Cellulose

, Volume 24, Issue 2, pp 781–796

Cellulose acetate membrane embedded with graphene oxide-silver nanocomposites and its ability to suppress microbial proliferation

  • Andreia Fonseca de Faria
  • Ana Carolina Mazarin de Moraes
  • Patricia Fernanda Andrade
  • Douglas Soares da Silva
  • Maria do Carmo Gonçalves
  • Oswaldo Luiz Alves
Original Paper

Abstract

Bacterial adhesion and consequent biofilm formation are one the biggest hurdles in membrane-based technologies. Due to numerous problems associated with bacterial colonization on membrane surfaces, the development of new approaches to prevent microbial growth has been encouraged. Graphene oxide, produced by the chemical exfoliation of graphite, is a highly water-dispersible nanomaterial which has been used as a platform for the anchoring of nanoparticles and bioactive molecules. In this present study, we propose the fabrication of antimicrobial membranes through the incorporation of graphene oxide-silver nanocomposites into a cellulose acetate polymeric matrix. Transmission electron microscopy, Raman, and UV–visible diffuse reflectance spectroscopy measurements confirmed the presence of graphene oxide-silver sheets in the modified membranes. In comparison to pristine membranes, membranes containing graphene oxide-silver nanocomposites showed larger surface pores and increased pure water flux. In addition, membranes embedded with graphene oxide-silver presented strong antibacterial activity, being able to inactivate adhered bacteria at a rate of 90% compared to pristine cellulose acetate membranes. Our results strongly suggest that the incorporation of graphene oxide-silver nanocomposites to cellulose acetate is a promising strategy to produce membranes that are able to minimize bacterial attachment and growth.

Graphical Abstract

Keywords

Graphene oxide Silver nanoparticles Graphene-based nanocomposites Cellulose acetate membranes Antimicrobial activity 

Supplementary material

10570_2016_1140_MOESM1_ESM.docx (1.5 mb)
Supplementary material 1 (DOCX 1551 kb)

