From mechanical stimulus to bone formation: A review

Medical Engineering and Physics

Volumn 37, Issue 8, 2015, Pages 719-728

  Rosa, Natacha ^a   Simoes, Ricardo ^b,c   Magalhães, Fernão D ^a   Marques, Antonio Torres ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b Instituto Politcnico do Cvado e do Ave   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

Author keywords

Bone; Mechanical stimulus; Mechanotransduction; Muscles; Osteocyte; Test model

Indexed keywords

BEHAVIORAL RESEARCH; MUSCLE;

EXTERNAL STIMULUS; MECHANICAL FORCE; MECHANICAL STIMULATION; MECHANICAL STIMULUS; MECHANOTRANSDUCTION; OSTEOCYTES; STRUCTURAL DEVELOPMENT; TEST MODELING;

BONE;

BONE MASS; BONE STRESS; COMPUTER MODEL; EX VIVO STUDY; FLUID FLOW; HUMAN; IN VIVO STUDY; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; OSSIFICATION; OSTEOCYTE; PIEZOELECTRICITY; PRIORITY JOURNAL; REVIEW; SHEAR FLOW; ANIMAL; BIOMECHANICS; BONE; BONE DEVELOPMENT; MECHANICAL STRESS; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; BIOMECHANICAL PHENOMENA; BONE AND BONES; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MUSCLE, SKELETAL; OSTEOCYTES; OSTEOGENESIS; STRESS, MECHANICAL;

EID: 84937515363     PISSN: 13504533     EISSN: 18734030     Source Type: Journal    
DOI: 10.1016/j.medengphy.2015.05.015     Document Type: Review

References (164)

1. Galilei G. Discorsi e dimostrazioni matematiche intorno a due nuove scienze attenenti alla meccanica ed ai movimenti locali 1638, Società Editrice Fiorentina, Leida. 1st ed.
2. von Meyer G.H. Die architektur der spongiosa. Arch Anat Physiol Wiss Med 1867, 34:615-628.
3. Culmann K. Die graphische statik 1866, Meyer & Zeller, Zürich.
4. Roux W. Die entwicklungsmechanik; ein neuer Zweig der biologischen Wissenschaft. Roux, Vorträge und Aufsätze, part I 1905, Engelmann, Leipzig.
5. Skedros J.G., Brand R.A. Biographical sketch: Georg Hermann von Meyer (1815-1892). Clin Orthop Relat Res 2011, 469:3072-3076.
6. Carter D.R. Mechanical loading histories and cortical bone remodeling. Calcif Tissue Int 1984, 36:S19-S24.
7. Huiskes R. If bone is the answer, then what is the question. J Anat 2000, 197:145-156.
8. Wolff J. Das gesetz der transformation der knochen 1892, Verlag von August Hirschwald, Berlin.
9. Duncan R.L., Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int 1995, 57:344-358.
10. Ahn A.C., Grodzinsky A.J. Relevance of collagen piezoelectricity to "Wolff 's Law": a critical review. Med Eng Phys 2009, 31:733-741.
11. Skerry T.M. One mechanostat or many? Modifications of the site-specific response of bone to mechanical loading by nature and nurture. J Musculoskel Neuron Interact 2006, 6:122-127.
12. Burr D.B. Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 1997, 12:1547-1551.
13. Bakker A.D., Soejima K., Klein-Nulend J., Burger E.H. The production of nitric oxide and prostaglandin E2 by primary bone cells is shear stress dependent. J Biomech 2001, 34:671-677.
14. Duda G.N., Heller M., Albinger J., Schulz O., Schneider E., Claes L. Influence of muscle forces on femoral strain distribution. J Biomech 1998, 31:841-846.
15. Rittweger J., Reeves N.D., Narici M.V., Belavý D.L., Maganaris C.N., Maffulli N. Persisting side-to-side differences in bone mineral content, but not in muscle strength and tendon stiffness after anterior cruciate ligament reconstruction. Clin Physiol Funct Imaging 2011, 31:73-79.
