Abstract
Collagen hydrogel applications in tissue engineering are limited due to its weak physical and mechanical properties, e.g. loss of water, destruction in the biological medium, weak mechanical properties, and handling difficulty. To improve the physical and mechanical properties of collagen hydrogel, cellulose nanofibers (CNF) were introduced to the collagen hydrogel. Up to 8% CNF, by total dry weight, was added to cold collagen acidic solution and the solution underwent gel formation by increasing pH and temperature to 7.4 and 37 °C, respectively. The gelation time was decreased when CNF was added to the collagen solution. The scanning electron microscopy images of collagen/CNF nanocomposites illustrated porous morphology with larger pore and denser nanofibrous structure than pure collagen. More water retention ability of collagen/CNF hydrogels along with lower hydrolytic degradation rate indicated higher stability of CNF composite hydrogels than pure collagen hydrogel. Mechanical testing demonstrated enhancement in both compression strength and fracture strain when CNF was added to the collagen hydrogel. The presence of free CNF and possible interactions between collagen and CNF was demonstrated by thermogravimetric and Fourier-transform infrared analysis. While the stability and mechanical properties of collagen hydrogel was enhanced by adding CNF, the MTT assay revealed the same cell viability for collagen/CNF scaffold as collagen. Furthermore, the live-dead assay demonstrated excellent capability of CNF nanocomposite for cell 3D culturing.
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Abou Neel EA, Cheema U, Knowles JC, Brown RA, Nazhat SN (2006) Use of multiple unconfined compression for control of collagen gel scaffold density and mechanical properties. Soft Matter 2(11):986–992. https://doi.org/10.1039/b609784g
Ahmed E-F, Jae Ho L, Eun-Jung L, Hae-Won K (2013) Collagen hydrogels incorporated with surface-aminated mesoporous nanobioactive glass: improvement of physicochemical stability and mechanical properties is effective for hard tissue engineering. Acta Biomater 9(12):9508–9521. https://doi.org/10.1016/j.actbio.2013.07.036
Antoine EE, Vlachos PP, Rylander MN (2014) Review of collagen I hydrogels for bioengineered tissue microenvironments: characterization of mechanics, structure, and transport. Tissue Eng Part B Rev 20(6):683–696
Arunan E, Desiraju GR, Klein RA, Sadlej J, Scheiner S, Alkorta I, Clary DC, Crabtree RH, Dannenberg JJ, Hobza P, Kjaergaard HG, Legon AC, Mennucci B, Nesbitt DJ (2011) Definition of the hydrogen bond (IUPAC Recommendations 2011). Pure Appl Chem 83(8):1637–1641. https://doi.org/10.1351/pac-rec-10-01-02
Bohlouli N, Mirzaei E, Ghanbari H, Sorkhabadi R, Mahdi S, Faridi-Majid R (2018) Reinforcing mechanical strength of electrospun chitosan nanofibrous scaffold using cellulose nanofibers. In: Journal of Nano Research. Trans Tech Publication, pp 71–79. https://doi.org/10.4028/www.scientific.net/JNanoR.52.71
Brown RA, Wiseman M, Chuo CB, Cheema U, Nazhat SN (2005) Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano-and microstructures by plastic compression. Adv Funct Mater 15(11):1762–1770. https://doi.org/10.1002/adfm.200500042
Cheng Y, Lu J, Liu S, Zhao P, Lu G, Chen J (2014) The preparation, characterization and evaluation of regenerated cellulose/collagen composite hydrogel films. Carbohydr Polym 107:57–64. https://doi.org/10.1016/j.carbpol.2014.02.034
De France KJ, Hoare T, Cranston ED (2017) Review of hydrogels and aerogels containing nanocellulose. Chem Mater 29(11):4609–4631. https://doi.org/10.1021/acs.chemmater.7b00531
Delgado LM, Bayon Y, Pandit A, Zeugolis DI (2015) To cross-link or not to cross-link? Cross-linking associated foreign body response of collagen-based devices. Tissue Eng Part B Rev 21(3):298–313. https://doi.org/10.1089/ten.teb.2014.0290
Dong C, Lv Y (2016) Application of collagen scaffold in tissue engineering: recent advances and new perspectives. Polymers 8(2):42. https://doi.org/10.3390/polym8020042
El Miri N, Abdelouahdi K, Barakat A, Zahouily M, Fihri A, Solhy A, El Achaby M (2015) Bio-nanocomposite films reinforced with cellulose nanocrystals: rheology of film-forming solutions, transparency, water vapor barrier and tensile properties of films. Carbohydr Polym 129:156–167. https://doi.org/10.1016/j.carbpol.2015.04.051
