Rapid prototyped porous nickel–titanium scaffolds as bone substitutes

Journal of Tissue Engineering

Volumn 5, Issue , 2014, Pages

  Hoffmann, Waldemar ^a,b   Bormann, Therese ^b,c   Rossi, Antonella ^d,e   Müller, Bert ^c   Schumacher, Ralf ^b   Martin, Ivan ^a   de Wild, Michael ^b   Wendt, David ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF APPLIED SCIENCES AND ARTS NORTHWESTERN SWITZERLAND   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d ETH ZURICH   (Switzerland)

^e UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Bone tissue engineering; nickel titanium; osteogenic differentiation; scaffold; selective laser melting

Indexed keywords

BIOMECHANICS; CALCIUM PHOSPHATE; DENTAL ALLOYS; DENTAL PROSTHESES; GENE EXPRESSION; MELTING; METAL IMPLANTS; NICKEL; SCAFFOLDS (BIOLOGY); SELECTIVE LASER MELTING; TENSILE STRENGTH; TITANIUM ALLOYS;

BONE SUBSTITUTES; BONE TISSUE ENGINEERING; MESENCHYMAL STROMAL CELLS; NICKEL-TITANIUM; OSTEOGENIC DIFFERENTIATION; POROUS NICKEL; SELECTIVE LASER MELTING; TITANIA; TITANIUM SCAFFOLDS; TITANIUM SUBSTRATES;

BONE;

NITINOL; OSTEOCALCIN; SIALOPROTEIN;

ARTICLE; BIOMECHANICS; BONE DEVELOPMENT; BONE PROSTHESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; MATERIALS TESTING; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; MTT ASSAY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SURFACE PROPERTY; TISSUE SCAFFOLD; X RAY PHOTOELECTRON SPECTROSCOPY;

EID: 85060664725     PISSN: None     EISSN: 20417314     Source Type: Journal    
DOI: 10.1177/2041731414540674     Document Type: Article

References (63)

