A new model to simulate the elastic properties of mineralized collagen fibril

Biomechanics and Modeling in Mechanobiology

Volumn 10, Issue 2, 2011, Pages 147-160

  Yuan, Fang ^a   Stock, Stuart R ^b   Haeffner, Dean R ^c   Almer, Jonathan D ^c   Dunand, David C ^a   Brinson, L Catherine ^a  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Bone; Collagen fibril; Finite element analysis; Modeling; Structure property relationship

Indexed keywords

BONE; COLLAGEN; ELASTICITY; HYDROXYAPATITE; MINERALS; STIFFNESS; STRUCTURAL PROPERTIES; X RAY DIFFRACTION;

COLLAGEN FIBRILS; COMPOSITES STRUCTURES; ELASTIC PROPERTIES; FINITE ELEMENT ANALYSE; HIERARCHICAL COMPOSITE; MINERALIZED COLLAGEN FIBRILS; MODELING; STRUCTURAL DEFORMATION; STRUCTURAL ORDERING; STRUCTURE-PROPERTIES RELATIONSHIPS;

FINITE ELEMENT METHOD;

FIBRILLAR COLLAGEN; MINERAL;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; DOG; FINITE ELEMENT ANALYSIS; MECHANICAL STRESS; REPRODUCIBILITY; SMALL ANGLE SCATTERING; X RAY DIFFRACTION; YOUNG MODULUS;

ANIMALS; COMPUTER SIMULATION; DOGS; ELASTIC MODULUS; FIBRILLAR COLLAGENS; FINITE ELEMENT ANALYSIS; MINERALS; MODELS, BIOLOGICAL; REPRODUCIBILITY OF RESULTS; SCATTERING, SMALL ANGLE; STRESS, MECHANICAL; X-RAY DIFFRACTION;

EID: 79957976156     PISSN: 16177959     EISSN: 16822978     Source Type: Journal    
DOI: 10.1007/s10237-010-0223-9     Document Type: Article

References (59)

