Methods for assessing bone quality: a review

wbldb

Donnelly, Eve¹

Methods for assessing bone quality: a review

Clin Orthop Relat Res. August 2011;469:2128-2138

©2010 The Association of Bone and Joint Surgeons

Affiliations

¹Mineralized Tissues Laboratory, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021, USA
Abstract

Background: Bone mass, geometry, and tissue material properties contribute to bone structural integrity. Thus, bone strength arises from both bone quantity and quality. Bone quality encompasses the geometric and material factors that contribute to fracture resistance.

Questions/purposes: This review presents an overview of the methods for assessing bone quality across multiple length scales, their outcomes, and their relative advantages and disadvantages.

Methods: A PubMed search was conducted to identify methods related to bone mechanical testing, imaging, and compositional analysis. Using various exclusion criteria, articles were selected for inclusion.

Results: Methods for assessing mechanical properties include whole-bone, bulk tissue, microbeam, and micro- and nanoindentation testing techniques. Outcomes include structural strength and material modulus. Advantages include direct assessment of bone strength; disadvantages include specimen destruction during testing. Methods for characterizing bone geometry and microarchitecture include quantitative CT, high-resolution peripheral quantitative CT, high-resolution MRI, and micro-CT. Outcomes include three-dimensional whole-bone geometry, trabecular morphology, and tissue mineral density. The primary advantage is the ability to image noninvasively; disadvantages include the lack of a direct measure of bone strength. Methods for measuring tissue composition include scanning electron microscopy, vibrational spectroscopy, nuclear magnetic resonance imaging, and chemical and physical analytical techniques. Outcomes include mineral density and crystallinity, elemental composition, and collagen crosslink composition. Advantages include the detailed material characterization; disadvantages include the need for a biopsy.

Conclusions: Although no single method can completely characterize bone quality, current noninvasive imaging techniques can be combined with ex vivo mechanical and compositional techniques to provide a comprehensive understanding of bone quality.
Links

DOI: 10.1007/s11999-010-1702-0

PubMed: 21116752

WoS: 000292271700005
History

Online: 2010-11-30

Cited Works (59)