16. Sievänen H., Heinonen A., Kannus P. Adaptation of bone to altered loading environment: a biomechanical approach using X-ray absorptiometric data from the patella of a young woman. Bone 1996, 19:55-59.
17. Schönau E., Werhahn E., Schiedermaier U., Mokow E., Schiessl H., Scheidhauer K., et al. Influence of muscle strength on bone strength during childhood and adolescence. Horm Res 1996, 45:63-66.
18. Klein-Nulend J., Bacabac R.G., Mullender M.G. Mechanobiology of bone tissue. Pathol Biol 2005, 53:576-580.
19. Pauwels F. Biomechanics of the Locomotor Apparatus 1980, Springer Berlin Heidelberg, Berlin.
20. Munih M., Kralj A., Bajd T. Bending moments in lower extremity bones for two standing postures. J Biomed Eng 1992, 14:293-302.
21. Lanyon L.E. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone 1996, 18:S37-S43.
22. Aarden E.M., Nijweide P.J., Burger E.H. Function of osteocytes in bone. J Cell Biochem 1994, 55:287-299.
23. Rubin C.T., McLeod K.J., Bain S.D. Functional strains and cortical bone adaptation: epigenetic assurance of skeletal integrity. J Biomech 1990, 23:43-54.
24. Turner C.H., Pavalko F.M. Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J Orthop Sci 1998, 3:346-355.
25. Waung J.A., Bassett J.H.D., Williams G.R. Thyroid hormone metabolism in skeletal development and adult bone maintenance. Trends Endocrinol Metab 2012, 23:155-162.
26. Cauley J.A. Estrogen and bone health in men and women. Steroids 2015, 99:11-15.
27. Elefteriou F., Campbell P., Ma Y. Control of bone remodeling by the peripheral sympathetic nervous system. Calcif Tissue Int 2014, 94:140-151.
28. Redlich K., Smolen J.S. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat Rev Drug Discov 2012, 11:234-250.
29. Manolagas S.C., Parfitt A.M. What old means to bone. Trends Endocrinol Metab 2010, 21:369-374.
30. Temiyasathit S., Jacobs C.R. Osteocyte primary cilium and its role in bone mechanotransduction. Ann N Y Acad Sci 2010, 1192:422-428.
31. Isaacson B.M., Bloebaum R.D. Bone bioelectricity: what have we learned in the past 160 years?. J Biomed Mater Res 2010, 95:1270-1279.
32. Klein-Nulend J., Bakker A.D., Bacabac R.G., Vatsa A., Weinbaum S. Mechanosensation and transduction in osteocytes. Bone 2013, 54:182-190.
33. Rath Bonivtch A., Bonewald L.F., Nicolella D.P. Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech 2007, 40:2199-2206.
34. Vaughan T.J., Verbruggen S.W., McNamara L.M. Are all osteocytes equal? Multiscale modelling of cortical bone to characterise the mechanical stimulation of osteocytes. Int J Numer Method Biomed Eng 2013, 29:1361-1372.
35. McGarry J.G., Klein-Nulend J., Mullender M.G., Prendergast P.J. A comparison of strain and fluid shear stress in stimulating bone cell responses-a computational and experimental study. FASEB J 2005, 19:482-484.
36. Wang L., Dong J., Xian C.J. Strain amplification analysis of an osteocyte under static and cyclic loading: a finite element study. Biomed Res Int 2015, 2015:1-14.
37. Gardinier J.D., Townend C.W., Jen K.-P., Wu Q., Duncan R.L., Wang L. In situ permeability measurement of the mammalian lacunar-canalicular system. Bone 2010, 46:1075-1081.
38. Ajubi N.E., Klein-Nulend J., Nijweide P.J., Vrijheid-Lammers T., Alblas M.J., Burger E.H. Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes-a cytoskeleton-dependent process. Biochem Biophys Res Commun 1996, 225:62-68.
39. Bacabac R.G., Smit T.H., Mullender M.G., Dijcks S.J., Van Loon J.J.W.A., Klein-Nulend J. Nitric oxide production by bone cells is fluid shear stress rate dependent. Biochem Biophys Res Commun 2004, 315:823-829.
