Advertisement

The Use of Electrospinning Technique on Osteochondral Tissue Engineering

  • Marta R. Casanova
  • Rui L. Reis
  • Albino Martins
  • Nuno M. Neves
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1058)

Abstract

Electrospinning, an electrostatic fiber fabrication technique, has attracted significant interest in recent years due to its versatility and ability to produce highly tunable nanofibrous meshes. These nanofibrous meshes have been investigated as promising tissue engineering scaffolds since they mimic the scale and morphology of the native extracellular matrix. The sub-micron diameter of fibers produced by this process presents various advantages like the high surface area to volume ratio, tunable porosity, and the ability to manipulate the nanofiber composition in order to get desired properties and functionality. Electrospun fibers can be oriented or arranged randomly, giving control over both mechanical properties and the biological response to the fibrous scaffold. Moreover, bioactive molecules can be integrated with the electrospun nanofibrous scaffolds in order to improve the cellular response. This chapter presents an overview of the developments on electrospun polymer nanofibers including processing, structure, and their applications in the field of osteochondral tissue engineering.

Keywords

Nanofibrous meshes Processing parameters Topographies Surface functionalization 

References

  1. 1.
    Martins A, Reis RL, Neves NM (2008) Electrospinning: processing technique for tissue engineering scaffolding. Int Mater Rev 53(5):257–274.  https://doi.org/10.1179/174328008x353547 CrossRefGoogle Scholar
  2. 2.
    Rajesh KP, Natarajan TS (2009) Electrospun polymer nanofibrous membrane for filtration. J Nanosci Nanotechnol 9(9):5402–5405CrossRefGoogle Scholar
  3. 3.
    Beringer LT, Xu X, Shih W, Shih WH, Habas R, Schauer CL (2015) An electrospun PVDF-TrFe fiber sensor platform for biological applications. Sensor Actuat A Phys 222:293–300.  https://doi.org/10.1016/j.sna.2014.11.012 CrossRefGoogle Scholar
  4. 4.
    Smith LA, Ma PX (2004) Nano-fibrous scaffolds for tissue engineering. Colloid Surf B 39(3):125–131.  https://doi.org/10.1016/j.colsurfb.2003.12.004 CrossRefGoogle Scholar
  5. 5.
    Martins A, Pinho ED, Faria S, Pashkuleva I, Marques AP, Reis RL, Neves NM (2009) Surface modification of electrospun polycaprolactone nanofiber meshes by plasma treatment to enhance biological performance. Small 5(10):1195–1206.  https://doi.org/10.1002/smll.200801648 CrossRefPubMedGoogle Scholar
  6. 6.
    Casper CL, Stephens JS, Tassi NG, Chase DB, Rabolt JF (2004) Controlling surface morphology of electrospun polystyrene fibers: effect of humidity and molecular weight in the electrospinning process. Macromolecules 37(2):573–578.  https://doi.org/10.1021/ma0351975 CrossRefGoogle Scholar
  7. 7.
    Araujo JV, Martins A, Leonor IB, Pinho ED, Reis RL, Neves NM (2008) Surface controlled biomimetic coating of polycaprolactone nanofiber meshes to be used as bone extracellular matrix analogues. J Biomater Sci Polym E 19(10):1261–1278.  https://doi.org/10.1163/156856208786052335 CrossRefGoogle Scholar
  8. 8.
    da Silva MA, Crawford A, Mundy J, Martins A, Araujo JV, Hatton PV, Reis RL, Neves NM (2009) Evaluation of extracellular matrix formation in polycaprolactone and starch-compounded polycaprolactone nanofiber meshes when seeded with bovine articular chondrocytes. Tissue Eng Part A 15(2):377–385.  https://doi.org/10.1089/ten.tea.2007.0327 CrossRefPubMedGoogle Scholar
  9. 9.
    Rezvani Z, Venugopal JR, Urbanska AM, Mills DK, Ramakrishna S, Mozafari M (2016) A bird’s eye view on the use of electrospun nanofibrous scaffolds for bone tissue engineering: current state-of-the-art, emerging directions and future trends. Nanomedicine 12(7):2181–2200.  https://doi.org/10.1016/j.nano.2016.05.014 CrossRefPubMedGoogle Scholar
  10. 10.