Year	Entry
1975	Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech. 1975;8(6):393-405.
2007	Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. April 2007;40(4):1144-1151.
2007	MacNeil JA, Boyd SK. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. December 2007;29(10):1096-1105.
2010	Burghardt AJ, Kazakia GJ, Sode M, de Papp AE, Link TM, Majumdar S. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res. December 2010;25(12):2558-2571.
2001	Morgan EF, Keaveny TM. Dependence of yield strain of human trabecular bone on anatomic site. J Biomech. 2001;34(5):569-577.
1999	Brodt MD, Ellis CB, Silva MJ. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res. December 1999;14(12):2159-2166.
2006	Donnelly E, Williams RM, Downs SA, Dickinson ME, Baker SP, van der Meulen MCH. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res. August 2006;21(8):2106-2117.
1996	Rüegsegger P, Koller B, Müller R. A microtomographic system for the nondestructive evaluation of bone architecture. Calcif Tiss Int. 1996;58(1):24-29.
2010	Keaveny TM. Biomechanical computed tomography: noninvasive bone strength analysis using clinical computed tomography scans. Annals NY Acad Sci. 2010;1192(1):57-65.
2008	Nyman JS, Ni Q, Nicolella DP, Wang X. Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone. January 2008;42(1):193-199.
2006	Lang TF, Leblanc AD, Evans HJ, Lu Y. Adaptation of the proximal femur to skeletal reloading after long-duration spaceflight. J Bone Miner Res. August 2006;21(8):1224-1230.
1969	Currey JD. The relationship between the stiffness and the mineral content of bone. J Biomech. October 1969;2(4):477-480.
2007	Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA. Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of qct scans in women with osteoporosis. J Bone Miner Res. January 2007;22(1):149-157.
2005	Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. December 2005;90(12):6508-6515.
2008	Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. March 2008;42(3):456-466.
1997	Bloebaum RD, Skedros JG, Vajda EG, Bachus KN, Constantz BR. Determining mineral content variations in bone using backscattered electron imaging. Bone. May 1997;20(5):485-490.
2009	Zysset PK. Indentation of bone tissue: a short review. Osteoporos Int. June 2009;20(6):1049-1055.
2008	Kazakia GJ, Burghardt AJ, Cheung S, Majumdar S. Assessment of bone tissue mineralization by conventional x-ray microcomputed tomography: comparison with synchrotron radiation microcomputed tomography and ash measurements. Med Phys. 2008;35(7):3170-3179.
1993	Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14(4):595-608.
1977	Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg. 1977;59A(7):954-962.
1998	Gordon CL, Lang TF, Augat P, Genant HK. Image-based assessment of spinal trabecular bone structure from high-resolution CT images. Osteoporos Int. August 1998;8(4):317-325.
2005	Boskey AL, Mendelsohn R. Infrared analysis of bone in health and disease. J Biomed Opt. May–June 2005;10(3):031102.
2004	Waarsing JH, Day JS, van der Linden JC, Ederveen AG, Spanjers C, De Clerck N, Sasov A, Verhaar JAN, Weinans H. Detecting and tracking local changes in the tibiae of individual rats: a novel method to analyse longitudinal in vivo micro-ct data. Bone. January 2004;34(1):163-169.
2002	Cummings SR, Bates D, Black DM. Clinical use of bone densitometry: scientific review. JAMA. October 16, 2002;288(15):1889-1897.
1998	Peyrin F, Salome M, Cloetens P, Laval-Jeantet AM, Ritman E, Rüegsegger P. Micro-ct examinations of trabecular bone samples at different resolutions: 14, 7 and 2 micron level. Technol Health Care. 1998;6(5-6):391-401.
2001	Pistoia W, van Rietbergen B, Laib A, Rüegsegger P. High-resolution three-dimensional-pqct images can be an adequate basis for in-vivo μfe analysis of bone. J Biomech Eng. October 2001;123(2):176-183.
1988	Currey JD. The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. J Biomech. 1988;21(2):131-139.
1994	Keaveny TM, Wachtel EF, Ford CM, Hayes WC. Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. J Biomech. 1994;27(9):1137-1146.
2000	Carden A, Morris MD. Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt. July 2000;5(3):259-268.
1990	Choi K, Kuhn JL, Ciarelli MJ, Goldstein SA. The elastic moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus. J Biomech. 1990;23(11):1103-1113.