40. Piekarski K. Transport mechanism operating between blood supply and osteocytes in long bones. Nature 1977, 269:80-82.
41. Verbruggen S.W., Vaughan T.J., McNamara L.M. Fluid flow in the osteocyte mechanical environment: a fluid-structure interaction approach. Biomech Model Mechanobiol 2014, 13:85-97.
42. Morris H.L., Reed C.I., Haycock J.W., Reilly G.C. Mechanisms of fluid-flow-induced matrix production in bone tissue engineering. Proc Inst Mech Eng H J Eng Med 2010, 224:1509-1521.
43. Delaine-Smith R.M., MacNeil S., Reilly G.C. Matrix production and collagen structure are enhanced in two types of osteogenic progenitor cells by a simple fluid shear stress stimulus. Eur Cell Mater 2012, 24:162-174.
44. Young Y.-N., Espinha L.C., Nguyen A.M., Jacobs C.R. Multiscale modeling of primary cilia. Multiscale modeling in biomechanics and mechanobiology 2015, 87-110. Springer. S. De, W. Hwang, E. Kuhl (Eds.).
45. Donahue T.L.H., Haut T.R., Yellowley C.E., Donahue H.J., Jacobs C.R. Mechanosensitivity of bone cells to oscillating fluid flow induced shear stress may be modulated by chemotransport. J Biomech 2003, 36:1363-1371.
46. Case N., Sen B., Thomas J.A., Styner M., Xie Z., Jacobs C.R., et al. Steady and oscillatory fluid flows produce a similar osteogenic phenotype. Calcif Tissue Int 2011, 88:189-197.
47. Jacobs C.R., Yellowley C.E., Davis B.R., Zhou Z., Cimbala J.M., Donahue H.J. Differential effect of steady versus oscillating flow on bone cells. J Biomech 1998, 31:969-976.
48. Hastings G., Mahmud F. Electrical effects in bone. J Biomed Eng 1988, 10:515-521.
49. Starkebaum W., Pollack S.R., Korostoff E. Midroelectrode studies of stress-generated potentials in four-point bending of bone. J Biomed Mater Res 1979, 13:729-751.
50. Salzstein R.A., Pollack S.R., Mak A.F.T., Petrov N. Electromechanical potentials in cortical bone-I. A continuum approach. J Biomech 1987, 20:261-270.
51. Salzstein R.A., Pollack S.R. Electromechanical potentials in cortical bone-II. Experimental analysis. J Biomech. 1987, 20:271-280.
52. Yasuda I. The classic: fundamental aspects of fracture treatment, reprinted from J Kyoto Med Soc, 4:395-406, 1953. Clin Orthop Relat Res 1977, 124:5-8.
53. Fukada E., Yasuda I. On the piezoelectric effect of bone. J Physical Soc Jpn 1957, 12:1158-1162.
54. Marino A.A., Becker R.O., Soderholm S.C. Origin of the piezoelectric effect in bone. Calcif Tissue Res 1971, 8:177-180.
55. Minary-Jolandan M., Yu M.-F. Nanoscale characterization of isolated individual type I collagen fibrils: polarization and piezoelectricity. Nanotechnology 2009, 20:085706.
56. Lemaire T., Capiez-Lernout E., Kaiser J., Naili S., Rohan E., Sansalone V. A multiscale theoretical investigation of electric measurements in living bone. Bull Math Biol 2011, 73:2649-2677.
57. Schaffler M.B., Cheung W.-Y., Majeska R., Kennedy O. Osteocytes: master orchestrators of bone. Calcif Tissue Int 2013, 94:1-20.
58. Iolascon G., Resmini G., Tarantino U. Mechanobiology of bone. Aging Clin Exp Res 2013, 25:3-7.
59. Han Y., Cowin S.C., Schaffler M.B., Weinbaum S. Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci USA 2004, 101:16689-16694.
60. Adachi T., Aonuma Y., Tanaka M., Hojo M., Takano-Yamamoto T., Kamioka H. Calcium response in single osteocytes to locally applied mechanical stimulus: differences in cell process and cell body. J Biomech 2009, 42:1989-1995.
