Evolution of bone biomechanical properties at the micrometer scale around titanium implant as a function of healing time

Physics in Medicine and Biology

Volumn 59, Issue 6, 2014, Pages 1389-1406

  Vayron, Romain ^a   Matsukawa, Mami ^b   Tsubota, Ryo ^b   Mathieu, Vincent ^a   Barthel, Etienne ^a   Haiat, Guillaume ^a  

^a CNRS   (France)

^b DOSHISHA UNIVERSITY   (Japan)

Author keywords

bone; elastic wave velocity; implant; mechanical properties; micro Brillouin scattering; nanoindentation; osseointegration

Indexed keywords

BIOMECHANICAL PROPERTIES; BONE MECHANICAL PROPERTIES; BONE MICROSTRUCTURE; ELASTIC WAVE VELOCITY; HISTOLOGICAL ANALYSIS; INDENTATION MODULUS; MICRO-BRILLOUIN SCATTERING; OSSEOINTEGRATION;

BIOMECHANICS; IMPLANTS (SURGICAL); MECHANICAL PROPERTIES; NANOINDENTATION; TISSUE; TISSUE ENGINEERING; WAVE PROPAGATION;

BONE;

TITANIUM;

ANIMAL; ARTICLE; BIOMECHANICS; BONE DENSITY; BONE REGENERATION; FEMALE; MATERIALS TESTING; PHYSIOLOGY; PROSTHESES AND ORTHOSES; RABBIT; SURFACE PROPERTY; TIBIA; TIME; WOUND HEALING; YOUNG MODULUS;

ANIMALS; BIOMECHANICAL PHENOMENA; BONE DENSITY; ELASTIC MODULUS; FEMALE; MATERIALS TESTING; OSSEOINTEGRATION; PROSTHESES AND IMPLANTS; RABBITS; SURFACE PROPERTIES; TIBIA; TIME FACTORS; TITANIUM; WOUND HEALING;

EID: 84896797044     PISSN: 00319155     EISSN: 13616560     Source Type: Journal    
DOI: 10.1088/0031-9155/59/6/1389     Document Type: Article

References (91)

