080/08927010500484854CrossRefPubMedGoogle Scholar
  89. 89.
    Liu W, Liu X, Fangteng J, Wang S, Fang L, Shen H, Xiang S, Sun H, Yang B (2014) Bioinspired polyethylene terephthalate nanocone arrays with underwater superoleophobicity and anti-bioadhesion properties. Nanoscale 6:13845–13853.  https://doi.org/10.1039/c4nr04471aCrossRefPubMedGoogle Scholar
  90. 90.
    Jin L, Guo W, Xue P, Gao H, Zhao M, Zheng C, Zhang Y, Han D (2015) Quantitative assay for the colonization ability of heterogeneous bacteria on controlled nanopillar structures. Nanotechnology 26:055702.  https://doi.org/10.1088/0957-4484/26/5/055702CrossRefPubMedGoogle Scholar
  91. 91.
    Izquierdo-Barba I, García-Martín JM, Álvarez R, Palmero A, Esteban J, Pérez-Jorge C, Arcos D, Vallet-Regí M (2015) Nanocolumnar coatings with selective behavior towards osteoblast and Staphylococcus aureus proliferation. Acta Biomater 15:20–28.  https://doi.org/10.1016/J.ACTBIO.2014.12.023CrossRefPubMedGoogle Scholar
  92. 92.
    Lüdecke C, Roth M, Yu W, Horn U, Bossert J, Jandt KD (2016) Nanorough titanium surfaces reduce adhesion of Escherichia coli and Staphylococcus aureus via nano adhesion points. Colloids Surf B Biointerfaces 145:617–625.  https://doi.org/10.1016/J.COLSURFB.2016.05.049CrossRefPubMedGoogle Scholar
  93. 93.
    Wu S, Zhang B, Liu Y, Suo X, Li H (2018) Influence of surface topography on bacterial adhesion: a review (review). Biointerphases 13:060801.  https://doi.org/10.1116/1.5054057CrossRefPubMedGoogle Scholar
  94. 94.
    Desrousseaux C, Sautou V, Descamps S, Traoré O (2013) Modification of the surfaces of medical devices to prevent microbial adhesion and biofilm formation. J Hosp Infect 85:87–93.  https://doi.org/10.1016/J.JHIN.2013.06.015CrossRefPubMedGoogle Scholar
  95. 95.
    DEWIDAR MM, KHALIL KA, LIM JK (2007) Processing and mechanical properties of porous 316L stainless steel for biomedical applications. Trans Nonferrous Met Soc Chin 17:468–473.  https://doi.org/10.1016/S1003-6326(07)60117-4CrossRefGoogle Scholar
  96. 96.
    Bagherifard S, Hickey DJ, de Luca AC, Malheiro VN, Markaki AE, Guagliano M, Webster TJ (2015) The influence of nanostructured features on bacterial adhesion and bone cell functions on severely shot peened 316L stainless steel. Biomaterials 73:185–197.  https://doi.org/10.1016/j.biomaterials.2015.09.019CrossRefPubMedGoogle Scholar
  97. 97.
    Sundararaj K, Bangaru M, Mohan B (2017) In vitro biocompatibility study on stainless steel 316L after nano finishing. ASME Paper No. IMECE2017-72606: V003T04A064.  https://doi.org/10.1115/IMECE2017-72606
  98. 98.
    Jang Y, Choi WT, Johnson CT, García AJ, Singh PM, Breedveld V, Hess DW, Champion JA (2018) Inhibition of bacterial adhesion on nanotextured stainless steel 316L by electrochemical etching. ACS Biomater Sci Eng 4:90–97.  https://doi.org/10.1021/acsbiomaterials.7b00544CrossRefPubMedGoogle Scholar
  99. 99.
    Lin Y, Gallucci GO, Buser D, Bosshardt D, Belser UC, Yelick PC (2011) Bioengineered periodontal tissue formed on titanium dental implants. J Dent Res 90:251–256.  https://doi.org/10.1177/0022034510384872CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Michelle Grandin H, Berner S, Dard M (2012) A review of titanium zirconium (TiZr) alloys for use in endosseous dental implants. Materials (Basel) 5:1348–1360.  https://doi.org/10.3390/ma5081348CrossRefPubMedCentralGoogle Scholar
  101. 101.
    Neoh KG, Hu X, Zheng D, Kang ET (2012) Balancing osteoblast functions and bacterial adhesion on functionalized titanium surfaces. Biomaterials 33:2813–2822.  https://doi.org/10.1016/j.biomaterials.2012.01.018CrossRefPubMedGoogle Scholar
  102. 102.
    Sengstock C, Lopian M, Motemani Y, Borgmann A, Khare C, Buenconsejo PJS, Schildhauer TA, Ludwig A, Köller M (2014) Structure-related antibacterial activity of a titanium nanostructured surface fabricated by glancing angle sputter deposition. Nanotechnology 25:195101.  https://doi.org/10.1088/0957-4484/25/19/195101CrossRefPubMedGoogle Scholar
  103. 103.
