The emergence of an unusual stiffness profile in hierarchical biological tissues

Acta Biomaterialia

Volumn 9, Issue 9, 2013, Pages 8099-8109

  Bar On, Benny ^a   Wagner, H Daniel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Biological composites; Bone mechanics; Multi scale bio materials; Staggered structure

Indexed keywords

BONE; COLLAGEN; ELASTIC MODULI; HISTOLOGY;

BIO-MATERIALS; BIOLOGICAL COMPOSITES; BIOLOGICAL TISSUES; BONE MECHANICS; MINERALIZED COLLAGEN FIBRILS; MINERALIZED TISSUE; MULTI-SCALE BIO-MATERIAL; MULTI-SCALES; STAGGERED ARRAYS; STAGGERED STRUCTURES;

STIFFNESS;

BIOMATERIAL; COLLAGEN FIBRIL;

ARTICLE; BIOMINERALIZATION; BONE STRUCTURE; BONE TISSUE; PHASE TRANSITION; PRIORITY JOURNAL; RIGIDITY; SIMULATION; YOUNG MODULUS;

EID: 84880919967     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.04.052     Document Type: Article

References (65)

1. P. Fratzl, and R. Weinkammer Nature's hierarchical materials Prog Mater Sci 50 2007 855 879
2. F. Barthelat A review on the structure and mechanical properties of mollusk shells - perspectives on synthetic biomimetic materials Appl Scan Probe Meth XIII 2009 17 44
3. B. Ji, and H. Gao Mechanical principles of biological nanocomposites Annu Rev Mater Res 40 2010 77 100
4. Z. Zhang On optimal hierarchy of load-bearing biological materials Proc R Soc Lond B 278 2011 519 525
5. J.D. Currey The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone J Biomech 21 2 1988 131 139 (Pubitemid 18037416)
6. J.H. Kinney The importance of interfibrillar mineralization of collagen on the mechanical properties of dentin J Dent Res 82 12 2003 957 961 (Pubitemid 41713811)
7. H.S. Gupta Syncrotron diffraction study of deformation mechanisms in mineralized tendon Phys Rev Lett 93 15 2004 158101
8. W.J. Landis, and F.H. Silver The structure and function of normally mineralizing avian tendons Comp Biochem Physiol A 133 2002 1135 1157 (Pubitemid 35463166)
9. D. Hull An introduction to composite materials 1981 Cambridge University Press Cambridge
10. S. Nikolov, and D. Raabe Hierarchical modeling of the elastic properties of bone at submicron scales: the role of extrafibrillar mineralization Biophys J 94 2008 4220 4232
11. Y.J. Yoon, and S.C. Cowin The estimated elastic constants for a single bone osteonal lamella Biomech Model Mechanobiol 7 2008 1 11
12. I. Jager, and P. Fratzl Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles Biophy J 79 2000 1737 1746
13. Kotha A shear lag model to account for interaction effects between inclusions in composites reinforced with rectangular platelets Compos Sci Technol 60 2000 2147 2158
14. Kotha Micromechanical model for nacre in tension J Mater Sci 36 2001 2001 2007
15. Gao Material become insensitive to flaw at nanoscale: lessons from nature Proc Natl Acad Sci 100 2003 5597 5600 (Pubitemid 36576853)
16. B. Ji, and H. Gao Mechanical properties of nanostructure of biological materials J Mech Phys Solids 52 2004 1963 1990
17. B. Ji, and H. Gao Elastic properties of nanocomposite structure of bone Compos Sci Technol 66 2006 1212 1218
18. B. Bar-On, and H.D. Wagner Mechanical model for staggered bio-structure J Mech Phys Solids 59 2011 1685 1701
19. B. Bar-On, and H.D. Wagner New insights into the Young's modulus of staggered biological composites Mater Sci Eng C 33 2 2013 603 607
20. B. Bar-On, and H.D. Wagner Elastic modulus of hard tissues J Biomech 45 2012 672 678
21. B. Bar-On, and H.D. Wagner Enamel and dentin as multi-scale bio-composites J Mech Behav Biomed Mater 12 2012 174 183
22. B. Bar-On, and H.D. Wagner Stiffness of the extrafibrillar phase in staggered biological arrays Phys Rev Lett 109 7 2012 078102
23. H.L. Cox The elasticity and stress of paper and other fibrous materials Br J Appl Phys 3 1952 72
24. J. Ji Tensile mechanics of electrospun collagen and collagen- hydroxyapatite nanofibers J Mech Behav Biomed Mater 13 2012 185 193
25. Traub Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers Proc Natl Acad Sci 86 1989 9822 9826 (Pubitemid 20030726)
26. J.L. Katz Hard tissues as a composite material, I. Bond on the elastic behavior J Biomech 4 1971 455 473
27. M.J. Buehler Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies J Mech Behav Biomed Mater 1 2008 59 67 (Pubitemid 47557528)
28. A. Gautieri Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up Nano Lett 11 2011 757 766
29. S. Weiner, and H.D. Wagner The material bone: structure-mechanical function relations Annu Rev Mater Sci 28 1998 271 298 (Pubitemid 128631421)
30. Akiva et al. Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone J Mater Sci 3 6 1998 1497 1509
31. S.J. Eppell Nano measurements with micro-devices: mechanical properties of hydrated collagen fibrils J Biomech 23 8 1990 837 844
