Abstract
The objective of this study was to integrate inorganic halloysite nanotubes (HNT) with chitosan and hyaluronic acid to obtain hybrid nanocomposites with opposing charges and to investigate their potential in the controlled release of drug model probes. Two oppositely charged polysaccharides, chitosan and hyaluronic acid, were selected for their biocompatibility and their importance in biomedical applications. The high surface area and the hollow nanometric-sized lumen of HNT allowed for the efficient loading of rhodamine 110 and carboxyfluorescein, used as models for oppositely charged drugs. In the case of chitosan, the preparation of the nanocomposite was carried out exploiting the electrostatic interaction between the polymer and HNT in water, while with hyaluronic acid, a covalent functionalization strategy was employed to couple the polymer with the clay. Nanocomposites were characterized with thermal, microscopic, and spectroscopic techniques, and the release kinetics of the model compounds was assessed by fluorescence measurements. The release curves were fitted with a model able to account for the desorption process from the external and the internal halloysite surfaces. The results show that both polymeric coatings alter the release of the probes, indicating a key role of both charge and coating composition on the initial and final amount of released dye, as well as on the rate of the desorption process.
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Abdelmouleh M, Boufi S, ben Salah A et al (2002) Interaction of silane coupling agents with cellulose. Langmuir 18:3203–3208
Abdullayev E, Lvov Y (2013) Halloysite clay nanotubes as a ceramic “skeleton” for functional biopolymer composites with sustained drug release. J Mater Chem B 1:2894–2903. doi:10.1039/C3TB20059K
Agnihotri SA, Mallikarjuna NN, Aminabhavi TM (2004) Recent advances on chitosan-based micro- and nanoparticles in drug delivery. J Control Release 100:5–28. doi:10.1016/j.jconrel.2004.08.010
Aguzzi C, Viseras C, Cerezo P et al (2013) Release kinetics of 5-aminosalicylic acid from halloysite. Colloids Surf B 105:75–80. doi:10.1016/j.colsurfb.2012.12.041
Arcudi F, Cavallaro G, Lazzara G et al (2014) Selective functionalization of halloysite cavity by click reaction: structured filler for enhancing mechanical properties of bionanocomposite films. J Phys Chem C 118:15095–15101. doi:10.1021/jp504388e
Bai H, Zhang H, He Y et al (2014) Enhanced proton conduction of chitosan membrane enabled by halloysite nanotubes bearing sulfonate polyelectrolyte brushes. J Membr Sci 454:220–232. doi:10.1016/j.memsci.2013.12.005
Baldrick P (2010) The safety of chitosan as a pharmaceutical excipient. Regul Toxicol Pharmacol 56:290–299. doi:10.1016/j.yrtph.2009.09.015
Bariana M, Aw MS, Kurkuri M, Losic D (2013) Tuning drug loading and release properties of diatom silica microparticles by surface modifications. Int J Pharm 443:230–241. doi:10.1016/j.ijpharm.2012.12.012
Barrett EP, Joyner LG, Halenda PP (1951) The determination of pore volume and area distributions in porous substances. I. Computations from nitrogen isotherms. J Am Chem Soc 73:373–380. doi:10.1021/ja01145a126
Berthold A, Cremer K, Kreuter J (1996) Preparation and characterization of chitosan microspheres as drug carrier for prednisolone sodium phosphate as model for anti-inflammatory drugs. J Control Release 39:17–25. doi:10.1016/0168-3659(95)00129-8
Brunauer S, Emmett PH, Teller E (1938) Adsorption of gases in multimolecular layers. J Am Chem Soc 60:309–319. doi:10.1021/ja01269a023
Buchtová N, Réthoré G, Boyer C et al (2013) Nanocomposite hydrogels for cartilage tissue engineering: mesoporous silica nanofibers interlinked with siloxane derived polysaccharide. J Mater Sci 24:1875–1884. doi:10.1007/s10856-013-4951-0
Burdick JA, Prestwich GD (2011) Hyaluronic acid hydrogels for biomedical applications. Adv Mater 23:H41–H56. doi:10.1002/adma.201003963
Calvert P (2001) Inkjet printing for materials and devices. Chem Mater 13:3299–3305. doi:10.1021/cm0101632