1983	Goldstein SA, Wilson DL, Sonstegard DA, Matthews LS. The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J Biomech. 1983;16(12):965-969.
2009	Gourion‐Arsiquaud S, Faibish D, Myers E, Spevak L, Compston J, Hodsman A, Shane E, Recker RR, Boskey ER, Boskey AL. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res. September 2009;24(9):1565-1571.
1987	Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. December 1987;2(6):595-610.
1992	Oliver WC, Pharr GM. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res. 1992;7(6):1564-1583.
2007	Boskey A, Camacho NP. FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials. May 2007;28(15):2465-2478.
1999	Camacho NP, Hou L, Toledano TR, Ilg WA, Brayton CF, Raggio CL, Root L, Boskey AL. The material basis for reduced mechanical properties in oim mice bones. J Bone Miner Res. February 1999;14(2):264-272.
2001	Boskey AL. Bone mineralization. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:5-1–5-33.
1996	Ziv V, Wagner HD, Weiner S. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. May 1996;18(5):417-428.
2009	Voide R, Schneider P, Stauber M, Wyss P, Stampanoni M, Sennhauser U, van Lenthe GH, Müller R. Time-lapsed assessment of microcrack initiation and propagation in murine cortical bone at submicrometer resolution. Bone. August 2009;45(2):164-173.
2003	Hengsberger S, Enstroem J, Peyrin F, Zysset P. How is the indentation modulus of bone tissue related to its macroscopic elastic response? a validation study. J Biomech. October 2003;36(10):1503-1509.
2002	Hengsberger S, Kulik A, Zysset P. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone. 2002;30(1):178-184.
2003	Judex S, Boyd S, Qin Y-X, Miller L, Müller R, Rubin C. Combining high-resolution micro-computed tomography with material composition to define the quality of bone tissue. Curr Osteoporos Rep. June 2003;1(1):11-19.
2006	Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF. Glucocorticoid‐treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo‐treated or estrogen‐deficient mice. J Bone Miner Res. March 2006;21(3):466-476.
1989	Kuhn JL, Goldstein SA, Choi K, London M, Feldkamp LA, Matthews LS. Comparison of the trabecular and cortical tissue moduli from human iliac crests. J Orthop Res. November 1989;7(6):876-884.
1999	Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L. Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tiss Int. September 1999;65(3):203-210.
1997	Majumdar S, Genant HK, Grampp S, Newitt DC, Truong V-H, Lin JC, Mathur A. Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res. January 1997;12(1):111-118.
2003	Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744-750.
2009	Morgan EF, Mason ZD, Chien KB, Pfeiffer AJ, Barnes GL, Einhorn TA, Gerstenfeld LC. Micro-computed tomography assessment of fracture healing: relationships among callus structure, composition, and mechanical function. Bone. February 2009;44(2):335-344.
2004	Fernández-Seara MA, Wehrli SL, Takahashi M, Wehrli FW. Water content measured by proton-deuteron exchange NMR predicts bone mineral density and mechanical properties. J Bone Miner Res. February 2004;19(2):289-296.
2006	Donnelly E, Baker SP, Boskey AL, van der Meulen MC. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res. May 2006;A77(2):426-435.
1998	Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK. High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone. May 1998;22(5):445-454.
1975	Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg. October 1975;57A(7):956-961.
1999	Rho J-Y, Roy ME II, Tsui TY, Pharr GM. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res. 1999;A45(1):48-54.
2007	Vashishth D. The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep. June 2007;5(2):62-66.
2008	Techawiboonwong A, Song HK, Leonard MB, Wehrli FW. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging. Radiology. September 2008;248(3):824-833.
1969	Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. March 1969;2(1):1-11.
1996	Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. May 18, 1996;312(7041):1254-1259.
2003	Bouxsein ML. Bone quality: where do we go from here? Osteoporos Int. September 2003;14(suppl 5):S118-S127.
2001	van der Meulen MCH, Jepsen KJ, Mikić B. Understanding bone strength: size isn’t everything. Bone. July 2001;29(1):101-104.

