Skip to main content

Nanomechanical mapping of bone tissue regenerated by magnetic scaffolds

Journal of Materials Science: Materials in Medicine volume 26, Article number: 35 (2015) Cite this article

Abstract

Nanoindentation can provide new insights on the maturity stage of regenerating bone. The aim of the present study was the evaluation of the nanomechanical properties of newly-formed bone tissue at 4 weeks from the implantation of permanent magnets and magnetic scaffolds in the trabecular bone of rabbit femoral condyles. Three different groups have been investigated: MAG-A (NdFeB magnet + apatite/collagen scaffold with magnetic nanoparticles directly nucleated on the collagen fibers during scaffold synthesis); MAG-B (NdFeB magnet + apatite/collagen scaffold later infiltrated with magnetic nanoparticles) and MAG (NdFeB magnet). The mechanical properties of different-maturity bone tissues, i.e. newly-formed immature, newly-formed mature and native trabecular bone have been evaluated for the three groups. Contingent correlations between elastic modulus and hardness of immature, mature and native bone have been examined and discussed, as well as the efficacy of the adopted regeneration method in terms of “mechanical gap” between newly-formed and native bone tissue. The results showed that MAG-B group provided regenerated bone tissue with mechanical properties closer to that of native bone compared to MAG-A or MAG groups after 4 weeks from implantation. Further, whereas the mechanical properties of newly-formed immature and mature bone were found to be fairly good correlated, no correlation was detected between immature or mature bone and native bone. The reported results evidence the efficacy of nanoindentation tests for the investigation of the maturity of newly-formed bone not accessible through conventional analyses.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Kallai I, van Lenthe GH, Ruffoni D, Zilberman Y, Muller R, Pelled G, et al. Quantitative, structural, and image-based mechanical analysis of nonunion fracture repaired by genetically engineered mesenchymal stem cells. J Biomech. 2010;43:2315–20.

    Article  Google Scholar 

  2. Boskey AL, Baker SP, van der Meulen MCH. Contribution of mineral to bone structural behavior and tissue mechanical properties. Calc Tissue Int. 2010;87:450–60.

    Article  Google Scholar 

  3. Cipitria A, Lange C, Schell H, Wagermaier W, Reichert JC, Hutmacher DW, et al. Porous scaffold architecture guides tissue formation. J Bone Miner Res. 2012;27:1275–88.

    Article  Google Scholar 

  4. Hoc T, Henry L, Verdier M, Aubry D, Sedel L, Meunier A. Bone. 2006;38:466–74.

    Article  Google Scholar 

  5. Matos MA, Araujo FP, Paixao FB. Histomorphometric evaluation of bone healing in rabbit fibular osteotomy model without fixation. J Orthop Surg Res. 2008;3:4.

    Article  Google Scholar 

  6. Skedros JG, Dayton MR, Sybrowsky CL, Bloebaum RD, Bachus KN. The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone. J Exp Biol. 2006;209:3025–42.

    Article  Google Scholar 

  7. Ziv V, Wagner HD, Weiner S. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. 1996;18:417–28.

    Article  Google Scholar 

  8. Ebenstein DM, Pruitt L. Nanoindentation of biological materials. Nano Today. 2006;1:26–33.

    Article  Google Scholar 

  9. Lewis G, Nyman JS. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. J Biomed Mater Res Part B. 2008;87:286–301.

    Article  Google Scholar 

  10. Oliver WC, Parr GM. Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology. J Mater Res. 2004;19:3–20.

    Article  Google Scholar 

  11. Bianchi M, Russo A, Lopomo N, Boi M, Maltarello MC, Sprio S, et al. Pulsed plasma deposition of zirconia thin films on UHMWPE: proof of concept of a novel approach for joint prosthetic implants. J Mater Chem. 2013;1:310–8.

    Article  Google Scholar 

  12. Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech. 1999;32:1005–12.

    Article  Google Scholar 

  13. Faingold A, Cohen SR, Wagner HD. Nanoindentation of osteonal bone lamellae. J Mech Behav Biomed Mater. 2012;9:198–206.

    Article  Google Scholar 

  14. Rodriguez-Florez N, Oyen ML, Shefelbine SJ. Insight into differences in nanoindentation properties of bone. J Mech Behav Biomed Mater. 2013;18:90–9.

    Article  Google Scholar 

  15. Hengsberger S, Kulik A, Zysset P. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone. 2002;30:178–84.

    Article  Google Scholar 

  16. Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP. Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone. 2011;49:1279–89.

    Article  Google Scholar 

  17. Albert C, Jameson J, Toth JM, Smith P, Harris G. Bone properties by nanoindentation in mild and severe osteogenesis imperfecta. Clin Biomech. 2013;28:110–6.

    Article  Google Scholar 

  18. Cattani-Lorente M, Rizzoli R, Ammann P. In vitro bone exposure to strontium improves bone material level properties. Acta Biomater. 2013;9:7005–13.

    Article  Google Scholar 

  19. Vayron R, Barthel E, Mathieu V, Soffer E, Anagnostou F, Haiat G. Nanoindentation measurements of biomechanical properties in mature and newly formed bone tissue surrounding an implant. J Biomech Eng. 2012;134:021007–0210070.

    Article  Google Scholar 

  20. Arrigoni E, de Girolamo L, Di Giancamillo A, Stanco D, Dellavia C, Carnelli D, et al. Adipose-derived stem cells and rabbit bone regeneration: histomorphometric, immunohistochemical and mechanical characterization. J Orth Sci. 2013;18:331–9.

    Article  Google Scholar 

  21. Tai K, Pelled G, Sheyn D, Bershteyn A, Han L, Kallai I, et al. Nanobiomechanics of repair bone regenerated by genetically modified mesenchymal stem cells. Tissue Eng. 2008;14:1709–20.