References

  1. Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B 28:313–318. doi:10.1016/S0927-7765(02)00174-1 CrossRefGoogle Scholar
  2. Akhavan O, Ghaderi E (2010) Toxicity of Graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–5736. doi:10.1021/nn101390x CrossRefGoogle Scholar
  3. Akhavan O, Ghaderi E, Esfandiar A (2011) Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. J Phys Chem B 115:6279–6288. doi:10.1021/jp200686k CrossRefGoogle Scholar
  4. Al-Amoudi A, Lovitt RW (2007) Fouling strategies and the cleaning system of NF membranes and factors affecting cleaning efficiency. J Membr Sci 303:4–28. doi:10.1016/j.memsci.2007.06.002 CrossRefGoogle Scholar
  5. Andrade PF, de Faria AF, Oliveira SR, Arruda MAZ, Gonçalves MdC (2015a) Improved antibacterial activity of nanofiltration polysulfone membranes modified with silver nanoparticles. Water Res 81:333–342. doi:10.1016/j.watres.2015.05.006 CrossRefGoogle Scholar
  6. Andrade PF, Faria AF, Quites FJ, Oliveira SR, Alves OL, Arruda MAZ, Gonçalves dMC (2015b) Inhibition of bacterial adhesion on cellulose acetate membranes containing silver nanoparticles. Cellulose 22:3895–3906. doi:10.1007/s10570-015-0752-6 CrossRefGoogle Scholar
  7. Barud HS et al (2008) Self-supported silver nanoparticles containing bacterial cellulose membranes. Mater Sci Eng C 28:515–518. doi:10.1016/j.msec.2007.05.001 CrossRefGoogle Scholar
  8. Basri H, Ismail AF, Aziz M (2011) Polyethersulfone (PES)–silver composite UF membrane: effect of silver loading and PVP molecular weight on membrane morphology and antibacterial activity. Desalination 273:72–80. doi:10.1016/j.desal.2010.11.010 CrossRefGoogle Scholar
  9. Cai X et al (2012) The use of polyethyleneimine-modified reduced graphene oxide as a substrate for silver nanoparticles to produce a material with lower cytotoxicity and long-term antibacterial activity. Carbon 50:3407–3415. doi:10.1016/j.carbon.2012.02.002 CrossRefGoogle Scholar
  10. Campbell P et al (1999) Quantitative structure–activity relationship (QSAR) analysis of surfactants influencing attachment of a Mycobacterium sp. to cellulose acetate and aromatic polyamide reverse osmosis membranes. Biotechnol Bioeng 64:527–544. doi:10.1002/(SICI)1097-0290(19990905)64:5<527:AID-BIT3>3.0.CO;2-X CrossRefGoogle Scholar
  11. Chatterjee PK, Conrad CM (1968) Thermogravimetric analysis of cellulose. J Polym Sci A-1 Polym Chem 6:3217–3233. doi:10.1002/pol.1968.150061202 CrossRefGoogle Scholar
  12. Crock CA, Rogensues AR, Shan W, Tarabara VV (2013) Polymer nanocomposites with graphene-based hierarchical fillers as materials for multifunctional water treatment membranes. Water Res 47:3984–3996. doi:10.1016/j.watres.2012.10.057 CrossRefGoogle Scholar
  13. Das MR, Sarma RK, Saikia R, Kale VS, Shelke MV, Sengupta P (2010) Synthesis of silver nanoparticles in an aqueous suspension of graphene oxide sheets and its antimicrobial activity. Colloids Surf B 1:16–22. doi:10.1016/j.colsurfb.2010.10.033 Google Scholar
  14. de Faria AF, Martinez DST, Meira SMM, de Moraes ACM, Brandelli A, Filho AGS, Alves OL (2014a) Anti-adhesion and antibacterial activity of silver nanoparticles supported on graphene oxide sheets. Colloids Surf B 113:115–124. doi:10.1016/j.colsurfb.2013.08.006 CrossRefGoogle Scholar
  15. de Faria AF, Martinez DST, Meira SMM, de Moraes ACM, Brandelli A, Filho AGS, Alves OL (2014b) Anti-adhesion and antibacterial activity of silver nanoparticles supported on graphene oxide sheets. Colloids Surf B 113:115–124. doi:10.1016/j.colsurfb.2013.08.006 CrossRefGoogle Scholar
  16. de Faria AF, Perreault F, Shaulsky E, Arias Chavez LH, Elimelech M (2015) Antimicrobial electrospun biopolymer nanofiber mats functionalized with graphene oxide-silver nanocomposites. ACS Appl Mater Interfaces 7:12751–12759. doi:10.1021/acsami.5b01639 CrossRefGoogle Scholar
  17. de Moraes ACM et al (2015) Fabrication of transparent and ultraviolet shielding composite films based on graphene oxide and cellulose acetate. Carbohydr Polym 123:217–227. doi:10.1016/j.carbpol.2015.01.034 CrossRefGoogle Scholar
  18. Dresselhaus MS, Dresselhaus G, Saito R, Jorio A (2005) Raman spectroscopy of carbon nanotubes. Phys Rep 409:47–99. doi:10.1016/j.physrep.2004.10.006 CrossRefGoogle Scholar