1. Akca K, Chang T L, Tekdemir I and Fanuscu M I 2006 Biomechanical aspects of initial intraosseous stability and implant design: a quantitative micro-morphometric analysis Clin. Oral Implants Res. 17 465-72
2. Artzi Z, Givol N, Rohrer M D, Nemcovsky C E, Prasad H S and Tal H 2003 Qualitative and quantitative expression of bovine bone mineral in experimental bone defects. Part 2: morphometric analysis J. Periodontol. 74 1153-60
3. Baker M I, Eberhardt A W, Martin D M, McGwin G and Lemons J E 2010 Bone properties surrounding hydroxyapatite-coated custom osseous integrated dental implants J. Biomed. Mater. Res. B 95 218-24
4. Ballarre J, Manjubala I, Schreiner W H, Orellano J C, Fratzl P and Cere S 2009 Improving the osteointegration and bone-implant interface by incorporation of bioactive particles in sol-gel coatings of stainless steel implants Acta Biomater. 6 1601-9
5. Bensamoun S, Tho M C H, Luu S, Gherbezza J M and de Belleval J F 2004 Spatial distribution of acoustic and elastic properties of human femoral cortical bone J. Biomech. 37 503-10
6. Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie L G, Meunier P J and Delmas P D 2008 The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients Bone 43 532-8
7. Brennan O, Kennedy O D, Lee T C, Rackard S M and O'Brien F J 2009 Biomechanical properties across trabeculae from the proximal femur of normal and ovariectomised sheep J. Biomech. 42 498-503
8. Chang M C, Ko C C, Liu C C, Douglas W H, DeLong R, Seong W J, Hodges J and An K N 2003 Elasticity of alveolar bone near dental implant-bone interfaces after one month's healing J. Biomech. 36 1209-14
9. Chevallier N, Anagnostou F, Zilber S, Bodivit G, Maurin S, Barrault A, Bierling P, Hernigou P, Layrolle P and Rouard H 2009 Osteoblastic differentiation of human mesenchymal stem cells with platelet lysate Biomaterials 31 270-8
10. Cusack S and Miller A 1979 Determination of the elastic constants of collagen by Brillouin light scattering J. Mol. Biol. 135 39-51
11. Damzen M J, Vlad V I, Babin V and Mocofanescu A 2003 Stimulated Brillouin Scattering: Fundamentals and Applications (Bristol: Institute of Physics Publishing)
12. Duyck J, Vandamme K, Geris L, Van Oosterwyck H, De Cooman M, Vandersloten J, Puers R and Naert I 2006 The influence of micro-motion on the tissue differentiation around immediately loaded cylindrical turned titanium implants Arch. Oral Biol. 51 1-9
13. Freemont A J 1998 The tissues we deal with - (I) Bone Curr. Orthop. 12 181-92
14. Frost H M 2003 Bone's mechanostat: a 2003 update Anat. Rec. A 275 1081-101
15. Fukui K, Takayanagi S, Suga D and Matsukawa M 2012a Measurement of wave velocity in cortical bone by micro-Brillouin scattering technique: effect of bone tissue properties Japan. J. Appl. Phys. 51 10-11
16. Fukui K, Takayanagi S, Suga D and Matsukawa M 2012b Measurement of wave velocity in cortical bone by micro-Brillouin scattering technique: effect of bone tissue properties Japan. J. Appl. Phys. 51 07GF20
17. Gupta H S, Stachewicz U, Wagermaier W, Roschger P, Wagner H D and Fratzl P 2006 Mechanical modulation at the lamellar level in osteonal bone J. Mater. Res. 21 1913-21
18. Hadjidakis D J and Androulakis II 2006 Women's Health and Disease: Gynecologic, Endocrine, and Reproductive Issues ed G Creatsas et al (Oxford: Blackwell) pp 385-96
19. Haiat G, Sasso M, Naili S and Matsukawa M 2008 Ultrasonic velocity dispersion in bovine cortical bone: an experimental study J. Acoust. Soc. Am. 124 1811-21
20. Haiat G, Wang H L and Brunski J B 2014 Effects of biomechanical properties of the bone-implant interface on dental implant stability: from in silico approaches to the patient's mouth Annu. Rev. Biomed. Eng. at press
21. Hengsberger S, Ammann P, Legros B, Rizzoli R and Zysset P 2005 Intrinsic bone tissue properties in adult rat vertebrae: modulation by dietary protein Bone 36 134-41
22. Hoc T, Henry L, Verdier M, Aubry D, Sedel L and Meunier A 2006 Effect of microstructure on the mechanical properties of Haversian cortical bone Bone 38 466-74
