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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Alginate-based Composite Microspheres: Preparations and Applications for Bone Tissue Engineering

Author(s): Venkatesan Jayachandran*, Sesha Subramanian Murugan, Pandurang Appana Dalavi, Yashaswini Devi Gurushanthappa Vishalakshi and Gi Hun Seong*

Volume 28, Issue 13, 2022

Published on: 02 June, 2022

Page: [1067 - 1081] Pages: 15

DOI: 10.2174/1381612828666220518142911

Price: $65

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Abstract

Alginate-based biomaterials have been extensively studied for bone tissue engineering. Scaffolds, microspheres, and hydrogels can be developed using alginate, which is biocompatible, biodegradable, and able to deliver growth factors and drugs. Alginate microspheres can be produced using crosslinking, microfluidic, three-dimensional printing, extrusion, and emulsion methods. The sizes of the alginate microspheres range from 10 μm to 4 mm. This review describes the chemical characterization and mechanical assessment of alginatebased microspheres. Combinations of alginate with hydroxyapatite, chitosan, collagen, polylactic acid, polycaprolactone, and bioglass were discussed for bone tissue repair and regeneration. In addition, alginate combinations with bone morphogenetic proteins, vascular endothelial growth factor, transforming growth factor beta- 3, other growth factors, cells, proteins, drugs, and osteoinductive drugs were analyzed for tissue engineering applications. Furthermore, the biocompatibility of developed alginate microspheres was discussed for different cell lines. Finally, alginate microsphere-based composites with stem cell interaction for bone tissue regeneration were presented. In the present review, we have assessed the preclinical research on in vivo models of alginatebased microspheres for bone tissue repair and regeneration. Overall, alginate-based microspheres are potential candidates for graft substitutes and the treatment of various bone-related diseases.

Keywords: Alginate, bone tissue engineering, chitosan, mesenchymal stem cells, microspheres, regenerative medicine.

[1]
Goodman SB, Pajarinen J, Yao Z, Lin T. Inflammation and bone repair: From particle disease to tissue regeneration. Front Bioeng Biotechnol 2019; 7: 230.
[http://dx.doi.org/10.3389/fbioe.2019.00230] [PMID: 31608274]
[2]
Casadei A, Epis R, Ferroni L, et al. Adipose tissue regeneration: A state of the art. J Biomed Biotechnol 2012; 2012, 462543.
[http://dx.doi.org/10.1155/2012/462543] [PMID: 23193362]
[3]
Sakkas A, Wilde F, Heufelder M, Winter K, Schramm A. Autogenous bone grafts in oral implantology-is it still a “gold standard”? A consecutive review of 279 patients with 456 clinical procedures. Int J Implant Dent 2017; 3(1): 23.
[http://dx.doi.org/10.1186/s40729-017-0084-4] [PMID: 28573552]
[4]
Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: Recent advances and challenges. Crit Rev Biomed Eng 2012; 40(5): 363-408.
[http://dx.doi.org/10.1615/CritRevBiomedEng.v40.i5.10] [PMID: 23339648]
[5]
Murugan SS, Anil S, Sivakumar P, Shim MS, Venkatesan J. 3D-printed chitosan composites for biomedical applications Chitosan for Biomaterials IV: Biomedical Applications . Springer International Publishing: Cham. 2021; 87-116.
[6]
Eivazzadeh-Keihan R, Maleki A, de la Guardia M, et al. Carbon based nanomaterials for tissue engineering of bone: Building new bone on small black scaffolds: A review. J Adv Res 2019; 18: 185-201.
[http://dx.doi.org/10.1016/j.jare.2019.03.011] [PMID: 31032119]
[7]
Dhandayuthapani B, Yoshida Y, Maekawa T, Kumar DS. Polymeric scaffolds in tissue engineering application: A review . Int J Polym Sci 2011; 2011..
[http://dx.doi.org/10.1155/2011/290602]
[8]
Giannoudis PV, Pountos I. Tissue regeneration. The past, the present and the future. Injury 2005; 36(Suppl. 4): S2-5.
[http://dx.doi.org/10.1016/j.injury.2005.10.006] [PMID: 16288758]
[9]
Do AV, Khorsand B, Geary SM, Salem AK. 3D printing of scaffolds for tissue regeneration applications. Adv Health Mater 2015; 4(12): 1742-62.
[http://dx.doi.org/10.1002/adhm.201500168] [PMID: 26097108]
[10]
Tabata Y. Tissue regeneration based on tissue engineering technology. Congenit Anom (Kyoto) 2004; 44(3): 111-24.
[http://dx.doi.org/10.1111/j.1741-4520.2004.00024.x] [PMID: 15327480]
[11]
Mhanna R, Hasan A. Introduction to tissue engineering. Trends Biomater Artif Organs 2017; 1-34.
[12]
Ilhan E, Ulag S, Sahin A, et al. Fabrication of tissue-engineered tympanic membrane patches using 3D-printing technology. J Mech Behav Biomed 2021; 114, 104219.
[http://dx.doi.org/10.1016/j.jmbbm.2020.104219] [PMID: 33302170]
[13]
Liu Q, Li Q, Xu S, Zheng Q, Cao X. Preparation and properties of 3D printed alginate–chitosan polyion complex hydrogels for tissue engineering. Polymers (Basel) 2018; 10: 664.
