Abstract
Hybrid materials (HMs) based on a combination of bacterial cellulose (BC) and hydroxyapatite (HA) have demonstrated promising capabilities, especially for bone repair. The insertion of strontium into a BC/HA matrix has a role in the body related to bone remodeling. This study aimed to obtain HMs containing BC/HA doped with strontium ions (Sr2+) by two routes of synthesis, differing in the way strontium was inserted. The HMs produced were characterized to elucidate the morphology and metal/biopolymer interaction, and also strontium adsorption/desorption profiles were evaluated. The biomaterials produced were able to interact with Sr2+, showing a distinct adsorption/desorption profile for each material. BC/CaHA/Sr showed an ion exchange between Ca2+ present in hydroxyapatite by the Sr2+ in solution, characterized by mainly a physisorption mechanism. BC/SrAp demonstrated a chemical bond of Sr2+ on the BC surface by a chemisorption mechanism. The desorption study showed that the Sr release reached a plateau after 11 and 60 days and after 4 months, 91 and 6% of the adsorbed Sr2+ was released by BC/CaHA/Sr and BC/SrAp, respectively. These results suggest that the delivery of Sr2+ can be modulated during bone repair depending on the way Sr2+ is inserted into the hybrid matrix.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn SJ et al (2015) Characterization of hydroxyapatite-coated bacterial cellulose scaffold for bone tissue engineering. Biotechnol Bioprocess Eng 20:948–955. https://doi.org/10.1007/s12257-015-0176-z
Bhatnagar VM (1967) Infrared spectrum of strontium hydroxyapatit. Experientia 23:697–699. https://doi.org/10.1007/bf02154118
Brunauer S, Emmett PH, Teller E (1938) Adsorption of gases in multimolecular layers. J Am Chem Soc 60:309–319. https://doi.org/10.1021/ja01269a023
Cacicedo ML et al (2016) Modified bacterial cellulose scaffolds for localized doxorubicin release in human colorectal HT-29 cells. Colloids Surf B 140:421–429. https://doi.org/10.1016/j.colsurfb.2016.01.007
Capitani D, Crescenzi V, De Angelis AA, Segre AL (2001) Water in hydrogels. an nmr study of water/polymer interactions in weakly cross-linked chitosan networks. Macromolecules 34:4136–4144. https://doi.org/10.1021/ma002109x
Ceratti DR et al (2015) Critical effect of pore characteristics on capillary infiltration in mesoporous films. Nanoscale 7:5371–5382. https://doi.org/10.1039/c4nr03021d
Chen S et al (2009) Carboxymethylated-bacterial cellulose for copper and lead ion removal. J Hazard Mater 161:1355–1359. https://doi.org/10.1016/j.jhazmat.2008.04.098
Chen Y et al (2012) Role of calcium in metalloenzymes: effects of calcium removal on the axial ligation geometry and magnetic properties of the catalytic diheme center in MauG. Biochemistry 51:1586–1597. https://doi.org/10.1021/bi201575f
Doğan M et al (2006) Adsorption kinetics of maxilon blue GRL onto sepiolite from aqueous solutions. Chem Eng. J 124:89–101. https://doi.org/10.1016/j.cej.2006.08.016
Dolinina ES et al (2017) Effect of trehalose on structural state of bovine serum albumin adsorbed onto mesoporous silica and the protein release kinetics in vitro. Colloids Surf A 527:101–108. https://doi.org/10.1016/j.colsurfa.2017.05.014
Duarte EB et al (2015) Production of hydroxyapatite–bacterial cellulose nanocomposites from agroindustrial wastes. Cellulose 22:3177–3187. https://doi.org/10.1007/s10570-015-0734-8