Cited By (56)

Year	Entry
2017	Isaksson H, Le Cann S, Perdikouri C, Turunen MJ, Kaestner A, Tägil M, Hall SA, Tudisco E. Neutron tomographic imaging of bone-implant interface: comparison with X-ray tomography. Bone. October 2017;103:295-301.
2020	Sadoughi S, vom Scheidt A, Nawathe S, Zhu S, Moini A, Keaveny TM. Effect of variations in tissue-level ductility on human vertebral strength. Bone. August 2020;137:115445.
2021	Surowiec RK, Ram S, Idiyatullin D, Goulet R, Schlecht SH, Galban CJ, Kozloff KM. In vivo quantitative imaging biomarkers of bone quality and mineral density using multi-band-SWIFT magnetic resonance imaging. Bone. February 2021;143:115615.
2021	Mandair GS, Akhter MP, Esmonde-White FW, Lappe JM, Bare SP, Lloyd WR, Long JP, Lopez J, Kozloff KM, Recker RR, Morris MD. Altered collagen chemical compositional structure in osteopenic women with past fractures: a case-control Raman spectroscopic study. Bone. July 2021;148:115962.
2021	Stürznickel J, Schmidt FN, Schäfer HS, Beil FT, Frosch K-H, Schlickewei C, Amling M, Barg A, Rolvien T. Bone microarchitecture of the distal fibula assessed by HR-pQCT. Bone. October 2021;151:116057.
2018	Zhao S, Arnold M, Ma S, Abel RL, Cobb JP, Hansen U, Boughton O. Standardizing compression testing for measuring the stiffness of human bone. Bone Joint Res. August 2018;7(8):524-538.
2018	Unal M, Creecy A, Nyman JS. The role of matrix composition in the mechanical behavior of bone. Curr Osteoporos Rep. June 2018;16(3):205-215.
2014	Lambers FM, Bouman AR, Tkachenko EV, Keaveny TM, Hernandez CJ. The effects of tensile-compressive loading mode and microarchitecture on microdamage in human vertebral cancellous bone. J Biomech. November 28, 2014;47(15):3605-3612.
2013	Gourion-Arsiquaud S, Lukashova L, Power J, Loveridge N, Reeve J, Boskey AL. Fourier transform infrared imaging of femoral neck bone: reduced heterogeneity of mineral-to-matrix and carbonate-to-phosphate and more variable crystallinity in treatment-naive fracture cases compared with fracture-free controls. J Bone Miner Res. January 2013;28(1):150-161.
2017	Hernandez CJ, van der Meulen MCH. Understanding bone strength is not enough. J Bone Miner Res. June 2017;32(6):1157-1162.
2021	Lewis JR, Voortman T, Ioannidis JP. Evaluating and strengthening the evidence for nutritional bone research: ready to break new ground? J Bone Miner Res. February 2021;36(2):219-226.
2023	Bott KN, Feldman E, de Souza RJ, Comelli EM, Klentrou P, Peters SJ, Ward WE. Lipopolysaccharide-induced bone loss in rodent models: a systematic review and meta-analysis. J Bone Miner Res. January 2023;38(1):198-213.
2019	Asgari M, Abi-Rafeh J, Hendy GN, Pasini D. Material anisotropy and elasticity of cortical and trabecular bone in the adult mouse femur via AFM indentation. J Mech Behav Biomed Mater. May 2019;93:81-92.
2020	Nedelkovski V, Hahn R, Mayrhofer PH, Steiger-Thirsfeld A, Bernardi J, Thurner PJ. Influence of experimental constraints on micromechanical assessment of micromachined hard-tissue samples. J Mech Behav Biomed Mater. June 2020;106:103741.
2020	Obata Y, Bale HA, Barnard HS, Parkinson DY, Alliston T, Acevedo C. Quantitative and qualitative bone imaging: a review of synchrotron radiation microtomography analysis in bone research. J Mech Behav Biomed Mater. October 2020;110:103887.
2014	Fonseca H, Moreira-Gonçalves D, Coriolano H-JA, Duarte JA. Bone quality: the determinants of bone strength and fragility. Sports Med. January 2014;44(1):37-53.
2022	Bott KN. Effects of Exogenous Lipopolysaccharide Exposure on Bone Outcomes in Rodent Models [PhD thesis]. Brock University; 2022.
2017	Unal M. Classification of Bound Water and Collagen Denaturation Status of Cortical Bone by Raman Spectroscopy [PhD thesis]. Cleveland, OH: Case Western Reserve University; January 2017.
2017	Heveran CM. Bone Tissue Material Properties Are Altered in Chronic Kidney Disease to Lower Fracture Resistance Determining Bone Quality [PhD thesis]. University of Colorado; 2017.
2021	Coulombe JC. Diminished Bone Structural Quality in Aging and Microgravity Follow Impairments of the Osteocyte Lacunar-Canalicular System [PhD thesis]. University of Colorado; 2021.
2022	Senwar B. Bone Material Quality, Structure, and Functional Relationships Contribute to Bone Strength and Toughness [Master's thesis]. University of Colorado; 2022.
2018	Chen JTH. Alterations in Bone Tissue Properties With Parathyroid Hormone Treatment [PhD thesis]. Ithaca, NY: Cornell University; May 2018.
2018	Torres AM. Fatigue Behavior of Cancellous Bone, Microdamage Accumulation, and Biologically Inspired Cellular Solids [PhD thesis]. Ithaca, NY: Cornell University; August 2018.
2022	Peruzzi CRP. Nanoscale Deformation Mechanisms and Yield Prediction of Lamellar Bone [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2022.