    Doshi J, Reneker DH (1995) Electrospinning process and applications of electrospun fibers. J Electrostat 35(2-3):151–160.  https://doi.org/10.1016/0304-3886(95)00041-8 CrossRefGoogle Scholar
  11. 11.
    Ganan-Calvo AM, Davila J, Barrero A (1997) Current and droplet size in the electrospraying of liquids. Scaling laws. J Aerosol Sci 28(2):249–275.  https://doi.org/10.1016/S0021-8502(96)00433-8 CrossRefGoogle Scholar
  12. 12.
    Formhals A (1934) Method and apparatus for spinning. US patent 1975504Google Scholar
  13. 13.
    Gibson P, Schreuder-Gibson H, Rivin D (2001) Transport properties of porous membranes based on electrospun nanofibers. Colloid Surf A 187:469–481.  https://doi.org/10.1016/S0927-7757(01)00616-1 CrossRefGoogle Scholar
  14. 14.
    Ghorani B, Tucker N (2015) Fundamentals of electrospinning as a novel delivery vehicle for bioactive compounds in food nanotechnology. Food Hydrocolloid 51:227–240.  https://doi.org/10.1016/j.foodhyd.2015.05.024 CrossRefGoogle Scholar
  15. 15.
    Taylor G (1964) Disintegration of water drops in an electric field. Proc R Soc Lond Ser A Math Phys Sci 280(1382):383–397.  https://doi.org/10.1098/rspa.1964.0151 CrossRefGoogle Scholar
  16. 16.
    Dabirian F, Ravandi SAH, Pishevar AR, Abuzade RA (2011) A comparative study of jet formation and nanofiber alignment in electrospinning and electrocentrifugal spinning systems. J Electrost 69(6):540–546.  https://doi.org/10.1016/j.elstat.2011.07.006 CrossRefGoogle Scholar
  17. 17.
    Li D, Wang YL, Xia YN (2004) Electrospinning nanofibers as uniaxially aligned arrays and layer-by-layer stacked films. Adv Mater 16(4):361–366.  https://doi.org/10.1002/adma.200306226 CrossRefGoogle Scholar
  18. 18.
    Sharma N, Jaffari GH, Shah SI, Pochan DJ (2010) Orientation-dependent magnetic behavior in aligned nanoparticle arrays constructed by coaxial electrospinning. Nanotechnology 21(8):85707.  https://doi.org/10.1088/0957-4484/21/8/085707 CrossRefPubMedGoogle Scholar
  19. 19.
    Teo WE, Ramakrishna S (2006) A review on electrospinning design and nanofibre assemblies. Nanotechnology 17(14):R89–R106.  https://doi.org/10.1088/0957-4484/17/14/R01 CrossRefPubMedGoogle Scholar
  20. 20.
    Bognitzki M, Frese T, Steinhart M, Greiner A, Wendorff JH, Schaper A, Hellwig M (2001) Preparation of fibers with nanoscaled morphologies: electrospinning of polymer blends. Polym Eng Sci 41(6):982–989.  https://doi.org/10.1002/pen.10799 CrossRefGoogle Scholar
  21. 21.
    Lee JS, Choi KH, Do Ghim H, Kim SS, Chun DH, Kim HY, Lyoo WS (2004) Role of molecular weight of atactic poly(vinyl alcohol) (PVA) in the structure and properties of PVA nanofabric prepared by electrospinning. J Appl Polym Sci 93(4):1638–1646.  https://doi.org/10.1002/app.20602 CrossRefGoogle Scholar
  22. 22.
    Alves da Silva M, Martins A, Costa-Pinto AR, Monteiro N, Faria S, Reis RL, Neves NM (2017) Electrospun nanofibrous meshes cultured with Wharton’s jelly stem cell: an alternative for cartilage regeneration, without the need of growth factors. Biotechnol J 12.  https://doi.org/10.1002/biot.201700073
  23. 23.