Dufresne A (2012) Nanocellulose: from nature to high performance tailored materials. E-book. Walter de Gruyter, Berlin
Foresti ML, Vázquez A, Boury B (2017) Applications of bacterial cellulose as precursor of carbon and composites with metal oxide, metal sulfide and metal nanoparticles: a review of recent advances. Carbohydr Polym 157:447–467. https://doi.org/10.1016/j.carbpol.2016.09.008
Gea S et al (2011) Investigation into the structural, morphological, mechanical and thermal behaviour of bacterial cellulose after a two-step purification process. Bioresour Technol 102:9105–9110. https://doi.org/10.1016/j.biortech.2011.04.077
Grande CJ et al (2009) Nanocomposites of bacterial cellulose/hydroxyapatite for biomedical applications. Acta Biomater 5:1605–1615. https://doi.org/10.1016/j.actbio.2009.01.022
Heinze T, Liebert T, Koschella A (2014) Esterification of polysaccharides. Springer, Berlin
Henderson CMB et al (2016) X-ray absorption study of 3d transition-metals and Mg in glasses and analogue crystalline materials in A Fe 3 + Si 2 O 6 and A 2 X 2 + Si 5 O 12, where A = K, Rb, or Cs and X = Mg, Mn, Fe Co, Ni, Cu, or Zn. J Non-Cryst Solids 451:23–48. https://doi.org/10.1016/j.jnoncrysol.2016.05.016
Hestrin S, Schramm M (1954) Synthesis of cellulose by Acetobacte rxylinum. Preparation of freeze-dried cells capable of polymerizing glucose to cellulose. Biochem J 58:345–352
Hidalgo-Carrillo J et al (2010) A study on the potential application of natural phosphate in photocatalytic processes. J Colloid Interface Sci 344:475–481. https://doi.org/10.1016/j.jcis.2010.01.020
Hidalgo-Carrillo J et al (2012) XPS evidence for structure-performance relationship in selective hydrogenation of crotonaldehyde to crotyl alcohol on platinum systems supported on natural phosphates. J Colloid Interface Sci 382:67–73. https://doi.org/10.1016/j.jcis.2012.05.050
Hing KA (2005) Bioceramic bone graft substitutes: influence of porosity and chemistry. Int J App Ceram Technol 2:184–199. https://doi.org/10.1111/j.1744-7402.2005.02020.x
Hutchens S (2007). Characterization of a biomimetic calcium-deficient hydroxyapatite-bacterial cellulose composite. Ph.D. Dissertation, University of Tennessee
Hutchens S et al (2006) Biomimetic synthesis of calcium-deficient hydroxyapatite in a natural hydrogel. Biomaterials 27:4661–4670. https://doi.org/10.1016/j.biomaterials.2006.04.032
Ide-Ektessabi A, Yamaguchi T, Tanaka Y (2005) RBS and XPS analyses of the composite calcium phosphate coatings for biomedical applications. Nucl Instrum Methods Phys Res B 241:685–688. https://doi.org/10.1016/j.nimb.2005.07.165
Khiari R et al (2017) Synthesis and characterization of cellulose carbonate using greenchemistry: surface modification of Avicel. Carbohyd Polym 163:254–260. https://doi.org/10.1016/j.carbpol.2017.01.037
Lin KSK et al (2005) Mechanistic study of apatite formation on bioactive glass surface using31P solid-state NMR spectroscopy. Chem Mater 17:4493–4501. https://doi.org/10.1021/cm050654c
Liu Y et al (2005) Crosslinked organic-inorganic hybrid chitosan membranes for pervaporation dehydration of isopropanol-water mixtures with a long-term stability. J Membr Sci 251:233–238. https://doi.org/10.1016/j.memsci.2004.12.003
Marie PJ, Felsenberg D, Brandi ML (2010) How strontium ranelate, via opposite effects on bone resorption and formation, prevents osteoporosis. Osteoporos Int 22:1659–1667. https://doi.org/10.1007/s00198-010-1369-0