[http://dx.doi.org/10.3390/polym10060664]
[14]
Ren Y, Lou R, Liu X, et al. A self-healing hydrogel formation strategy via exploiting endothermic interactions between polyelectrolytes. Chem Commun (Camb) 2016; 52(37): 6273-6.
[http://dx.doi.org/10.1039/C6CC02472F] [PMID: 27078585]
[15]
Akkineni AR, Ahlfeld T, Lode A, Gelinsky M. A versatile method for combining different biopolymers in a core/shell fashion by 3D plotting to achieve mechanically robust constructs. Biofabrication 2016; 8(4), 045001.
[http://dx.doi.org/10.1088/1758-5090/8/4/045001] [PMID: 27716641]
[16]
Lee KY, Mooney DJ. Alginate: Properties and biomedical applications. Prog Polym Sci 2012; 37(1): 106-26.
[http://dx.doi.org/10.1016/j.progpolymsci.2011.06.003] [PMID: 22125349]
[17]
Zhang H, Cheng J, Ao Q. Preparation of alginate-based biomaterials and their applications in biomedicine. Mar Drugs 2021; 19(5): 264.
[http://dx.doi.org/10.3390/md19050264] [PMID: 34068547]
[18]
Andriamanantoanina H, Rinaudo M. Characterization of the alginates from five Madagascan brown algae. Carbohydr Polym 2010; 82: 555-60.
[http://dx.doi.org/10.1016/j.carbpol.2010.05.002]
[19]
Bertagnolli C, Espindola AP, Kleinübing SJ, Tasic L, da Silva MG. Sargassum filipendula alginate from Brazil: Seasonal influence and characteristics. Carbohydr Polym 2014; 111: 619-23.
[http://dx.doi.org/10.1016/j.carbpol.2014.05.024] [PMID: 25037396]
[20]
Mohammed A, Rivers A, Stuckey DC, Ward K. Alginate extraction from Sargassum seaweed in the Caribbean region: Optimization using response surface methodology. Carbohydr Polym 2020; 245, 116419.
[http://dx.doi.org/10.1016/j.carbpol.2020.116419] [PMID: 32718593]
[21]
Fenoradosoa TA, Ali G, Delattre C, et al. Extraction and characterization of an alginate from the brown seaweed Sargassum turbinarioides Grunow. J Appl Phycol 2010; 22: 131-7.
[http://dx.doi.org/10.1007/s10811-009-9432-y]
[22]
Fawzy MA, Gomaa M, Hifney AF, Abdel-Gawad KM. Optimization of alginate alkaline extraction technology from Sargassum latifolium and its potential antioxidant and emulsifying properties. Carbohydr Polym 2017; 157: 1903-12.
[http://dx.doi.org/10.1016/j.carbpol.2016.11.077] [PMID: 27987910]
[23]
Gomez CG, Pérez Lambrecht MV, Lozano JE, Rinaudo M, Villar MA. Influence of the extraction-purification conditions on final properties of alginates obtained from brown algae (Macrocystis pyrifera). Int J Biol Macromol 2009; 44(4): 365-71.
[http://dx.doi.org/10.1016/j.ijbiomac.2009.02.005] [PMID: 19428468]
[24]
Latifi AM, Sadegh Nejad E, Babavalian H. Comparison of extraction different methods of sodium alginate from brown alga Sargassum sp. localized in the southern of Iran. J Appl Biotechnol Rep 2015; 2: 251-5.
[25]
Dhamecha D, Movsas R, Sano U, Menon JU. Applications of alginate microspheres in therapeutics delivery and cell culture: Past, present and future. Int J Pharm 2019; 569: 118627-27.
[http://dx.doi.org/10.1016/j.ijpharm.2019.118627] [PMID: 31421199]
[26]
Cattalini JP, Roether J, Hoppe A, et al. Nanocomposite scaffolds with tunable mechanical and degradation capabilities: Co-delivery of bioactive agents for bone tissue engineering. Biomed Mater 2016; 11(6), 065003.
[http://dx.doi.org/10.1088/1748-6041/11/6/065003] [PMID: 27767020]
[27]
Bian L, Zhai DY, Tous E, Rai R, Mauck RL, Burdick JA. Enhanced MSC chondrogenesis following delivery of TGF-β3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo. Biomaterials 2011; 32(27): 6425-34.
[http://dx.doi.org/10.1016/j.biomaterials.2011.05.033] [PMID: 21652067]
[28]
Zhang B, Li H, He L, et al. Surface-decorated hydroxyapatite scaffold with on-demand delivery of dexamethasone and stromal cell derived factor-1 for enhanced osteogenesis. Mater Sci Eng C 2018; 89: 355-70.
[http://dx.doi.org/10.1016/j.msec.2018.04.008] [PMID: 29752108]
[29]
Varini E, Sánchez-Salcedo S, Malavasi G, Lusvardi G, Vallet-Regí M, Salinas AJ. Cerium (III) and (IV) containing mesoporous glasses/alginate beads for bone regeneration: Bioactivity, biocompatibility and reactive oxygen species activity. Mater Sci Eng C 2019; 105.
[http://dx.doi.org/10.1016/j.msec.2019.109971]
[30]
Carmo ABXD, Sartoretto SC, Alves ATNN, et al. Alveolar bone repair with strontium- containing nanostructured carbonated hydroxyapatite. J Appl Oral Sci 2018; 26, e20170084.