Chao C, Liu J, Wang J et al (2013) Surface modification of halloysite nanotubes with dopamine for enzyme immobilization. ACS Appl Mater Interfaces 5:10559–10564. doi:10.1021/am4022973
Chen M, Liu X, Fahr A (2011) Skin penetration and deposition of carboxyfluorescein and temoporfin from different lipid vesicular systems: in vitro study with finite and infinite dosage application. Int J Pharm 408:223–234. doi:10.1016/j.ijpharm.2011.02.006
Collins MN, Birkinshaw C (2013) Hyaluronic acid based scaffolds for tissue engineering—a review. Carbohydr Polym 92:1262–1279. doi:10.1016/j.carbpol.2012.10.028
Connell LS, Romer F, Suárez M et al (2014) Chemical characterisation and fabrication of chitosan–silica hybrid scaffolds with 3-glycidoxypropyl trimethoxysilane. J Mater Chem B 2:668. doi:10.1039/c3tb21507e
Deen I, Zhitomirsky I (2014) Electrophoretic deposition of composite halloysite nanotube–hydroxyapatite–hyaluronic acid films. J Alloys Compd 586(1):S531–S534. doi:10.1016/j.jallcom.2013.01.088
Du M, Guo B, Jia D (2010) Newly emerging applications of halloysite nanotubes: a review. Polym Int 59:574–582
Duarte HA, Lourenco MP, Heine T, Guimares L (2012) Clay mineral nanotubes: stability, structure and properties. INTECH Open Access Publisher, Rijeka
Dulbecco R, Vogt M (1954) Plaque formation and isolation of pure lines with poliomyelitis viruses. J Exp Med 99:167–182
Falcone SJ, Berg RA (2008) Crosslinked hyaluronic acid dermal fillers: a comparison of rheological properties. J Biomed Mater Res A 87:264–271. doi:10.1002/jbm.a.31675
Forster S, Thumser AE, Hood SR, Plant N (2012) Characterization of rhodamine-123 as a tracer dye for use in in vitro drug transport assays. PLoS ONE 7:e33253. doi:10.1371/journal.pone.0033253
Fox JD, Capadona JR, Marasco PD, Rowan SJ (2013) Bioinspired water-enhanced mechanical gradient nanocomposite films that mimic the architecture and properties of the squid beak. J Am Chem Soc 135:5167–5174. doi:10.1021/ja4002713
Ghebaur A, Garea SA, Iovu H (2012) New polymer–halloysite hybrid materials—potential controlled drug release system. Int J Pharm 436:568–573. doi:10.1016/j.ijpharm.2012.07.014
Ghorai S, Sarkar A, Panda AB, Pal S (2013) Evaluation of the flocculation characteristics of polyacrylamide grafted xanthan gum/silica hybrid nanocomposite. Ind Eng Chem Res 52:9731–9740. doi:10.1021/ie400550m
Gu BK, Park SJ, Kim MS et al (2013) Fabrication of sonicated chitosan nanofiber mat with enlarged porosity for use as hemostatic materials. Carbohydr Polym 97:65–73. doi:10.1016/j.carbpol.2013.04.060
Ha DI, Lee SB, Chong MS et al (2006) Preparation of thermo-responsive and injectable hydrogels based on hyaluronic acid and poly(N-isopropylacrylamide) and their drug release behaviors. Macromol Res 14:87–93. doi:10.1007/BF03219073
Habibi Y, Dufresne A (2008) Highly filled bionanocomposites from functionalized polysaccharide nanocrystals. Biomacromolecules 9:1974–1980. doi:10.1021/bm8001717
Haxaire K, Marechal Y, Milas M, Rinaudo M (2003) Hydration of polysaccharide hyaluronan observed by IR spectrometry. I. Preliminary experiments and band assignments. Biopolymers 72:10–20. doi:10.1002/bip.10245
Hejazi R, Amiji M (2003) Chitosan-based gastrointestinal delivery systems. J Control Release 89:151–165. doi:10.1016/S0168-3659(03)00126-3
Horcajada P, Chalati T, Serre C et al (2010) Porous metal-organic-framework nanoscale carriers as a potential platform for drug delivery and imaging. Nat Mater 9:172–178. doi:10.1038/nmat2608
Issa MM, Köping-Höggård M, Artursson P (2005) Chitosan and the mucosal delivery of biotechnology drugs. Drug Discov Today 2:1–6. doi:10.1016/j.ddtec.2005.05.008
Jayakumar R, Menon D, Manzoor K et al (2010a) Biomedical applications of chitin and chitosan based nanomaterials—a short review. Carbohydr Polym 82:227–232. doi:10.1016/j.carbpol.2010.04.074
Jayakumar R, Prabaharan M, Nair SV, Tamura H (2010b) Novel chitin and chitosan nanofibers in biomedical applications. Biotechnol Adv 28:142–150. doi:10.1016/j.biotechadv.2009.11.001
Joussein E, Petit S, Churchman J et al (2005) Halloysite clay minerals—a review. Clay Miner 40:383–426. doi:10.1180/0009855054040180