23. Hodgskinson R, Currey J D and Evans G P 1989 Hardness, an indicator of the mechanical competence of cancellous bone J. Orthop. Res. 7 754-8
24. Hoffler C E, Moore K E, Kozloff K, Zysset P K, Brown M B and Goldstein S A 2000 Heterogeneity of bone lamellar-level elastic moduli Bone 26 603-9
25. Hofmann T, Heyroth F, Meinhard H, Franzel W and Raum K 2006 Assessment of composition and anisotropic elastic properties of secondary osteon lamellae J. Biomech. 39 2282-94
26. Ishimoto T, Nakano T, Yamamoto M and Tabata Y 2011 Biomechanical evaluation of regenerating long bone by nanoindentation J. Mater. Sci.-Mater. Med. 22 969-76
27. Katz J and Ukraincik K 1971 On the anisotropic elastic properties of hydroxyapatite J. Biomech. 4 221-7
28. Katz J L and Harper R A I 1990 Calcium phosphate and apatites Concise Encyclopaedia of Medical and Dental Materials (New York: Pergamon)
29. Kawabe M, Fukui K, Matsukawa M, Granke M, Saied A, Grimal Q and Laugier P 2012 Comparative investigation of elastic properties in a trabecula using micro-Brillouin scattering and scanning acoustic microscopy J. Acoust. Soc. Am. 132 EL54-60
30. Kawabe M, Matsukawa M and Ohtori N 2010 Measurement of wave velocity distribution in a trabecula by micro-Brillouin scattering technique Japan. J. Appl. Phys. 49 07HB05
31. Kruger J K, Embs J, Brierley J and Jimenez R 1998 A new Brillouin scattering technique for the investigation of acoustic and opto-acoustic properties: application to polymers J. Phys. D: Appl. Phys. 31 1913-7
32. Laugier P and Haïat G 2010 Bone Quantitative Ultrasound (Berlin: Springer)
33. Lees S and Klopholz D Z 1992 Sonic velocity and attenuation in wet compact cow femur for the frequency-range 5 to 100 MHz Ultrasound Med. Biol. 18 303-8
34. Leong P L and Morgan E F 2008 Measurement of fracture callus material properties via nanoindentation Acta Biomater. 4 1569-75
35. Leong P L and Morgan E F 2009 Correlation between nanoindentation modulus and mineral density in fracture callus tissues ASME Summer Bioengineering Conf. 2008, Parts A and B (New York: American Society of Mechanical Engineers) pp 675-6
36. Lewis G and Nyman J S 2008 The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review J. Biomed. Mater. Res. B 87 286-301
37. Li X and Bhushan B 2002 A review of nanoindentation continuous stiffness measurement technique and its applications next term Mater. Charact. 48 11-36
38. Luo G M, Sadegh A M, Alexander H, Jaffe W, Scott D and Cowin S C 1999 The effect of surface roughness on the stress adaptation of trabecular architecture around a cylindrical implant J. Biomech. 32 275-84
39. Maimoun L, Brennan T C, Badoud I, Dubois-Ferriere V, Rizzoli R and Ammann P 2010 Strontium ranelate improves implant osseointegration Bone 46 1436-41
40. Manjubala I, Liu Y, Epari D R, Roschger P, Schell H, Fratzl P and Duda G N 2009 Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing Bone 45 185-92
41. Martin R B, Lau S T, Mathews P V, Gibson V A and Stover S M 1996 Collagen fiber organization is related to mechanical properties and remodeling in equine bone. A comparison of two methods J. Biomech. 29 1515-21
42. Mathieu V, Anagnostou F, Soffer E and Haiat G 2010 Ultrasonic evaluation of dental implant biomechanical stability: an in vitro study Ultrasound Med. Biol. 37 262-70
43. Mathieu V, Anagnostou F, Soffer E and Haiat G 2011a Numerical simulation of ultrasonic wave propagation for the evaluation of dental implant biomechanical stability J. Acoust. Soc. Am. 129 4062-72
44. Mathieu V, Fukui K, Matsukawa M, Kawabe M, Vayron R, Soffer E, Anagnostou F and Haiat G 2011b Micro-Brillouin scattering measurements in mature and newly formed bone tissue surrounding an implant Trans. ASME, J. Biomech. Eng. 133 021006
45. Mathieu V, Vayron R, Barthel E, Dalmas D, Soffer E, Anagnostou F and Haiat G 2012a Mode III cleavage of a coin-shaped titanium implant in bone: effect of friction and crack propagation J. Mech. Behav. Biomed. Mater. 8 194-203