[http://dx.doi.org/10.1590/1678-7757-2017-0084] [PMID: 29364342]
[31]
Mateus AY, Barrias CC, Ribeiro C, Ferraz MP, Monteiro FJ. Comparative study of nanohydroxyapatite microspheres for medical applications. J Biomed Mater Res A 2008; 86(2): 483-93.
[http://dx.doi.org/10.1002/jbm.a.31634] [PMID: 17975824]
[32]
Martinez-Zelaya VR, Zarranz L, Herrera EZ, et al. In vitro and in vivo evaluations of nanocrystalline Zn-doped carbonated hydroxyapatite/alginate microspheres: Zinc and calcium bioavailability and bone regeneration. Int J Nanomedicine 2019; 14: 3471-90.
[http://dx.doi.org/10.2147/IJN.S197157] [PMID: 31190805]
[33]
Zhong Q, Li W, Su X, et al. Degradation pattern of porous CaCO3 and hydroxyapatite microspheres in vitro and in vivo for potential application in bone tissue engineering. Colloids Surf B Biointerfaces 2016; 143: 56-63.
[http://dx.doi.org/10.1016/j.colsurfb.2016.03.020] [PMID: 26998866]
[34]
Dalavi PA, Prabhu A, Shastry RP, Venkatesan J. Microspheres containing biosynthesized silver nanoparticles with alginate-nano hydroxyapatite for biomedical applications. J Biomater Sci Polym Ed 2020; 31(16): 2025-43.
[http://dx.doi.org/10.1080/09205063.2020.1793464] [PMID: 32648515]
[35]
Narayanan LK, Kumar A, Tan Z, Bernacki S, Starly B, Shirwaiker RA. Alginate microspheroid encapsulation and delivery of MG-63 cells into polycaprolactone scaffolds: A new biofabrication approach for tissue engineering constructs. J Nanotechnol Eng Med 2015; 6.
[http://dx.doi.org/10.1115/1.4031174]
[36]
Liu D, Liu Z, Zou J, et al. Synthesis and characterization of a hydroxyapatite-sodium alginate-chitosan scaffold for bone regeneration. Front Mater 2021; 8.
[http://dx.doi.org/10.3389/fmats.2021.648980]
[37]
Kong Y, Zhao Y, Li D, Shen H, Yan M. Dual delivery of encapsulated BM-MSCs and BMP-2 improves osteogenic differentiation and new bone formation. J Biomed Mater Res A 2019; 107(10): 2282-95.
[http://dx.doi.org/10.1002/jbm.a.36737] [PMID: 31152570]
[38]
Zhang H, Chen J, Zhang Y, Pan P, Zhang Q. Magnetic auto-fluorescent microspheres for a drug delivery system. Mater Lett 2014; 119: 143-5.
[http://dx.doi.org/10.1016/j.matlet.2014.01.008]
[39]
Del Rosario C, Rodríguez-Évora M, Reyes R, Delgado A, Évora C. BMP-2, PDGF-BB, and bone marrow mesenchymal cells in a macroporous β-TCP scaffold for critical-size bone defect repair in rats. Biomed Mater 2015; 10(4), 045008.
[http://dx.doi.org/10.1088/1748-6041/10/4/045008] [PMID: 26201844]
[40]
Lourenço AH, Torres AL, Vasconcelos DP, et al. Osteogenic, anti-osteoclastogenic and immunomodulatory properties of a strontium-releasing hybrid scaffold for bone repair. Mater Sci Eng C 2019; 99: 1289-303.
[http://dx.doi.org/10.1016/j.msec.2019.02.053] [PMID: 30889663]
[41]
Fahmy-Garcia S, Farrell E, Witte-Bouma J, et al. Follistatin effects in migration, vascularization, and osteogenesis in vitro and bone repair in vivo. Front Bioeng Biotechnol 2019; 7: 38.
[http://dx.doi.org/10.3389/fbioe.2019.00038] [PMID: 30881954]
[42]
Li X, Wang M, Deng Y, Chen X, Xiao Y, Zhang X. Fabrication and properties of Ca-P bioceramic spherical granules with interconnected porous structure. ACS Biomater Sci Eng 2017; 3(8): 1557-66.
[http://dx.doi.org/10.1021/acsbiomaterials.7b00232] [PMID: 33429641]
[43]
Pravdyuk AI, Petrenko YA, Fuller BJ, Petrenko AY. Cryopreservation of alginate encapsulated mesenchymal stromal cells. Cryobiology 2013; 66(3): 215-22.
[http://dx.doi.org/10.1016/j.cryobiol.2013.02.002] [PMID: 23419981]
[44]
Li Q, Hou T, Zhao J, Xu J. Vascular endothelial growth factor release from alginate microspheres under simulated physiological compressive loading and the effect on human vascular endothelial cells. Tissue Eng Part A 2011; 17(13-14): 1777-85.
[http://dx.doi.org/10.1089/ten.tea.2010.0616] [PMID: 21341993]
[45]
García-García P, Reyes R, Pérez-Herrero E, Arnau MR, Évora C, Delgado A. Alginate-hydrogel versus alginate-solid system. Efficacy in bone regeneration in osteoporosis. Mater Sci Eng C 2020; 115, 111009.
