{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,13]],"date-time":"2026-05-13T14:39:50Z","timestamp":1778683190450,"version":"3.51.4"},"reference-count":38,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2018,12,13]],"date-time":"2018-12-13T00:00:00Z","timestamp":1544659200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/F007906\/1"],"award-info":[{"award-number":["EP\/F007906\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/F001452\/1"],"award-info":[{"award-number":["EP\/F001452\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/M010619\/1"],"award-info":[{"award-number":["EP\/M010619\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"name":"UK Research Partnership Investment Fund (UKRPIF)","award":["-"],"award-info":[{"award-number":["-"]}]},{"name":"Higher education Funding Council for England UK (HEFCE)","award":["-"],"award-info":[{"award-number":["-"]}]},{"name":"European Research Council (ERC)","award":["695638 CORREL-CT"],"award-info":[{"award-number":["695638 CORREL-CT"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Materials"],"abstract":"<jats:p>Bone is a complex material comprising high stiffness, but brittle, crystalline bio-apatite combined with compliant, but tough, collagen fibres. It can accommodate significant deformation, and the bone microstructure inhibits crack propagation such that micro-cracks can be quickly repaired. Catastrophic failure (bone fracture) is a major cause of morbidity, particularly in aging populations, either through a succession of small fractures or because a traumatic event is sufficiently large to overcome the individual crack blunting\/shielding mechanisms. Indentation methods provide a convenient way of characterising the mechanical properties of bone. It is important to be able to visualise the interactions between the bone microstructure and the damage events in three dimensions (3D) to better understand the nature of the damage processes that occur in bone and the relevance of indentation tests in evaluating bone resilience and strength. For the first time, time-lapse laboratory X-ray computed tomography (CT) has been used to establish a time-evolving picture of bone deformation\/plasticity and cracking. The sites of both crack initiation and termination as well as the interconnectivity of cracks and pores have been visualised and identified in 2D and 3D.<\/jats:p>","DOI":"10.3390\/ma11122533","type":"journal-article","created":{"date-parts":[[2018,12,14]],"date-time":"2018-12-14T03:58:17Z","timestamp":1544759897000},"page":"2533","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["3D Imaging of Indentation Damage in Bone"],"prefix":"10.3390","volume":"11","author":[{"given":"Tristan","family":"Lowe","sequence":"first","affiliation":[{"name":"Henry Moseley X-ray Imaging Facility, Henry Royce Institute, School of Materials, The University of Manchester, Manchester M13 9PL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3244-1316","authenticated-orcid":false,"given":"Egemen","family":"Avcu","sequence":"additional","affiliation":[{"name":"Henry Moseley X-ray Imaging Facility, Henry Royce Institute, School of Materials, The University of Manchester, Manchester M13 9PL, UK"},{"name":"Ford Otosan Ihsaniye Automotive Vocational School, Machine and Metal Technologies, Kocaeli University, 41680 Kocaeli, Turkey"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8062-8911","authenticated-orcid":false,"given":"Etienne","family":"Bousser","sequence":"additional","affiliation":[{"name":"Henry Moseley X-ray Imaging Facility, Henry Royce Institute, School of Materials, The University of Manchester, Manchester M13 9PL, UK"},{"name":"Engineering Physics Department, Polytechnique Montr\u00e9al, Montreal H3T1J4, QC, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2913-5406","authenticated-orcid":false,"given":"William","family":"Sellers","sequence":"additional","affiliation":[{"name":"School of Earth and Environmental Sciences, The University of Manchester, Manchester M13 9PL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1946-5647","authenticated-orcid":false,"given":"Philip J.","family":"Withers","sequence":"additional","affiliation":[{"name":"Henry Moseley X-ray Imaging Facility, Henry Royce Institute, School of Materials, The University of Manchester, Manchester M13 9PL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2018,12,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Currey, J.D. (2002). Bones: Structure and Mechanics, Princeton University Press.","DOI":"10.1515\/9781400849505"},{"key":"ref_2","unstructured":"Alexander, R.M. (2006). Principles of Animal Locomotion, Princetown University Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1111\/bij.12066","article-title":"Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates","volume":"109","author":"Quemeneur","year":"2013","journal-title":"Biol. J. Linn. Soc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1126\/science.2251499","article-title":"Biomechanics of Mammalian Terrestrial Locomotion","volume":"250","author":"Biewener","year":"1990","journal-title":"Science"},{"key":"ref_5","first-page":"33","article-title":"Skeletal responses to space flight and the bed rest analog: A review","volume":"7","author":"LeBlanc","year":"2007","journal-title":"J. Musculoskelet. Neuronal Interact."