    Deitzel JM, Kleinmeyer J, Harris D, Tan NCB (2001) The effect of processing variables on the morphology of electrospun nanofibers and textiles. Polymer 42(1):261–272.  https://doi.org/10.1016/S0032-3861(00)00250-0 CrossRefGoogle Scholar
  24. 24.
    Deitzel JM, Kleinmeyer JD, Hirvonen JK, Tan NCB (2001) Controlled deposition of electrospun poly(ethylene oxide) fibers. Polymer 42(19):8163–8170.  https://doi.org/10.1016/S0032-3861(01)00336-6 CrossRefGoogle Scholar
  25. 25.
    Yarin AL, Koombhongse S, Reneker DH (2001) Taylor cone and jetting from liquid droplets in electrospinning of nanofibers. J Appl Phys 90(9):4836–4846.  https://doi.org/10.1063/1.1408260 CrossRefGoogle Scholar
  26. 26.
    Megelski S, Stephens JS, Chase DB, Rabolt JF (2002) Micro- and nanostructured surface morphology on electrospun polymer fibers. Macromolecules 35(22):8456–8466.  https://doi.org/10.1021/ma020444a CrossRefGoogle Scholar
  27. 27.
    Tan SH, Inai R, Kotaki M, Ramakrishna S (2005) Systematic parameter study for ultra-fine fiber fabrication via electrospinning process. Polymer 46(16):6128–6134.  https://doi.org/10.1016/j.polymer.2005.05.068 CrossRefGoogle Scholar
  28. 28.
    Frenot A, Chronakis IS (2003) Polymer nanofibers assembled by electrospinning. Curr Opin Colloid Interface Sci 8(1):64–75.  https://doi.org/10.1016/S1359-0294(03)00004-9 CrossRefGoogle Scholar
  29. 29.
    Reneker DH, Chun I (1996) Nanometre diameter fibres of polymer, produced by electrospinning. Nanotechnology 7(3):216–223.  https://doi.org/10.1088/0957-4484/7/3/009 CrossRefGoogle Scholar
  30. 30.
    Hsu CM, Shivkumar S (2004) Nano-sized beads and porous fiber constructs of poly(epsilon-caprolactone) produced by electrospinning. J Mater Sci 39(9):3003–3013.  https://doi.org/10.1023/B:JMSC.0000025826.36080.cf CrossRefGoogle Scholar
  31. 31.
    Thompson CJ, Chase GG, Yarin AL, Reneker DH (2007) Effects of parameters on nanofiber diameter determined from electrospinning model. Polymer 48(23):6913–6922.  https://doi.org/10.1016/j.polymer.2007.09.017 CrossRefGoogle Scholar
  32. 32.
    Reneker DH, Yarin AL (2008) Electrospinning jets and polymer nanofibers. Polymer 49(10):2387–2425.  https://doi.org/10.1016/j.polymer.2008.02.002 CrossRefGoogle Scholar
  33. 33.
    Geng XY, Kwon OH, Jang JH (2005) Electrospinning of chitosan dissolved in concentrated acetic acid solution. Biomaterials 26(27):5427–5432.  https://doi.org/10.1016/j.biomaterials.2005.01.066 CrossRefPubMedGoogle Scholar
  34. 34.
    Ki CS, Baek DH, Gang KD, Lee KH, Um IC, Park YH (2005) Characterization of gelatin nanofiber prepared from gelatin-formic acid solution. Polymer 46(14):5094–5102.  https://doi.org/10.1016/j.polymer.2005.04.040 CrossRefGoogle Scholar
  35. 35.
    Hohman MM, Shin M, Rutledge G, Brenner MP (2001) Electrospinning and electrically forced jets. I. Stability theory. Phys Fluids 13(8):2201–2220.  https://doi.org/10.1063/1.1383791 CrossRefGoogle Scholar
  36. 36.
    Sun B, Long YZ, Zhang HD, Li MM, Duvail JL, Jiang XY, Yin HL (2014) Advances in three-dimensional nanofibrous macrostructures via electrospinning. Prog Polym Sci 39(5):862–890.  https://doi.org/10.1016/j.progpolymsci.2013.06.002 CrossRefGoogle Scholar
  37. 37.