1. D.W.HutmacherJ.T.SchantzC.X.F.Lam. State of the art and future directions of scaffold-based bone engineering from a biomaterials perspective. J Tissue Eng Regen Med2007; 1(4): 245–260, http://dx.doi.org/10.1002/term.24
2. A.J.SalgadoO.P.CoutinhoR.L.Reis. Bone tissue engineering: state of the art and future trends. Macromol Biosci2004; 4(8): 743–765, http://dx.doi.org/10.1002/mabi.200400026
3. K.RezwanQ.Z.ChenJ.J.Blaker. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials2006; 27(18): 3413–3431, http://www.sciencedirect.com/science/article/pii/S0142961206001232
4. T.AlbrektssonC.Johansson. Osteoinduction, osteoconduction and osseointegration. Eur Spine J2001; 10(Suppl. 2): S96–S101, http://link.springer.com/article/10.1007/s005860100282 (accessed 6 November 2013).
5. S.TuguluK.LoweD.Scharnweber. Preparation of superhydrophilic microrough titanium implant surfaces by alkali treatment. J Mater Sci Mater Med2010; 21(10): 2751–2763, http://www.ncbi.nlm.nih.gov/pubmed/20725770
6. Y.GermanierS.TosattiN.Broggini. Enhanced bone apposition around biofunctionalized sandblasted and acid-etched titanium implant surfaces. A histomorphometric study in miniature pigs. Clin Oral Implants Res2006; 17(3): 251–257, http://www.ncbi.nlm.nih.gov/pubmed/16672019 (accessed 12 November 2012).
7. V.MilleretS.TuguluF.Schlottig. Alkali treatment of microrough titanium surfaces affects macrophage/monocyte adhesion, platelet activation and architecture of blood clot formation. Eur Cell Mater2011; 21: 430–444, http://www.ncbi.nlm.nih.gov/pubmed/21604243
8. S.NagR.Banerjee. Fundamentals of medical implant materials. In: (ed.) ASM handbook, volume 23: materials for medical devices. Materials Park, OH: ASM International, 2012, pp. 6–17.
9. R.HuiskesH.WeinansB.van Rietbergen. The relationship between stress shielding and bone resorption around total hip stems and the effects of flexible materials. Clin Orthop Relat Res1992; 274: 124–134, http://www.ncbi.nlm.nih.gov/pubmed/1728998 (accessed 19 August 2013).
10. M.De WildF.MeierT.Bormann. Damping of selective-laser-melted NiTi for medical implants. J Mater Eng Perform2014, http://link.springer.com/10.1007/s11665-014-0889-8 (accessed 17 February 2014).
11. L.MullenR.C.StampW.K.Brooks. Selective Laser Melting: a regular unit cell approach for the manufacture of porous, titanium, bone in-growth constructs, suitable for orthopedic applications. J Biomed Mater Res B Appl Biomater2009; 89(2): 325–334, http://www.ncbi.nlm.nih.gov/pubmed/18837456 (accessed 28 February 2014).
12. D.K.PattanayakA.FukudaT.Matsushita. Bioactive Ti metal analogous to human cancellous bone: fabrication by selective laser melting and chemical treatments. Acta Biomater2011, http://www.sciencedirect.com/science/article/B7GHW-51491KH-C/2/408b9a0545d42b82221a0f73be480024
13. T.BormannG.SchulzH.Deyhle. Combining micro computed tomography and three-dimensional registration to evaluate local strains in shape memory scaffolds. Acta Biomater2013; 10(2): 1024–1034, http://www.ncbi.nlm.nih.gov/pubmed/24257506 (accessed 22 November 2013).
14. J.M.SobralS.G.CaridadeR.A.Sousa. Three-dimensional plotted scaffolds with controlled pore size gradients: effect of scaffold geometry on mechanical performance and cell seeding efficiency. Acta Biomater2011; 7(3): 1009–1018, http://www.ncbi.nlm.nih.gov/pubmed/21056125 (accessed 14 March 2014).
15. S.Van BaelY.C.ChaiS.Truscello. The effect of pore geometry on the in vitro biological behavior of human periosteum-derived cells seeded on selective laser-melted Ti6Al4V bone scaffolds. Acta Biomater2012; 8(7): 2824–2834, http://www.ncbi.nlm.nih.gov/pubmed/22487930 (accessed 18 February 2014).
16. G.ZhaoO.ZingerZ.Schwartz. Osteoblast-like cells are sensitive to submicron-scale surface structure. Clin Oral Implants Res2006; 17(3): 258–264, http://www.ncbi.nlm.nih.gov/pubmed/16672020 (accessed 19 August 2013).
17. T.BormannM.de WildF.Beckmann. Assessing the morphology of selective laser melted NiTi-scaffolds for a three-dimensional quantification of the one-way shape memory effect. In: (ed), 2013, p. 868914, http://proceedings.spiedigitallibrary.org/proceeding.aspx?doi=10.1117/12.2012245 (accessed 20 May 2014).
18. Olympus. User’s manual: confocal scanning laser microscope LEXT OLS3100. Hamburg: Olympus Life Science Europa GMBH, 2008.
19. A.WennerbergT.Albrektsson. On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implants2009; 25(1): 63–74, http://www.ncbi.nlm.nih.gov/pubmed/20209188
20. M.CrobuA.RossiF.Mangolini. Chain-length-identification strategy in zinc polyphosphate glasses by means of XPS and ToF-SIMS. Anal Bioanal Chem2012; 403(5): 1415–1432, http://www.ncbi.nlm.nih.gov/pubmed/22451170 (accessed 2 April 2014).