61. Thi M.M., Suadicani S.O., Schaffler M.B., Weinbaum S., Spray D.C. Mechanosensory responses of osteocytes to physiological forces occur along processes and not cell body and require αVβ3 integrin. Proc Natl Acad Sci 2013, 110:21012-21017.
62. Thi M.M., Suadicani S.O., Schaffler M.B., Weinbaum S., Spray D.C. Mechanosensory responses of osteocytes to physiological forces occur along processes and not cell body and require αVβ3 integrin. Proc Natl Acad Sci USA 2013, 110:21012-21017.
63. Robling A.G., Turner C.H. Mechanical signaling for bone modeling and remodeling. Crit Rev Eukaryot Gene Exp 2009, 19:319-338.
64. Ross T.D., Coon B.G., Yun S., Baeyens N., Tanaka K., Ouyang M., et al. Integrins in mechanotransduction. Curr Opin Cell Biol 2013, 25:613-618.
65. Ozcivici E., Luu Y.K., Adler B., Qin Y.-X., Rubin J., Judex S., et al. Mechanical signals as anabolic agents in bone. Nat Rev Neurol 2010, 6:50-59.
66. Mikuni-Takagaki Y., Naruse K., Azuma Y., Miyauchi A. The role of calcium channels in osteocyte function. J Musculoskel Neuron Interact 2002, 2:252-255.
67. Liedert A., Kaspar D., Blakytny R., Claes L., Ignatius A. Signal transduction pathways involved in mechanotransduction in bone cells. Biochem Biophys Res Commun 2006, 349:1-5.
68. Rawlinson S.C.F., Pitsillides A.A., Lanyon L.E. Involvement of different ion channels in osteoblasts' and osteocytes' early responses to mechanical strain. Bone 1996, 19:609-614.
69. Malone A.M.D., Anderson C.T., Tummala P., Kwon R.Y., Johnston T.R., Stearns T., et al. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci USA 2007, 104:13325-13330.
70. Delaine-Smith R.M., Sittichokechaiwut A., Reilly G.C. Primary cilia respond to fluid shear stress and mediate flow-induced calcium deposition in osteoblasts. FASEB J 2014, 28:430-439.
71. Pajevic P.D. Recent progress in osteocyte research. Endocrinol Metab 2013, 28:255-261.
72. Hum J.M., Day R.N., Bidwell J.P., Wang Y., Pavalko F.M. Mechanical loading in osteocytes induces formation of a Src/Pyk2/MBD2 complex that suppresses anabolic gene expression. PLoS One 2014, 9:e97942.
73. Lu X.L., Huo B., Park M., Guo X.E. Calcium response in osteocytic networks under steady and oscillatory fluid flow. Bone 2012, 51:466-473.
74. Lemaire T., Naili S. Possible role of calcium permselectivity in bone adaptation. Med Hypotheses 2012, 78:367-369.
75. Fox S.W., Chambers T.J., Chow J.W. Nitric oxide is an early mediator of the increase in bone formation by mechanical stimulation. Am J Physiol Endocrinol Metab 1996, 270:E955-E960.
76. Chow J.W.M., Fox S.W., Lean J.M., Chambers T.J. Role of nitric oxide and prostaglandins in mechanically induced bone formation. J Bone Miner Res 1998, 13:1039-1044.
77. Klein-Nulend J., Van Oers R.F.M., Bakker A.D., Bacabac R.G. Nitric oxide signaling in mechanical adaptation of bone. Osteoporos Int 2014, 25:1427-1437.
78. Klein-Nulend J., Semeins C.M., Ajubi N.E., Nijweide P.J., Burger E.H. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts-correlation with prostaglandin upregulation. Biochem Biophys Res Commun 1995, 217:640-648.
79. Vatsa A., Mizuno D., Smit T.H., Schmidt C.F., MacKintosh F.C., Klein-Nulend J. Bio imaging of intracellular NO production in single bone cells after mechanical stimulation. J Bone Miner Res 2006, 21:1722-1728.