[http://dx.doi.org/10.1016/j.msec.2020.111009] [PMID: 32600680]
[46]
Lee YH, Lee BW, Jung YC, Yoon BI, Woo HM, Kang BJ. Application of alginate microbeads as a carrier of bone morphogenetic protein-2 for bone regeneration. J Biomed Mater Res B Appl Biomater 2019; 107(2): 286-94.
[http://dx.doi.org/10.1002/jbm.b.34119] [PMID: 29569344]
[47]
Quinlan E, López-Noriega A, Thompson EM, Hibbitts A, Cryan SA, O’Brien FJ. Controlled release of vascular endothelial growth factor from spray-dried alginate microparticles in collagen-hydroxyapatite scaffolds for promoting vascularization and bone repair. J Tissue Eng Regen Med 2017; 11(4): 1097-109.
[http://dx.doi.org/10.1002/term.2013] [PMID: 25783558]
[48]
Li H, Jiang F, Ye S, Wu Y, Zhu K, Wang D. Bioactive apatite incorporated alginate microspheres with sustained drug-delivery for bone regeneration application. Mater Sci Eng C 2016; 62: 779-86.
[http://dx.doi.org/10.1016/j.msec.2016.02.012] [PMID: 26952484]
[49]
Zhang Y, Wang X, Su Y, Chen D, Zhong W. A doxorubicin delivery system: Samarium/mesoporous bioactive glass/alginate composite microspheres. Mater Sci Eng C 2016; 67: 205-13.
[http://dx.doi.org/10.1016/j.msec.2016.05.019] [PMID: 27287115]
[50]
Kanafi MM, Ramesh A, Gupta PK, Bhonde RR. Dental pulp stem cells immobilized in alginate microspheres for applications in bone tissue engineering. Int Endod J 2014; 47(7): 687-97.
[http://dx.doi.org/10.1111/iej.12205] [PMID: 24127887]
[51]
Zhu Y, Wang J, Wu J, Zhang J, Wan Y, Wu H. Injectable hydrogels embedded with alginate microspheres for controlled delivery of bone morphogenetic protein-2. Biomed Mater 2016; 11(2), 025010.
[http://dx.doi.org/10.1088/1748-6041/11/2/025010] [PMID: 27007436]
[52]
Martinez-Zelaya VR, Archilha NL, Calasans-Maia M, Farina M, Rossi AM. Trabecular architecture during the healing process of a tibial diaphysis defect. Acta Biomater 2021; 120: 181-93.
[http://dx.doi.org/10.1016/j.actbio.2020.08.028] [PMID: 32860947]
[53]
Liu S, Huang D, Hu Y, et al. Sodium alginate/collagen composite multiscale porous scaffolds containing poly(ε-caprolactone) microspheres fabricated based on additive manufacturing technology. RSC Advances 2020; 10: 39241-50.
[http://dx.doi.org/10.1039/D0RA04581K]
[54]
Cuozzo RC, Sartoretto SC, Resende RFB, et al. Biological evaluation of zinc-containing calcium alginate-hydroxyapatite composite microspheres for bone regeneration. J Biomed Mater Res B Appl Biomater 2020; 108(6): 2610-20.
[http://dx.doi.org/10.1002/jbm.b.34593] [PMID: 32096353]
[55]
Khatami N, Khoshfetrat AB, Khaksar M, Zamani ARN, Rahbarghazi R. Collagen-alginate-nano-silica microspheres improved the osteogenic potential of human osteoblast-like MG-63 cells. J Cell Biochem 2019; 120(9): 15069-82.
[http://dx.doi.org/10.1002/jcb.28768] [PMID: 31020682]
[56]
Ingavle GC, Gionet-Gonzales M, Vorwald CE, et al. Injectable mineralized microsphere-loaded composite hydrogels for bone repair in a sheep bone defect model. Biomaterials 2019; 197: 119-28.
[http://dx.doi.org/10.1016/j.biomaterials.2019.01.005] [PMID: 30641263]
[57]
Santos GGD, Vasconcelos LQ, Poy SCDS, et al. Influence of the geometry of nanostructured hydroxyapatite and alginate composites in the initial phase of bone repair. Acta Cir Bras 2019; 34(2), e201900203.
[http://dx.doi.org/10.1590/s0102-8650201900203] [PMID: 30843936]
[58]
Lin Z, Wu J, Qiao W, et al. Precisely controlled delivery of magnesium ions thru sponge-like monodisperse PLGA/nano-MgO-alginate core-shell microsphere device to enable in-situ bone regeneration. Biomaterials 2018; 174: 1-16.
[http://dx.doi.org/10.1016/j.biomaterials.2018.05.011] [PMID: 29763774]
[59]
Lee H, Woo HM, Kang BJ. Impact of collagen-alginate composition from microbead morphological properties to microencapsulated canine adipose tissue-derived mesenchymal stem cell activities. J Biomater Sci Polym Ed 2018; 29(7-9): 1042-52.
[http://dx.doi.org/10.1080/09205063.2017.1399002] [PMID: 29082833]
[60]
Iqbal B, Sarfaraz Z, Muhammad N, et al. Ionic liquid as a potential solvent for preparation of collagen-alginate-hydroxyapatite beads as bone filler. J Biomater Sci Polym Ed 2018; 29(10): 1168-84.
