Skip to main content
Log in

Comparative study of PCL-HAp and PCL-bioglass composite scaffolds for bone tissue engineering

  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

The aim of this work is to compare the effect of hydroxyapatite (HAp) or bioglass (BG) nanoparticles in a polycaprolactone composite scaffold aimed to bone regeneration. To allow a comparison of the influence of both types of fillers, scaffolds made of PCL or composites containing up to 20 % by weight HAp or BG were obtained. Scaffolds showed acceptable mechanical properties for its use and high interconnected porosity apt for cellular colonization. To study the effect of the different materials on pre-osteoblast cells differentiation, samples with 5 % mineral reinforcement, were cultured for up to 28 days in osteogenic medium. Cells proliferated in all scaffolds. Nevertheless, differentiation levels for the selected markers were higher in pure PCL scaffolds than in the composites; inclusion of bioactive particles showed no positive effects on cell differentiation. In osteogenic culture conditions, the presence of bioactive particles is thus not necessary in order to observe good differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Palmer LC, Newcomb CJ, Kaltz SR, Spoerke ED, Stupp SI. Biomimetic systems for hydroxyapatite mineralization inspired by bone and enamel. Chem Rev. 2008;11:4754–83.

    Article  Google Scholar 

  2. Stevens MM. Biomaterials for bone tissue engineering. Mater Today. 2008;11:18–25.

    Article  CAS  Google Scholar 

  3. Shu R, McMullen R, Baumann MJ, McCabe LR. Hydroxyapatite accelerates differentiation and suppresses growth of MC3T3-E1 osteoblasts. J Biomed Mater Res Part A. 2003;67A:1196–204.

    Article  CAS  Google Scholar 

  4. Wutticharoenmongkol P, Pavasant P, Supaphol P. Osteoblastic phenotype expression of MC3T3-E1 cultured on electrospun polycaprolactone fiber mats filled with hydroxyapatite nanoparticles. Biomacromolecules. 2007;8:2602–10.

    Article  CAS  Google Scholar 

  5. Supova M. Problem of hydroxyapatite dispersion in polymer matrices: a review. J Mater Sci Mater Med. 2009;20:1201–13.

    Article  CAS  Google Scholar 

  6. Braye F, Irigaray JL, Jallot E, Oudadesse H, Weber G, Deschamps N, Deschamps C, Frayssinet P, Tourermet P, Tixier H, Terve S, Lefaivrell J, Amirabad A. Resorption kinetics of osseous substitute: natural coral and svnthetic hydroxyapatite. Biomaterials. 1996;17:1345–50.

    Article  CAS  Google Scholar 

  7. Valerio P, Pereira MM, Goes AM, Leite FM. The effect of ionic products from bioactive glass dissolution on osteoblast proliferation and collagen production. Biomaterials. 2004;25:2941–8.

    Article  CAS  Google Scholar 

  8. Reffitt DM, Ogston N, Jugdaohsingh R, Cheung HFJ, Evans BAJ, Thompson RPH, Powell JJ, Hampson GN. Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone. 2003;32:127–35.

    Article  CAS  Google Scholar 

  9. Lakshmi SN, Cato TL. Biodegradable polymers as biomaterials. Prog Polym Sci. 2007;32:762–98.

    Article  Google Scholar 

  10. Katsanevakis E, Wen X, Shi D, et al. Biomineralization of polymer scaffolds. Key Eng Mater. 2010;441:269–95.

    Article  CAS  Google Scholar 

  11. Zhang K, Wang Y, Hillmyer MA, Francis LF. Processing and properties of porous poly(l-lactide)/bioactive glass composites. Biomaterials. 2004;25:2489–500.

    Article  CAS  Google Scholar 

  12. Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials. 2006;27:3413–31.

    Article  CAS  Google Scholar 

  13. Murphy WL, Kohn DH, Mooney DJ. Growth of continuous bonelike mineral within porous poly(lactide-co-glycolide) scaffolds in vitro. J Biomed Mater Res A. 2000;50:1549–3296.

    Article  Google Scholar 

  14. Ma PX, Zhang R, Xiao G, Franceschi R. Engineering new bone tissue in vitro on highly porous poly(a-hydroxyl acids)/hydroxyapatite composite scaffolds. J Biomed Mater Res. 2000;54:284–93.