Melnikov P, Gonçalves RV (2015) Preparation and characterization of strontium hydroxyapatite Sr10(PO4)6(OH)2·10H2O suitable for orthopedic applications. Mater Lett 150:89–92. https://doi.org/10.1016/j.matlet.2015.02.110
Nishiyama Y et al (2015) Adsorption and removal of strontium in aqueous solution by synthetic hydroxyapatite. J Radioanal Nucl Chem 307:1279–1285. https://doi.org/10.1007/s10967-015-4228-9
Ohtsu N, Nakamura Y, Semboshi S (2012) Thin hydroxyapatite coating on titanium fabricated by chemical coating process using calcium phosphate slurry. Surf Coat Technol 206:2616–2621. https://doi.org/10.1016/j.surfcoat.2011.11.022
Pan HB et al (2009) Solubility of strontium-substituted apatite by solid titration. Acta Biomater 5:1678–1685. https://doi.org/10.1016/j.actbio.2008.11.032
Pértile RAN et al (2012) Bacterial cellulose: long-term biocompatibility studies. J Biomater Sci Polym 23:1–16. https://doi.org/10.1163/092050611x581516
Pigossi SC et al (2015) Bacterial cellulose-hydroxyapatite composites with osteogenic growth peptide (OGP) or pentapeptide OGP on bone regeneration in critical-size calvarial defect model. J Biomed Mater Res 103:3397–3406. https://doi.org/10.1002/jbm.a.35472
Querido W, Rossi AL, Farina M (2016) The effects of strontium on bone mineral: a review on current knowledge and microanalytical approaches. Micron 80:122–134. https://doi.org/10.1016/j.micron.2015.10.006
Rad MM et al (2017) Fabrication and characterization of two-layered nanofibrous membrane for guided bone and tissue regeneration application. Mater Sci Eng C 80:75–87. https://doi.org/10.1016/j.msec.2017.05.125
Rajwade JM, Paknikar KM, Kumbhar JV (2015) Applications of bacterial cellulose and its composites in biomedicine. Appl Microbiol Biotechnol 99:2491–2511. https://doi.org/10.1007/s00253-015-6426-3
Rakhmatia YD et al (2013) Current barrier membranes: titanium mesh and other membranes for guided bone regeneration in dental applications. J Prosthodont Res 57:3–14. https://doi.org/10.1016/j.jpor.2012.12.001
Rehman I, Bonfield W (1997) Characterization of hydroxyapatite and carbonated apatite by photo acoustic FTIR spectroscopy. J Mater Sci Mater Med 8:1–4. https://doi.org/10.1023/a:1018570213546
Retzepi M, Donos N (2010) Guided bone regeneration: biological principle and therapeutic applications. Clin Oral Implants Res 21:567–576. https://doi.org/10.1111/j.1600-0501.2010.01922.x
Saber-Samandari S, Saber-Samandari S, Gazi M (2013) Cellulose-graft-polyacrylamide/hydroxyapatite composite hydrogel with possible application in removal of Cu (II) ions. React Funct Polym 73:1523–1530. https://doi.org/10.1016/j.reactfunctpolym.2013.07.007
Saska S et al (2011) Bacterial cellulose-hydroxyapatite nanocomposites for bone regeneration. Int J Biomater 2011:1–8. https://doi.org/10.1155/2011/175362
Schumacher M et al (2016) Strontium substitution in apatitic CaP cements effectively attenuates osteoclastic resorption but does not inhibit osteoclastogenesis. Acta Biomater 37:184–194. https://doi.org/10.1016/j.actbio.2016.04.016
Shpak AP, Karbovskii VL, Vakhney AG (2004) Electronic structure of isomorphically substituted strontium apatite. J Electron Spectrosc Relat Phenom 137–140:585–589. https://doi.org/10.1016/j.elspec.2004.02.056
Sousa RCS et al (2014) Adsorption of alpha-lactalbumin from milk whey on hydroxyapatite: effect of ph and temperature and thermodynamic analysis. Quím Nova 37:950–955. https://doi.org/10.5935/0100-4042.20140149