1. Akiva U, Wagner HD, Weiner S (1998) Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone. J Mater Sci 33:1497-1509 (Pubitemid 128509574)
2. Almer JD, Stock SR (2007) Micromechanical response of mineral and collagen phases in bone. J Struct Biol 157:365-370. doi:10.1016/j.jsb.2006.09. 001 (Pubitemid 46127752)
3. Ashby MF (1993) Criteria for selecting the components of composites. Acta Metall Mater 41:1313-1335
4. Bertinetti L, Tampieri A, Landi E, Ducati C, Midgley PA, Coluccia S, Martra G (2007) Surface structure, hydration, and cationic sites of nanohydroxyapatite: UHR-TEM, IR, and microgravimetric studies. J Phys Chem C 111:4027-4035. doi:10.1021/jp066040s (Pubitemid 46548890)
5. Birk DE, Silver FH, Trelstad RL (1991) Matrix Assembly. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum, New York pp 221-254
6. Borah B, Gross GJ, Dufresne TE, Smith TS, Cockman MD, Chmielewski PA, Lundy MW, Hartke JR, Sod EW (2001) Thre edimensional microimaging (MR mu I and mu CT), finite element modeling, and rapid prototyping provide unique insights into bone architecture in osteoporosis. Anat Rec 265:101-110
7. Chen CQ, Shi Y, Zhang YS, Zhu J, Yan YJ (2006) Size dependence of Young's modulus in ZnO nanowires. Phys Rev Lett 96:075505. doi:10.1103/PhysRevLett.96. 075505 (Pubitemid 43291095)
8. Courtney TH (2000) Mechanical behavior of materials, 2edn. McGraw Hill, Boston
9. Craig AS, Birtles MJ, Conway JF, Parry DAD (1989) An estimate of the mean length of collagen fibrils in rat tail-tendon as a function of age. Connect Tissue Res 19:51-62
10. Cuenot S, Fretigny C, Demoustier-Champagne S, Nysten B (2004) Surface tension effect on the mechanical properties of nanomaterials measured by atomic force microscopy. Phys Rev B 69:165410. doi:10.1103/PhysRevB.69.165410
11. Currey JD (2003) Role of collagen and other organics in the mechanical properties of bone. Osteoporos Int 14: S29-S36. doi:10.1007/s00198-003-1470-8
12. Delmas PD, Tracy RP, Riggs BL, Mann KG (1984) Identification of the noncollagenous proteins of bovine bone by two-dimensional gel-electrophoresis. Calcif Tissue Int 36:308-316 (Pubitemid 14072399)
13. Dorozhkin SV, Epple M (2002) Biological and medical significance of calcium phosphates. Angew Chem Int Edit 41:3130-3146 (Pubitemid 35021275)
14. Fels IG (1964) Hydration and density of collagen and gelatin. J Appl Polym Sci 8:1813-1824
15. Fratzl P (2003) Cellulose and collagen: from fibres to tissues. Curr Opin Colloid Interface Sci 8:32-39. doi:10.1016/S1359-0294 (03) 00011-6 (Pubitemid 36740821)
16. Fratzl P, Gupta HS, Paschalis EP, Roschger P (2004) Structure and mechanical quality of the collagen-mineral nano-composite in bone. J Mater Chem 14:2115-2123. doi:10.1039/b402005g
17. Fratzl P, Weinkamer R (2007) Nature's hierarchical materials. Prog Mater Sci 52:1263-1334. doi:10.1016/j.pmatsci.2007.06.001 (Pubitemid 47374755)
18. Gao HJ, Ji BH, Jäger IL, Artz E, Fratzl P (2003) Materials become insensitive to flaws at nanoscale: lessons from nature. Proc Natl Acad Sci USA 100:5597-5600. doi:10.1073/pnas.0631609100 (Pubitemid 36576853)
19. Gilmore RS, Katz JL (1982) Elastic properties of apatites. J Mater Sci 17:1131-1141
20. Gong H, Zhang M, Qin L, Hou YJ (2007) Regional variations in the apparent and tissue-level mechanical parameters of vertebral trabecular bone with aging using micro-finite element analysis. Ann Biomed Eng 35:1622-1631. doi:10.1007/s10439-007-9332-8 (Pubitemid 350092437)
21. Gupta HS, Schratter S, Tesch W, Roschger P, Berzlanovich A, Schoeberl T, Klaushofer K, Fratzl P (2005) Two different correlations between nanoindentation modulus and mineral content in the bone-cartilage interface. J Struct Biol 149:138-148. doi:10.1016/j.jsb.2004.10.010 (Pubitemid 40170096)
22. Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P (2006) Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci USA 103:17741-17746. doi:10.1073/pnas.0604237103 (Pubitemid 44852230)
23. Gupta HS, Wagermaier W, Zickler GA, Aroush DRB, Funari SS, Roschger P, Wagner HD, Fratzl P (2005) Nanoscale deformation mechanisms in bone. Nano Lett 5:2108-2111. doi:10.1021/nl051584b (Pubitemid 41546347)
24. Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK (2004) High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35:4-10. doi:10.1016/j.bone.2004.02.024 (Pubitemid 38789142)
25. Heim AJ, Matthews WG, Koob TJ (2006) Determination of the elastic modulus of native collagen fibrils via radial indentation. Appl Phys Lett 89:181902. doi:10.1063/1.2367660 (Pubitemid 44705665)
26. Hoffmann U, Kwait DC, Handwerker J, Chan R, Lamuraglia G, Brady TJ (2003) Vascular calcification in ex vivo carotid specimens: precision and accuracy of measurements with multi-detector row CT. Radiology 229:375-381. doi:10.1148/radiol.2292021016 (Pubitemid 37310820)
27. Hulmes DJS (2002) Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137:2-10. doi:10.1006/jsbi.2002. 4450 (Pubitemid 35430415)
28. Hulmes DJS, Wess TJ, Prockop DJ, Fratzl P (1995) Radial packing, order, and disorder in collagen fibrils. Biophys J 68:1661-1670
29. Jäger I, Fratzl P (2000) Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J 79:1737-1746
