712
Views
22
CrossRef citations to date
0
Altmetric
Ultrastructure Imaging: Review Article

Multiscale imaging of bone microdamage

&
Pages 87-98 | Received 08 Oct 2014, Accepted 08 Jan 2015, Published online: 09 Feb 2015

References

  • Knudtson M. Osteoporosis: background and overview. J Nurse Pract 2009;5:S4–12
  • Bonnick SL, Shulman L. Monitoring osteoporosis therapy: bone mineral density, bone turnover markers, or both? Am J Med 2006;119:S25–31
  • Hui S, Slemenda CW, Johnston CC. Age and bone mass as predictors of fracture in a prospective study. J Clin Invest 1988;81:1804–9
  • Hernandez CJ, Keaveny TM. A biomechanical perspective on bone quality. Bone 2006;39:1173–81
  • Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995;17:521–5
  • Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone 1997;20:375–9
  • Diab T, Vashishth D. Effects of damage morphology on cortical bone fragility. Bone 2005;37:96–102
  • Zioupos P, Currey JD. The extent of microcracking and the morphology of microcracks in damaged bone. J Mater Sci 1994;29:978–86
  • Traub W, Weiner S. Bone structure: from angstroms to microns. FASEB J 1992;6:879–85
  • Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, Pechenik L, Cutroni JA, Cidade GAG, Stucky GD, Morse DE, Hansma PK. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Mater 2005;4:612–16
  • Fantner GE, Oroudjev E, Schitter G, Golde LS, Thurner P, Finch MM, Turner P, Gutsmann T, Morse DE, Hansma H, Hansma PK. Sacrificial bonds and hidden length: unraveling molecular mesostructures in tough materials. Biophys J 2006;90:1411
  • Fantner GE, Adams J, Turner P, Thurner PJ, Fisher LW, Hansma PK. Nanoscale ion mediated networks in bone: osteopontin can repeatedly dissipate large amounts of energy. Nano Lett 2007;7:2491–8
  • Hansma P, Fantner G, Kindt J, Thurner P, Schitter G, Turner P, Udwin S, Finch M. Sacrificial bonds in the interfibrillar matrix of bone. J Musculoskeletal Neuronal Interact 2005;5:313–15
  • Poundarik AP, Diab T, Sroga GE, Ural A, Boskey AL, Gundberg CM, Vashishth D. Dilatational band formation in bone. Proc Natl Acad Sci 2012;109:19178–83
  • Gupta HS, Wagermaier W, Zickler GA, Raz-Ben Aroush D, Funari SS, Roschger P, Wagner HD, Fratzl P. Nanoscale deformation mechanisms in bone. Nano Lett 2005;5:2108–11
  • Wenzel TE, Schaffler MB, Fyhrie DP. In vivo trabecular microcracks in human vertebral bone. Bone 1996;19:89–95
  • Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995;17:521–5
  • Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone;1997;20:375–9
  • Frost HM. Presence of microscopic cracks in vivo in bone H Ford Hos Med Bull 1960;8:25–35
  • Vashishth D, Tanner KE, Bonfield W. Experimental validation of a crack propagation mechanism in cortical bone. J Biomech 2003;36:121–4
  • Diab T, Condon KW, Burr DB, Vashishth D. Age-related change in the damage morphology in human cortical bone and its role in bone fragility. Bone 2006;38:427–31
  • Vashishth DJ, Koontz Qiu S, Cannon-Lundin D, Yeni YN, Schaffler MB, Fyhrie DP. In vivo diffuse damage in human trabecular bone. Bone 2000;26:147–52
  • Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone 2007;40:612–18
  • Nalla RK, Kruzic JJ, Ritchie RO. On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 2004;34:790–8
  • Nalla RK, Stolken JS, Kinney JH, Ritchie RO. Fracture in human cortical bone: local fracture criteria and toughening mechanisms. J Biomech 2005;38:1517–25
