Microindentation for in vivo measurement of bone tissue mechanical properties in humans

Diez‐Perez, Adolfo; Güerri, Roberto; Nogues, Xavier; Cáceres, Enric; Peña, Maria Jesus; Mellibovsky, Leonardo; Randall, Connor; Bridges, Daniel; Weaver, James C.; Proctor, Alexander; Brimer, Davis; Koester, Kurt J.; Ritchie, Robert O.; Hansma, Paul K.

Keywords

Keywords: bone; fracture; bone quality; instrument; clinical trials

Links

DOI: 10.1002/jbmr.73

PubMed: 20200991

WoS: 000281325000019

Cited Works (26)

Year	Entry
2009	Ritchie R, Buehler M, Hansma P. Plasticity and toughness in bone. Phys Today. June 2009;62(6):41-47.
2008	Boutroy S, Van Rietbergen B, Sornay-Rendu E, Munoz F, Bouxsein ML, Delmas PD. Finite element analysis based on in vivo HR-pQCT images of the distal radius is associated with wrist fracture in postmenopausal women. J Bone Miner Res. March 2008;23(3):392-399.
2005	Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials. January 2005;26(2):217-231.
2001	NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. February 14, 2001;285(6):785-795.
1989	Carando S, Portigliatti Barbos M, Ascenzi A, Boyde A. Orientation of collagen in human tibial and fibular shaft and possible correlation with mechanical properties. Bone. 1989;10(2):139-142.
2002	Turner CH. Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int. February 2002;13(2):97-104.
2002	Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, LaCroix AZ, Black DM. Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am J Med. March 2002;112(4):281-289.
2004	Fratzl P, Gupta HS, Paschalis EP, Roschger P. Structure and mechanical quality of the collagen–mineral nano-composite in bone. J Mater Chem. 2004;14(14):2115-2123.
2000	Garner P, Sornay-Rendu E, Claustrat B, Delmas PD. Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. J Bone Miner Res. August 2000;15(8):1526-1536.
1997	Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech. August 1997;30(8):763-769.
2003	Boskey A. Bone mineral crystal size. Osteoporos Int. September 2003;14(suppl 5):S16-S20.
2002	Habelitz S, Marshall GW Jr, Balooch M, Marshall SJ. Nanoindentation and storage of teeth. J Biomech. July 2002;35(7):995-998.
2005	Gupta HS, Wagermaier W, Zickler GA, Aroush DR-B, Funari SS, Roschger P, Wagner HD, Fratzl P. Nanoscale deformation mechanisms in bone. Nano Lett. October 2005;5(10):2108-2111.
2006	Peterlik H, Roschger P, Klaushofer K, Fratzl P. From brittle to ductile fracture of bone. Nat Mater. January 2006;5(1):52-55.
2007	Thurner PJ, Erickson B, Jungmann R, Schriock Z, Weaver JC, Fantner GE, Schitter G, Morse DE, Hansma PK. High-speed photography of compressed human trabecular bone correlates whitening to microscopic damage. Eng Fract Mech. 2007;74(12):1928-1941.
2007	Taylor D, Hazenberg JG, Lee TC. Living with cracks: damage and repair in human bone. Nat Mater. April 2007;6(4):263-268.
2004	Currey J. Incompatible mechanical properties in compact bone. J Theo Biol. December 21, 2004;231(4):569-580.
2008	Koester KJ, Ager JW III, Ritchie RO. The true toughness of human cortical bone measured with realistically short cracks. Nat Mater. August 2008;7(8):672-677.
2006	Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, Christiansen C, Delmas PD. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone. March 2006;38(3):300-309.
2006	Seeman E, Delmas PD. Bone quality: the material and structural basis of bone strength and fragility. NEJM. May 25, 2006;354(21):2250-2261.
2003	Burr D. Microdamage and bone strength. Osteoporos Int. September 2003;14(suppl 5):S67-S72.
2002	Burr DB. The contribution of the organic matrix to bone's material properties. Bone. July 2002;31(1):8-11.
2005	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. Nat Mater. August 2005;4(8):612-616.
1979	Currey JD. Changes in the impact energy absorption of bone with age. J Biomech. 1979;12(6):459-469.
2007	Gupta HS, Fratzl P, Kerschnitzki M, Benecke G, Wagermaier W, Kirchner HOK. Evidence for an elementary process in bone plasticity with an activation enthalpy of 1 eV. J R Soc Interface. April 22, 2007;4(3):277-282.
2003	Bouxsein ML. Bone quality: where do we go from here? Osteoporos Int. September 2003;14(suppl 5):S118-S127.

