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Injectability study and rheological evaluation of Pluronic-derived thermosensitive hydrogels containing mesoporous bioactive glass nanoparticles for bone regeneration

  • Materials for life sciences
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Abstract

Thermosensitive injectable hydrogels are widely investigated as a minimally invasive tool for the delivery of therapeutic agents. Here, Pluronic F-127 hydrogels containing mesoporous bioactive glass nanoparticles were obtained as a novel device to improve bone tissue regeneration. Thermosensitive behavior and injectability of the obtained nanocomposites hydrogels were evaluated, showing feasibility for minimally invasive administration and sol–gel phase transition in the range of 18 to 23 °C, suitable for use as an injectable system. Rheological evaluation showed that adding bioactive glass improved the hydrogel elastic properties and stability at body temperature, also increasing the storage modulus (G’) and residence time. The injectability evaluation showed that all formulations were able to be administrated using a maximum force of up to 2.4 ± 0.4 N, compatible with manual injection. The results shows that Pluronic F-127/mesoporous bioactive glass systems are potential candidates to be applied as injectable systems for therapeutic agents release in situ.

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References

  1. Moreira CDF et al (2019) Injectable chitosan/gelatin/bioactive glass nanocomposite hydrogels for potential bone regeneration: in vitro and in vivo analyses. Int J Biol Macromol 132:811–821

    Article  CAS  Google Scholar 

  2. Amirthalingam S et al (2021) Combinatorial effect of nano whitlockite/nano bioglass with FGF-18 in an injectable hydrogel for craniofacial bone regeneration. Biomater Sci 9:2439–2453

    Article  CAS  Google Scholar 

  3. Liao J et al (2017) Injectable alginate hydrogel cross-linked by calcium gluconate- loaded porous microspheres for cartilage tissue engineering. ACS Omega. https://doi.org/10.1021/acsomega.6b00495

    Article  Google Scholar 

  4. Cai Z et al (2021) Anti-Inflammatory and prochondrogenic in situ-formed injectable hydrogel crosslinked by strontium-doped bioglass for cartilage regeneration. ACS Appl Mater Interfaces 13:59772–59786

    Article  CAS  Google Scholar 

  5. Vitale-Brovarone C et al (2018) Hybrid injectable platforms for the in situ delivery of therapeutic ions from mesoporous glasses. Chem Eng J 340:103–113

    Article  CAS  Google Scholar 

  6. Sang X, Zhao X, Yan L, Jin X, Wang X (2022) Thermosensitive hydrogel loaded with primary chondrocyte- derived exosomes promotes cartilage repair by regulating macrophage polarization in osteoarthritis. Tissue Eng Regen Med 19:629–642

    Article  CAS  Google Scholar 

  7. Chatterjee S, Hui PC, Kan C (2018) Thermoresponsive hydrogels and their biomedical applications: special insight into their applications in textile based transdermal therapy. Polymers. https://doi.org/10.3390/polym10050480

    Article  Google Scholar 

  8. Moreira CDF et al (2018) Nanostructured chitosan/gelatin/bioactive glass in situ forming hydrogel composites as a potential injectable matrix for bone tissue engineering. Mater Chem Phys 218:304–316

    Article  CAS  Google Scholar 

  9. Deliormanlı AM, Türk M (2020) Flow behavior and drug release study of injectable Pluronic F - 127 hydrogels containing bioactive glass and carbon - based nanopowders. J Inorg Organomet Polym Mater 30:1184–1196

    Article  CAS  Google Scholar 

  10. Zambanini T et al (2021) Holmium-containing bioactive glasses dispersed in poloxamer 407 hydrogel as a theragenerative composite for bone cancer treatment. Materials (Basel). https://doi.org/10.3390/ma14061459

    Article  Google Scholar 

  11. Gyles D, Diniz L, Otávio J, Silva C, Ribeiro-costa RM (2017) A review of the designs and prominent biomedical advances of natural and synthetic hydrogel formulations. Eur Polym J 88:373–392

    Article  CAS  Google Scholar 

  12. Klouda L (2015) Thermoresponsive hydrogels in biomedical applications a seven-year update. Eur J Pharm Biopharm. https://doi.org/10.1016/j.ejpb.2015.05.017

    Article  Google Scholar 

  13. Kjøniksen A, Calejo MT, Zhu K, Nystr B, Sande SA (2014) Stabilization of pluronic gels in the presence of different polysaccharides. J Appl Polym Sci 40465:1–8

    Google Scholar 

  14. Hom WL, Bhatia SR (2017) Significant enhancement of elasticity in alginate-clay nanocomposite hydrogels with PEO-PPO-PEO copolymers. Polymer (Guildf) 109:170–175