  • Nalla RK, Kinney JH, Ritchie RO. Mechanistic fracture criteria for the failure of human cortical bone. Nature Mater 2003;2:164–8
  • Hiller LP, Stover SM, Gibson VA, Gibeling JC, Prater CS, Hazelwood SJ, Yeh OC, Martin RB. Osteon pullout in the equine third metacarpal bone: effects of ex-vivo fatigue. J Orthop Res 2003;21:481–8
  • Vashishth D, Tanner KE, Bonfield W. Contribution, development and morphology of microcracking in cortical bone during crack propagation. J Biomech 2000;33:1169–74
  • Mohsin S, O’Brien FJ, Lee TC. Osteonal crack barriers in ovine compact bone. J Anat 2006;208:81–9
  • Matheson GO, Clemen DB, McKenzie DC, Tauntan JE, Lloyd-Smith DR, MacIntgre JG. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1985;13:342–8
  • Meurman KAO, Elfving S. Stress fracture in soldiers: a multifocal bone disorder. Radiology 1980;134:483–7
  • Daffner RH, Pavlov H. Stress fractures: current concepts. Am J Roentgen 1992;159:245–52
  • Frost HM. Bone remodeling and its relationship to metabolic bone diseases. Springfield (IL): Charles C. Thomas; 1973
  • Martin RB, Burr DB. Structure, function and adaptation of compact bone. New York (NY): Raven Press; 1989
  • Mori S, Burr DB. Increased intracortical remodeling following fatigue damage. Bone 1993;14:103–9
  • Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB. Intracortical remodelling in adult rat long bones after fatigue loading. Bone 1998;23:275–81
  • Burr DB. Damage detection and behaviour in bone. In: Prendergast PJ, Lee TC, Carr AJ, eds. Proceedings of the 12th Conference of the European Society of Biomechanics. Dublin: Royal Academy of Medicine in Ireland. 2000:38–9
  • Lee TC, Staines A, Taylor D. Bone adaptation to load: microdamage as a stimulus for bone remodelling. J Anat 2002;201:437–46
  • Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodelling after fatifue in vivo. J Bone Miner 2000;15:60–7
  • Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. Am Soc Bone Mineral Res 2009;2:597–5
  • Kennedy OD, Herman BC, Laudier DM, Majeska RJ, Sun HB, Schaffler MB. Activation of resorption in fatigue-oaded bone involves both apoptosis and active pro-steoclastogenic signaling by distinct osteocyte populations. Bone 2012;50:1115–22
  • Fondrk M, Bahniuk E, Davy DT, Michaels C. Some viscoplastic charactercteristics of bovine and human cortical bone. J Biomech 1988;21:623–30
  • Keaveny TM, Wachtel EF, Guo XE, Hayes WC. Mechanical behavior of damaged trabecular bone. J Biomechanics 1994;27:1309–18
  • Lee TC, Mohsin S, Taylor D, Parkesh T, Gunnlaugsson T, O’Brien FJ, Giehl M, Gowin W. Detecting microdamage in bone. J Anat 2003;203:161–72
  • Rost FWD. Fluorescence microscopy. II. Cambridge: Cambridge University Press; 1995
  • Burr DB, Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop 1990;260:305–8
  • Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodelling in response to in vivo fatigue microdamage. J Biomech 1985;18:189–200
  • Vashishth D, Johnson C, Clovis N, Tanner KE, Bonfield W. Double staining technique for histological evaluation of microcracks in cortical bone. Proc 2nd World Cong Biomech 1994;I:44
  • Vashishth D. Hierarchy of bone microdamage at multiple length. Int J Fatigue 2007;29:1024–33
  • Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech 1997;30:763–9
  • Seref-Ferlengez Z, Basta-Pljakic J, Kennedy Oran D, Philemon Claudy J, Schaffler Mitchell B. Structural and mechanical repair of diffuse damage in cortical bone in vivo. J Bone Miner Res 2014;29:2537–44