Kaur S, Dhillon GS (2014) The versatile biopolymer chitosan: potential sources, evaluation of extraction methods and applications. Crit Rev Microbiol 40:155–175. doi:10.3109/1040841X.2013.770385
Kean T, Thanou M (2010) Biodegradation, biodistribution and toxicity of chitosan. Adv Drug Deliv Rev 62:3–11. doi:10.1016/j.addr.2009.09.004
Khoo WS, Ismail H, Ariffin A (2012) Tensile, swelling, and oxidative degradation properties of crosslinked polyvinyl alcohol/chitosan/halloysite nanotube composites. Int J Polym Mater 62:390–396. doi:10.1080/00914037.2012.719133
Kulterer MR, Reichel VE, Kargl R et al (2012) Functional polysaccharide composite nanoparticles from cellulose acetate and potential applications. Adv Funct Mater 22:1749–1758. doi:10.1002/adfm.201102350
Lee H, Lee K, Park TG (2008) Hyaluronic acid–paclitaxel conjugate micelles: synthesis, characterization, and antitumor activity. Bioconjug Chem 19:1319–1325. doi:10.1021/bc8000485
Levis SR, Deasy PB (2002) Characterisation of halloysite for use as a microtubular drug delivery system. Int J Pharm 243:125–134
Levis SR, Deasy PB (2003) Use of coated microtubular halloysite for the sustained release of diltiazem hydrochloride and propranolol hydrochloride. Int J Pharm 253:145–157
Liu Tsang V, Bhatia SN (2004) Three-dimensional tissue fabrication. Adv Drug Deliv Rev 56:1635–1647. doi:10.1016/j.addr.2004.05.001
Liu M, Zhang Y, Wu C et al (2012) Chitosan/halloysite nanotubes bionanocomposites: structure, mechanical properties and biocompatibility. Int J Biol Macromol 51:566–575. doi:10.1016/j.ijbiomac.2012.06.022
Liu M, Wu C, Jiao Y et al (2013) Chitosan–halloysite nanotubes nanocomposite scaffolds for tissue engineering. J Mater Chem B 1:2078–2089. doi:10.1039/C3TB20084A
Liu M, Shen Y, Ao P et al (2014) The improvement of hemostatic and wound healing property of chitosan by halloysite nanotubes. RSC Adv 4:23540–23553. doi:10.1039/C4RA02189D
Lvov YM, Shchukin DG, Möhwald H, Price RR (2008) Halloysite clay nanotubes for controlled release of protective agents. ACS Nano 2:814–820
Marney DCO, Yang W, Russell LJ et al (2012) Phosphorus intercalation of halloysite nanotubes for enhanced fire properties of polyamide 6. Polym Adv Technol 23:1564–1571. doi:10.1002/pat.3030
Massaro M, Riela S, Cavallaro G et al (2014) Eco-friendly functionalization of natural halloysite clay nanotube with ionic liquids by microwave irradiation for Suzuki coupling reaction. J Organomet Chem 749:410–415. doi:10.1016/j.jorganchem.2013.10.044
Mi F-L, Tan Y-C, Liang H-F, Sung H-W (2002) In vivo biocompatibility and degradability of a novel injectable-chitosan-based implant. Biomaterials 23:181–191. doi:10.1016/S0142-9612(01)00094-1
Murugan R, Ramakrishna S (2004) Bioresorbable composite bone paste using polysaccharide based nano hydroxyapatite. Biomaterials 25:3829–3835. doi:10.1016/j.biomaterials.2003.10.016
Ortona O, D’Errico G, Mangiapia G, Ciccarelli D (2008) The aggregative behavior of hydrophobically modified chitosans with high substitution degree in aqueous solution. Carbohydr Polym 74:16–22. doi:10.1016/j.carbpol.2008.01.009
Pandey S, Goswami GK, Nanda KK (2013) Green synthesis of polysaccharide/gold nanoparticle nanocomposite: an efficient ammonia sensor. Carbohydr Polym 94:229–234. doi:10.1016/j.carbpol.2013.01.009
Price R, Gaber BP, Lvov Y (2001) In-vitro release characteristics of tetracycline HCl, khellin and nicotinamide adenine dineculeotide from halloysite; a cylindrical mineral. J Microencapsul 18:713–722. doi:10.1080/02652040010019532
Ritger PL, Peppas NA (1987a) A simple equation for description of solute release I. Fickian and non-fickian release from non-swellable devices in the form of slabs, spheres, cylinders or discs. J Control Release 5:23–36. doi:10.1016/0168-3659(87)90034-4
Ritger PL, Peppas NA (1987b) A simple equation for description of solute release II. Fickian and anomalous release from swellable devices. J Control Release 5:37–42. doi:10.1016/0168-3659(87)90035-6