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/j.bone.2012.01.002","article-title":"Microindentation can discriminate between damaged and intact human bone tissue","volume":"50","author":"Schmidt","year":"2012","journal-title":"Bone"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.jmbbm.2014.06.017","article-title":"A methodology for the investigation of toughness and crack propagation in mouse bone","volume":"39","author":"Carriero","year":"2014","journal-title":"J. Mech. Behav. Biomed. Mats"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/s12018-016-9222-4","article-title":"Bone quality assessment techniques: Geometric, compositional, and mechanical characterization from macroscale to nanoscale","volume":"14","author":"Hunt","year":"2016","journal-title":"Clin. Rev. Bone Miner. Metab."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1557\/jmr.2004.19.1.3","article-title":"Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology","volume":"19","author":"Oliver","year":"2011","journal-title":"J. Mater. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1007\/s11914-016-0314-3","article-title":"Tissue-Level Mechanical Properties of Bone Contributing to Fracture Risk","volume":"14","author":"Nyman","year":"2016","journal-title":"Curr. Osteoporos. Rep."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s12018-018-9249-9","article-title":"Clinical Measurements of Bone Tissue Mechanical Behavior Using Reference Point Indentation","volume":"16","author":"Chang","year":"2018","journal-title":"Clin. Revn Bone Miner. Metab."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1006\/jtbi.2003.3148","article-title":"Fatigue Damage, Remodeling, and the Minimization of Skeletal Weight","volume":"220","year":"2003","journal-title":"J. Theor. Biol."},{"key":"ref_13","unstructured":"Lee, T.C., O\u2019Brien, F.L., Parkesh, R., and Gunnlaugsson, T. (2005, January 20\u201325). Visualisation and Quantification of Fatigue Induced Microdamage in Bone: Histology and Radiology. Proceedings of the 11th International Conference on Fracture 2005 (ICF 11), Turin, Italy."},{"key":"ref_14","unstructured":"Alexander, R.M. (1968). Animal Mechanics, Sidgwick & Jackson."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1111\/j.1469-7580.2006.00509.x","article-title":"Osteonal crack barriers in ovine compact bone","volume":"208","author":"Mohsin","year":"2006","journal-title":"J. Anat."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Larrue, A., Rattner, A., Peter, Z.A., Olivier, C., Laroche, N., Vico, L., and Peyrin, F. (2011). Synchrotron radiation micro-CT at the micrometer scale for the analysis of the three-dimensional morphology of microcracks in human trabecular bone. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0021297"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1046\/j.1469-7580.2000.19730413.x","article-title":"Visualisation of three-dimensional microcracks in compact bone","volume":"197","author":"Taylor","year":"2000","journal-title":"J. Anat."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.bone.2006.01.147","article-title":"Time-lapsed investigation of three-dimensional failure and damage accumulation in trabecular bone using synchrotron light","volume":"39","author":"Thurner","year":"2006","journal-title":"Bone"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1046\/j.1469-7580.2003.00211.x","article-title":"Detecting microdamage in bone","volume":"203","author":"Lee","year":"2003","journal-title":"J. Anat."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Metscher, B.D. (2009). MicroCT for comparative morphology: Simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol., 9.","DOI":"10.1186\/1472-6793-9-11"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1179\/1743280413Y.0000000023","article-title":"Quantitative X-ray tomography","volume":"59","author":"Maire","year":"2013","journal-title":"Int. Mater. Rev."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/BF03026332","article-title":"Mouse models in skeletal physiology and osteoporosis: Experiences and data on 14,839 cases from the Hamburg Mouse Archives","volume":"23","author":"Pogoda","year":"2005","journal-title":"J. Bone Miner. Metab."