  • Frost HM, Villanueva AR, Roth H, Stanisavljevic S. Tetracycline bone labeling. J New Drugs 1961;1:206–16
  • Frost HM. Tetracycline-based analysis of bone remodelling. Calcif Tissue Res 1969;3:211–37
  • Lee TC, Arthur TL, Gibson LJ, Hayes WC. Sequential labelling of microdamage in bone using chelating agents. J Orthop Res 2000;18:322–5
  • O'Brien FJ, Taylor D, Lee TC. An improved labelling technique for monitoring microcrack growth in compact bone. J Biomech 2002;35:523–6
  • Parkesh R, Mohsin S, Lee TC, Gunnlaugsson T. Histological, spectroscopic, and surface analysis of microdamage in bone: toward real-time analysis using fluorescent sensors. Chem Mater 2007;19:1656–63
  • Parkesh R, Lee TC, Gunnlaugsson T. Fluorescence imaging of bone cracks (microdamage) using visibly emitting 1,8-naphthalimide-based PET sensors. Tetrahedron Lett 2009;50:4114–16
  • Stover SM, Marti RB, Pool RR, Taylor KT, Harrington TM. In vivo labeling of microdamage in cortical bone tissue. Proc Orthop Res Soc 1993;18:541
  • O’Brien FJ, Taylor D, Lee TC. The effect of bone microstructure on the initiation and growth of microcracks. J Orthop Res 2005;23:475–80
  • Kazakia GJ, Lee JJ, Singh M, Bigley RF, Martin RB, Keaveny TM. Automated high-resolution three-dimensional fluorescence imaging of large biological specimens. J Microsc 2007;225:109–17
  • Slyfield Jr CR, Niemeyer KE, Tkachenko EV, Tomlinson RE, Steyer GG, Patthanacharoenphon CG, Kazakia GJ, Wilson DL, Hernandez CJ. Three-dimensional surface texture visualization of bone tissue through epifluorescence-based serial block face imaging. J Microsc 2009;236:52–9
  • Boyde A, Vesely P, Gray C, Jones SJ. High temporal and spatial resolution studies of bone cells sing real-time confocal reflection microscopy. Scanning 1994;16:285–94
  • Zarrinkalam KH, Kuliwaba JS, Martin RB, Wallwork MA, Fazzalari NL. New insights into the propagation of fatigue damage in cortical bone using confocal microscopy and chelating fluorochromes. Eur J Morphol 2005;42:81–90
  • Rahn BA. Polychrome fluorescence labelling of bone formation, instrumental aspects and experimental use. Zeiss Information 1977;22:36–9
  • Zioupos P. Accumulation of in-vivo fatigue microdamage and its relation to biomechanical properties in ageing human cortical bone. J Microsc 2001;201:270–8
  • Reilly GC, Currey JD. The effects of damage and microcracking on the impact strength of bone. J Biomech 2000;33:337–43
  • Boyce TM, Fyhrie DP, Glotkowski MC, Radin EL, Schaffler MB. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res 1998;16:322–9
  • O'Brien FJ, Taylor D, Dickson GR, Lee TC. Visualisation of three dimensional microcracks in compact bone. J Anat 2000;197:413–20
  • Taylor D, Lee TC. Measuring the shape and size of microcracks in bone. J Biomech 1998;31:1177–80
  • Wang L, Ye T, Deng L, Shao J, Qi J, Zhou Q, Wei L, Qiu S. Repair of microdamage in osteonal cortical bone adjacent to bone screw. PLoS ONE 2014;9:e89343
  • Kerschnitzki M, Wagermaier W, Roschger P, Seto J, Shahar R, Duda GN, Mundlos S, Fratzl P. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J Struct Biol 2011;173:303–11
  • Leng H, VanDersarl JJ, Niebur GL, Roeder RK. Microdamage in bovine cortical bone measured using micro-computed tomography. Trans Orthop Res Soc 2005;30:665
  • Tang SY, Vashishth D. A non-invasive in vitro technique for the three-dimensional quantification of microdamage in trabecular bone. Bone 2007;40:1259–64