46. Mathieu V, Vayron R, Richard G, Lambert G, Naili S, Meningaud J P and Haiat G 2014 Biomechanical determinants of the stability of dental implants: influence of the bone-implant interface properties J. Biomech. 47 3-13
47. Mathieu V, Vayron R, Soffer E, Anagnostou F and Haiat G 2012b Influence of healing time on the ultrasonic response of the bone-implant interface Ultrasound Med. Biol. 38 611-8
48. Matos M A, Araujo F P and Paixao F B 2008 Histomorphometric evaluation of bone healing in rabbit fibular osteotomy model without fixation J. Orthop. Surg. Res. 3 4
49. Matsukawa M, Ohtori N, Nagai I, Bohn K P and Kruger J K 1997 Brillouin scattering and ultrasonic study on an epoxy prepolymer Japan. J. Appl. Phys. 36 2976-80
50. Matsukawa M, Tsubota R, Masahiko K and Fukui K 2014 Application of a micro-Brillouin scattering technique to characterize bone in the GHz range Ultrasonics at press
51. Meredith N 1998 Assessment of implant stability as a prognostic determinant Int. J. Prosthodont. 11 491-501
52. Mori S and Burr D B 1993 Increased intracortical remodeling following fatigue damage Bone 14 103-9
53. Norman J, Shapter J G, Short K, Smith L J and Fazzalari N L 2008 Micromechanical properties of human trabecular bone: a hierarchical investigation using nanoindentation J. Biomed. Mater. Res. A 87 196-202
54. Noyama Y, Nakano T, Ishimoto T, Sakai T and Yoshikawa H 2013 Design and optimization of the oriented groove on the hip implant surface to promote bone microstructure integrity Bone 52 659-67
55. Oliver W C and Pharr G M 1992 An improved technique for determining hardness and elastic-modulus using load and displacement sensing indentation experiments J. Mater. Res. 7 1564-83
56. Oliver W C and Pharr G M 2004 Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology J. Mater. Res. 19 3-20
57. Orlik J, Zhurov A and Middleton J 2003 On the secondary stability of coated cementless hip replacement: parameters that affected interface strength Med. Eng. Phys. 25 825-31
58. Oyen M L 2006 Nanoindentation hardness of mineralized tissues J. Biomech. 39 2699-702
59. Pilliar R M, Lee J M and Maniatopoulos C 1986 Observations on the effect of movement on bone ingrowth into porous-surfaced implants Clin. Orthop. Relat. Res. 208 108-13
60. Rabel A, Kohler S G and Schmidt-Westhausen A M 2007 Clinical study on the primary stability of two dental implant systems with resonance frequency analysis Clin. Oral Investig. 11 257-65
61. Rho J Y, Zioupos P, Currey J D and Pharr G M 1999 Variations in the individual thick lamellar properties within osteons by nanoindentation Bone 25 295-300
62. Rho J Y, Zioupos P, Currey J D and Pharr G M 2002 Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation J. Biomech. 35 189-98
63. Ronold H J and Ellingsen J E 2002a Effect of micro-roughness produced by TiO2 blasting - tensile testing of bone attachment by using coin-shaped implants Biomaterials 23 4211-9
64. Ronold H J and Ellingsen J E 2002b The use of a coin shaped implant for direct in situ measurement of attachment strength for osseointegrating biomaterial surfaces Biomaterials 23 2201-9
65. Ronold H J, Ellingsen J E and Lyngstadaas S P 2003a Tensile force testing of optimized coin-shaped titanium implant attachment kinetics in the rabbit tibiae J. Mater. Sci., Mater. Med. 14 843-9
66. Ronold H J, Lyngstadaas S P and Ellingsen J E 2003b Analysing the optimal value for titanium implant roughness in bone attachment using a tensile test Biomaterials 24 4559-64
67. Ronold H J, Lyngstadaas S P and Ellingsen J E 2003c A study on the effect of dual blasting with TiO(2) on titanium implant surfaces on functional attachment in bone J. Biomed. Mater. Res. A 67 524-30
68. Rupin F, Saïed A, Dalmas D, Peyrin F, Haupert S, Raum K, Barthel E, Boivin G and Laugier P 2009 Assessment of microelastic properties of bone using scanning acoustic microscopy : a face-to-face comparison with nanoindentation J. Clin. Densitom. 12 126
69. Sakai M 1999 The Meyer hardness: a measure for plasticity? J. Mater. Res. 14 3630-9