El-Fiqi A, Lee JH, Lee E-J, Kim H-W (2013) Collagen hydrogels incorporated with surface-aminated mesoporous nanobioactive glass: improvement of physicochemical stability and mechanical properties is effective for hard tissue engineering. Acta Biomater 9(12):9508–9521. https://doi.org/10.1016/j.actbio.2013.07.036
Fadaie M, Mirzaei E, Geramizadeh B, Asvar Z (2018) Incorporation of nanofibrillated chitosan into electrospun PCL nanofibers makes scaffolds with enhanced mechanical and biological properties. Carbohydr Polym 199:628–640. https://doi.org/10.1016/j.carbpol.2018.07.061
Gupta D, Tator CH, Shoichet MS (2006) Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 27(11):2370–2379. https://doi.org/10.1016/j.biomaterials.2005.11.015
Habibi Y, Goffin A-L, Schiltz N, Duquesne E, Dubois P, Dufresne A (2008) Bionanocomposites based on poly(ε-caprolactone)-grafted cellulose nanocrystals by ring-opening polymerization. J Mater Chem 18(41):5002–5010. https://doi.org/10.1039/b809212e
Helary C, Bataille I, Abed A, Illoul C, Anglo A, Louedec L, Letourneur D, Meddahi-Pellé A, Giraud-Guille MM (2010) Concentrated collagen hydrogels as dermal substitutes. Biomaterials 31(3):481–490. https://doi.org/10.1016/j.biomaterials.2009.09.073
Hesse E, Hefferan TE, Tarara JE, Haasper C, Meller R, Krettek C, Lu L, Yaszemski MJ (2010) Collagen type I hydrogel allows migration, proliferation, and osteogenic differentiation of rat bone marrow stromal cells. J Biomed Mater Res Part A 94A(2):442–449. https://doi.org/10.1002/jbm.a.32696
Iafisco M, Foltran I, Sabbatini S, Tosi G, Roveri N (2012) Electrospun nanostructured fibers of collagen-biomimetic apatite on titanium alloy. Bioinorg Chem Appl 2012:8. https://doi.org/10.1155/2012/123953
Ji C, Annabi N, Khademhosseini A, Dehghani F (2011) Fabrication of porous chitosan scaffolds for soft tissue engineering using dense gas CO2. Acta Biomater 7(4):1653–1664. https://doi.org/10.1016/j.actbio.2010.11.043
Ji Y-l, Wolfe PS, Rodriguez IA, Bowlin GL (2012) Preparation of chitin nanofibril/polycaprolactone nanocomposite from a nonaqueous medium suspension. Carbohydr Polym 87(3):2313–2319. https://doi.org/10.1016/j.carbpol.2011.10.066
Karimizade A, Sakine T, Mirzaei E (2018) Evaluating the effect of pH on mechanical strength and cell compatibility of nanostructured collagen hydrogel by the plastic compression method. Nanomed J 5(3):180–185. https://doi.org/10.22038/nmj.2018.005.0008
Li W, Lan Y, Guo R, Zhang Y, Xue W, Zhang Y (2015) In vitro and in vivo evaluation of a novel collagen/cellulose nanocrystals scaffold for achieving the sustained release of basic fibroblast growth factor. J Biomater Appl 29(6):882–893. https://doi.org/10.1177/0885328214547091
Lin S, Gu L (2015) Influence of crosslink density and stiffness on mechanical properties of type I collagen gel. Materials 8(2):551–560. https://doi.org/10.3390/ma8020551
Mathew AP, Oksman K, Pierron D, Harmad M-F (2012) Crosslinked fibrous composites based on cellulose nanofibers and collagen with in situ pH induced fibrillation. Cellulose 19(1):139–150. https://doi.org/10.1007/s10570-011-9624-x
Mathew AP, Oksman K, Pierron D, Harmand M-F (2013) biocompatible fibrous networks of cellulose nanofibres and collagen crosslinked using genipin: potential as artificial ligament/tendons. Macromol Biosci 13(3):289–298. https://doi.org/10.1002/mabi.201200317
Moraes PRFdS, Saska S, Barud H, Lima LRd, Martins VdCA, Plepis AMdG, Ribeiro SJL, Gaspar AMM (2016) Bacterial cellulose/collagen hydrogel for wound healing. Mater Res 19(1):106–116
Nguyen D, Hägg DA, Forsman A, Ekholm J, Nimkingratana P, Brantsing C, Kalogeropoulos T, Zaunz S, Concaro S, Brittberg M, Lindahl A, Gatenholm P, Enejder A, Simonsson S (2017) Cartilage tissue engineering by the 3D bioprinting of IPS cells in a nanocellulose/alginate bioink. Sci Rep 7(1):658. https://doi.org/10.1038/s41598-017-00690-y
Nöth U, Rackwitz L, Heymer A, Weber M, Baumann B, Steinert A, Schütze N, Jakob F, Eulert J (2007) Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. J Biomed Mater Res Part A 83A(3):626–635. https://doi.org/10.1002/jbm.a.31254