[http://dx.doi.org/10.1080/09205063.2018.1443604] [PMID: 29460709]
[61]
Yan M, Ni J, Shen H, Song D, Ding M, Huang J. Local controlled release of simvastatin and PDGF from core/shell microspheres promotes bone regeneration in vivo. RSC Advances 2017; 7: 19621-9.
[http://dx.doi.org/10.1039/C7RA01503H]
[62]
Hu Y, Ma S, Yang Z, et al. Facile fabrication of poly(L-lactic acid) microsphere-incorporated calcium alginate/hydroxyapatite porous scaffolds based on pickering emulsion templates. Colloids Surf B Biointerfaces 2016; 140: 382-91.
[http://dx.doi.org/10.1016/j.colsurfb.2016.01.005] [PMID: 26774574]
[63]
Della PG, Nguyen BNB, Campardelli R, Reverchon E, Fisher JP. Synergistic effect of sustained release of growth factors and dynamic culture on osteoblastic differentiation of mesenchymal stem cells. J Biomed Mater Res A 2015; 103(6): 2161-71.
[http://dx.doi.org/10.1002/jbm.a.35354] [PMID: 25346530]
[64]
Endo K, Anada T, Yamada M, Seki M, Sasaki K, Suzuki O. Enhancement of osteoblastic differentiation in alginate gel beads with bioactive octacalcium phosphate particles. Biomed Mater 2015; 10(6), 065019.
[http://dx.doi.org/10.1088/1748-6041/10/6/065019] [PMID: 26657659]
[65]
Reyes R, Delgado A, Sánchez E, Fernández A, Hernández A, Evora C. Repair of an osteochondral defect by sustained delivery of BMP-2 or TGFβ1 from a bilayered alginate-PLGA scaffold. J Tissue Eng Regen Med 2014; 8(7): 521-33.
[PMID: 22733683]
[66]
Miao T, Rao KS, Spees JL, Oldinski RA. Osteogenic differentiation of human mesenchymal stem cells through alginate-graft-poly(ethylene glycol) microsphere-mediated intracellular growth factor delivery. J Control Release 2014; 192: 57-66.
[http://dx.doi.org/10.1016/j.jconrel.2014.06.029] [PMID: 24979209]
[67]
Wu X, Hou T, Luo F, et al. Vascular endothelial growth factor and physiological compressive loading synergistically promote bone formation of tissue-engineered bone. Tissue Eng Part A 2013; 19(21-22): 2486-94.
[http://dx.doi.org/10.1089/ten.tea.2013.0124] [PMID: 23786586]
[68]
Poldervaart MT, Wang H, van der Stok J, et al. Sustained release of BMP-2 in bioprinted alginate for osteogenicity in mice and rats. PLoS One 2013; 8(8), e72610.
[http://dx.doi.org/10.1371/journal.pone.0072610] [PMID: 23977328]
[69]
Soran Z. Aydın RS, Gümüşderelioğlu M. Chitosan scaffolds with BMP-6 loaded alginate microspheres for periodontal tissue engineering. J Microencapsul 2012; 29(8): 770-80.
[http://dx.doi.org/10.3109/02652048.2012.686531] [PMID: 22612554]
[70]
Man Y, Wang P, Guo Y, et al. Angiogenic and osteogenic potential of platelet-rich plasma and adipose-derived stem cell laden alginate microspheres. Biomaterials 2012; 33(34): 8802-11.
[http://dx.doi.org/10.1016/j.biomaterials.2012.08.054] [PMID: 22981779]
[71]
Wu C, Zhang Y, Ke X, et al. Bioactive mesopore-glass microspheres with controllable protein-delivery properties by biomimetic surface modification. J Biomed Mater Res A 2010; 95(2): 476-85.
[http://dx.doi.org/10.1002/jbm.a.32873] [PMID: 20648544]
[72]
Endres M, Wenda N, Woehlecke H, et al. Microencapsulation and chondrogenic differentiation of human mesenchymal progenitor cells from subchondral bone marrow in Ca-alginate for cell injection. Acta Biomater 2010; 6(2): 436-44.
[http://dx.doi.org/10.1016/j.actbio.2009.07.022] [PMID: 19622399]
[73]
Bidarra SJ, Barrias CC, Barbosa MA, Soares R, Granja PL. Immobilization of human mesenchymal stem cells within RGD-grafted alginate microspheres and assessment of their angiogenic potential. Biomacromolecules 2010; 11(8): 1956-64.
[http://dx.doi.org/10.1021/bm100264a] [PMID: 20690708]
[74]
Evangelista MB, Hsiong SX, Fernandes R, et al. Upregulation of bone cell differentiation through immobilization within a synthetic extracellular matrix. Biomaterials 2007; 28(25): 3644-55.
[http://dx.doi.org/10.1016/j.biomaterials.2007.04.028] [PMID: 17532040]
[75]
Luginbuehl V, Wenk E, Koch A, Gander B, Merkle HP, Meinel L. Insulin-like growth factor I-releasing alginate-tricalciumphosphate composites for bone regeneration. Pharm Res 2005; 22(6): 940-50.
[http://dx.doi.org/10.1007/s11095-005-4589-9] [PMID: 15948038]
[76]
Szekalska M. Puciłowska A, Szymańska E, Ciosek P, Winnicka K. Alginate: Current use and future perspectives in pharmaceutical and biomedical applications. Int J Polym Sci 2016; 2016: 1.