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Year	Entry
2015	Milovanovic P, Zimmermann EA, Riedel C, vom Scheidt A, Herzog L, Krause M, Djonic D, Djuric M, Püschel K, Amling M, Ritchie RO, Busse B. Multi-level characterization of human femoral cortices and their underlying osteocyte network reveal trends in quality of young, aged, osteoporotic and antiresorptive-treated bone. Biomaterials. March 2015;45:46-55.
2013	Gallant MA, Brown DM, Organ JM, Allen MR, Burr DB. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone. March 2013;53(1):301-305.
2015	Katsamenis OL, Jenkins T, Thurner PJ. Toughness and damage susceptibility in human cortical bone is proportional to mechanical inhomogeneity at the osteonal-level. Bone. July 2015;76:158-168.
2016	Farr JN, Khosla S. Determinants of bone strength and quality in diabetes mellitus in humans. Bone. January 2016;82:28-34.
2016	Mirzaali MJ, Schwiedrzik JJ, Thaiwichai S, Best JP, Michler J, Zysset PK, Wolfram U. Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone. December 2016;93:196-211.
2020	Rezaee T, Bouxsein ML, Karim L. Increasing fluoride content deteriorates rat bone mechanical properties. Bone. July 2020;136:115369.
2020	Taylor EA, Donnelly E. Raman and Fourier transform infrared imaging for characterization of bone material properties. Bone. October 2020;139:115490.
2016	Diez-Perez A, Bouxsein M, Eriksen E, Khosla S, Nyman J, Papapoulos S, Tang S. Technical note: recommendations for a standard procedure to assess cortical bone at the tissue-level in vivo using impact microindentation. Bone Rep. December 2016;5:181-185.
2021	Rajput S, Mehta P, Mittal M, Rajender S, Chattopadhyay N. Human relevance of preclinical studies on the skeletal impact of inflammatory bowel disease: a systematic review and meta-analysis. Calcif Tiss Int. June 2021;108(6):708-724.
2020	Mirzaali MJ, Libonati F, Böhm C, Rinaudo L, Cesana BM, Ulivieri FM, Vergani L. Fatigue-caused damage in trabecular bone from clinical, morphological and mechanical perspectives. Int J Fatigue. April 2020;133:105451.
2014	Farr JN, Drake MT, Amin S, Melton LJ III, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. April 2014;29(4):787-795.
2015	Granke M, Makowski AJ, Uppuganti S, Does MD, Nyman JS. Identifying novel clinical surrogates to assess human bone fracture toughness. J Bone Miner Res. July 2015;30(7):1290-1300.
2017	Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellström D, Rudäng R, Zoulakis M, Wallander M, Darelid A, Lorentzon M. Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population‐based study. J Bone Miner Res. May 2017;32(5):1062-1071.
2021	Diniz‐Sousa F, Veras L, Boppre G, Sa‐Couto P, Devezas V, Santos‐Sousa H, Preto J, Vilas‐Boas JP, Machado L, Oliveira J, Fonseca H. The effect of an exercise intervention program on bone health after bariatric surgery: a randomized controlled trial. J Bone Miner Res. March 2021;36(3):489-499.
2022	Ahmed R, Uppuganti S, Derasari S, Meyer J, Pennings JS, Elefteriou F, Nyman JS. Identifying bone matrix impairments in a mouse model of neurofibromatosis type 1 (NF1) by clinically translatable techniques. J Bone Miner Res. August 2022;37(8):1603-1621.
2023	Hariri H, Kose O, Bezdjian A, Daniel SJ, St-Arnaud R. USP53 regulates bone homeostasis by controlling rankl expression in osteoblasts and bone marrow adipocytes. J Bone Miner Res. April 2023;38(4):578-596.
2016	Furst JR, Bandeira LC, Fan W-W, Agarwal S, Nishiyama KK, McMahon DJ, Dworakowski E, Jiang H, Silverberg SJ, Rubin MR. Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab. June 2016;101(6):2502-2510.
