Nanofibrillated cellulose, obtained from rice straw agricultural wastes was used as a substrate for the preparation of a new injectable and mineralized hydrogel for bone regeneration. Tetramethyl pyridine oxyl (TEMPO) oxidized nanofibrillated cellulose, was mineralized through the incorporation of a prepared and characterized biphasic calcium phosphate at a fixed ratio of 50 wt%. The TEMPO-oxidized rice straw nanofibrillated cellulose was characterized using transmission electron microscopy, Fourier transform infrared, and carboxylic content determination. The injectability and viscosity of the prepared hydrogel were evaluated using universal testing machine and rheometer testing, respectively. Cytotoxicity and alkaline phosphatase level tests on osteoblast like-cells for in vitro assessment of the biocompatibility were investigated. Results revealed that the isolated rice straw nanofibrillated cellulose is a nanocomposite of the cellulose nanofibers and silica nanoparticles. Rheological properties of the tested materials are suitable for use as injectable material and of nontoxic effect on osteoblast-like cells, as revealed by the positive alkaline phosphate assay. However, nanofibrillated cellulose/ biphasic calcium phosphate hydrogel showed higher cytotoxicity and lower bioactivity test results when compared to that of nanofibrillated cellulose.
KopečekJ.Hydrogel biomaterials: a smart future?Biomaterials2007;
28: 5185–5192.
2.
ChangC andZhangL.Cellulose-based hydrogels: present status and application prospects. Carbohydr Polym2011;
84: 40–53.
3.
KlemmDPhilippBHeinzeTet al.Comprehensive cellulose chemistry, fundamentals and analytical methods (
Vol.1).
New York, NY:
Wiley-VCH, 1998.
4.
YaoWR andXuQH.Research progress in nanocellulose preparation. AMR2014;
988: 101–105.
5.
KlemmDKramerFMoritzSet al.
Nanocelluloses: a new family of nature-based materials. Angew Chem Int Ed2011;
50: 5438–5466.
6.
SiroI andPlackettD.Microfibrillated cellulose and new nanocomposite materials: a review. Cellulose2010;
17: 459–494.
7.
SaitoTKimuraSNishiyamaYet al.
Cellulose nanofibers prepared by TEMPO-mediated oxidation of native cellulose. Biomacromolecules2007;
8: 2485–2491.
8.
DamienCJ andParsonsJR.Bone-graft and bone-graft substitutes: a review of current technology and applications. J Appl Biomater1991;
2: 187–208.
9.
HammerleCHFOlahAJSchmidJet al.
The biological effect of natural bone mineral on bone neoformation on the rabbit skull. Clin Oral Implants Res1997;
8: 198–207.
10.
DaculsiGLeGerosRZHeugheaertMet al.
Formation of carbonate apatite apatite crystals after implantation of calcium phosphate ceramics. Calcif Tissue Int1990;
46: 20–27.
11.
ValloCIMontemartiniPEFanovichMAet al.
Polymethylmethacrylate-based bone cement modified with hydroxyapatite. J Biomed Mater Res: Appl Biomater1999;
48: 150–158.
12.
HarperEJ.Bioactive bone cements. Proc Inst Mech Eng H1998;
212: 113–120.
13.
QuPWangXCuiXXet al.
Biomimetic mineralization of rod-like cellulose nano-whiskers and spectrum analysis. Guang Pu Xue Yu Guang Pu Fen Xi/Spectrosc Spectral Anal2012;
5: 1418–1422.
14.
QuPZhangXZhouYet al.
Biomimetic synthesis of hydroxyapatite on cellulose nanofibrils and its application. Sci Adv Mater2012; 4: 187–192.
15.
KhripunovAKBaklaginaYGSinyaevVAet al.
Investigation of nanocomposites based on hydrated calcium phosphates and cellulose Acetobacter xylinum. Glass Phys Chem2008;
2: 192–200.
16.
YinNChenSYOuyangYet al.