    Article  Google Scholar 

  15. El-Ghannam A, Ducheyne P, Shapiro IM. Porous bioactive glass and hydroxyapatite ceramic affect bone cell function in vitro along different time lines. J Biomed Mater Res. 1998;36:167–80.

    Article  Google Scholar 

  16. Matsuura T, Hosokawa R, Okamoto K, Kimoto T, Akagawa Y. Diverse mechanisms of osteoblast spreading on hydroxyapatite and titanium. Biomaterials. 2000;21:1121–7.

    Article  CAS  Google Scholar 

  17. Woo KM, Seo J, Zhang R, Ma PX. Suppression of apoptosis by enhanced protein adsorption on polymer/hydroxyapatite composite scaffolds. Biomaterials. 2007;28:2622–30.

    Article  CAS  Google Scholar 

  18. Kilpadi KL, Chang PL, Bellis SL. Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. J Biomed Mater Res. 2001;57:258–67.

    Article  CAS  Google Scholar 

  19. Shor L, Güçeri S, Wen X, Gandhi M, Sun W. Fabrication of three-dimensional polycaprolactone/hydroxyapatite tissue scaffolds and osteoblast-scaffold interactions in vitro. Biomaterials. 2007;28:5291–7.

    Article  CAS  Google Scholar 

  20. Chuenjitkuntaworn B, Inrung W, Damrongsri D, Mekaapiruk K, Supaphol P, Pavasant P. Polycaprolactone/hydroxyapatite composite scaffolds: preparation, characterization, and in vitro and in vivo biological responses of human primary bone cells. J Biomed Mater Res A. 2010;94:241–51.

    Google Scholar 

  21. Lua Y, Zhu A, Wang W, Shi H. New bioactive hybrid material of nano-hydroxyapatite based on N-carboxyethylchitosan for bone tissue engineering. Appl Surf Sci. 2010;256:7228–33.

    Article  Google Scholar 

  22. Teng S, Chen L, Guo Y, Shi J. Formation of nano-hydroxyapatite in gelatin droplets and the resulting porous composite microspheres. J Inorg Biochem. 2007;101:686–91.

    Article  CAS  Google Scholar 

  23. Li Z, Yubao L, Aiping Y, Xulein P, Xuejiang W, Xiang Z. Preparation and in vitro investigation of chitosan/nano-hydroxyapatite composite used as bone substitute materials. J Mater Sci Mater Med. 2005;16:213–9.

    Article  Google Scholar 

  24. Puppi D, Chiellini F, Piras AM, Chiellini E. Polymeric materials for bone and cartilage repair. Prog Polym Sci. 2010;35:403–40.

    Article  CAS  Google Scholar 

  25. Martin C, Winet H, Baot JY. Acidity near eroding polylactide–polyglycolide in vitro and in vivo in rabbit tibial bone chambers. Biomaterials. 1996;17:2373–80.

    Article  CAS  Google Scholar 

  26. Diba M, Kharaziha M, Fathi MH, Gholipourmalekabadi M, Samadikuchaksaraei A. Preparation and characterization of polycaprolactone/forsterite nanocomposite porous scaffolds designed for bone tissue regeneration. Compos Sci Technol. 2012;72:716–23.

    Article  CAS  Google Scholar 

  27. Rizzi SC, Heath DJ, Coombes AGA, Bock N, Textor M, Downes S. Biodegradable polymer/hydroxyapatite composites: surface analysis and initial attachment of human osteoblasts. J Biomed Mater Res. 2001;55:475–86.

    Article  CAS  Google Scholar 

  28. Fabbri P, Cannillo V, Sola A, Dorigato A, Chiellini F. Highly porous polycaprolactone-45S5 Bioglass® scaffolds for bone tissue engineering. Compos Sci Technol. 2011;70:1869–78.

    Article  Google Scholar 

  29. Cannillo V, Chiellini F, Fabbri P, Sola A. Production of Bioglass® 45S5–polycaprolactone composite scaffolds via salt-leaching. Compos struct. 2010;92:1823–32.

    Article  Google Scholar 

  30. Deb S, Mandegaran R, Di Silvio L. A porous scaffold for bone tissue engineering/45S5 Bioglass® derived porous scaffolds for co-culturing osteoblasts and endothelial cells. J Mater Sci Mater Med. 2010;21:893–905.

    Article  CAS  Google Scholar 

  31. Lebourg M, Suay Antón J, Gomez Ribelles JL. Hybrid structure in PCL-HAp scaffold resulting from biomimetic apatite growth. J Mater Sci Mater Med. 2010;21:33–44.