80. Tan S.D., de Vries T.J., Kuijpers-Jagtman A.M., Semeins C.M., Everts V., Klein-Nulend J. Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone 2007, 41:745-751.
81. Vezeridis P.S., Semeins C.M., Chen Q., Klein-Nulend J. Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun 2006, 348:1082-1088.
82. Dirckx N., Hul M., Maes C. Osteoblast recruitment to sites of bone formation in skeletal development, homeostasis, and regeneration. Birth Defects Res C Embryo Today 2013, 99:170-191.
83. Hambli R., Rieger R. Physiologically based mathematical model of transduction of mechanobiological signals by osteocytes. Biomech Model Mechanobiol 2012, 11:83-93.
84. Robling A.G., Castillo A.B., Turner C.H. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 2006, 8:455-498.
85. Sims N.A., Vrahnas C. Regulation of cortical and trabecular bone mass by communication between osteoblasts, osteocytes and osteoclasts. Arch Biochem Biophys 2014, 561:22-28.
86. Ehrlich P.J., Lanyon L.E. Mechanical strain and bone cell function: a review. Osteoporos Int 2002, 13:688-700.
87. Hert J., Liskova M., Landrgot B. Influence of the long-term, continuous bending on the bone an experimental study on the tibia of the rabbit. Folia Morphol 1969, 17:389.
88. Hert J., Liskova M., Landa J. Reaction of bone to mechanical stimuli 1. Continuous and intermittent loading of tibia in rabbit. Folia Morphol. 1971, 19:290-300.
89. Kunnel J.G., Gilbert J.L., Stern P.H. In vitro mechanical and cellular responses of neonatal mouse bones to loading using a novel micromechanical-testing device. Calcif Tissue Int 2002, 71:499-507.
90. Fritton S.P., McLeod K.J., Rubin C.T. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech 2000, 33:317-325.
91. Hoshaw S.J., Fyhrie D.P., Takano Y., Burr D.B., Milgrom C. A method suitable for in vivo measurement of bone strain in humans. J Biomech 1997, 30:521-524.
92. Lanyon L.E., Hampson W.G.J., Goodship A.E., Shah J.S. Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft. Acta Orthop Scand 1975, 46:256-268.
93. Mikić B., Carter D.R. Bone strain gage data and theoretical models of functional adaptation. J Biomech 1995, 28:465-469.
94. Frost H.M. Bone "mass" and the "mechanostat": a proposal. Anat Rec 1987, 219:1-9.
95. Frost H.M. Bone's mechanostat: a 2003 update. Anat Rec 2003, 275:1081-1101.
96. Burr D.B., Milgrom C., Fyhrie D., Forwood M., Nyska M., Finestone A., et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996, 18:405-410.
97. Ekenman I., Halvorsen K., Westblad P., Fellãnder-Tsai L., Rolf C. Local bone deformation at two predominant sites for stress fractures of the tibia: an in vivo study. Foot Ankle Int 1998, 19:479-484.
98. Milgrom C., Finestone A., Levi Y., Simkin A., Ekenman I., Mendelson S., et al. Do high impact exercises produce higher tibial strains than running?. Br J Sports Med 2000, 34:195-199.
99. Weinbaum S., Cowin S.C., Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 1994, 27:339-360.
100. Henstock J.R., Rotherham M., Rose J.B., El Haj A.J. Cyclic hydrostatic pressure stimulates enhanced bone development in the foetal chick femur in vitro. Bone 2013, 53:468-477.
101. Poliachik S.L., Threet D., Srinivasan S., Gross T.S. 32 wk old C3H/HeJ mice actively respond to mechanical loading. Bone 2008, 42:653-659.
102. Rubin C.T., Lanyon L.E. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 1985, 37:411-417.
103. Turner C.H., Forwood M.R., Rho J.-Y., Yoshikawa T. Mechanical loading thresholds for lamellar and woven bone formation. J Bone Miner Res 1994, 9:87-97.
104. Al Nazer R., Rantalainen T., Heinonen A., Sievänen H., Mikkola A. Flexible multibody simulation approach in the analysis of tibial strain during walking. J Biomech 2008, 41:1036-1043.