Biomimetic mineralization synthesis of hydroxyapatite bacterial cellulose nanocomposites. Prog Nat Sci: Mater Int2011;
6: 472–477.
17.
ZimmermannKALeblancJMSheetsKTet al.
Biomimetic design of a bacterial cellulose/hydroxyapatite nanocomposite for bone healing applications. Mater Sci Eng C2011;
1: 43–49.
18.
SaskaSBarudHSGasparAMMet al.
Bacterial cellulose-hydroxyapatite nanocomposites for bone regeneration. Int J Biomater2011;
2011: 1753621–1753628.
19.
KondiahPJChoonaraYEKondiahPPDet al.
A review of injectable polymeric hydrogel systems for application in bone tissue engineering. Molecules2016;
21: 1580.
20.
HassanML.Bagasse and rice straw nanocellulosic materials and their applications. In: PandeyJTakagiHNakagaitoAet al. (eds) Handbook of polymer nanocomposites. processing, performance and application.
Berlin, Heidelberg, Germany:
Springer, 2015, pp. 47–64.
21.
ZhangSGuoYDongYet al.
A novel nanosilver/nanosilica hydrogel for bone regeneration in infected bone defects. ACS Appl Mater Interfac2016;
8: 13242–13250.
22.
GaihreBLecka-CzernikBJayasuriyaACet al.
Injectable nanosilica–chitosan microparticles for bone regeneration applications. J Biomater Appl2018;
32: 813–825.
23.
KimMHKimBSParkHet al.
Injectable methylcellulose hydrogel containing calcium phosphate nanoparticles for bone regeneration.Int J Biol Macromol2018;
109: 57–64.
SongSHYunYPKimHJet al.
Bone formation in a rat tibial defect model using carboxymethyl cellulose/BioC/bone morphogenic protein-2 hybrid materials. Biomed Res Int2014;
2014: 230152.
26.
De FreitasDGOsthuesRM andDa SilvaSN.Study of the cytotoxicity of a composite of carboxymethylcellulose (CMC) and a BioCeramic (biphasic calcium phosphate-BCP) injection for use in articular cartilage repair. Key Eng Mater2012;
493: 703–708.
27.
StruillouXBoutignyHBadranZet al.
Treatment of periodontal defects in dogs using an injectable composite hydrogel/biphasic calcium phosphate.J Mater Sci: Mater Med2011;
22: 1707–1717.
28.
DaculsiGUzelAPWeissPet al.
Developments in injectable multiphasic biomaterials. The performance of microporous biphasic calcium phosphate granules and hydrogels. J Mater Sci: Mater Med2010;
21: 855–861.
29.
FatimiA.Rheological behavior of biomaterials for osteoarticular and dental tissue engineering: synthetic extracellular matrix and calcium phosphate suspensions [Comportement rhéologique de biomatériaux pour l'ingénierie ostéoarticulaire et dentaire: matrices extracellulaires synthétiques et suspensions phosphocalciques]. IRBM2009;
30: 139–140.
30.
FellahBHWeissPGauthierOet al.
Bone repair using a new injectable self-crosslinkable bone substitute.J Orthop Res2006;
24: 628–635.
31.
TrojaniCBoukhechbaFScimecaJCet al.
Ectopic bone formation using an injectable biphasic calcium phosphate/Si-HPMC hydrogel composite loaded with undifferentiated bone marrow stromal cells. Biomaterials2006;
27: 3256–3264.
32.
LiuWZhangJRethoreGet al.
A novel injectable, cohesive and toughened Si-HPMC (silanized-hydroxypropyl methylcellulose) composite calcium phosphate cement for bone substitution. Acta Biomater2014;
10: 3335–3345.
33.
WiseLEMurphyM andD’addiecoAA.Chlorite holocellulose, its fractionation and bearing on summative wood analysis and studies on the hemicelluloses. Pap Trade J1946;
122: 35–43.
34.
BrowningBL.Methods of wood chemistry.