    Koski A, Yim K, Shivkumar S (2004) Effect of molecular weight on fibrous PVA produced by electrospinning. Mater Lett 58(3–4):493–497.  https://doi.org/10.1016/S0167-577x(03)00532-9 CrossRefGoogle Scholar
  38. 38.
    Bhardwaj N, Kundu SC (2010) Electrospinning: a fascinating fiber fabrication technique. Biotechnol Adv 28(3):325–347.  https://doi.org/10.1016/j.biotechadv.2010.01.004 CrossRefPubMedGoogle Scholar
  39. 39.
    Brown TD, Daltona PD, Hutmacher DW (2016) Melt electrospinning today: an opportune time for an emerging polymer process. Prog Polym Sci 56:116–166.  https://doi.org/10.1016/j.progpolymsci.2016.01.001 CrossRefGoogle Scholar
  40. 40.
    Rodoplu D, Mutlu M (2012) Effects of electrospinning setup and process parameters on nanofiber morphology intended for the modification of quartz crystal microbalance surfaces. J Eng Fiber Fabr 7(2):118–123Google Scholar
  41. 41.
    Pelipenko J, Kristl J, Jankovic B, Baumgartner S, Kocbek P (2013) The impact of relative humidity during electrospinning on the morphology and mechanical properties of nanofibers. Int J Pharm 456(1):125–134.  https://doi.org/10.1016/j.ijpharm.2013.07.078 CrossRefPubMedGoogle Scholar
  42. 42.
    Dersch R, Liu TQ, Schaper AK, Greiner A, Wendorff JH (2003) Electrospun nanofibers: internal structure and intrinsic orientation. J Polym Sci Pol Chem 41(4):545–553.  https://doi.org/10.1002/pola.10609 CrossRefGoogle Scholar
  43. 43.
    Martins A, da Silva MLA, Faria S, Marques AP, Reis RL, Neves NM (2011) The influence of patterned nanofiber meshes on human mesenchymal stem cell osteogenesis. Macromol Biosci 11(7):978–987.  https://doi.org/10.1002/mabi.201100012 CrossRefPubMedGoogle Scholar
  44. 44.
    Martins A, Reis R, Neves N (2012) Critical aspects of electrospun meshes for biomedical applications. In: Neves N (ed) Electrospinning for advanced biomedical applications and therapies, pp 69–87Google Scholar
  45. 45.
    Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002) Electrospinning of collagen nanofibers. Biomacromolecules 3(2):232–238CrossRefGoogle Scholar
  46. 46.
    Kameoka J, Orth R, Yang YN, Czaplewski D, Mathers R, Coates GW, Craighead HG (2003) A scanning tip electrospinning source for deposition of oriented nanofibres. Nanotechnology 14(10):1124–1129.  https://doi.org/10.1088/0957-4484/14/10/310. pii: S0957-4484(03)61381-4CrossRefGoogle Scholar
  47. 47.
    Zussman E, Rittel D, Yarin AL (2003) Failure modes of electrospun nanofibers. Appl Phys Lett 82(22):3958–3960.  https://doi.org/10.1063/1.1579125 CrossRefGoogle Scholar
  48. 48.
    Buttafoco L, Kolkman NG, Engbers-Buijtenhuijs P, Poot AA, Dijkstra PJ, Vermes I, Feijen J (2006) Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials 27(5):724–734.  https://doi.org/10.1016/j.biomaterials.2005.06.024 CrossRefPubMedGoogle Scholar
  49. 49.
    Greiner A, Wendorff JH (2007) Electrospinning: a fascinating method for the preparation of ultrathin fibers. Angew Chem Int Ed Engl 46(30):5670–5703.  https://doi.org/10.1002/anie.200604646 CrossRefPubMedGoogle Scholar
  50. 50.
    Kidoaki S, Kwon IK, Matsuda T (2005) Mesoscopic spatial designs of nano- and microfiber meshes for tissue-engineering matrix and scaffold based on newly devised multilayering and mixing electrospinning techniques. Biomaterials 26(1):37–46.  https://doi.org/10.1016/j.biomaterials.2004.01.063 CrossRefPubMedGoogle Scholar
  51. 51.