    Article  CAS  Google Scholar 

  32. Ho M-H, Kuo P-Y, Hsieh H-J, Hsien T-Y, Hou L-T, Lai J-Y, Wang D-M. Preparation of porous scaffolds by using freeze-extraction and freeze-gelation methods. Biomaterials. 2004;25:129–38.

    Article  CAS  Google Scholar 

  33. Storrie H, Stupp SI. Cellular response to zinc-containing organoapatite: an in vitro study of proliferation, alkaline phosphatase activity and biomineralization. Biomaterials. 2005;26:5492–9.

    Article  CAS  Google Scholar 

  34. Meloan SN, Puchtler H. Chemical mechanisms of staining methods: von Kossa’s technique. What von Kossa really wrote and a modified reaction for selective demonstration of inorganic phosphate. J Histotechnol. 1985;8:11–3.

    Article  Google Scholar 

  35. Habibovic P, Sees TM, van den Doel MA, van Blitterswijk CA, de Groot K. Osteoinduction by biomaterials-physicochemical and structural influences. J Biomed Mater Res A. 2006;77A:747–62.

    Article  CAS  Google Scholar 

  36. Bohner M, Lemaitre J. Can bioactivity be tested in vitro with SBF solution? Biomaterials. 2009;30:2175–9.

    Article  CAS  Google Scholar 

  37. Li X, van Blitterswijk CA, Feng Q, Cui F, Watari F. The effect of calcium phosphate microstructure on bone-related cells in vitro. Biomaterials. 2008;29:3306–16.

    Article  CAS  Google Scholar 

  38. Denis FA, Hanarp P, Sutherland DS, Gold J, Mustin C, Rouxhet PG, Dufrêne YF. Protein adsorption on model surfaces with controlled nanotopography and chemistry. Langmuir. 2002;18:819–28.

    Article  CAS  Google Scholar 

  39. Galli C, Coen MC, Hauert R, Katanaev VL, Gröning P, Schlapbach L. Creation of nanostructures to study the topographical dependency of protein adsorption. Colloids Surf B Biointerfaces. 2002;26:255–67.

    Article  CAS  Google Scholar 

  40. Cai L, Guinn AS, Wang S. Exposed hydroxyapatite particles on the surface of photo-crosslinked nanocomposites for promoting MC3T3 cell proliferation and differentiation. Acta Biomater. 2011;7:2185–99.

    Article  CAS  Google Scholar 

  41. Pitt CG, Zhong-wei G. Modification of the rates of chain cleavage of poly(ϵ-caprolactone) and related polyesters in the solid state. J Control Release. 1987;4(4):283–92.

    Article  CAS  Google Scholar 

  42. Kaysinger KK, Ramp WK. Extracellular pH modulates the activity of cultured human osteoblasts. J Cell Biochem. 1998;68:83–9.

    Article  CAS  Google Scholar 

  43. Wei G, Ma PX. Structure and properties of nano-hydroxyapatite/polymer composite scaffolds for bone tissue engineering. Biomaterials. 2004;25:4749–57.

    Article  CAS  Google Scholar 

  44. Lee HJ, Kim SE, Choi HW, Kim CW, Kim KJ, Lee SC. The effect of surface-modified nano-hydroxyapatite on biocompatibility of poly(ε-caprolactone)/hydroxyapatite nanocomposites. Eur Polym J. 2007;43:1602–8.

    Article  CAS  Google Scholar 

  45. Verrier S, Blaker JJ, Maquet V, Hencha LL, Boccaccini AR. PDLLA/bioglass composites for soft-tissue and hard tissue engineering: an in vitro cell biology assessment. Biomaterials. 2004;25:3013–21.

    Article  CAS  Google Scholar 

  46. Lian JB, Stein GS. Concepts of osteoblast growth osteoblast growth and differentiation: modulation of bone cell development and tissue formation. Critical Rev Oral Biol Med. 1992;3(3):269–305.

    CAS  Google Scholar 

  47. Choi JY, lee BH, Song KB, Park RW, Kim IS, Sohn KY, Jo JS, Ryoo HM. Expression patterns of bone-related proteins during osteoblastic differentiation in MC3T3-E1 cells. J Cell Biochem. 1996;61:609–18.