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"094001","DOI":"10.1088\/0957-0233\/19\/9\/094001","article-title":"Sub-micron resolution CT for failure analysis and process development","volume":"19","author":"Feser","year":"2008","journal-title":"Meas. Sci. Technol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.bone.2014.09.020","article-title":"Reference point indentation is not indicative of whole mouse bone measures of stress intensity fracture toughness","volume":"69","author":"Carriero","year":"2014","journal-title":"Bone"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1243\/09544119JEIM634","article-title":"Microindentation on cortical human bone: Effects of tissue condition and indentation location on hardness values","volume":"223","author":"Zwierzak","year":"2009","journal-title":"Proc. Inst. Mech. Eng. Part H J. Eng. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1007\/s10856-007-2306-4","article-title":"Microindentation in bone: Hardness variation with five independent variables","volume":"18","author":"Johnson","year":"2007","journal-title":"J. Mater. Sci. Mater. Med"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/j.jmbbm.2008.10.008","article-title":"Indentation techniques for evaluating the fracture toughness of biomaterials and hard tissues","volume":"2","author":"Kruzic","year":"2009","journal-title":"J. Mech. Behav. Biomed. Mater."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1557\/jmr.2011.322","article-title":"Size effects in indentation of hydrated biological tissues","volume":"27","author":"Oyen","year":"2011","journal-title":"J. Mater. Res."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Boughton, O.R., Ma, S., Zhao, S., Arnold, M., Lewis, A., Hansen, U., Cobb, J.P., Giuliani, F., and Abel, R.L. (2018). Measuring bone stiffness using spherical indentation. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0200475"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.polymertesting.2016.04.003","article-title":"The effects of pile-up, viscoelasticity and hydrostatic stress on polymer matrix nanoindentation","volume":"52","author":"Hardiman","year":"2016","journal-title":"Polym. Test."},{"key":"ref_31","first-page":"1","article-title":"Examining the Effect of Pileup on the Accuracy of Sharp Indentation Testing","volume":"2015","author":"Tang","year":"2015","journal-title":"Adv. Mater. Sci. Eng."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1007\/s00198-009-0854-9","article-title":"Indentation of bone tissue: A short review","volume":"20","author":"Zysset","year":"2009","journal-title":"Osteoporosis"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1111\/j.1475-1305.2006.00282.x","article-title":"Fracture and Ageing in Bone: Toughness and Structural Characterization","volume":"42","author":"Ritchie","year":"2006","journal-title":"Strain"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1877","DOI":"10.1002\/jbmr.73","article-title":"Microindentation for in vivo measurement of bone tissue mechanical properties in humans","volume":"25","author":"Guerri","year":"2010","journal-title":"J. Bone Miner. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.1557\/jmr.2006.0242","article-title":"Fracture, aging, and disease in bone","volume":"21","author":"Ager","year":"2011","journal-title":"J. Mater. Res."},{"key":"ref_36","unstructured":"Hauthier, R. (2017). Crack Propagation Mechanisms in Human Cortical Bone on Different Paired Anatomical locations: Biomechanical, Tomographic and Biochemical Approaches. [Ph.D. Thesis, Universit\u00e9 de Lyon]."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1038\/bonekey.2015.112","article-title":"The fracture mechanics of human bone: Influence of disease and treatment","volume":"4","author":"Zimmermann","year":"2015","journal-title":"BoneKEy Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1948","DOI":"10.1007\/s11999-009-0784-z","article-title":"Measurement of the mechanical properties of bone: A recent history","volume":"467","author":"Currey","year":"2009","journal-title":"Clin. Orthop. Relat. Res."}],"container-title":["Materials"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1996-1944\/11\/12\/2533\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:33:41Z","timestamp":1760196821000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1996-1944\/11\/12\/2533"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,12,13]]},"references-count":38,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["ma11122533"],"URL":"https:\/\/doi.org\/10.3390\/ma11122533","relation":{},"ISSN":["1996-1944"],"issn-type":[{"value":"1996-1944","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,12,13]]}}}