21. ISO 10993-5:2009. Biological evaluation of medical devices—part 5: tests for in vitro cytotoxicity.
22. A.BracciniD.WendtC.Jaquiery. Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells2005; 23(8): 1066–1072, http://www.ncbi.nlm.nih.gov/pubmed/16002780 (accessed 12 August 2013).
23. O.FrankM.HeimM.Jakob. Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem2002; 85(4): 737–746, http://www.ncbi.nlm.nih.gov/pubmed/11968014
24. D.WendtA.MarsanoM.Jakob. Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol Bioeng2003; 84(2): 205–214, http://www.ncbi.nlm.nih.gov/pubmed/12966577
25. D.WendtS.StroebelM.Jakob. Uniform tissues engineered by seeding and culturing cells in 3D scaffolds under perfusion at defined oxygen tensions. Biorheology2006; 43(3–4): 481–488, http://www.ncbi.nlm.nih.gov/pubmed/16912419
26. E.PiccininiN.SadrI.Martin. Ceramic materials lead to underestimated DNA quantifications: a method for reliable measurements. Eur Cell Mater2010; 20: 38–44, http://www.ncbi.nlm.nih.gov/pubmed/20652860 (accessed 22 November 2012).
27. A.BarberoS.PloegertM.Heberer. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum2003; 48(5): 1315–1325, http://www.ncbi.nlm.nih.gov/pubmed/12746904
28. E.A.Vogler. Structure and reactivity of water at biomaterial surfaces. Adv Colloid Interface Sci1998; 74: 69–117, http://www.ncbi.nlm.nih.gov/pubmed/9561719 (accessed 12 November 2012).
29. D.AddariA.MignaniE.Scavetta. An XPS investigation on glucose oxidase and Ni/Al hydrotalcite interaction. Surf Interface Anal2011; 43(4): 816–822, http://doi.wiley.com/10.1002/sia.3636 (accessed 2 April 2014).
30. Y.T.SulC.B.JohanssonY.Jeong. Oxidized implants and their influence on the bone response. J Mater Sci Mater Med2001; 12(10–12): 1025–1031, http://www.ncbi.nlm.nih.gov/pubmed/15348359 (accessed 4 March 2014).
31. B.-S.KangY.-T.SulS.-J.Oh. XPS, AES and SEM analysis of recent dental implants. Acta Biomater2009; 5(6): 2222–2229, http://www.ncbi.nlm.nih.gov/pubmed/19261554 (accessed 4 March 2014).
32. D.D.DeligianniN.KatsalaS.Ladas. Effect of surface roughness of the titanium alloy Ti-6Al-4V on human bone marrow cell response and on protein adsorption. Biomaterials2001; 22(11): 1241–1251, http://www.ncbi.nlm.nih.gov/pubmed/11336296 (accessed 26 February 2014).
33. U.HempelT.HeftiP.Dieter. Response of human bone marrow stromal cells, MG-63, and SaOS-2 to titanium-based dental implant surfaces with different topography and surface energy. Clin Oral Implants Res2013; 24(2): 174–82, http://dx.doi.org/10.1111/j.1600-0501.2011.02328.x (accessed 12 May 2014).
34. J.Y.MartinZ.SchwartzT.W.Hummert. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res1995; 29(3): 389–401, http://www.ncbi.nlm.nih.gov/pubmed/7542245 (accessed 4 February 2013).
35. L.PonsonnetV.ComteA.Othmane. Effect of surface topography and chemistry on adhesion, orientation and growth of fibroblasts on nickel–titanium substrates. Mater Sci Eng C2002; 21(1–2): 157–165, http://linkinghub.elsevier.com/retrieve/pii/S0928493102000978 (accessed 4 February 2013).
36. A.WennerbergT.Albrektsson. Effects of titanium surface topography on bone integration: a systematic review. Clin Oral Implants Res2009; 20(Suppl. 4): 172–184, http://www.ncbi.nlm.nih.gov/pubmed/19663964 (accessed 28 November 2013).
37. H.J.RønoldS.P.LyngstadaasJ.E.Ellingsen. Analysing the optimal value for titanium implant roughness in bone attachment using a tensile test. Biomaterials2003; 24(25): 4559–4564, http://linkinghub.elsevier.com/retrieve/pii/S0142961203002564 (accessed 4 December 2013).
38. F.RuppL.ScheidelerN.Olshanska. Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. J Biomed Mater Res A2006; 76(2): 323–334, http://www.ncbi.nlm.nih.gov/pubmed/16270344 (accessed 23 May 2013).
39. A.A.MamalisS.S.Silvestros. Analysis of osteoblastic gene expression in the early human mesenchymal cell response to a chemically modified implant surface: an in vitro study. Clin Oral Implants Res2011; 22(5): 530–537, http://www.ncbi.nlm.nih.gov/pubmed/21121959 (accessed 23 May 2013).
40. J.L.M.PuttersD.M.K.S.Kaulesar SukulG.R.de Zeeuw. Comparative cell culture effects of shape memory metal (Nitinol®), nickel and titanium: a biocompatibility estimation. Eur Surg Res1992; 24(6): 378–382, http://www.karger.com/DOI/10.1159/000129231
41. T.HabijanO.BremmS.A.Esenwein. Influence of nickel ions on human multipotent mesenchymal stromal cells (hMSCs). Materwiss Werksttech2007; 38(12): 969–974, http://doi.wiley.com/10.1002/mawe.200700231 (accessed 12 November 2012).
42. M.M.Es-SouniH.Fischer-Brandies. Assessing the biocompatibility of NiTi shape memory alloys used for medical applications. Anal Bioanal Chem2005; 381(3): 557–567, http://www.ncbi.nlm.nih.gov/pubmed/15660223 (accessed 12 February 2013).