    Article  CAS  Google Scholar 

  48. Al-Jallad HF, Nakano Y, Chen JLY, McMillan E, Lefebvre C, Kaartinen MT. Transglutaminase activity regulates osteoblast differentiation and matrix mineralization in MC3T3-E1 osteoblast cultures. Matrix Biol. 2006;25:135–48.

    Article  CAS  Google Scholar 

  49. Varanasi VG, Saiz E, Loomer PM, Ancheta B, Uritani N, Ho SP, Tomsia AP, Marshall SJ, Marshall GW. Enhanced osteocalcin expression by osteoblast-like cells (MC3T3-E1) exposed to bioactive coating glass (SiO2–CaO–P2O5–MgO–K2O–Na2O system) ions. Acta Biomater. 2009;5:3536–47.

    Article  CAS  Google Scholar 

  50. Foppiano S, Marshall SJ, Marshall GW, Saiz E, Tomsia AP. Bioactive glass coatings affect the behavior of osteoblast-like cells. Acta Biomater. 2007;3:765–71.

    Article  CAS  Google Scholar 

  51. Reilly GC, Radin S, Chen AT, Ducheyne P. Differential alkaline phosphatase responses of rat and human bone marrow derived mesenchymal stem cells to 45S5 bioactive glass. Biomaterials. 2007;28:4091–7.

    Article  CAS  Google Scholar 

  52. Li LH, Kommareddy KP, Pilz C, Zhou CR, Fratzl P, Manjubala I. In vitro bioactivity of bioresorbable porous polymeric scaffolds incorporating hydroxyapatite microspheres. Acta Biomater. 2010;6:2525–31.

    Article  CAS  Google Scholar 

  53. Schneider GB, Perinpanayagam H, Clegg M, Zaharias R, Seabold D, Keller J, Stanford C. Implant surface roughness affects osteoblast gene expression. J Dent Res. 2003;82:372–6.

    Article  CAS  Google Scholar 

  54. Alliot-Licht B, Gregoire M, Orly I, Menanteau J. Cellular activity of osteoblasts in the presence of hydroxyapatite: an in vitro experiment. Biomaterials. 1991;12:752–6.

    Article  CAS  Google Scholar 

  55. Prigodich RV, Vesely MR. Characterization of the complex between bovine osteocalcin and type I collagen. Arch Biochem Biophys. 1997;345(2):339–41.

    Article  CAS  Google Scholar 

  56. Wenstrup RJ, Fowlkes JL, Wittei DP, Florer JB. Discordant expression of osteoblast markers in MC3T3-E1 cells that synthesize a high turnover matrix. J Biol Chem. 1996;271(17):10271–6.

    Article  CAS  Google Scholar 

  57. Franceschi RT, Iyer BS, Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res. 1994;9:843–54.

    Article  CAS  Google Scholar 

  58. Bonewald LF. Cell–cell and cell–matrix interactions in bone. In: Bradshaw RA, Dennis EA, editors. Handbook of Cell Signaling (Second Edition). Elsevier Academic Press; 2009. pp 109-124.

  59. Xu L, Anderson AL, Lu Q, Wang J. Role of fibrillar structure of collagenous carrier in bone sialoprotein-mediated matrix mineralization and osteoblast differentiation. Biomaterials. 2007;28:750–61.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

JLGR acknowledges the support of the Spanish Ministry of Science and Education through project No. MAT2010-21611-C03-01 (including the FEDER financial support), and from Generalitat Valenciana, ACOMP/2012/075 Project.. Lebourg acknowledges the support of UPV through Project PAID-O6-10 and thanks CIBER-BBN for funding her post-doc research. CIBER-BBN is an initiative funded by the VI National R&D&i Plan 2008–2011, Iniciativa Ingenio 2010, Consolider Program, CIBER Actions and financed by the Instituto de Salud Carlos III with assistance from the European Regional Development Fund. J. Ródenas acknowledges the funding of his PhD by the Generalitat Valenciana through VALi+d Grant. The authors also wish to thank the microscopy service of Universidad Politécnica de Valencia as well as the confocal microscopy service of the Research Centre Principe Felipe for useful help and advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joaquín Ródenas-Rochina.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ródenas-Rochina, J., Ribelles, J.L.G. & Lebourg, M. Comparative study of PCL-HAp and PCL-bioglass composite scaffolds for bone tissue engineering. J Mater Sci: Mater Med 24, 1293–1308 (2013). https://doi.org/10.1007/s10856-013-4878-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10856-013-4878-5

Keywords

Navigation