    Article  CAS  Google Scholar 

  15. Yang J, Yeom J, Woo B, Hoffman AS, Kwang S (2014) In situ -forming injectable hydrogels for regenerative medicine. Prog Polym Sci 39:1973–1986

    Article  CAS  Google Scholar 

  16. Jones JR (2013) Review of bioactive glass: from Hench to hybrids. Acta Biomater 9:4457–4486

    Article  CAS  Google Scholar 

  17. Barabadi Z et al (2016) Fabrication of hydrogel based nanocomposite scaffold containing bioactive glass nanoparticles for myocardial tissue engineering. Mater Sci Eng C 69:1137–1146

    Article  CAS  Google Scholar 

  18. Mosqueira L et al (2021) Strontium-releasing sol–gel bioactive glass spheres and their ability to stimulate osteogenic differentiation in osteoporotic bone marrow mesenchymal stem cells. J Mater Res 36:459–474

    Article  CAS  Google Scholar 

  19. Nawaz Q et al (2018) Synthesis and characterization of manganese containing mesoporous bioactive glass nanoparticles for biomedical applications. J Mater Sci Mater Med. https://doi.org/10.1007/s10856-018-6070-4

    Article  Google Scholar 

  20. Liu M et al (2017) Injectable hydrogels for cartilage and bone tissue engineering. Bone Res. https://doi.org/10.1038/boneres.2017.14

    Article  Google Scholar 

  21. Jones JR (2009) New trends in bioactive scaffolds: the importance of nanostructure. J Eur Ceram Soc 29:1275–1281

    Article  CAS  Google Scholar 

  22. Utech S, Boccaccini AR (2016) A review of hydrogel-based composites for biomedical applications: enhancement of hydrogel properties by addition of rigid inorganic fillers. J Mater Sci 51:271–310

    Article  CAS  Google Scholar 

  23. Won D, Kim M, Tae G (2015) Colloids and surfaces B: biointerfaces systemic modulation of the stability of pluronic hydrogel by a small amount of graphene oxide. Coll Surf B Biointerfaces 128:515–521

    Article  CAS  Google Scholar 

  24. Gioffredi E et al (2016) Pluronic F127 hydrogel characterization and biofabrication in cellularized constructs for tissue engineering applications. Procedia CIRP 49:125–132

    Article  Google Scholar 

  25. Moreira CDF, Carvalho SM, Mansur HS, Pereira MM (2016) Thermogelling chitosan-collagen-bioactive glass nanoparticle hybrids as potential injectable systems for tissue engineering. Mater Sci Eng C 58:1207–1216

    Article  CAS  Google Scholar 

  26. Chen S et al (2020) Biodegradable zinc-containing mesoporous silica nanoparticles for cancer therapy. Mater Today Adv. https://doi.org/10.1016/j.mtadv.2020.100066

    Article  Google Scholar 

  27. Boonlai W, Tantishaiyakul V, Hirun N, Sangfai T, Suknuntha K (2018) Thermosensitive poloxamer 407/Poly(Acrylic Acid) hydrogels with potential application as injectable drug delivery system. AAPS PharmSciTech 19:2103–2117

    Article  CAS  Google Scholar 

  28. Radivojša M, Grabnar I, Grabnar PA (2013) Thermoreversible in situ gelling poloxamer-based systems with chitosan nanocomplexes for prolonged subcutaneous delivery of heparin: design and in vitro evaluation. Eur J Pharm Sci 50:93–101

    Article  CAS  Google Scholar 

  29. Boffito M et al (2016) Novel polyurethane-based thermosensitive hydrogels as drug release and tissue engineering platforms: design and in vitro characterization. Polym Int. https://doi.org/10.1002/pi.5080

    Article  Google Scholar 

  30. Xin C, Lihong W, Qiuyuan L, Hongzhuo L (2014) Injectable long-term control-released in situ gels of hydrochloric thiothixene for the treatment of schizophrenia: preparation, in vitro and in vivo evaluation. Int J Pharm 469:23–30

    Article  CAS  Google Scholar 

  31. Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials. https://doi.org/10.1016/j.biomaterials.2011.01.004

    Article  Google Scholar 

  32. Zheng K, Boccaccini AR (2017) Sol-gel processing of bioactive glass nanoparticles: a review. Adv Coll Interface Sci 249:363–373

    Article  CAS  Google Scholar 

  33. Thommes M et al (2015) Physisorption of gases, with special reference to the evaluation of surface area and pore size distribution (IUPAC Technical Report). Pure Appl Chem 87:1051–1069