  19. Dreyer DR, Park S, Bielawski CW, Ruoff RS (2010) The chemistry of graphene oxide. Chem Soc Rev 39:228–240. doi:10.1039/B917103G CrossRefGoogle Scholar
  20. Dreyer DR, Todd AD, Bielawski CW (2014) Harnessing the chemistry of graphene oxide. Chem Soc Rev. doi:10.1039/C4CS00060A Google Scholar
  21. Edgar KJ, Buchanan CM, Debenham JS, Rundquist PA, Seiler BD, Shelton MC, Tindall D (2001) Advances in cellulose ester performance and application. Prog Polym Sci 26:1605–1688. doi:10.1016/S0079-6700(01)00027-2 CrossRefGoogle Scholar
  22. Elimelech M, Xiaohua Z, Childress AE, Seungkwan H (1997) Role of membrane surface morphology in colloidal fouling of cellulose acetate and composite aromatic polyamide reverse osmosis membranes. J Membr Sci 127:101–109. doi:10.1016/S0376-7388(96)00351-1 CrossRefGoogle Scholar
  23. Faria AF et al (2012) Unveiling the role of oxidation debris on the surface chemistry of graphene through the anchoring of Ag nanoparticles. Chem Mater 24:4080–4087. doi:10.1021/cm301939s CrossRefGoogle Scholar
  24. Ganesh BM, Isloor AM, Ismail AF (2013) Enhanced hydrophilicity and salt rejection study of graphene oxide-polysulfone mixed matrix membrane. Desalination 313:199–207. doi:10.1016/j.desal.2012.11.037 CrossRefGoogle Scholar
  25. Gao X, Jang J, Nagase S (2009) Hydrazine and thermal reduction of graphene oxide: reaction mechanisms, product structures, and reaction design. J Phys Chem C 114:832–842. doi:10.1021/jp909284g CrossRefGoogle Scholar
  26. Geim AK, Novoselov KS (2007) The rise of graphene. Nat Mater 6:183–191CrossRefGoogle Scholar
  27. Glasser WG (2004) 6. Prospects for future applications of cellulose acetate. Macromol Symp 208:371–394. doi:10.1002/masy.200450416 CrossRefGoogle Scholar
  28. Hu W et al (2010) Graphene-based antibacterial paper. ACS Nano 4:4317–4323. doi:10.1021/nn101097v CrossRefGoogle Scholar
  29. Hummers WS, Offman RE (1958) Preparation of graphitic oxide. J Am Chem Soc 80:1339CrossRefGoogle Scholar
  30. Jayalakshmi A, Kim I-C, Kwon Y-N (2015) Cellulose acetate graft-(glycidylmethacrylate-g-PEG) for modification of AMC ultrafiltration membranes to mitigate organic fouling. RSC Adv 5:48290–48300. doi:10.1039/C5RA03499J CrossRefGoogle Scholar
  31. Kunst B, Sourirajan S (1974) An approach to the development of cellulose acetate ultrafiltration membranes. J Appl Polym Sci 18:3423–3434. doi:10.1002/app.1974.070181121 CrossRefGoogle Scholar
  32. Lee J et al (2013) Graphene oxide nanoplatelets composite membrane with hydrophilic and antifouling properties for wastewater treatment. J Membr Sci 448:223–230. doi:10.1016/j.memsci.2013.08.017 CrossRefGoogle Scholar
  33. Li J, Liu C (2010) Ag–graphene heterostructures: synthesis, characterization and optical properties. Eur J Inorg Chem. doi:10.1002/ejic.200901048 Google Scholar
  34. Li Q, Mahendra S, Lyon DY, Brunet L, Liga MV, Li D, Alvarez PJJ (2008a) Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res 42:4591–4602. doi:10.1016/j.watres.2008.08.015 CrossRefGoogle Scholar
  35. Li X, Wang Y, Lu X, Xiao C (2008b) Morphology changes of polyvinylidene fluoride membrane under different phase separation mechanisms. J Membr Sci 320:477–482. doi:10.1016/j.memsci.2008.04.033 CrossRefGoogle Scholar
  36. Li J, Kuang D, Feng Y, Zhang F, Xu Z, Liu M, Wang D (2013) Green synthesis of silver nanoparticles–graphene oxide nanocomposite and its application in electrochemical sensing oftryptophan. Biosens Bioelectron 42:198–206. doi:10.1016/j.bios.2012.10.029 CrossRefGoogle Scholar
  37. Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175CrossRefGoogle Scholar
  38. Liu L, Wang Y, Yan X, Sun DD (2011a) Facile synthesis of monodispersed silver nanoparticles on graphene oxide sheets with enhanced antibacterial activity. New J Chem 35:1418–1423. doi:10.1039/C1NJ20076C CrossRefGoogle Scholar
  39. Liu S et al (2011b) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5:6971–6980. doi:10.1021/nn202451x CrossRefGoogle Scholar
  40. Liu S et al (2012) Lateral dimension-dependent antibacterial activity of graphene oxide sheets. Langmuir 28:12364–12372. doi:10.1021/la3023908 CrossRefGoogle Scholar