[http://dx.doi.org/10.1155/2016/7697031]
[77]
Li L, Fang Y, Vreeker R, Appelqvist I, Mendes E. Reexamining the egg-box model in calcium-alginate gels with X-ray diffraction. Biomacromolecules 2007; 8(2): 464-8.
[http://dx.doi.org/10.1021/bm060550a] [PMID: 17291070]
[78]
Ahmad Raus R, Wan Nawawi WMF, Nasaruddin RR. Alginate and alginate composites for biomedical applications. Asian J Pharm Sci 2021; 16(3): 280-306.
[http://dx.doi.org/10.1016/j.ajps.2020.10.001] [PMID: 34276819]
[79]
Sharma N, Purwar N, Gupta PC. Microspheres as drug carriers for controlled drug delivery: A review. Int J Pharm Sci Res 2015; 6: 4579.
[80]
Uyen NTT, Hamid ZAA, Tram NXT, Ahmad N. Fabrication of alginate microspheres for drug delivery: A review. Int J Biol Macromol 2020; 153: 1035-46.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.10.233] [PMID: 31794824]
[81]
Lengyel M, Kállai-Szabó N, Antal V, Laki AJ, Antal I. Microparticles, microspheres, and microcapsules for advanced drug delivery. Sci Pharm 2019; 87: 20.
[http://dx.doi.org/10.3390/scipharm87030020]
[82]
Berkland C, King M, Cox A, Kim K, Pack DW. Precise control of PLG microsphere size provides enhanced control of drug release rate. J Control Release 2002; 82(1): 137-47.
[http://dx.doi.org/10.1016/S0168-3659(02)00136-0] [PMID: 12106984]
[83]
El-Newehy MH, Elsherbiny AS, Mori H. Influence of molecular weight on kinetics release of metronidazole from proline-based polymers prepared by RAFT polymerization. RSC Advances 2016; 6: 72761-7.
[http://dx.doi.org/10.1039/C6RA14307E]
[84]
Moreira APD, Sader MS. Soares GDdA, Leão MHMR. Strontium incorporation on microspheres of alginate/β-tricalcium phosphate as delivery matrices. Mater Res 2014; 17: 967-73.
[http://dx.doi.org/10.1590/S1516-14392014005000095]
[85]
Zhao F, Zhang W, Fu X, Xie W, Chen X. Fabrication and characterization of bioactive glass/alginate composite scaffolds by a self-crosslinking processing for bone regeneration. RSC Advances 2016; 6: 91201-8.
[http://dx.doi.org/10.1039/C6RA18309C]
[86]
Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick JE. Scaffold design for bone regeneration. J Nanosci Nanotechnol 2014; 14(1): 15-56.
[http://dx.doi.org/10.1166/jnn.2014.9127] [PMID: 24730250]
[87]
Ho HV, Tripathi G, Gwon J, Lee S-Y, Lee B-T. Novel TOCNF reinforced injectable alginate/β-tricalcium phosphate microspheres for bone regeneration. Mater Des 2020; 194.
[http://dx.doi.org/10.1016/j.matdes.2020.108892]
[88]
Oliveira SM, Barrias CC, Almeida IF, et al. Injectability of a bone filler system based on hydroxyapatite microspheres and a vehicle with in situ gel-forming ability. J Biomed Mater Res B Appl Biomater 2008; 87(1): 49-58.
[http://dx.doi.org/10.1002/jbm.b.31066] [PMID: 18437700]
[89]
Oliveira SM, Almeida IF, Costa PC, et al. Characterization of polymeric solutions as injectable vehicles for hydroxyapatite microspheres. AAPS PharmSciTech 2010; 11(2): 852-8.
[http://dx.doi.org/10.1208/s12249-010-9447-3] [PMID: 20490958]
[90]
Cuozzo RC, da Rocha Leão MHM, de Andrade Gobbo L, et al. Zinc alginate–hydroxyapatite composite microspheres for bone repair. Ceram Int 2014; 40: 11369-75.
[http://dx.doi.org/10.1016/j.ceramint.2014.02.107]
[91]
Hou F, Zhu Y, Zou Q, et al. One-step preparation of multifunctional alginate microspheres loaded with in situ-formed gold nanostars as a photothermal agent. Mater Chem Front 2019; 3: 2018-24.
[http://dx.doi.org/10.1039/C9QM00276F]
[92]
Zhang S, Li G, Man J, et al. Fabrication of microspheres from high-viscosity bioink using a novel microfluidic-based 3D bioprinting nozzle. Micromachines (Basel) 2020; 11(7): 681.
[http://dx.doi.org/10.3390/mi11070681] [PMID: 32674334]
[93]
Ye B, Xu H, Bao B, Xuan J, Zhang L. 3D-printed air-blast microfluidic nozzles for preparing calcium alginate microparticles. RSC Advances 2017; 7: 48826-34.
[http://dx.doi.org/10.1039/C7RA08611C]
[94]
Baimark Y, Srisuwan Y. Preparation of alginate microspheres by water-in-oil emulsion method for drug delivery: Effect of Ca2+ post-cross-linking. Adv Powder Technol 2014; 25: 1541-6.
[http://dx.doi.org/10.1016/j.apt.2014.05.001]
[95]
Lupo B, Maestro A, Porras M, Gutiérrez JM, González C. Preparation of alginate microspheres by emulsification/internal gelation to encapsulate cocoa polyphenols. Food Hydrocoll 2014; 38: 56-65.