    Bhadra CM, Khanh Truong V, Pham VTH, Al Kobaisi M, Seniutinas G, Wang JY, Juodkazis S, Crawford RJ, Ivanova EP (2015) Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci Rep 5:16817.  https://doi.org/10.1038/srep16817CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Hasan J, Jain S, Chatterjee K (2017) Nanoscale topography on black titanium imparts multi-biofunctional properties for orthopedic applications. Sci Rep 7:41118.  https://doi.org/10.1038/srep41118CrossRefPubMedGoogle Scholar
  105. 105.
    Tsimbouri PM, Fisher L, Holloway N, Sjostrom T, Nobbs AH, Meek RMD, Su B, Dalby MJ (2016) Osteogenic and bactericidal surfaces from hydrothermal titania nanowires on titanium substrates. Sci Rep 6:36875.  https://doi.org/10.1038/srep36857CrossRefGoogle Scholar
  106. 106.
    Hizal F, Zhuk I, Sukhishvili S, Busscher HJ, Van Der Mei HC, Choi CH (2015) Impact of 3D hierarchical nanostructures on the antibacterial efficacy of a bacteria-triggered self-defensive antibiotic coating. ACS Appl Mater Interfaces 7:20304–20313.  https://doi.org/10.1021/acsami.5b05947CrossRefPubMedGoogle Scholar
  107. 107.
    Sjöström T, Nobbs AH, Su B (2016) Bactericidal nanospike surfaces via thermal oxidation of Ti alloy substrates. Mater Lett 167:22–26.  https://doi.org/10.1016/j.matlet.2015.12.140CrossRefGoogle Scholar
  108. 108.
    Wang X, Bhadra CM, Yen Dang TH, Buividas R, Wang J, Crawford RJ, Ivanova EP, Juodkazis S (2016) A bactericidal microfluidic device constructed using nano-textured black silicon. RSC Adv 6:26300–26306.  https://doi.org/10.1039/c6ra03864fCrossRefGoogle Scholar
  109. 109.
    Pham VTH, Truong VK, Orlowska A, Ghanaati S, Barbeck M, Booms P, Fulcher AJ, Bhadra CM, Buividas R, Baulin V, James Kirkpatrick C, Doran P, Mainwaring DE, Juodkazis S, Crawford RJ, Ivanova EP (2016) Race for the surface: eukaryotic cells can win. ACS Appl Mater Interfaces 8:22025–22031.  https://doi.org/10.1021/acsami.6b06415CrossRefPubMedGoogle Scholar
  110. 110.
    Li X (2015) Bactericidal mechanism of nanopatterned surfaces. Phys Chem Chem Phys 18:1311–1316.  https://doi.org/10.1039/c5cp05646bCrossRefGoogle Scholar
  111. 111.
    Xue F, Liu J, Guo L, Zhang L, Li Q (2015) Theoretical study on the bactericidal nature of nanopatterned surfaces. J Theor Biol 385:1–7.  https://doi.org/10.1016/j.jtbi.2015.08.011CrossRefPubMedGoogle Scholar
  112. 112.
    Nowlin K, Boseman A, Covell A, LaJeunesse D (2014) Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces. J R Soc Interface 12:20140999.  https://doi.org/10.1098/rsif.2014.0999CrossRefGoogle Scholar
  113. 113.
    Dickson MN, Liang EI, Rodriguez LA, Vollereaux N, Yee AF (2015) Nanopatterned polymer surfaces with bactericidal properties. Biointerphases 10:021010.  https://doi.org/10.1116/1.4922157CrossRefPubMedGoogle Scholar
  114. 114.
    Michalska M, Gambacorta F, Divan R, Aranson IS, Sokolov A, Noirot P, Laible PD (2018) Tuning antimicrobial properties of biomimetic nanopatterned surfaces. Nanoscale 10:6639–6650.  https://doi.org/10.1039/c8nr00439kCrossRefPubMedGoogle Scholar
  115. 115.
    Lin N, Berton P, Moraes C, Rogers RD, Tufenkji N (2018) Nanodarts, nanoblades, and nanospikes: mechano-bactericidal nanostructures and where to find them. Adv Colloid Interface Sci 252:55–68.  https://doi.org/10.1016/j.cis.2017.12.007CrossRefPubMedGoogle Scholar
  116. 116.
    Elbourne A, Crawford RJ, Ivanova EP (2017) Nano-structured antimicrobial surfaces: from nature to synthetic analogues. J Colloid Interface Sci 508:603–616.  https://doi.org/10.1016/j.jcis.2017.07.021CrossRefPubMedGoogle Scholar
  117. 117.
    Feng G, Cheng Y, Wang SY, Hsu LC, Feliz Y, Borca-Tasciuc DA, Worobo RW, Moraru CI (2014) Alumina surfaces with nanoscale topography reduce attachment and biofilm formation by Escherichia coli and Listeria spp. Biofouling 30:1253–1268.  https://doi.org/10.1080/08927014.2014.976561CrossRefPubMedGoogle Scholar
  118. 118.
    Kim S, Jung UT, Kim SK, Lee JH, Choi HS, Kim CS, Jeong MY (2015) Nanostructured multifunctional surface with antireflective and antimicrobial characteristics. ACS Appl Mater Interfaces 7:326–331.  https://doi.org/10.1021/am506254rCrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Chemical EngineeringUniversity of FloridaGainesvilleUSA
  2. 2.School of Chemical and Biological Engineering, Seoul National UniversitySeoulRepublic of Korea

Personalised recommendations