  41. Malard LM, Pimenta MA, Dresselhaus G, Dresselhaus MS (2009) Raman spectroscopy in graphene. Phys Rep 473:51–87. doi:10.1016/j.physrep.2009.02.003 CrossRefGoogle Scholar
  42. Mansouri J, Harrisson S, Chen V (2010) Strategies for controlling biofouling in membrane filtration systems: challenges and opportunities. J Mater Chem 20:4567–4586. doi:10.1039/B926440J CrossRefGoogle Scholar
  43. Marambio-Jones C, Hoek EV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551. doi:10.1007/s11051-010-9900-y CrossRefGoogle Scholar
  44. Nguyen T, Roddick AF, Fan L (2012) Biofouling of water treatment membranes: a review of the underlying causes, monitoring techniques and control measures. Membranes. doi:10.3390/membranes2040804 Google Scholar
  45. Orth ES, Fonsaca JES, Domingues SH, Mehl H, Oliveira MM, Zarbin AJG (2013) Targeted thiolation of graphene oxide and its utilization as precursor for graphene/silver nanoparticles composites. Carbon 61:543–550. doi:10.1016/j.carbon.2013.05.032 CrossRefGoogle Scholar
  46. Pasmore M, Todd P, Smith S, Baker D, Silverstein J, Coons D, Bowman CN (2001) Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling. J Membr Sci 194:15–32. doi:10.1016/S0376-7388(01)00468-9 CrossRefGoogle Scholar
  47. Perreault F, de Faria AF, Nejati S, Elimelech M (2015a) Antimicrobial properties of graphene oxide nanosheets: why size matters. ACS Nano 9:7226–7236. doi:10.1021/acsnano.5b02067 CrossRefGoogle Scholar
  48. Perreault F, de Faria AF, Elimelech M (2015b) Environmental applications of graphene-based nanomaterials. Chem Soc Rev 44:5861–5896. doi:10.1039/C5CS00021A CrossRefGoogle Scholar
  49. Porcelli N, Judd S (2010) Chemical cleaning of potable water membranes: a review. Sep Purif Technol 71:137–143. doi:10.1016/j.seppur.2009.12.007 CrossRefGoogle Scholar
  50. Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83. doi:10.1016/j.biotechadv.2008.09.002 CrossRefGoogle Scholar
  51. Ramanathan T et al (2008) Functionalized graphene sheets for polymer nanocomposites. Nat Nano 3:327–331CrossRefGoogle Scholar
  52. Rodrigues DF, Elimelech M (2010) Toxic effects of single-walled carbon nanotubes in the development of E. coli biofilm. Environ Sci Technol 44:4583–4589. doi:10.1021/es1005785 CrossRefGoogle Scholar
  53. Rodrigues-Filho UP, Gushikem Y, Gonçalves MdC, Cachichi RC, de Castro SC (1996) Composite membranes of cellulose acetate and zirconium dioxide: preparation and study of physicochemical characteristics. Chem Mater 8:1375–1379. doi:10.1021/cm950528g CrossRefGoogle Scholar
  54. Rodriguez-Perez L, Herranz MaA, Martin N (2013) The chemistry of pristine graphene. Communications 49:3721–3735. doi:10.1039/C3CC38950B Google Scholar
  55. Rourke JP, Pandey PA, Moore JJ, Bates M, Kinloch IA, Young RJ, Wilson NR (2011) The real graphene oxide revelead: stripping the oxidative debris from the graphene-like sheets. Angew Chem 50:3173–3177CrossRefGoogle Scholar
  56. Ruiz ON et al (2011) Graphene oxide: a nonspecific enhacer of cellular growth. ACS Nano 5:8100–8107. doi:10.1021/nn202699t CrossRefGoogle Scholar
  57. Shi X, Tal G, Hankins NP, Gitis V (2014) Fouling and cleaning of ultrafiltration membranes: a review. J Water Process Eng 1:121–138. doi:10.1016/j.jwpe.2014.04.003 CrossRefGoogle Scholar
  58. Shibata T (2004) 5.6 Cellulose acetate in separation technology. Macromol Symp 208:353–370. doi:10.1002/masy.200450415 CrossRefGoogle Scholar
  59. Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275:177–182. doi:10.1016/j.jcis.2004.02.012 CrossRefGoogle Scholar
  60. Soroush A, Ma W, Silvino Y, Rahaman MS (2015) Surface modification of thin film composite forward osmosis membrane by silver-decorated graphene-oxide nanosheets. Environ Sci Nano 2:395–405. doi:10.1039/C5EN00086F CrossRefGoogle Scholar
  61. Tang J et al (2013) Graphene oxide–silver nanocomposite as a highly effective antibacterial agent with species-specific mechanisms. ACS Appl Mater Interfaces 5:3867–3874. doi:10.1021/am4005495 CrossRefGoogle Scholar
  62. Tung VC, Allen MJ, Yang Y, Kaner RB (2009) High-throughput solution processing of large-scale graphene. Nat Nano 4:25–29CrossRefGoogle Scholar