[http://dx.doi.org/10.1016/j.foodhyd.2013.11.003]
[96]
Bi YG, Lin ZT, Deng ST. Fabrication and characterization of hydroxyapatite/sodium alginate/chitosan composite microspheres for drug delivery and bone tissue engineering. Mater Sci Eng C 2019; 100: 576-83.
[http://dx.doi.org/10.1016/j.msec.2019.03.040] [PMID: 30948094]
[97]
Boanini E, Bigi A. Biomimetic gelatin-octacalcium phosphate core-shell microspheres. J Colloid Interface Sci 2011; 362(2): 594-9.
[http://dx.doi.org/10.1016/j.jcis.2011.06.061] [PMID: 21784431]
[98]
Chiu C-T, Chang WC, Wang YJ. Microspheres of collagen/β-TCP with an open network fibrillar structure strengthened by chitosan. Artif Cells Blood Substit Immobil Biotechnol 2007; 35(3): 309-17.
[http://dx.doi.org/10.1080/10731190701378626] [PMID: 17573629]
[99]
Neves N, Campos BB, Almeida IF, et al. Strontium-rich injectable hybrid system for bone regeneration. Mater Sci Eng C 2016; 59: 818-27.
[http://dx.doi.org/10.1016/j.msec.2015.10.038] [PMID: 26652437]
[100]
Lin JH, Chen CK, Wen SP, Lou CW. Poly-L-lactide/sodium alginate/chitosan microsphere hybrid scaffolds made with braiding manufacture and adhesion technique: Solution to the incongruence between porosity and compressive strength. Mater Sci Eng C 2015; 52: 111-20.
[http://dx.doi.org/10.1016/j.msec.2015.03.034] [PMID: 25953547]
[101]
Ylä-Soininmäki A, Moritz N, Turco G, Paoletti S, Aro HT. Quantitative characterization of porous commercial and experimental bone graft substitutes with microcomputed tomography. J Biomed Mater Res B Appl Biomater 2013; 101(8): 1538-48.
[http://dx.doi.org/10.1002/jbm.b.32975] [PMID: 23744797]
[102]
Calasans-Maia MD, Barboza Junior CAB, Soriano-Souza CA, et al. Microspheres of alginate encapsulated minocycline-loaded nanocrystalline carbonated hydroxyapatite: Therapeutic potential and effects on bone regeneration. Int J Nanomedicine 2019; 14: 4559-71.
[http://dx.doi.org/10.2147/IJN.S201631] [PMID: 31417258]
[103]
Mun A, Simaan Yameen H, Edelbaum G, Seliktar D. Alginate hydrogel beads embedded with drug-bearing polycaprolactone microspheres for sustained release of paclobutrazol. Sci Rep 2021; 11(1): 10877.
[http://dx.doi.org/10.1038/s41598-021-90338-9] [PMID: 34035364]
[104]
Ren B, Chen X, Du S, et al. Injectable polysaccharide hydrogel embedded with hydroxyapatite and calcium carbonate for drug delivery and bone tissue engineering . Int J Biol Macromol 2018; 118(Pt A): 1257-66..
[http://dx.doi.org/10.1016/j.ijbiomac.2018.06.200] [PMID: 30021396]
[105]
Ionita M, Pandele MA, Iovu H. Sodium alginate/graphene oxide composite films with enhanced thermal and mechanical properties. Carbohydr Polym 2013; 94(1): 339-44.
[http://dx.doi.org/10.1016/j.carbpol.2013.01.065] [PMID: 23544547]
[106]
Sahoo DR, Biswal T. Alginate and its application to tissue engineering. SN Appl Sci 2021; 3: 30.
[http://dx.doi.org/10.1007/s42452-020-04096-w]
[107]
Yang G, Yang X, Zhang L, et al. Counterionic biopolymers-reinforced bioactive glass scaffolds with improved mechanical properties in wet state. Mater Lett 2012; 75: 80-3.
[http://dx.doi.org/10.1016/j.matlet.2012.01.122]
[108]
Bhakta G, Lee KH, Magalhães R, et al. Cryopreservation of alginate-fibrin beads involving bone marrow derived mesenchymal stromal cells by vitrification. Biomaterials 2009; 30(3): 336-43.
[http://dx.doi.org/10.1016/j.biomaterials.2008.09.030] [PMID: 18930316]
[109]
Grellier M, Granja PL, Fricain J-C, et al. The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect. Biomaterials 2009; 30(19): 3271-8.
[http://dx.doi.org/10.1016/j.biomaterials.2009.02.033] [PMID: 19299013]
[110]
Penolazzi L, Tavanti E, Vecchiatini R, et al. Encapsulation of mesenchymal stem cells from Wharton’s jelly in alginate microbeads. Tissue Eng Part C Methods 2010; 16(1): 141-55.
[http://dx.doi.org/10.1089/ten.tec.2008.0582] [PMID: 19402785]
[111]
Vecchiatini R, Penolazzi L, Lambertini E, et al. Effect of dynamic three-dimensional culture on osteogenic potential of human periodontal ligament-derived mesenchymal stem cells entrapped in alginate microbeads. J Periodontal Res 2015; 50(4): 544-53.