Sugiyama S (2003) Enhancement of the catalytic activities in propane oxidation and H-D exchangeability of hydroxyl groups by the incorporation with cobalt into strontium hydroxyapatite. J Catal 214:8–14. https://doi.org/10.1016/s0021-9517(02)00101-x
Swift P (1982) Adventitious carbon-the panacea for energy referencing? Surf Interface Anal 4:47–51. https://doi.org/10.1002/sia.740040204
Tiwari G et al (2012) Drug delivery systems: an updated review. Int J Pharma Investig 2:2–11. https://doi.org/10.4103/2230-973x.96920
Ummartyotin S, Thiangtham S, Manuspiya H (2017) Strontium-modified bacterial cellulose and a polyvinylidene fluoride composite as an electroactive material. For Prod J 67:288–296. https://doi.org/10.13073/fpj-d-16-00041
Vallet-Regí M, Ruiz-Hernández E (2011) Bioceramics: from bone regeneration to cancer nanomedicine. Adv Mater 23:5177–5218. https://doi.org/10.1002/adma.201101586
Vallet-Regí M, Balas F, Arcos D (2007) Mesoporous materials for drug delivery. Angew Chem Int Ed 46:7548–7558. https://doi.org/10.1002/anie.200604488
Venugopal A, Scurrell MS (2003) Hydroxyapatite as a novel support for gold and ruthenium catalysts behaviour in the water gas shift reaction. Appl Catal 245:137–147. https://doi.org/10.1016/s0926-860x(02)00647-6
Wang X et al (2009) Towards predicting Ca2 + -binding sites with different coordination numbers in proteins with atomic resolution. Proteins Struct Funct Bioinform 75:787–798. https://doi.org/10.1002/prot.22285
Yukhnevich GV (1973) Infrared spectroscopy of water. Nauka, Moscow
Zeng X, Ruckenstein E (1996) Control of pore sizes in macroporous chitosan and chitin membranes. Ind Eng Chem Res 35:4169–4175. https://doi.org/10.1021/ie960270j
Zhang W et al (2011) Effects of strontium in modified biomaterials. Acta Biomater 7:800–808. https://doi.org/10.1016/j.actbio.2010.08.031
Zhang H et al (2014) Universal influenza vaccines, a dream to be realized soon. Viruses 6:1974–1991. https://doi.org/10.3390/v6051974
Zhong LR et al (2013) Nitric oxide regulates neuronal activity via calcium-activated potassium channels. PLoS ONE 8:1–12. https://doi.org/10.1371/journal.pone.0078727
Zhou Y et al (2012) Probing Ca2 + -binding capability of viral proteins with the EF-hand motif by grafting approach. Methods Mol Biol 963:37–53. https://doi.org/10.1007/978-1-62703-230-8_3
Zimmermann KA et al (2011) Biomimetic design of a bacterial cellulose/hydroxyapatite nanocomposite for bone healing applications. Mater Sci Eng C 31:43–49. https://doi.org/10.1016/j.msec.2009.10.007
Acknowledgments
The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES), National Counsel of Technological and Scientific Development (CNPq), Cearense Foundation for the Support of Scientific and Technological Development (FUNCAP), and the Embrapa Agroindústria Tropical for funding this research. This research was also supported by the following projects: FUNCAP/CNPq (PR2-0101-00023.01.00/15), CNPq (No. 305504/2016-9), PROCAD/CAPES (88881.068439/2014-01) and CTQ2015-68951-C3-3R (Ministerio de Economía y Competitividad, Spain and FEDER Funds). A.I.M. thanks the Ministry of Economy and Competitiveness for a Ramón y Cajal contract (RyC2015-17870).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Luz, E.P.C.G., Borges, M.F., Andrade, F.K. et al. Strontium delivery systems based on bacterial cellulose and hydroxyapatite for guided bone regeneration. Cellulose 25, 6661–6679 (2018). https://doi.org/10.1007/s10570-018-2008-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10570-018-2008-8