  • Leng H, Wang X, Ross RD, Niebur GL, Roeder RK. Micro-computed tomography of fatigue microdamage in cortical bone using a barium sulfate contrast agent. J Mech Behav Biomed Mater 2008;1:68–75
  • Wang X, Masse DB, Leng H, Hess KP, Ross RD, Roeder RK, Niebur GL. Detection of trabecular bone microdamage by micro-computed tomography. J Biomech 2007;40:3397–403
  • Turnbull TL, Gargac JA, Niebur GL, Roeder RK. Detection of fatigue microdamage in whole rat femora using contrast-enhanced micro-computed tomography. J Biomech 2011;44:2395–400
  • Parkesh R, Lee TC, Gunnlaugsson T, Gowin W. Microdamage in bone: surface analysis and radiological detection. J Biomech 2006;39:1552–6
  • Silva MJ, Uthgenannt BA, Rutlin JR, Wohl GR, Lewis JS, Welch MJ. In vivo skeletal imaging of 18F-fluoride with positron emission tomography reveals damage- and time-dependent responses to fatigue loading in the rat ulna. Bone 2006;39:229–36
  • Li J, Miller MA, Hutchins GD, Burr DB. Imaging bone microdamage in vivo with positron emission tomography. Bone 2005;37:819–24
  • Goldstein JI, Newbury DE, Echlin P, Joy DC, Fiori C, Lifshin E. Scanning electron microscopy and X-ray microanalysis. New York: Plenum Press; 1981
  • Tang SY, Vashishth D. Non-enzymatic glycation alters microdamage formation in human cancellous bone. Bone 2010;46:148–54
  • Karim L, Vashishth D. Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS ONE 2012;7:e35047
  • Brock GR, Kim G, Ingraffea AR, Andrews JC, Pianetta P, van der Meulen MCH. Nanoscale examination of microdamage in sheep cortical bone using synchrotron radiation transmission X-ray microscopy. PLoS One 2013;8:e57942
  • Schaffler MB, Pitchford W, Choi K, Riddle JM. Examination of compact bone microdamage using back-scattered electron microscopy. Bone 1994;15:483–8
  • Wise LM, Wang Z, Grynpas MD. The use of fractography to supplement analysis of bone mechanical properties in different strains of mice. Bone 2007;41:620–30
  • George WT, Vashishth D. Damage mechanisms and failure modes of cortical bone under components of physiological loading. J Orthop Res 2005;23:1047–53
  • Braidotti P, Branca SP, Stagni L. Scanning electron microscopy of human cortical bone failure surfaces. J Biomech 1997;30:155–62
  • Braidotti P, Bemporad E, D’Alessio T, Sciuto SA, Stagni L. Tensile experiments and SEM fractography on bovine subchondral bone. J Biomech 2000;33:1153–7
  • Yeni YN, Norman TL. Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. J Biomed Mater Res 2000;51:504–9
  • Thurner PJ, Oroudjev E, Jungmann R, Kreutz C, Kindt JH, Schitter G, Okouneva TO, Lauer ME, Fantner GE, Hansma H, Hansma PK. Imaging of bone ultrastructure using atomic force microscopy. In: Méndez-Vilas A, Díaz J, editors. Modern research and educational topics in microscopy (Microscopy Book Series 3). Spain: Formatex; 2007:37–48
  • Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 2004;35:4–10
  • Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK. Bone indentation recovery time correlates with bond reforming time. Nature 2001;414:773–6
  • Nicolella DP, Moravits DE, Siller-Jackson AJ, Railsback RJ, Timmons SF, Jepsen KJ, Davy DT, Lankford J. Ultrastructural characterization of damaged cortical bone using atomic force microscopy. ASME-BED 1999;42:319–20
  • Diab T, Sit S, Kim D, Rho J, Vashishth D. Age-dependent fatigue behaviour of human cortical bone. Eur J Morphol 2005;42:53–9

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.