43. T.HabijanC.HaberlandH.Meier. The biocompatibility of dense and porous Nickel–Titanium produced by selective laser melting. Mater Sci Eng C2013; 33(1): 419–426, http://linkinghub.elsevier.com/retrieve/pii/S0928493112004407 (accessed 13 November 2012).
44. I.V.ShishkovskyL.T.VolovaM.V.Kuznetsov. Porous biocompatible implants and tissue scaffolds synthesized by selective laser sintering from Ti and NiTi. J Mater Chem2008; 18(12): 1309–1317, http://xlink.rsc.org/?DOI=b715313a (accessed 30 April 2014).
45. C.-M.ChanS.TrigwellT.Duerig. Oxidation of an NiTi alloy. Surf Interface Anal1990; 15(6): 349–354, http://dx.doi.org/10.1002/sia.740150602 (accessed 19 May 2014).
46. S.A.ShabalovskayaH.TianJ.W.Anderegg. The influence of surface oxides on the distribution and release of nickel from Nitinol wires. Biomaterials2009; 30(4): 468–477, http://dx.doi.org/10.1016/j.biomaterials.2008.10.014 (accessed 18 February 2013).
47. P.LiC.OhtsukiT.Kokubo. The role of hydrated silica, titania, and alumina in inducing apatite on implants. J Biomed Mater Res1994; 28(1): 7–15, http://dx.doi.org/10.1002/jbm.820280103 (accessed 4 March 2014).
48. J.E.SundgrenP.BodöI.Lundström. Auger electron spectroscopic studies of stainless-steel implants. J Biomed Mater Res1985; 19(6): 663–671, http://dx.doi.org/10.1002/jbm.820190606 (accessed 4 March 2014).
49. P.HabibovicT.M.SeesM.A.van den Doel. Osteoinduction by biomaterials—physicochemical and structural influences. J Biomed Mater Res Part A2006; 77(4): 747–762, http://dx.doi.org/10.1002/jbm.a.30712
50. H.YoshikawaA.Myoui. Bone tissue engineering with porous hydroxyapatite ceramics. J Artif Organs2005; 8(3): 131–136, http://www.ncbi.nlm.nih.gov/pubmed/16235028 (accessed 4 March 2014).
51. C.LarssonP.ThomsenB.O.Aronsson. Bone response to surface-modified titanium implants: studies on the early tissue response to machined and electropolished implants with different oxide thicknesses. Biomaterials1996; 17(6): 605–616, http://www.ncbi.nlm.nih.gov/pubmed/8652779 (accessed 4 March 2014).
52. Y.-T.SulC.B.JohanssonY.Jeong. Resonance frequency and removal torque analysis of implants with turned and anodized surface oxides. Clin Oral Implants Res2002; 13(3): 252–259, http://www.ncbi.nlm.nih.gov/pubmed/12010155 (accessed 4 March 2014).
53. P.BiancoM.RiminucciG.Silvestrini. Localization of bone sialoprotein (BSP) to Golgi and post-Golgi secretory structures in osteoblasts and to discrete sites in early bone matrix. J Histochem Cytochem1993; 41(2): 193–203, http://www.ncbi.nlm.nih.gov/pubmed/8419459 (accessed 12 March 2013).
54. G.Wolf. Function of the bone protein osteocalcin: definitive evidence. Nutr Rev1996; 54(10): 332–323, http://doi.wiley.com/10.1111/j.1753-4887.1996.tb03798.x (accessed 12 March 2013).
55. P.V.HauschkaJ.B.LianD.E.Cole. Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev1989; 69(3): 990–1047, http://www.ncbi.nlm.nih.gov/pubmed/2664828 (accessed 28 August 2013).
56. A.NeveA.CorradoF.P.Cantatore. Osteocalcin: skeletal and extra-skeletal effects. J Cell Physiol2013; 228(6): 1149–1153, http://dx.doi.org/10.1002/jcp.24278
57. J.B.LianG.S.Stein. Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med1992; 3: 269–305.
58. S.J.Hollister. Porous scaffold design for tissue engineering. Nat Mater2005; 4(7): 518–524, http://www.ncbi.nlm.nih.gov/pubmed/16003400 (accessed 12 November 2012).
59. A.ScherberichR.GalliC.Jaquiery. Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells2007; 25(7): 1823–1829, http://www.ncbi.nlm.nih.gov/pubmed/17446558 (accessed 20 March 2014).
60. E.M.ByrneE.FarrellL.A.McMahon. Gene expression by marrow stromal cells in a porous collagen-glycosaminoglycan scaffold is affected by pore size and mechanical stimulation. J Mater Sci Mater Med2008; 19(11): 3455–3463, http://www.ncbi.nlm.nih.gov/pubmed/18584120 (accessed 31 January 2013).
61. F.Van EijkD.B.F.SarisL.B.Creemers. The effect of timing of mechanical stimulation on proliferation and differentiation of goat bone marrow stem cells cultured on braided PLGA scaffolds. Tissue Eng Part A2008; 14(8): 1425–1433, http://www.ncbi.nlm.nih.gov/pubmed/18637726 (accessed 30 January 2013).
62. S.StraußS.DudziakR.Hagemann. Induction of osteogenic differentiation of adipose derived stem cells by microstructured nitinol actuator-mediated mechanical stress. PLoS One2012; 7(12): e51264, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3517541&;tool=pmcentrez&rendertype=abstract (accessed 3 January 2013).
63. P.LeuchtJ.KimR.Wazen. Effect of mechanical stimuli on skeletal regeneration around implants. Bone2007; 40(4): 919–930, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1987325&;tool=pmcentrez&rendertype=abstract (accessed 11 March 2013).