Pietrucha K (2015) Development of collagen cross-linked with dialdehyde cellulose as a potential 3D scaffold for neural tissue engineering. In: 6th European conference of the international federation for medical and biological engineering. Springer, Cham, pp 349–352
Ragab TI, Wasfy A, Amer H, El-Gendi A, Abdel-Hady M, Liebner F (2014) Synthesis of cellulose acetate membrane from the Egyptian rice straws. J Appl Sci 14(24):3424–3435
Rajan N, Habermehl J, Cote MF, Doillon CJ, Mantovani D (2006) Preparation of ready-to-use, storable and reconstituted type I collagen from rat tail tendon for tissue engineering applications. Nat Protoc 1(6):2753–2758. https://doi.org/10.1038/nprot.2006.430
Rizwan M, Hamdi M, Basirun W (2017) Bioglass® 45S5-based composites for bone tissue engineering and functional applications. J Biomed Mater Res Part A 105(11):3197–3223. https://doi.org/10.1002/jbm.a.36156
Saska S, Teixeira LN, Tambasco de Oliveira P, Minarelli Gaspar AM, Lima Ribeiro SJ, Messaddeq Y, Marchetto R (2012a) Bacterial cellulose-collagen nanocomposite for bone tissue engineering. J Mater Chem 22(41):22102–22112. https://doi.org/10.1039/c2jm33762b
Saska S, Teixeira LN, de Oliveira PT, Gaspar AM, Ribeiro SJ, Messaddeq Y, Marchetto R (2012b) Bacterial cellulose-collagen nanocomposite for bone tissue engineering. J Mater Chem. https://doi.org/10.1039/C2JM33762B
Shin SR, Zihlmann C, Akbari M, Assawes P, Cheung L, Zhang K, Manoharan V, Zhang YS, Yüksekkaya M, Wan K-t, Nikkhah M, Dokmeci MR, Tang X, Khademhosseini A (2016) Reduced graphene oxide-GelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small 12(27):3677–3689. https://doi.org/10.1002/smll.201600178
Takallu S, Mirzaei E, Azadi A, Karimizade A, Tavakol S (2019) Plate-shape carbonated hydroxyapatite/collagen nanocomposite hydrogel via in situ mineralization of hydroxyapatite concurrent with gelation of collagen at pH = 7.4 and 37°C. J Biomed Mater Res B Appl Biomater 107(6):1920–1929. https://doi.org/10.1002/jbm.b.34284
Wahl DA, Czernuszka JT (2006) Collagen-hydroxyapatite composites for hard tissue repair. Eur Cells Mater 11:43–56. https://doi.org/10.22203/eCM.v011a06
Wang Y, Chen L (2011) Impacts of nanowhisker on formation kinetics and properties of all-cellulose composite gels. Carbohydr Polym 83(4):1937–1946. https://doi.org/10.1016/j.carbpol.2010.10.071
Wang J, Wei L, Ma Y, Li K, Li M, Yu Y, Wang L, Qiu H (2013) Collagen/cellulose hydrogel beads reconstituted from ionic liquid solution for Cu(II) adsorption. Carbohydr Polym 98(1):736–743. https://doi.org/10.1016/j.carbpol.2013.06.001
Wang M, Li X, Hua W, Deng L, Li P, Zhang T, Wang X (2018) Superelastic three-dimensional nanofiber-reconfigured spongy hydrogels with superior adsorption of lanthanide ions and photoluminescence. Chem Eng J 348:95–108. https://doi.org/10.1016/j.cej.2018.04.135
Yu X, Tang C, Xiong S, Yuan Q, Gu Z, Li Z, Hu Y (2016) Modification of collagen for biomedical applications: a review of physical and chemical methods. Curr Org Chem 20(17):1797–1812
Yue Y, Han J, Han G, French AD, Qi Y, Wu Q (2016) Cellulose nanofibers reinforced sodium alginate-polyvinyl alcohol hydrogels: core–shell structure formation and property characterization. Carbohydr Polym 147:155–164. https://doi.org/10.1016/j.carbpol.2016.04.005
Zhang M, Ding C, Chen L, Huang L (2014) The preparation of cellulose/collagen composite films using 1-ethyl-3-methylimidazolium acetate as a solvent. BioResources 9(1):756–771
Zhao LZ, Zhou CH, Wang J, Tong DS, Yu WH, Wang H (2015) Recent advances in clay mineral-containing nanocomposite hydrogels. Soft Matter 11(48):9229–9246. https://doi.org/10.1039/c5sm01277e
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This project was financially supported by Shiraz University of Medical Sciences (SUMS), Shiraz, Iran (Grant No. 97-01-74-18851).
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Lohrasbi, S., Mirzaei, E., Karimizade, A. et al. Collagen/cellulose nanofiber hydrogel scaffold: physical, mechanical and cell biocompatibility properties. Cellulose 27, 927–940 (2020). https://doi.org/10.1007/s10570-019-02841-y
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DOI: https://doi.org/10.1007/s10570-019-02841-y