105. Milgrom C., Radeva-Petrova D.R., Finestone A., Nyska M., Mendelson S., Benjuya N., et al. The effect of muscle fatigue on in vivo tibial strains. J Biomech 2007, 40:845-850.
106. Milgrom C., Finestone A., Simkin A., Ekenman I., Mendelson S., Millgram M., et al. In vivo strain measurements to evaluate the strengthening potential of exercises on the tibial bone. J Bone Joint Surg Br 2000, 82:591-594.
107. Huang R.P., Rubin C.T., McLeod K.J. Changes in postural muscle dynamics as a function of age. J Gerontol A Biol Sci Med Sci 1999, 54:B352-B357.
108. Rubin C.T., Sommerfeldt D.W., Judex S., Qin Y.-X. Inhibition of osteopenia by low magnitude, high-frequency mechanical stimuli. Drug Discov Today 2001, 6:848-858.
109. Judex S., Rubin C.T. Is bone formation induced by high-frequency mechanical signals modulated by muscle activity?. J Musculoskel Neuron Interact 2010, 10:3-11.
110. Afzal S.Y., Wender A.R., Jones M.D., Fung E.B., Pico E.L. The effect of low magnitude mechanical stimulation (LMMS) on bone density in patients with Rett syndrome: a pilot and feasibility study. J Pediatr Rehabil Med 2014, 7:167-178.
111. Padilla F., Puts R., Vico L., Raum K. Stimulation of bone repair with ultrasound: a review of the possible mechanic effects. Ultrasonics 2014, 54:1125-1145.
112. Dionyssiotis Y., Stathopoulos K., Trovas G., Papaioannou N., Skarantavos G., Papagelopoulos P. Impact on bone and muscle area after spinal cord injury. BoneKEy Rep 2015, 4.
113. Lloyd S.A., Lang C.H., Zhang Y., Paul E.M., Laufenberg L.J., Lewis G.S., et al. Interdependence of muscle atrophy and bone loss induced by mechanical unloading. J Bone Miner Res 2014, 29:1118-1130.
114. Hsieh Y.-F., Robling A.G., Ambrosius W.T., Burr D.B., Turner C.H. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 2001, 16:2291-2297.
115. Noble B.S., Peet N., Stevens H.Y., Brabbs A., Mosley J.R., Reilly G.C., et al. Mechanical loading: Biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol-Cell Physiol 2003, 284:C934-C943.
116. Robling A.G., Niziolek P.J., Baldridge L.A., Condon K.W., Allen M.R., Alam I., et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 2008, 283:5866-5875.
117. Raab-Cullen D.M., Akhter M.P., Kimmel D.B., Recker R.R. Periosteal bone formation stimulated by externally induced bending strains. J Bone Miner Res 1994, 9:1143-1152.
118. Moustafa A., Sugiyama T., Saxon L.K., Zaman G., Sunters A., Armstrong V.J., et al. The mouse fibula as a suitable bone for the study of functional adaptation to mechanical loading. Bone 2009, 44:930-935.
119. Pearce A., Richards R.G., Milz S., Schneider E., Pearce S.G. Animal models for implant biomaterial research in bone: a review. Eur Cell Mater 2007, 13:1-10.
120. Jones D.B., Broeckmann E., Pohl T., Smith E.L. Development of a mechanical testing and loading system for trabecular bone studies for long term culture. Eur Cell Mater 2003, 5:48-59.
121. Papadimitropoulos A., Scherberich A., Guven S., Theilgaard N., Crooijmans H.J., Santini F., et al. A 3D in vitro bone organ model using human progenitor cells. Eur Cell Mater 2011, 21:445-458.
122. Meakin L.B., Price J.S., Lanyon L.E. The contribution of experimental in vivo models to understanding the mechanisms of adaptation to mechanical loading in bone. Front Endocrinol 2014, 5:1-13.
123. Davies C.M., Jones D.B., Stoddart M.J., Koller K., Smith E., Archer C.W., et al. Mechanically loaded ex vivo bone culture system 'Zetos': systems and culture preparation. Eur Cell Mater 2006, 11:57-75.