    Casper CL, Yang WD, Farach-Carson MC, Rabolt JF (2007) Coating electrospun collagen and gelatin fibers with perlecan domain I for increased growth factor binding. Biomacromolecules 8(4):1116–1123.  https://doi.org/10.1021/bm061003s CrossRefPubMedGoogle Scholar
  52. 52.
    Li D, Xia YN (2004) Electrospinning of nanofibers: reinventing the wheel? Adv Mater 16(14):1151–1170.  https://doi.org/10.1002/adma.200400719 CrossRefGoogle Scholar
  53. 53.
    Malda J, Rouwkema J, Martens DE, le Comte EP, Kooy FK, Tramper J, van Blitterswijk CA, Riesle J (2004) Oxygen gradients in tissue-engineered PEGT/PBT cartilaginous constructs: measurement and modeling. Biotechnol Bioeng 86(1):9–18.  https://doi.org/10.1002/bit.20038 CrossRefPubMedGoogle Scholar
  54. 54.
    Sun ZC, Zussman E, Yarin AL, Wendorff JH, Greiner A (2003) Compound core-shell polymer nanofibers by co-electrospinning. Adv Mater 15(22):1929.  https://doi.org/10.1002/adma.200305136 CrossRefGoogle Scholar
  55. 55.
    Konno M, Kishi Y, Tanaka M, Kawakami H (2014) Core/shell-like structured ultrafine branched nanofibers created by electrospinning. Polym J 46(11):792–799.  https://doi.org/10.1038/pj.2014.74 CrossRefGoogle Scholar
  56. 56.
    Shin YM, Kim KS, Lim YM, Nho YC, Shin H (2008) Modulation of spreading, proliferation, and differentiation of human mesenchymal stem cells on gelatin-immobilized poly(L-lactide-co-epsilon-caprolactone) substrates. Biomacromolecules 9(7):1772–1781.  https://doi.org/10.1021/bm701410g CrossRefPubMedGoogle Scholar
  57. 57.
    Sahoo S, Ang LT, Goh JCH, Toh SL (2010) Growth factor delivery through electrospun nanofibers in scaffolds for tissue engineering applications. J Biomed Mater Res A 93a(4):1539–1550.  https://doi.org/10.1002/jbm.a.32645 CrossRefGoogle Scholar
  58. 58.
    Martins A, Gang W, Pinho ED, Rebollar E, Chiussi S, Reis RL, Leon B, Neves NM (2010) Surface modification of a biodegradable composite by UV laser ablation: in vitro biological performance. J Tissue Eng Regen Med 4(6):444–453.  https://doi.org/10.1002/term.255 CrossRefPubMedGoogle Scholar
  59. 59.
    Oberbossel G, Probst C, Giampietro VR, von Rohr PR (2017) Plasma afterglow treatment of polymer powders: process parameters, wettability improvement, and aging effects. Plasma Process Polym 14(3):e1600144.  https://doi.org/10.1002/ppap.201600144 CrossRefGoogle Scholar
  60. 60.
    Liu W, Zhan JC, Su Y, Wu T, Wu CC, Ramakrishna S, Mo XM, Al-Deyab SS, El-Newehy M (2014) Effects of plasma treatment to nanofibers on initial cell adhesion and cell morphology. Colloid Surf B 113:101–106.  https://doi.org/10.1016/j.colsurfb.2013.08.031 CrossRefGoogle Scholar
  61. 61.
    Chen F, Tang QL, Zhu YJ, Wang KW, Zhang ML, Zhai WY, Chang JA (2010) Hydroxyapatite nanorods/poly(vinyl pyrolidone) composite nanofibers, arrays and three-dimensional fabrics: electrospun preparation and transformation to hydroxyapatite nanostructures. Acta Biomater 6(8):3013–3020.  https://doi.org/10.1016/j.actbio.2010.02.015 CrossRefPubMedGoogle Scholar
  62. 62.