  63. Turkevich J, Stevenson PC, Hillier J (1951) A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc 11:55–75CrossRefGoogle Scholar
  64. Verdejo R, Bernal MM, Romasanta LJ, Lopez-Manchado MA (2011) Graphene filled polymer nanocomposites. J Mater Chem 21:3301–3310. doi:10.1039/C0JM02708A CrossRefGoogle Scholar
  65. Viscarra Rossel RA, Walvoort DJJ, McBratney AB, Janik LJ, Skjemstad JO (2006) Visible, near infrared, mid infrared or combined diffuse reflectance spectroscopy for simultaneous assessment of various soil properties. Geoderma 131:59–75. doi:10.1016/j.geoderma.2005.03.007 CrossRefGoogle Scholar
  66. Vrouwenvelder HS, van Paassen JAM, Folmer HC, Hofman JAMH, Nederlof MM, van der Kooij D (1998) Biofouling of membranes for drinking water production. Desalination 118:157–166. doi:10.1016/S0011-9164(98)00116-7 CrossRefGoogle Scholar
  67. Wang Z, Yu H, Xia J, Zhang F, Li F, Xia Y, Li Y (2012) Novel GO-blended PVDF ultrafiltration membranes. Desalination 299:50–54. doi:10.1016/j.desal.2012.05.015 CrossRefGoogle Scholar
  68. Xu C, Wang X (2009) Fabrication of flexible metal-nanoparticle films using graphene oxide sheets as substrates. Small 5:2212–2217. doi:10.1002/smll.200900548 CrossRefGoogle Scholar
  69. Xu W-P et al (2011) Facile synthesis of silver@graphene oxide nanocomposites and their enhanced antibacterial properties. J Mater Chem 21:4593–4597. doi:10.1039/C0JM03376F CrossRefGoogle Scholar
  70. Yu L, Zhang Y, Zhang B, Liu J, Zhang H, Song C (2013) Preparation and characterization of HPEI-GO/PES ultrafiltration membrane with antifouling and antibacterial properties. J Membr Sci 447:452–462. doi:10.1016/j.memsci.2013.07.042 CrossRefGoogle Scholar
  71. Zhang M, Zhang K, De Gusseme B, Verstraete W (2012) Biogenic silver nanoparticles (bio-Ag0) decrease biofouling of bio-Ag0/PES nanocomposite membranes. Water Res 46:2077–2087. doi:10.1016/j.watres.2012.01.015 CrossRefGoogle Scholar
  72. Zhao C, Xu X, Chen J, Yang F (2013) Effect of graphene oxide concentration on the morphologies and antifouling properties of PVDF ultrafiltration membranes. J Environ Chem Eng 1:349–354. doi:10.1016/j.jece.2013.05.014 CrossRefGoogle Scholar
  73. Zhao C, Xu X, Chen J, Yang F (2014) Optimization of preparation conditions of poly(vinylidene fluoride)/graphene oxide microfiltration membranes by the Taguchi experimental design. Desalination 334:17–22. doi:10.1016/j.desal.2013.07.011 CrossRefGoogle Scholar
  74. Zhou X et al (2009a) In situ synthesis of metal nanoparticles on single-layer graphene oxide and reduced graphene oxide surfaces. J Phys Chem C 113:10842–10846. doi:10.1021/jp903821n CrossRefGoogle Scholar
  75. Zhou X et al (2009b) In situ synthesis of metal nanoparticles on single-layer graphene oxide and reduced graphene oxide surfaces. J Phys Chem C 113:10842–10846. doi:10.1021/jp903821n CrossRefGoogle Scholar
  76. Zhu X, Elimelech M (1997) Colloidal fouling of reverse osmosis membranes: measurements and fouling mechanisms. Environ Sci Technol 31:3654–3662. doi:10.1021/es970400v CrossRefGoogle Scholar
  77. Zhu M, Chen P, Liu M (2011) Graphene oxide enwrapped Ag/AgX (X = Br, Cl) nanocomposite as a highly efficient visible-light plasmonic photocatalyst. ACS Nano 5:4529–4536. doi:10.1021/nn200088x CrossRefGoogle Scholar
  78. Zinadini S, Zinatizadeh AA, Rahimi M, Vatanpour V, Zangeneh H (2014) Preparation of a novel antifouling mixed matrix PES membrane by embedding graphene oxide nanoplates. J Membr Sci 453:292–301. doi:10.1016/j.memsci.2013.10.070 CrossRefGoogle Scholar
  79. Zodrow K, Brunet L, Mahendra S, Li D, Zhang A, Li Q, Alvarez PJJ (2009) Polysulfone ultrafiltration membranes impregnated with silver nanoparticles show improved biofouling resistance and virus removal. Water Res 43:715–723. doi:10.1016/j.watres.2008.11.014 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Andreia Fonseca de Faria
    • 1
  • Ana Carolina Mazarin de Moraes
    • 1
  • Patricia Fernanda Andrade
    • 1
  • Douglas Soares da Silva
    • 1
  • Maria do Carmo Gonçalves
    • 1
  • Oswaldo Luiz Alves
    • 1
  1. 1.Institute of ChemistryUniversity of CampinasCampinasBrazil

Personalised recommendations