124. Brown T.D. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech 2000, 33:3-14.
125. Brown T.D. Devices and techniques for in vitro mechanical stimulation of bone cells. Bone mechanics handbook 2001, CRC Press, Florida, 27-1-2. 2nd ed. S.C. Cowin (Ed.).
126. Glucksmann A. The role of mechanical stresses in bone formation in vitro. J Anat 1942, 76:231-239.
127. Frangos J.A., McIntire L.V., Eskin S.G. Shear stress induced stimulation of mammalian cell metabolism. Biotechnol Bioeng 1988, 32:1053-1060.
128. Nauman E.A., Risic K.J., Keaveny T.M., Satcher R.L. Quantitative assessment of steady and pulsatile flow fields in a parallel plate flow chamber. Ann Biomed Eng 1999, 27:194-199.
129. Huesa C., Helfrich M.H., Aspden R.M. Parallel-plate fluid flow systems for bone cell stimulation. J Biomech 2010, 43:1182-1189.
130. Kadow-Romacker A., Hoffmann J.E., Duda G., Wildemann B., Schmidmaier G. Effect of mechanical stimulation on osteoblast-and osteoclast-like cells in vitro. Cells Tissues Organs 2008, 190:61-68.
131. Chang Y.-H., Brady R.T., Brennan O., O'Brien F.J. A 3D environment influences osteocyte function. BMC proceedings 2015, A7. BioMed Central Ltd, Dublin, Ireland.
132. Keogh M.B., O'Brien F.J., Daly J.S. A novel collagen scaffold supports human osteogenesis-applications for bone tissue engineering. Cell Tissue Res 2010, 340:169-177.
133. Su W.-T., Wang Y.-T., Chou C.-M. Optimal fluid flow enhanced mineralization of MG-63 cells in porous chitosan scaffold. J Taiwan Inst Chem Eng 2014, 45:1111-1118.
134. Plunkett N., O'Brien F.J. Bioreactors in tissue engineering. Technol Health Care 2011, 19:55-69.
135. Porter B.D., Lin A.S.P., Peister A., Hutmacher D., Guldberg R.E. Noninvasive image analysis of 3D construct mineralization in a perfusion bioreactor. Biomaterials 2007, 28:2525-2533.
136. Haycock J.W. 3D cell culture: a review of current approaches and techniques. 3D cell culture 2011, 1-15. Springer. J.W. Haycock (Ed.).
137. Vetsch J.R., Müller R., Hofmann S. The evolution of simulation techniques for dynamic bone tissue engineering in bioreactors. J Tissue Eng Regen Med 2013.
138. Murphy C.M., Haugh M.G., O'Brien F.J. The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010, 31:461-466.
139. O'Brien F.J., Harley B.A., Waller M.A., Yannas I.V., Gibson L.J., Prendergast P.J. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol Health Care 2007, 15:3-17.
140. Murphy C.M., O'Brien F.J., Little D.G., Schindeler A. Cell-scaffold interactions in the bone tissue engineering triad. Eur Cell Mater 2013, 26:120-132.
141. Cartmell S.H., Porter B.D., García A.J., Guldberg R.E. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng 2003, 9:1197-1203.
142. McCoy R.J., Jungreuthmayer C., O'Brien F.J. Influence of flow rate and scaffold pore size on cell behavior during mechanical stimulation in a flow perfusion bioreactor. Biotechnol Bioeng 2012, 109:1583-1594.
143. Jungreuthmayer C., Jaasma M.J., Al-Munajjed A.A., Zanghellini J., Kelly D.J., O'Brien F.J. Deformation simulation of cells seeded on a collagen-GAG scaffold in a flow perfusion bioreactor using a sequential 3D CFD-elastostatics model. Med Eng Phys 2009, 31:420-427.
144. McCoy R.J., O'Brien F.J. Visualizing feasible operating ranges within tissue engineering systems using a "windows of operation" approach: a perfusion-scaffold bioreactor case study. Biotechnol Bioeng 2012, 109:3161-3171.
145. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26:433-441.
146. McCoy R.J., O'Brien F.J. Influence of shear stress in perfusion bioreactor cultures for the development of three-dimensional bone tissue constructs: a review. Tissue Eng Part C Rev 2010, 16:587-601.
147. Bonewald L.F. The amazing osteocyte. J Bone Miner Res 2011, 26:229-238.
148. Mauney J.R., Sjostorm S., Blumberg J., Horan R., O'leary J.P., Vunjak-Novakovic G., et al. Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro. Calcif Tissue Int 2004, 74:458-468.
149. Meghji S., Hill P.A., Harris M. Bone organ cultures. Methods in bone biology 1998, 106-126. Springer, London. 1st ed. T.R. Arnett, B. Henderson (Eds.).
150. David V., Guignandon A., Martin A., Malaval L., Lafage-Proust M.-H., Rattner A., et al. Ex vivo bone formation in bovine trabecular bone cultured in a dynamic 3D bioreactor is enhanced by compressive mechanical strain. Tissue Eng 2008, 14:117-126.
151. Fell H.B., Mellanby E. The effect of hypervitaminosis A on embryonic limb-bones cultivated in vitro. J Physiol 1952, 116:320-349.
152. Pitsillides A.A., Rawlinson SCF Using cell and organ culture models to analyze responses of bone cells to mechanical stimulation. Bone research protocols 2012, 593-619. Springer, New York. 2nd ed. M.H. Helfrich, S.H. Ralston (Eds.).
153. Davies C.M., Jones D.B., Alini M., Archer C., Richards R.G. Ex-vivo trabecular bone percolation system: development for evaluation of implant surfaces. Eur Cell Mater 2001, 2:63.
154. Defranoux N.A., Stokes C.L., Young D., Kahn A.J. In silico modeling and simulation of bone biology: a proposal. J Bone Miner Res 2005, 20:1079-1084.
155. Colloca M., Blanchard R., Hellmich C., Ito K., van Rietbergen B. A multiscale analytical approach for bone remodeling simulations: linking scales from collagen to trabeculae. Bone 2014, 64:303-313.
156. Idhammad A., Abdali A., Alaa N. Computational simulation of the bone remodeling using the finite element method: an elastic-damage theory for small displacements. Theor Biol Med Model 2013, 10:1-11.
157. Schulte F.A., Ruffoni D., Lambers F.M., Christen D., Webster D.J., Kuhn G., et al. Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level. PLoS One 2013, 8:e62172.
158. Geris L., Vander Sloten J., Van Oosterwyck H. In silico biology of bone modelling and remodelling: regeneration. Philos Trans R Soc A Math Phys Eng Sci 2009, 367:2031-2053.
159. Levchuk A., Zwahlen A., Weigt C., Lambers F.M., Badilatti S.D., Schulte F.A., et al. The clinical biomechanics award 2012-presented by the European society of biomechanics: large scale simulations of trabecular bone adaptation to loading and treatment. Clin Biomech 2014, 29:355-362.
160. Birkhold A.I., Razi H., Duda G.N., Weinkamer R., Checa S., Willie B.M. Mineralizing surface is the main target of mechanical stimulation independent of age: 3D dynamic in vivo morphometry. Bone 2014, 66:15-25.
161. Hambli R. Connecting mechanics and bone cell activities in the bone remodeling process: an integrated finite element modeling. Front Bioeng Biotechnol 2014, 2:1-12.
162. Kameo Y., Adachi T. Interstitial fluid flow in canaliculi as a mechanical stimulus for cancellous bone remodeling: in silico validation. Biomech Model Mechanobiol 2014, 13:851-860.
163. Yang H., Butz K.D., Duffy D., Niebur G.L., Nauman E.A., Main R.P. Characterization of cancellous and cortical bone strain in the in vivo mouse tibial loading model using microCT-based finite element analysis. Bone 2014, 66:131-139.
164. Webster D., Müller R. In silico models of bone remodeling from macro to nano-from organ to cell. Wiley Interdilscip Rev Syst Biol Med 2011, 3:241-251.