    Puppi D, Piras AM, Chiellini F, Chiellini E, Martins A, Leonor IB, Neves N, Reis R (2011) Optimized electro- and wet-spinning techniques for the production of polymeric fibrous scaffolds loaded with bisphosphonate and hydroxyapatite. J Tissue Eng Regen Med 5(4):253–263.  https://doi.org/10.1002/term.310 CrossRefPubMedGoogle Scholar
  63. 63.
    Zhang YZ, Venugopal JR, El-Turki A, Ramakrishna S, Su B, Lim CT (2008) Electrospun biomimetic nanocomposite nanofibers of hydroxyapatite/chitosan for bone tissue engineering. Biomaterials 29(32):4314–4322.  https://doi.org/10.1016/j.biomaterials.2008.07.038 CrossRefPubMedGoogle Scholar
  64. 64.
    Song JH, Kim HE, Kim HW (2008) Electrospun fibrous web of collagen-apatite precipitated nanocomposite for bone regeneration. J Mater Sci Mater Med 19(8):2925–2932.  https://doi.org/10.1007/s10856-008-3420-7 CrossRefPubMedGoogle Scholar
  65. 65.
    Phipps MC, Clem WC, Catledge SA, Xu Y, Hennessy KM, Thomas V, Jablonsky MJ, Chowdhury S, Stanishevsky AV, Vohra YK, Bellis SL (2011) Mesenchymal stem cell responses to bone-mimetic electrospun matrices composed of polycaprolactone, collagen I and nanoparticulate hydroxyapatite. PLoS One 6(2):e16813.  https://doi.org/10.1371/journal.pone.0016813 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Xie J, Lou X, Wang X, Yang L, Zhang Y (2015) Electrospun nanofibers of hydroxyapatite/collagen/chitosan promote osteogenic differentiation of the induced pluripotent stem cell-derived mesenchymal stem cells. J Control Release 213:e53.  https://doi.org/10.1016/j.jconrel.2015.05.087 CrossRefPubMedGoogle Scholar
  67. 67.
    Zhou Y, Yao H, Wang J, Wang D, Liu Q, Li Z (2015) Greener synthesis of electrospun collagen/hydroxyapatite composite fibers with an excellent microstructure for bone tissue engineering. Int J Nanomed 10:3203–3215.  https://doi.org/10.2147/IJN.S79241 CrossRefGoogle Scholar
  68. 68.
    Kwon GW, Gupta KC, Jung KH, Kang IK (2017) Lamination of microfibrous PLGA fabric by electrospinning a layer of collagen-hydroxyapatite composite nanofibers for bone tissue engineering. Biomater Res 21:11.  https://doi.org/10.1186/s40824-017-0097-3 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Monteiro N, Martins A, Pires R, Faria S, Fonseca NA, Moreira JN, Reisa RL, Neves NM (2014) Immobilization of bioactive factor-loaded liposomes on the surface of electrospun nanofibers targeting tissue engineering. Biomater Sci 2(9):1195–1209.  https://doi.org/10.1039/c4bm00069b CrossRefGoogle Scholar
  70. 70.
    Zhu Y, Mao ZW, Gao CY (2013) Aminolysis-based surface modification of polyesters for biomedical applications. RSC Adv 3(8):2509–2519.  https://doi.org/10.1039/c2ra22358a CrossRefGoogle Scholar
  71. 71.
    Oliveira C, Costa-Pinto AR, Reis RL, Martins A, Neves NM (2014) Biofunctional nanofibrous substrate comprising immobilized antibodies and selective binding of autologous growth factors. Biomacromolecules 15(6):2196–2205.  https://doi.org/10.1021/bm500346s CrossRefPubMedGoogle Scholar
  72. 72.
    Piai JF, da Silva MA, Martins A, Torres AB, Faria S, Reis RL, Muniz EC, Neves NM (2017) Chondroitin sulfate immobilization at the surface of electrospun nanofiber meshes for cartilage tissue regeneration approaches. Appl Surf Sci 403:112–125.  https://doi.org/10.1016/j.apsusc.2016.12.135 CrossRefGoogle Scholar
  73. 73.