[http://dx.doi.org/10.1111/jre.12225] [PMID: 25251713]
[112]
Chen MJ, Lu Y, Simpson NE, et al. In Situ transplantation of alginate bioencapsulated adipose tissues derived stem cells (ADSCs) via hepatic injection in a mouse model. PLoS One 2015; 10(9), e0138184.
[http://dx.doi.org/10.1371/journal.pone.0138184] [PMID: 26372641]
[113]
Xiong L, Zeng J, Yao A, et al. BMP2-loaded hollow hydroxyapatite microspheres exhibit enhanced osteoinduction and osteogenicity in large bone defects. Int J Nanomedicine 2015; 10: 517-26.
[http://dx.doi.org/10.2147/IJN.S74677] [PMID: 25609957]
[114]
Guo YH, Zhao S, Du YX, Xing QJ, Chen BL, Yu CQ. Effects of ginsenoside Rg1-loaded alginate-chitosan microspheres on human bone marrow stromal cells. Biosci Rep 2017; 37(3): 37.
[http://dx.doi.org/10.1042/BSR20160566] [PMID: 28536312]
[115]
Ribeiro CC, Barrias CC, Barbosa MA. Calcium phosphate-alginate microspheres as enzyme delivery matrices. Biomaterials 2004; 25(18): 4363-73.
[http://dx.doi.org/10.1016/j.biomaterials.2003.11.028] [PMID: 15046927]
[116]
Barrias CC, Lamghari M, Granja PL, Sá Miranda MC, Barbosa MA. Biological evaluation of calcium alginate microspheres as a vehicle for the localized delivery of a therapeutic enzyme. J Biomed Mater Res A 2005; 74(4): 545-52.
[http://dx.doi.org/10.1002/jbm.a.30348] [PMID: 16028235]
[117]
Fahmy-Garcia S, Mumcuoglu D, de Miguel L, et al. Novel in situ gelling hydrogels loaded with recombinant collagen peptide microspheres as a slow-release system induce ectopic bone formation. Adv Healthc Mater 2018; 7(21), e1800507.
[http://dx.doi.org/10.1002/adhm.201800507] [PMID: 30230271]
[118]
Bayer EA, Jordan J, Roy A, et al. Programmed platelet-derived growth factor-BB and bone morphogenetic protein-2 delivery from a hybrid calcium phosphate/alginate scaffold. Tissue Eng Part A 2017; 23(23-24): 1382-93.
[http://dx.doi.org/10.1089/ten.tea.2017.0027] [PMID: 28537482]
[119]
Bhowmik D, Gopinath H, Kumar BP, Duraivel S, Kumar KS. Controlled release drug delivery systems. Pharma Innov 2012; 1.
[120]
Vasir JK, Tambwekar K, Garg S. Bioadhesive microspheres as a controlled drug delivery system. Int J Pharm 2003; 255(1-2): 13-32.
[http://dx.doi.org/10.1016/S0378-5173(03)00087-5] [PMID: 12672598]
[121]
Huang W, Li X, Shi X, Lai C. Microsphere based scaffolds for bone regenerative applications. Biomater Sci 2014; 2(9): 1145-53.
[http://dx.doi.org/10.1039/C4BM00161C] [PMID: 32481887]
[122]
Segredo-Morales E, García-García P, Reyes R, Pérez-Herrero E, Delgado A, Évora C. Bone regeneration in osteoporosis by delivery BMP-2 and PRGF from tetronic-alginate composite thermogel. Int J Pharm 2018; 543(1-2): 160-8.
[http://dx.doi.org/10.1016/j.ijpharm.2018.03.034] [PMID: 29567197]
[123]
Rumian Ł, Tiainen H, Cibor U, et al. Ceramic scaffolds enriched with gentamicin loaded poly(lactide-co-glycolide) microparticles for prevention and treatment of bone tissue infections. Mater Sci Eng C 2016; 69: 856-64..
[http://dx.doi.org/10.1016/j.msec.2016.07.065] [PMID: 27612780]
[124]
Wang X, Wenk E, Zhang X, Meinel L, Vunjak-Novakovic G, Kaplan DL. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J Control Release 2009; 134(2): 81-90.
[http://dx.doi.org/10.1016/j.jconrel.2008.10.021] [PMID: 19071168]
[125]
Wüst S, Godla ME, Müller R, Hofmann S. Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater 2014; 10(2): 630-40.
[http://dx.doi.org/10.1016/j.actbio.2013.10.016] [PMID: 24157694]
[126]
Queen D, Orsted H, Sanada H, Sussman G. A dressing history. Int Wound J 2004; 1(1): 59-77.
[http://dx.doi.org/10.1111/j.1742-4801.2004.0009.x] [PMID: 16722898]
[127]
Khanna O, Larson JC, Moya ML, Opara EC, Brey EM. Generation of alginate microspheres for biomedical applications. J Vis Exp 2012; (66): 3388.
[http://dx.doi.org/10.3791/3388] [PMID: 22907205]
[128]
Mohanty S, Wu Y, Chakraborty N, Mohanty P, Ghosh G. Impact of alginate concentration on the viability, cryostorage, and angiogenic activity of encapsulated fibroblasts. Mater Sci Eng C 2016; 65: 269-77.
[http://dx.doi.org/10.1016/j.msec.2016.04.055] [PMID: 27157752]

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