2011	Jungmann R, Szabo ME, Schitter G, Tang RY-S, Vashishth D, Hansma PK, Thurner PJ. Local strain and damage mapping in single trabeculae during three-point bending tests. J Mech Behav Biomed Mater. May 2011;4(4):523-534.
2015	Poundarik AA, Wu P-C, Evis Z, Sroga GE, Ural A, Rubin M, Vashishth D. A direct role of collagen glycation in bone fracture. J Mech Behav Biomed Mater. December 2015;52:120-130.
2017	Sandino C, McErlain DD, Schipilow J, Boyd SK. Mechanical stimuli of trabecular bone in osteoporosis: a numerical simulation by finite element analysis of microarchitecture. J Mech Behav Biomed Mater. February 2017;66:19-27.
2023	Visser N, Rezaie E, Ducharme A, Shin AY, Bishop AT. The effect of surgical revascularization on the mechanical properties of cryopreserved bone allograft in a porcine tibia model. J Orthop Res. April 2023;41(4):815-822.
2020	Ballesta S, Güerri-Fernández RC, Chillarón JJ, Güell A, Herrera S, Torres E, Ascoeta NG, Le-Roux JAF, Díez A. The use of microindentation for the study of bone properties in type 1 diabetes mellitus patients. Osteoporos Int. January 2020;31(1):175-180.
2020	Starr JR, Tabacco G, Majeed R, Omeragic B, Bandeira L, Rubin MR. PTH and bone material strength in hypoparathyroidism as measured by impact microindentation. Osteoporos Int. February 2020;31(2):327-333.
2013	Kim G. The Effects of Mineralization and Crystallinity on the Mechanical Behavior of Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2013.
2020	Taylor EA. Validation and Implementation of Vibrational Spectroscopic Measures of Bone Composition [PhD thesis]. Ithaca, NY: Cornell University; December 2020.
2016	Oei L. Epidemiological, Radiological and Genetic Aspects of Endocrine Bone Diseases [PhD thesis]. Erasmus University Rotterdam; December 14, 2016.
2013	Bart ZR. Multi-Scale Analysis of Morphology, Mechanics, and Composition of Collagen in Murine Osteogenesis Imperfecta [Master's thesis]. Indianapolis, IN: Purdue University; August 2013.
2015	Clauser CA. In Vivo Tibial Loading of Healthy and Osteolathrytic Mice [Master's thesis]. Indianapolis, IN: Purdue University; May 2015.
2016	Hammond MA. The Influence of Collagen Crosslinking and Treadmill Exercise on the Mechanics, Composition, and Morphology of Bone At Multiple Length Scales [PhD thesis]. Purdue University; May 2016.
2011	Karim L. The Biomolecular Basis of Bone Fracture [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; November 2011.
2013	Poundarik A. The Role of Non-Collagenous Proteins, in Particular, Osteocalcin and Osteopontin, in the Determination of Bone Matrix Quality [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; May 2013.
2015	Grover K. Osteopenia Uncovered by Remodeling in Spatial Distribution of Elastic Moduli in Orthogonal Orientations: A Nanoindentation Study [Master's thesis]. Stony Brook, NY: Stony Brook University; May 2015.
2012	Tjhia CKH. Bone Quality of Patients With Atypical Fractures and Severely Suppressed Bone Turnover [PhD thesis]. Davis, University of California; 2012.
2016	Jones DA. Reference Point Indentation of Human Trabecular Bone Treated With Bisphosphonates for Varying Durations [Master's thesis]. University of Kentucky; 2016.
2022	Rezaee T. Effect of Clinically Relevant Alterations of Mineral and Protein on Bone Biomechanics [PhD thesis]. University of Massachusetts at Dartmouth; May 2022.
2014	Makowski AJ. Evaluation of Raman Spectroscopy for Fracture Resistance Assessment [PhD thesis]. Nashville, TN: Vanderbilt University; December 2014.
2013	Tomlinson RE. The Role of Angiogenesis in Osteogenic Mechanical Loading [PhD thesis]. St. Louis, MO: Washington University in St. Louis; May 2013.