32. Z.L. Shen Stress train experiments on individual collagen fibrils Biophys J 95 2008 3956 3963
33. Z.L. Shen Viscoelastic properties of isolated collagen fibrils Biophys J 100 2011 3008 3015
34. A.J. Heim, and W.G. Matthews Determination of the elastic modulus of native collagen fibrils via radial indentation Appl Phys Lett 89 2006 18192
35. N. Sasaki, and S. Odajima Elongation mechanisms of collagen fibrils and force-strain relations of tendon at each level of the structural hierarchy J Biomech 29 9 1996 1131 1136 (Pubitemid 26302178)
36. J.A. Van-der Rijt Micromechanical testing of individual collagen fibrils Macromol Biosci 6 9 2006 697 702
37. M.P.E. Wegner Mechanical properties of collagen fibrils Biophys J 93 2007 1255 1263
38. F. Hang, and A.H. Barber Nano-mechanical properties of individual mineralized collagen fibrils from bone tissue J Roy Soc Int 8 57 2011 500 505
39. Chang-Lee Effect of processing on proximate composition and mineral content of sea cucumbers J Food Sci 54 1989 567 572
40. Ozer Effect of handling procedures on the chemical composition of sea cucumbers Turk J Fish Aquat Sci 4 2004 71 74
41. P. Fratzl Cellulose and collagen: from fibers to tissues Colloid Interface Sci 8 2003 32 39
42. C.J. Hooley, and R.E. Chohen A model for creep behavior of tendon Int J Biol Macromol 1 3 1979 123-13
43. Craig An estimation of the mean length of collagen fibrils in rat tail-tendon as a function of age Connect Tissue Res 19 1989 51 62
44. Raspani Structural aspects of extracellular matrix of the tendon: an atomic force and scanning electron microscopy study Arch Histol Cytol 65 1 2002 37 43
45. F.H. Silver The role of mineral in the storage of elastic energy in turkey tendons Biomacromolecules 1 2000 180 185
46. A. Masik Observations on multiscale stress-induced changes of collagen orientation in tendon by polarized Raman spectroscopy Biomacromolecules 12 2011 3989 3996
47. W.J. Landis A study on the relationship between mineral content and mechanical properties of turkey gastrocnemius tendon J Bone Miner Res 10 6 1995 859 867
48. W.J. Freeman, and F.H. Silver Analysis of mineral deposition in turkey tendons and self assembled collagen fibers using mechanical techniques Connect Tissue Res 45 2004 131 141 (Pubitemid 39429751)
49. P.Y. Chen Comparison of the structure and mechanical properties of boline femur and antler of the North American elk Acta Biomater 5 2009 693 706
50. M.E. Launey Mechanistic aspects of the fracture toughness of elk antler bone Acta Biomater 6 2010 1505 1514
51. N. Reznikov Three-dimensional imaging of collagen fibril organization in rat circumferential lamellar bone using a dual beam electron microscope reveals ordered and disordered sub-lamellar structures Bone 52 2 2013 676 683
52. A. Faingold Osteonal lamellae elementary units: lamellar microstructure, curvature and mechanical properties Acta Biomater 9 4 2012 5956 5962
53. I.D. Cave, and L. Hutt The anisotropic elasticity of the plant well wall Wood Sci Technol 2 1968 268 278
54. W. Wagermaier Spiral twisting of fiber orientation inside bone lamellae Biointerphases 1 1 2006 1 5
55. J.D. Currey Mechanical properties of bone tissues with greatly differing functions J Biomech 12 1979 313 319 (Pubitemid 9172379)
56. A. Rajaram, and N. Ramanathan Tensile properties of antler bone Calcif Tissue Int 34 1982 301 305 (Pubitemid 12060445)
57. R.W. Blob, and M. LaBarbera Correlates of variation in deer antler stiffness: age, mineral content, intra-antler location, habitat and phylogeny Biol J Linn Soc 74 2001 113 120 (Pubitemid 32930692)
58. T. Landete-Castillejos Influence of physiological effort of growth and chemical composition on antler bone mechanical properties Bone 41 2007 794 803 (Pubitemid 47576837)
59. J.D. Currey The effect of strain rate, reconstruction and mineral content on some mechanical properties of bovine bone J Biomech 12 1975 313 319
60. H.Ch. Spatz Young's moduli and shear moduli in cortical bone Proc R Soc Lond B 263 1996 287 294
61. J.D. Currey Bones - structure and mechanics 2002 Princeton University Press Princeton, NJ
62. S. Nemat-Nasser, and M. Hori Micromechanics: overall properties of heterogeneous materials 1999 Elsevier Amsterdam
63. S. Zuo, and Y. Wei Effective elastic modulus of bone-like hierarchical materials Acta Mech Solida Sin 20 2007 198 205
64. G. Liu, B. Ji, K.-C. Hwang, and B.C. Khoo Analytical solutions of the displacement and stress fields of the nanocomposite structure of biological materials Compos Sci Technol 71 2011 1190 1195
65. Bar-On B and Wagner HD. Structural motifs and elastic properties of hierarchical biological tissues - A review, Journal of Structural Biology, 2013, http://dx.doi.org/10.1016/j.jsb.2013.05.012.