    Article  CAS  Google Scholar 

  34. Zheng Y et al (2016) In vitro study of calcium phosphate layers on hydroxyapatite ceramics surface mineralized in different solutions. Ceram Int 42:1660–1665

    Article  CAS  Google Scholar 

  35. Li Y, Chen X, Ning C, Yuan B, Hu Q (2015) Facile synthesis of mesoporous bioactive glasses with controlled shapes. Mater Lett 161:605–608

    Article  CAS  Google Scholar 

  36. Nawaz A, Bano S, Yasir M, Wadood A, Ur Rehman MA (2020) Ag and Mn-doped mesoporous bioactive glass nanoparticles incorporated into the chitosan/gelatin coatings deposited on PEEK/bioactive glass layers for favorable osteogenic differentiation and antibacterial activity. Mater Adv 1:1273–1284

    Article  CAS  Google Scholar 

  37. Yap LS, Yang MC (2016) Evaluation of hydrogel composing of Pluronic F127 and carboxymethyl hexanoyl chitosan as injectable scaffold for tissue engineering applications. Coll Surf B Biointerfaces 146:204–211

    Article  CAS  Google Scholar 

  38. Xie Y, Tang J, Lu Z, Sun Z, An L (2013) Effects of poly(Propylene Oxide)–Poly(Ethylene Oxide)–Poly(Propylene Oxide) triblock copolymer on the gelation of poly(Ethylene Oxide)–poly(Propylene Oxide)–poly(Ethylene Oxide) aqueous solutions. J Macromol Sci Part B 52:1183–1197

    Article  CAS  Google Scholar 

  39. Bonacucina G, Cespi M, Mencarelli G, Giorgioni G, Palmieri GF (2011) Thermosensitive self-assembling block copolymers as drug delivery systems. Polymers. https://doi.org/10.3390/polym3020779

    Article  Google Scholar 

  40. Matanović MR, Kristl J, Grabnar PA (2014) Thermoresponsive polymers: Insights into decisive hydrogel characteristics, mechanisms of gelation, and promising biomedical applications. Int J Pharm 472:262–275

    Article  CAS  Google Scholar 

  41. Boucenna I, Royon L, Colinart P, Guedeau-Boudeville MA, Mourchid A (2010) Structure and thermorheology of concentrated pluronic copolymer micelles in the presence of laponite particles. Langmuir 26:14430–14436

    Article  CAS  Google Scholar 

  42. Carlfors J, Edsman K, Petersson R, Jörnving K (1998) Rheological evaluation of Gelrite® in situ gels for ophthalmic use. Eur J Pharm Sci 6:113–119

    Article  CAS  Google Scholar 

  43. Dou Q, Karim AA, Loh XJ (2016) Modification of thermal and mechanical properties of PEG-PPG-PEG copolymer (F127) with MA-POSS. Polymers (Basel). https://doi.org/10.3390/polym8090341

    Article  Google Scholar 

  44. Zhang M, Djabourov M, Bourgaux C, Bouchemal K (2013) Nanostructured fluids from pluronic® mixtures. Int J Pharm 454:599–610

    Article  CAS  Google Scholar 

  45. Gentile L, De Luca G, Antunes FE, Rossi CO, Ranieri GA (2010) Thermogelation analysis of F127-water mixtures by physical Chemistry techniques. Appl Rheol 20:1–12

    Google Scholar 

  46. Zhang L, Parsons DL, Navarre C, Kompella UB (2002) Development and in-vitro evaluation of sustained release Poloxamer 407 (P407) gel formulations of ceftiofur. J Control Rel 85:73–81

    Article  CAS  Google Scholar 

  47. Won DA, Kim M, Tae G (2015) Systemic modulation of the stability of pluronic hydrogel by a small amount of graphene oxide. Coll Surf B Biointerfaces 128:515–521

    Article  CAS  Google Scholar 

  48. Branca C, Khouzami K, Wanderlingh U, D’Angelo G (2018) Effect of intercalated chitosan/clay nanostructures on concentrated pluronic F127 solution: a FTIR-ATR, DSC and rheological study. J Coll Interface Sci 517:221–229

    Article  CAS  Google Scholar 

  49. Sergi R, Bellucci D, Cannillo V (2020) A review of bioactive glass/natural polymer composites: state of the art. Materials (Basel) 13:1–38

    Google Scholar 

  50. Martins T et al (2017) Novel 3D composites with highly flexible behavior based on chitosan and bioactive glass for biomedical applications. Mater Chem Phys 189:1–11