    Article  Google Scholar 

  22. Manjubala I, Liu Y, Epari DR, Roschger P, Schell H, Fratzl P, et al. Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing. Bone. 2009;45:185–92.

    Article  Google Scholar 

  23. Ishimoto T, Nakano T, Yamamoto M, Tabata Y. Biomechanical evaluation of regenerating long bone by nanoindentation. J Mater Sci Mater Med. 2011;22:969–76.

    Article  Google Scholar 

  24. Zapata U, Opperman LA, Kontogiorgos E, Elsalanty ME, Dechow PC. Biomechanical characteristics of regenerated cortical bone in the canine mandible. J Tissue Eng Regen Med. 2011;5:551–9.

    Article  Google Scholar 

  25. Panseri S, Russo A, Sartori M, Giavaresi G, Sandri M, Fini M, et al. Modifying bone scaffold architecture in vivo with permanent magnets to facilitate fixation of magnetic scaffolds. Bone. 2013;56:432–9.

    Article  Google Scholar 

  26. Russo A, Shelyakova T, Casino D, Lopomo N, Strazzari A, Ortolani A, et al. A new approach to scaffold fixation by magnetic forces: application to large osteochondral defects. Med Eng Phys. 2012;34:1287–93.

    Article  Google Scholar 

  27. Tampieri A, Landi E, Valentini F, Sandri M, D’Alessandro T, Dediu V, et al. A conceptually new type of bio-hybrid scaffold for bone regeneration. Nanotechnology. 2011;22:015104.

    Article  Google Scholar 

  28. Bock N, Riminucci A, Dionigi C, Russo A, Tampieri A, Landi E, et al. A novel route in bone tissue engineering: magnetic biomimetic scaffolds. Acta Biomater. 2010;6:786–98.

    Article  Google Scholar 

  29. Franchi M, Bacchelli B, Giavaresi G, De Pasquale V, Martini D, Fini M, et al. Influence of different implant surfaces on peri-implant osteogenesis: histomorphometric analysis in sheep. J Periodontol. 2007;78:879–88.

    Article  Google Scholar 

  30. Panseri S, Cunha C, D’Alessandro T, Sandri M, Russo A, Giavaresi G, et al. Magnetic hydroxyapatite bone substitutes to enhance tissue regeneration: evaluation in vitro using osteoblast-like cells and in vivo in a bone defect. PLoS ONE. 2012;7:e38710.

    Article  Google Scholar 

  31. Wang X, Rao DS, Ajdelsztajn L, Ciarelli TE, Lavernia EJ, Fyhrie DP. Human iliac crest cancellous bone elastic modulus and hardness differ with bone formation rate per bone surface but not by existence of prevalent vertebral fracture. J Biomed Mater Res. 2008;85B:68–77.

    Article  Google Scholar 

  32. Oyen ML. Nanoindentation hardness of mineralized tissues. J Biomech. 2006;39:2699–702.

    Article  Google Scholar 

  33. Bala Y, Depalle B, Douillard T, Meille S, Clement P, Follet H, et al. Respective roles of organic and mineral components of human cortical bone matrix in micromechanical behavior: an instrumented indentation study. J Mech Behav Biomed Mater. 2011;4:1473–82.

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the European Project “Magnetic Scaffolds for in vivo Tissue Engineering” (NMP3-LA-2008-214686) and by the project “Nanostructured Coatings Enhancing Material Performances in Joint Arthroplasty” (project code_2012-1838) co-founded by the Italian Ministry of Health. The authors would like to particularly thank Dr. Elettra Pignotti for her contribution to the statistical analysis.

Author information

Authors and Affiliations

  1. Laboratory of Nano-Biotechnologies (NaBi), Rizzoli Orthopaedic Institute, Via Gobetti 1/10, Bologna, 40136, Italy

    Michele Bianchi, Marco Boi, Nicola Lopomo, Maurilio Marcacci & Alessandro Russo

  2. Laboratory of Biocompatibility, Innovative Technologies and Advanced Therapies (BITTA), Rizzoli Orthopaedic Institute, Via di Barbiano 1/10, Bologna, 40136, Italy

    Maria Sartori, Gianluca Giavaresi & Milena Fini

  3. Laboratory of Preclinical and Surgical Studies, Rizzoli Orthopaedic Institute, Via di Barbiano 1/10, Bologna, 40136, Italy

    Gianluca Giavaresi & Milena Fini

  4. Laboratory of Biomechanics and Technology Innovation, Rizzoli Orthopaedic Institute, Via di Barbiano 1/10, Bologna, 40136, Italy

    Nicola Lopomo, Maurilio Marcacci & Alessandro Russo

  5. Institute for the Study of Nanostructured Materials (ISMN), National Research Council, Via Gobetti 101, Bologna, 40129, Italy

    Alek Dediu

  6. Laboratory of Bioceramics and Bio-hybrid Composites, Institute of Science and Technology for Ceramics, National Research Council, Via Granarolo 64, Faenza, 48018, Italy

    Anna Tampieri

Authors
  1. Michele Bianchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Boi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Sartori
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gianluca Giavaresi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicola Lopomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Milena Fini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alek Dediu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anna Tampieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maurilio Marcacci
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alessandro Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michele Bianchi.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bianchi, M., Boi, M., Sartori, M. et al. Nanomechanical mapping of bone tissue regenerated by magnetic scaffolds. J Mater Sci: Mater Med 26, 35 (2015). https://doi.org/10.1007/s10856-014-5363-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-014-5363-5

Keywords

  • Bone Tissue
  • Native Bone
  • Immature Bone
  • Nanoindentation Test
  • Mature Bone