    Zhu TH, Yu K, Bhutto MA, Guo XR, Shen W, Wang J, Chen WM, El-Hamshary H, Al-Deyab SS, Mo XM (2017) Synthesis of RGD-peptide modified poly(ester-urethane) urea electrospun nanofibers as a potential application for vascular tissue engineering. Chem Eng J 315:177–190.  https://doi.org/10.1016/j.cej.2016.12.134 CrossRefGoogle Scholar
  74. 74.
    Hartman O, Zhang C, Adams EL, Farach-Carson MC, Petrelli NJ, Chase BD, Rabolt JE (2010) Biofunctionalization of electrospun PCL-based scaffolds with perlecan domain IV peptide to create a 3-D pharmacokinetic cancer model. Biomaterials 31(21):5700–5718.  https://doi.org/10.1016/j.biomaterials.2010.03.017 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Kim BR, Nguyen TBL, Min YK, Lee BT (2014) In vitro and in vivo studies of BMP-2-loaded PCL-gelatin-BCP electrospun scaffolds. Tissue Eng Part A 20(23–24):3279–3289.  https://doi.org/10.1089/ten.tea.2014.0081 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Yin LH, Yang SH, He MM, Chang YC, Wang KJ, Zhu YD, Liu YH, Chang YR, Yu ZH (2017) Physicochemical and biological characteristics of BMP-2/IGF-1-loaded three-dimensional coaxial electrospun fibrous membranes for bone defect repair. J Mater Sci Mater Med 28(6).  https://doi.org/10.1007/s10856-017-5898-3
  77. 77.
    Niu BJ, Li B, Gu Y, Shen XF, Liu Y, Chen L (2017) In vitro evaluation of electrospun silk fibroin/nano-hydroxyapatite/BMP-2 scaffolds for bone regeneration. J Biomater Sci Polym E 28(3):257–270.  https://doi.org/10.1080/09205063.2016.1262163 CrossRefGoogle Scholar
  78. 78.
    Guex AG, Hegemann D, Giraud MN, Tevaearai HT, Popa AM, Rossi RM, Fortunato G (2014) Covalent immobilisation of VEGF on plasma-coated electrospun scaffolds for tissue engineering applications. Colloid Surf B 123:724–733.  https://doi.org/10.1016/j.colsurfb.2014.10.016 CrossRefGoogle Scholar
  79. 79.
    Wang K, Zhang QY, Zhao LQ, Pan YW, Wang T, Zhi DK, Ma SY, Zhang PX, Zhao TC, Zhang SM, Li W, Zhu MF, Zhu Y, Zhang J, Qiao MQ, Kong DL (2017) Functional modification of electrospun poly(epsilon-caprolactone) vascular grafts with the fusion protein VEGF-HGFI enhanced vascular regeneration. ACS Appl Mater Inter 9(13):11415–11427.  https://doi.org/10.1021/acsami.6b16713 CrossRefGoogle Scholar
  80. 80.
    Lee H, Lim S, Birajdar MS, Lee SH, Park H (2016) Fabrication of FGF-2 immobilized electrospun gelatin nanofibers for tissue engineering. Int J Biol Macromol 93:1559–1566.  https://doi.org/10.1016/j.ijbiomac.2016.07.041 CrossRefPubMedGoogle Scholar
  81. 81.
    Cui X, Liu MH, Wang JX, Zhou Y, Xiang Q (2015) Electrospun scaffold containing TGF-beta 1 promotes human mesenchymal stem cell differentiation towards a nucleus pulposus-like phenotype under hypoxia. IET Nanobiotechnol 9(2):76–84.  https://doi.org/10.1049/iet-nbt.2014.0006 CrossRefPubMedGoogle Scholar
  82. 82.
    Gomoll AH, Madry H, Knutsen G, van Dijk N, Seil R, Brittberg M, Kon E (2010) The subchondral bone in articular cartilage repair: current problems in the surgical management. Knee Surg Sports Traumatol Arthrosc 18(4):434–447.  https://doi.org/10.1007/s00167-010-1072-x CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Gao JZ, Dennis JE, Solchaga LA, Awadallah AS, Goldberg VM, Caplan AI (2001) Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng 7(4):363–371.  https://doi.org/10.1089/10763270152436427 CrossRefPubMedGoogle Scholar
  84. 84.