Roig-Roig F, Solans C, Esquena J, García-Celma MJ (2013) Preparation, characterization, and release properties of hydrogels based on hyaluronan for pharmaceutical and biomedical use. J Appl Polym Sci 130:1377–1382. doi:10.1002/app.39306
Roldo M, Fatouros DG (2011) Chitosan-derivative based hydrogels as drug delivery platforms: applications in drug delivery and tissue engineering. In: Zilberman M (ed) Act. Implants scaffolds tissue regen. Springer, Berlin, pp 351–376
Ruiz-Hitzky E, Van Meerbeek A (2006) Chapter 10.3 clay mineral- and organoclay-polymer nanocomposite. In: Bergaya F, Theng BKG, Lagaly G (eds) Developments in clay science. Elsevier, Amsterdam, pp 583–621
Ruiz-Hitzky E, Darder M, Fernandes FM et al (2013) Fibrous clays based bionanocomposites. Prog Polym Sci 38:1392–1414. doi:10.1016/j.progpolymsci.2013.05.004
Ryan G, Pandit A, Apatsidis DP (2006) Fabrication methods of porous metals for use in orthopaedic applications. Biomaterials 27:2651–2670. doi:10.1016/j.biomaterials.2005.12.002
Shchukin DG, Möhwald H (2011) Smart nanocontainers as depot media for feedback active coatings. Chem Commun 47:8730. doi:10.1039/c1cc13142g
Shchukin DG, Sukhorukov GB, Price RR, Lvov YM (2005) Halloysite nanotubes as biomimetic nanoreactors. Small 1:510–513
Shingel KI, Marchessault RH (2006) Iron-polysaccharide composites for pharmaceutical applications. Polysacch Drug Deliv Pharm Appl 934:271–287
Stodolak E, Paluszkiewicz C, Bogun M, Blazewicz M (2009) Nanocomposite fibres for medical applications. J Mol Struct 924–926:208–213. doi:10.1016/j.molstruc.2009.01.018
Sudina ML, Braga CRC, Marcus VL et al (2012) Application of infrared spectroscopy to analysis of chitosan/clay nanocomposites. InTech, Rijeka, pp 43–62
Suh DJ, Lim YT, Park OO (2000) The property and formation mechanism of unsaturated polyester–layered silicate nanocomposite depending on the fabrication methods. Polymer 41:8557–8563. doi:10.1016/S0032-3861(00)00216-0
Travan A, Marsich E, Donati I et al (2011) Silver–polysaccharide nanocomposite antimicrobial coatings for methacrylic thermosets. Acta Biomater 7:337–346. doi:10.1016/j.actbio.2010.07.024
Vallés-Lluch A, Poveda-Reyes S, Amorós P et al (2013) Hyaluronic acid-silica nanohybrid gels. Biomacromolecules 14:4217–4225. doi:10.1021/bm401041z
Veerabadran NG, Price RR, Lvov YM (2007) Clay nanotubes for encapsulation and sustained release of drugs. NANO 2:115–120
Vergaro V, Abdullayev E, Lvov YM et al (2010) Cytocompatibility and uptake of halloysite clay nanotubes. Biomacromolecules 11:820–826
Verma NK, Moore E, Blau W et al (2012) Cytotoxicity evaluation of nanoclays in human epithelial cell line A549 using high content screening and real-time impedance analysis. J Nanoparticle Res 14:1–11. doi:10.1007/s11051-012-1137-5
Wang Q, Zhang J, Zheng Y, Wang A (2014) Adsorption and release of ofloxacin from acid- and heat-treated halloysite. Colloids Surf B 113:51–58. doi:10.1016/j.colsurfb.2013.08.036
Ward CJ, Song S, Davis EW (2010) Controlled release of tetracycline-hcl from halloysite-polymer composite films. J Nanosci Nanotechnol 10:6641–6649. doi:10.1166/jnn.2010.2647
Yuan P, Southon PD, Liu Z et al (2008) Functionalization of halloysite clay nanotubes by grafting with γ-aminopropyltriethoxysilane. J Phys Chem C 112:15742–15751. doi:10.1021/jp805657t
Zhao Y, Wang S, Guo Q et al (2013) Hemocompatibility of electrospun halloysite nanotube- and carbon nanotube-doped composite poly(lactic-co-glycolic acid) nanofibers. J Appl Polym Sci 127:4825–4832. doi:10.1002/app.38054
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CSGI is acknowledged for financial support. Stefano Spezzani (Imerys Tiles Minerals Italia s.r.l.) is acknowledged for kindly providing HNT samples.
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Del Buffa, S., Grifoni, E., Ridi, F. et al. The effect of charge on the release kinetics from polysaccharide–nanoclay composites. J Nanopart Res 17, 146 (2015). https://doi.org/10.1007/s11051-015-2947-z
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DOI: https://doi.org/10.1007/s11051-015-2947-z