Vol. 2.
New York:
Wiley, 1967, p. 489.
35.
JungSCChongPC andSangHR.Bioactivity and osteoconductivity of biphasic calcium phosphates. Bioceram Dev Appl2011; 1:1–3.
36.
Khairoun IBoltongMGDriessensFCMet al.
Some factors controlling the injectability of calcium phosphate bone cements. J Mater Sci Mater Med1998;
9: 425–428.
37.
ISO 7886-3:2005. Sterile hypodermic syringes for single use—part 3: auto-disable syringes for fixed-dose immunization.
38.
NonoyamaTOgasawaraHTanakaMet al.
Calcium phosphate biomineralization in peptide hydrogels for injectable bone-filling materials. Soft Mater2012;
8: 11531–11536.
39.
IvanovaNVKorolenkoEAKorolikEVet al.
IR spectrum of cellulose. J Appl Spectrosc1989;
51: 847–851.
40.
LiouTH.Preparation and characterization of nano-structured silica from rice husk. Mater Sci Eng2004;
364: 313–323.
41.
LiuYGuoYZhuYet al.
A sustainable route for the preparation of activated carbon and silica from rice husk ash. J Hazard Mater2011;
186: 1314–1319.
42.
KalapathyUProctorA andShultzJ.A simple method for production of pure silica from rice hull ash. Bioresour Technol2000;
73: 257–262.
43.
ChaudhryAAHaqueSKelliciSet al.
Instant nano-hydroxyapatite: a continuous and rapid hydrothermal synthesis. Chem Commun2006;
21: 2286–2288.
44.
ZuidemaJMRivetCJGilbertRJet al.
A protocol for rheological characterization of hydrogels for tissue engineering strategies. J Biomed Mater Res Part Res2014;
102B: 1063–1073.
45.
BakotaELWangYDaneshFRet al.
Injectable multidomain peptide nanofiber hydrogel as a delivery agent for stem cell secretome. Biomacromolecules2011;
12: 1651–1657.
46.
BerridgeMVHerstPM andTanAS.Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev2005;
11: 127–152.
47.
MosmannT.Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods1983;
65: 55–63.
48.
IgnjatovićNNinkovPKojićVet al.
Cytotoxicity and fibroblast properties during in vitro test of biphasic calcium phosphate/poly-dl-lactide-co-glycolide (BCP/DLPLG) composite biomaterials suitable for bone tissue reparation. Microsc Res Tech2006;
69: 976–982.
49.
PiccininiMSglavoVM andBucciottiF. Synthetic porous calcium phosphate granules for bone substitutes. In: 20th EAO annual scientific congress, Athens, 2011.
50.
MalardOBoulerJMGuicheuxJet al.
Influence of biphasic calcium phosphate granulometry on bone ingrowth, ceramic resorption, and inflammatory reactions: preliminary in vitro and in vivo study. J Biomed Mater Res1999;
46: 103–111.
51.
WebleraGDZapatabMJMAgracLCet al.
Characterization and evaluation of cytotoxicity of biphasic calcium phosphate synthesized by a solid state reaction route. Curr Appl Phys2014;
14: 876–880.
52.
TamásLHuttováJMistrkIet al.
Effect of carboxymethyl chitin-glucan on the activity of some hydrolytic enzymes in maize plants. Chem Pap2002;
5: 326–329.
53.
LangePHMillanJLStigbrandTet al.
Placental alkaline phosphatase as a tumor marker for seminoma. Cancer Res1982;
8: 3244–3247.
54.
WeissPBohicSLapkowskiMet al.
Application of FT-IR microspectroscopy to the study of an injectable composite for bone and dental surgery. J Biomed Mater Res1998;
41: 167–170.
55.
SchiraldiCD'AgostinoAOlivaAet al.
Development of hybrid materials based on hydroxyethylmethacrylate as supports for improving cell adhesion and proliferation. Biomaterials2004;
25: 3645–3653.