70. Sakamoto M, Kawabe M, Matsukawa M, Koizumi N and Ohtori N 2008 Measurement of wave velocity in bovine bone tissue by micro-Brillouin scattering Japan. J. Appl. Phys. 47 4205-8
71. Sansalone V, Bousson V, Naili S, Bergot C, Peyrin F, Laredo J D and Haiat G 2012 Anatomical distribution of the degree of mineralization of bone tissue in human femoral neck: impact on biomechanical properties Bone 50 876-84
72. Sansalone V, Naili S, Bousson V, Bergot C, Peyrin F, Zarka J, Laredo J D and Haiat G 2010 Determination of the heterogeneous anisotropic elastic properties of human femoral bone: from nanoscopic to organ scale J. Biomech. 43 1857-63
73. Seong W J, Kim U K, Swift J Q, Hodges J S and Ko C C 2009 Correlations between physical properties of jawbone and dental implant initial stability J. Prosthet. Dent. 101 306-18
74. Shen L, Wang L, Liu T X and He C B 2006 Nanoindentation and morphological studies of epoxy nanocomposites Macromol. Mater. Eng. 291 1358-66
75. Shibata Y, He L H, Toda Y, Kataoka Y, Fujisawa N, Miyazaki T and Swain M V 2008 Micromechanical evaluation of mineralized multilayers J. Biomech. 41 3414-8
76. Skedros J G, Dayton M R, Sybrowsky C L, Bloebaum R D and Bachus K N 2006a The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone J. Exp. Biol. 209 3025-42
77. Skedros J G, Sorenson S M, Takano Y and Turner C H 2006b Dissociation of mineral and collagen orientations may differentially adapt compact bone for regional loading environments: results from acoustic velocity measurements in deer calcanei Bone 39 143-51
78. Soffer E, Ouhayoun J P, Meunier A and Anagnostou F 2006 Effects of autologous platelet lysates on ceramic particle resorption and new bone formation in critical size defects: the role of anatomical sites J. Biomed. Mater. Res. B 79 86-94
79. Sohn J-Y, Park J-C, Um Y-J, Jung U-W, Kim C-S, Cho K-S and Choi S-H 2010 Spontaneous healing capacity of rabbit cranial defects of various sizes J. Periodontal. Implant Sci. 40 180-7
80. Speziale S, Jiang F, Caylor C L, Kriminski S, Zha C S, Thorne R E and Duffy T S 2003 Sound velocity and elasticity of tetragonal lysozyme crystals by Brillouin spectroscopy Biophys. J. 85 3202-13
81. Vayron R, Barthel E, Mathieu V, Soffer E, Anagnostou F and Haiat G 2012 Nanoindentation measurements of biomechanical properties in mature and newly formed bone tissue surrounding an implant J. Biomech. Eng. 134 021007
82. Vayron R, Mathieu V, Michel A and Haiat G 2014 Assessment of the in vitro dental implant primary stability using an ultrasonic method Ultrasound Med. Biol. at press
83. Viceconti M, Brusi G, Pancanti A and Cristofolini L 2006 Primary stability of an anatomical cementless hip stem: a statistical analysis J. Biomech. 39 1169-79
84. Viceconti M, Monti L, Muccini R, Bernakiewicz M and Toni A 2001 Even a thin layer of soft tissue may compromise the primary stability of cementless hip stems Clin. Biomech. 16 765-75
85. Wang R Z, Cui F Z, Lu H B, Wen H B, Ma C L and Li H D 1995 Synthesis of nanophase hydroxyapatite collagen composite J. Mater. Sci. Lett. 14 490-2
86. Wang X, Allen M, Burr D, Lavernia E, Jeremić B and Fyhrie D P 2008 Identification of material parameters based on Mohr-Coulomb failure criterion for bisphosphonate treated canine vertebral cancellous bone Bone 43 775-80
87. Winter W, Heckmann S M and Weber H P 2004 A time-dependent healing function for immediate loaded implants J. Biomech. 37 1861-7
88. Wolfram U, Wilke H J and Zysset P K 2010 Rehydration of vertebral trabecular bone: influences on its anisotropy, its stiffness and the indentation work with a view to age, gender and vertebral level Bone 46 348-54
89. Yamato Y, Matsukawa M, Otani T, Yamazaki K and Nagano A 2006 Distribution of longitudinal wave properties in bovine cortical bone in vitro Ultrasonics 44 E233-7
90. Zysset P K 2009 Indentation of bone tissue: a short review Osteoporosis Int. 20 1049-55
91. Zysset P K, Guo X E, Hoffler C E, Moore K E and Goldstein S A 1999 Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur J. Biomech. 32 1005-12