30. Jokanovic V, Izvonar D, Dramicanin MD, Jokanovic B, Zivojinovic V, Markovic D, Dacic B (2006) Hydrothermal synthesis and nanostructure of carbonated calcium hydroxyapatite. J Mater Sci Mater Med 17:539-546. doi:10.1007/s10856-006-8937-z (Pubitemid 43725240)
31. Knowles TP, Fitzpatrick AW, Meehan S, Mott HR, Vendruscolo M, Dobson CM, Welland ME (2007) Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318:1900-1903. doi:10.1126/science.1150057
32. Koch CF, Johnson S, Kumar D, Jelinek M, Chrisey DB, Doraiswamy A, Jin C, Narayan RJ, Millailescu IN (2007) Pulsed laser deposition of hydroxyapatite thin films. Mater Sci Eng C Biomimetic Supramol Syst 27:484-494. doi:10.1016/j.msec.2006.05.025 (Pubitemid 46281611)
33. Landis WJ, Hodgens KJ, Arena J, Song MJ, McEwen BF (1996) Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc Res Tech 33:192-202
34. Landis WJ, Librizzi JJ, Dunn MG, Silver FH (1995) A study of the relationship between mineral content and mechanical properties of turkey gastrocnemius tendon. J Bone Miner Res 10:859-867
35. Lowenstam HA, Weiner S (1989) On Biomineralization. Oxford University, New York
36. Lozano LF, Pena-Rico MA, Heredia A, Octolan-Flores J, Gomez-Cortes A, Velazquez R, Belio IA, Bucio L (2003) Thermal analysis study of human bone. J Mater Sci 38:4777-4782
37. Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, New York
38. Meyers MA, Chen PY, Lin AYM, Seki Y (2008) Biological materials: Structure and mechanical properties. Prog Mater Sci 53:1-206. doi:10.1016/j.pmatsci.2007.05.002 (Pubitemid 350017839)
39. Nyman JS, Roy A, Shen XM, Acuna RL, Tyler JH, Wang XD (2006) The influence of water removal on the strength and toughness of cortical bone. J Biomech 39:931-938. doi:10.1016/j.jbiomech.2005.01.012 (Pubitemid 43243781)
40. Olszta MJ, Cheng XG, Jee SS, Kumar R, Kim YY, Kaufman MJ, Douglas EP, Gower LB (2007) Bone structure and formation: a new perspective. Mater Sci Eng R Rep 58:77-116. doi:10.1016/j. mser.2007.05.001 (Pubitemid 350051885)
41. Orgel JP, Wess TJ, Miller A (2000) The in situ conformation and axial location of the intermolecular cross-linked non-helical telopeptides of type I collagen. Struct Fold des 8:137-142 (Pubitemid 30097359)
42. Orgel JPRO, Irving TC, Miller A, Wess TJ (2006) Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci USA 103:9001-9005. doi:10.1073/pnas.0502718103 (Pubitemid 43902523)
43. Orgel JPRO, Miller A, Irving TC, Fischetti RF, Hammersley AP, Wess TJ (2001) The in situ supermolecular structure of type I collagen. Structure 9:1061-1069 (Pubitemid 33092109)
44. Oyen ML (2008) The materials science of bone: lessons from nature for biomimetic materials synthesis. MRS Bull 33:49-55 (Pubitemid 351224825)
45. Parry DAD, Craig AS (1984) Growth and development of collagen fibrils in connective tissue. In: Ruggeri A, Motta PM (eds) Ultrastructure of the connective tissue matrix. Martinus Nijhoff, Boston, pp 34-63
46. Perumal S, Antipova O, Orgel JPRO (2008) Collagen fibril architecture, domain organization, and triple-helical conformation govern its proteolysis. Proc Natl Acad Sci USA 105:2824-2829. doi:10. 1073/pnas.0710588105 (Pubitemid 351723628)
47. Posner AS (1969) Crystal chemistry of bone mineral. Physiol Rev 49:760-792
48. Puxkandl R, Zizak I, Paris O, Keckes J, Tesch W, Bernstorff S, Purslow P, Fratzl P (2002) Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc B Biol Sci 357:191-197. doi:10.1098/rstb.2001.1033 (Pubitemid 34276210)
49. Reid SA (1987) Micromorphological characterization of normal human-bone surfaces as a function of age. Scanning Micros 1:579-597 (Pubitemid 18516707)
50. Rho JY, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20:92-102 (Pubitemid 28318322)
51. Rubin MA, Jasiuk I, Taylor J, Rubin J, Ganey T, Apkarian RP (2003) TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 33:270-282. doi:10.1016/S8756-3282 (03) 00194-7 (Pubitemid 37103244)
52. Sasaki N, Enyo A (1995) Viscoelastic properties of bone as a function of water-content. J Biomech 28:809-815
53. Shen H, Li H, Brinson LC (2008) Effect of microstructural configurations on the mechanical responses of porous titanium: a numerical design of experiment analysis for orthopedic applications. Mech Mater 40:708-720. doi:10.1016/j.mechmat.008.03.009
54. Smith JW, Walmsley M (1959) Factors affecting the elasticity of bone. J Anat 93:503-523
55. Traub W, Arad T, Weiner S (1989) 3-dimensional ordered distribution of crystals in turkey tendon collagen-fibers. Proc Natl Acad Sci USA 86:9822-9826 (Pubitemid 20030726)
56. Vincent JFV (1990) Structural biomaterials, revised edn. Princeton University, Princeton
57. Wang XD, Puram S (2004) The toughness of cortical bone and its relationship with age. Ann Biomed Eng 32:123-135
58. Weiner S, Wagner HD (1998) The material bone: structure mechanical function relations. Ann Rev Mater Res 28:271-298 (Pubitemid 128631421)
59. Yamashita J, Furman BR, Rawls HR, Wang XD, Agrawal CM (2001) The use of dynamic mechanical analysis to assess the viscoelastic properties of human cortical bone. J Biomed Mater Res 58:47-53 (Pubitemid 32150700)