    Article  CAS  Google Scholar 

  51. Gantar A et al (2014) Nanoparticulate bioactive-glass-reinforced gellan-gum hydrogels for bone-tissue engineering. Mater Sci Eng C 43:27–36

    Article  CAS  Google Scholar 

  52. Leite AJ, Mano JF (2017) Biomedical applications of natural-based polymers combined with bioactive glass nanoparticles. J Mater Chem B 5:4555–4568

    Article  CAS  Google Scholar 

  53. Quah SP, Smith AJ, Preston AN, Laughlin ST, Bhatia SR (2018) Large-area alginate/PEO-PPO-PEO hydrogels with thermoreversible rheology at physiological temperatures. Polymer (Guildf) 135:171–177

    Article  CAS  Google Scholar 

  54. Dumortier G, Grossiord JL, Agnely F, Chaumeil JC (2006) A review of poloxamer 407 pharmaceutical and pharmacological characteristics. Pharm Res 23:2709–2728

    Article  CAS  Google Scholar 

  55. Su YL, Wang J, Liu HZ (2002) FTIR spectroscopic investigation of effects of temperature and concentration on PEO-PPO-PEO block copolymer properties in aqueous solutions. Macromolecules 35:6426–6431

    Article  CAS  Google Scholar 

  56. de Laia AGS et al (2020) Therapeutic cobalt ion incorporated in poly(vinyl alcohol)/bioactive glass scaffolds for tissue engineering. J Mater Sci 55:8710–8727

    Article  CAS  Google Scholar 

  57. Park KM et al (2009) Thermosensitive chitosan-Pluronic hydrogel as an injectable cell delivery carrier for cartilage regeneration. Acta Biomater 5:1956–1965

    Article  CAS  Google Scholar 

  58. Fu S et al (2009) Injectable biodegradable thermosensitive hydrogel composite for orthopedic tissue engineering. 1. Preparation and characterization of nanohydroxyapatite/ poly(ethylene glycol)-poly(ε-caprolactone)-poly(ethylene glycol) hydrogel nanocomposites. J Phys Chem B 113:16518–16525

    Article  CAS  Google Scholar 

  59. dos Santos DMM, de Carvalho SM, Pereira MM, Houmard M, Nunes EHM (2019) Freeze-cast composite scaffolds prepared from sol-gel derived 58S bioactive glass and polycaprolactone. Ceram Int 45:9891–9900

    Article  CAS  Google Scholar 

  60. Jung YP et al (2017) Thermo-sensitive injectable hydrogel based on the physical mixing of hyaluronic acid and Pluronic F-127 for sustained NSAID delivery. Carbohydr Polym 156:403–408

    Article  CAS  Google Scholar 

  61. Diniz IMA et al (2015) Pluronic F-127 hydrogel as a promising scaffold for encapsulation of dental-derived mesenchymal stem cells. J Mater Sci Mater Med 26:1–10

    Article  CAS  Google Scholar 

  62. Cilurzo F et al (2011) Injectability evaluation: an open issue. AAPS Pharm Sci Tech 12:604–609

    Article  Google Scholar 

  63. Rungseevijitprapa W, Bodmeier R (2009) Injectability of biodegradable in situ forming microparticle systems (ISM). Eur J Pharm Sci 36:524–531

    Article  CAS  Google Scholar 

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Acknowledgements

The authors also gratefully acknowledge financial support from CNPq, CAPES and FAPEMIG/Brazil.

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Authors and Affiliations

  1. Department of Metallurgical and Materials Engineering, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

    Priscilla Mol Queiroz, Breno Rocha Barrioni & Marivalda de Magalhães Pereira

  2. Institute of Engineering, Science and Technology, Federal University of Vales do Jequitinhonha e Mucuri, Janaúba, Minas Gerais, Brazil

    Breno Rocha Barrioni

  3. Department of Chemistry Engineering, Federal University of Minas Gerais, Belo Horizonte, , Minas Gerais, Brazil

    Jesús Nuncira

  4. Nanomaterials and Graphene Technology Center (CTNano-UFMG), Belo Horizonte, Minas Gerais, Brazil

    Jesús Nuncira

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  1. Priscilla Mol Queiroz
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  4. Marivalda de Magalhães Pereira
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Correspondence to Priscilla Mol Queiroz.

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Queiroz, P.M., Barrioni, B.R., Nuncira, J. et al. Injectability study and rheological evaluation of Pluronic-derived thermosensitive hydrogels containing mesoporous bioactive glass nanoparticles for bone regeneration. J Mater Sci 57, 13027–13042 (2022). https://doi.org/10.1007/s10853-022-07468-2

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