    Wei J, Herrler T, Liu K, Han D, Yang M, Dai CC, Li QF (2016) The role of cell seeding, bioscaffolds, and the in vivo microenvironment in the guided generation of osteochondral composite tissue. Tissue Eng Pt A 22(23–24):1337–1347.  https://doi.org/10.1089/ten.tea.2016.0186 CrossRefGoogle Scholar
  85. 85.
    Khorshidi S, Solouk A, Mirzadeh H, Mazinani S, Lagaron JM, Sharifi S, Ramakrishna S (2016) A review of key challenges of electrospun scaffolds for tissue-engineering applications. J Tissue Eng Regen Med 10(9):715–738.  https://doi.org/10.1002/term.1978 CrossRefPubMedGoogle Scholar
  86. 86.
    Erisken C, Kalyon DM, Wang HJ (2010) Viscoelastic and biomechanical properties of osteochondral tissue constructs generated from graded Polycaprolactone and Beta-Tricalcium phosphate composites. J Biomech Eng 132(9):091013.  https://doi.org/10.1115/1.4001884 CrossRefPubMedGoogle Scholar
  87. 87.
    Liverani L, Roether JA, Nooeaid P, Trombetta M, Schubert DW, Boccaccini AR (2012) Simple fabrication technique for multilayered stratified composite scaffolds suitable for interface tissue engineering. Mater Sci Eng A 557:54–58.  https://doi.org/10.1016/j.msea.2012.05.104 CrossRefGoogle Scholar
  88. 88.
    Yunos DM, Ahmad Z, Salih V, Boccaccini AR (2013) Stratified scaffolds for osteochondral tissue engineering applications: electrospun PDLLA nanofibre coated bioglass (R)-derived foams. J Biomater Appl 27(5):537–551.  https://doi.org/10.1177/0885328211414941 CrossRefPubMedGoogle Scholar
  89. 89.
    Mouthuy PA, Ye H, Triffitt J, Oommen G, Cui Z (2010) Physico-chemical characterization of functional electrospun scaffolds for bone and cartilage tissue engineering. Proc Inst Mech Eng H 224(H12):1401–1414.  https://doi.org/10.1243/09544119jeim824 CrossRefPubMedGoogle Scholar
  90. 90.
    Erisken C, Kalyon DM, Wang HJ, Ornek-Ballanco C, Xu JH (2011) Osteochondral tissue formation through adipose-derived stromal cell differentiation on biomimetic polycaprolactone nanofibrous scaffolds with graded insulin and beta-glycerophosphate concentrations. Tissue Eng Part A 17(9–10):1239–1252.  https://doi.org/10.1089/ten.tea.2009.0693 CrossRefPubMedGoogle Scholar
  91. 91.
    Yang WX, Yang F, Wang YN, Both SK, Jansen JA (2013) In vivo bone generation via the endochondral pathway on three-dimensional electrospun fibers. Acta Biomater 9(1):4505–4512.  https://doi.org/10.1016/j.actbio.2012.10.003 CrossRefPubMedGoogle Scholar
  92. 92.
    Liu YY, Yu HC, Liu Y, Liang G, Zhang T, Hu QX (2016) Dual drug spatiotemporal release from functional gradient scaffolds prepared using 3D bioprinting and electrospinning. Polym Eng Sci 56(2):170–177.  https://doi.org/10.1002/pen.24239 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Marta R. Casanova
    • 1
    • 2
  • Rui L. Reis
    • 1
    • 2
  • Albino Martins
    • 1
    • 2
  • Nuno M. Neves
    • 1
    • 2
  1. 1.3B’s Research Group—Biomaterials, Biodegradable and Biomimetics, Avepark—Parque de Ciência e Tecnologia, Zona Industrial da GandraBarco/GuimarãesPortugal
  2. 2.ICVS/3B’s—PT Government Associate LaboratoryBraga/GuimarãesPortugal

Personalised recommendations