2018	Muckatira SK. Error Estimation in Whole Bone Microstrain Measurement When Using Digital Volume Correlation [Master's thesis]. University of Illinois at Urbana-Champaign; 2018.
2015	Rodriguez-Florez N. Mechanics of Cortical Bone: Exploring the Micro- and Nano-Scale [PhD thesis]. Imperial College London; January 2015.
2021	Scott MC. Exercise and Bone: Older Adults, Type II Diabetes, and Ketogenic Diets [PhD thesis]. Louisiana State University; May 2021.
2017	Mathavan N. The Anabolic - Anti-Catabolic Paradigm of Augmenting Skeletal Regeneration: A Bone Quality Perspective [PhD thesis]. Lund, Sweden: Lund University; 2017.
2014	Jameson JR. Characterization of Bone Material Properties and Microstructure in Osteogenesis Imperfecta/brittle Bone Disease [PhD thesis]. Marquette University; December 2014.
2016	Creighton E-R. Investigating Hyperglycemic Bone Formation With High Resolution Microscopy Techniques [Master's thesis]. Hamilton, ON: McMaster University; August 2016.
2016	Hunckler MD. Investigation of a Rabbit Ulnar Loading Model for Atypical Fractures in Cortical Bone During Long-Term Bisphosphonate Treatment [Master's thesis]. University of Notre Dame; December 2016.
2018	Johnson TB. Effect of Guided Bone Regeneration With RhBMP-2 on Bone Quality Surrounding Dental Implants [Master's thesis]. The Ohio State University; 2018.
2016	Berman AG. Influence of Mechanical Stimulation on the Quantity and Quality of Bone During Modeling [Master's thesis]. Purdue University; August 2016.
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.
2019	Powell KM. The Effects of Zoledronate and Raloxifene Combination Therapy on Diseased Mouse Bone [Master's thesis]. Indianapolis, IN: Purdue University; May 2019.
2021	Zojaji M. Quantifying the Accuracy of Euler-Bernoulli and Timoshenko Beam Theories for Long Bones in Three- and Four-Point Bend Tests With Finite Element Analysis [Master's thesis]. Queen's University; September 2021.
2022	Kunath BA. Design and Validation of an Open-Source 3D Printable Bioreactor System for Ex Vivo Bone Culture [Master's thesis]. Queen's University; June 2022.
2019	Beltejar M-JG. Understanding the Genetic Basis for Bone-Matrix Quality [PhD thesis]. University of Rochester; 2019.
2016	Bailey SM. The Role of Extra-Cellular Matrix Proteins and Post-Translational Modifications on Bone Fracture [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; September 2016.
2018	Alousaimi H. A Study of Bone Quality in Femoral Neck of Osteoarthritis [Master's thesis]. Vancouver, BC: University of British Columbia; August 2018.
2014	Nour MA. Impact of Growth Hormone on Adult Bone Quality in Turner Syndrome: A High Resolution Peripheral Quantitative Computed Tomography Study [Master's thesis]. Calgary, AB: University of Calgary; January 2014.
2012	Tjhia CKH. Bone Quality of Patients With Atypical Fractures and Severely Suppressed Bone Turnover [PhD thesis]. Davis, University of California; 2012.
2019	Nguyen C. Multiscale Network Characterization of the Strength and Robustness of Trabecular Bone [PhD thesis]. Santa Barbara, CA: Santa Barbara, University of California; September 2019.
2015	Rys JP. Mechanobiology of TGFΒ Receptor Dynamics and Signaling in Chondrocytes [PhD thesis]. San Francisco, University of California; 2015.
2019	Surowiec R. Novel Models to Image and Quantify Bone Drug Efficacy and Disease Progression in Vivo: Addressing the Fragility Phenotype [PhD thesis]. University of Michigan; 2019.
2019	Küsters NV. Auswirkungen des Alters und der Knochenmikroarchitektur auf die trabekuläre Knochenmineralisationsdichteverteilung: Eine rasterelektronenmikroskopische Studie an 152 humanen Beckenkammbiopsien [PhD thesis]. Hamburg, Germany: Universität Hamburg; 2019.
2017	de Bakker CMJ. Structural Adaptations of the Maternal Skeleton in Response to Reproduction and Lactation [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2017.
2015	Lin C-L. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2015.
2016	Lin C-l. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2016.
2014	Carter Y. Quantitative Imaging of Sex and Age Differences in Human Cortical Bone Osteocyte Lacunae [PhD thesis]. University of Saskatchewan; July 2014.
2015	Ng AH-M. A Mouse Model of Adynamic Bone Disease (ABD) and Its Consequences on Bone Quality With Age [PhD thesis]. University of Toronto; 2015.
2018	Burke MV. Quantification of Changes in Vertebral Bone Quality in the Presence of Metastases [PhD thesis]. University of Toronto; 2018.
2019	Clement A. Image Based and Biomechanical Characterization of Osteoblastic Vertebral Metastases [Master's thesis]. University of Toronto; 2019.
2021	Feng GL. The Role of Arrestin-3 in Bone Catabolic Response to Hyperparathyroidism [Master's thesis]. University of Toronto; 2021.
2017	Tilak K. Finite Element Simulation of Nanoindentation in Lamellar Bone Composites [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; May 2017.
2018	Creecy A. Age- and Diabetes-Related Changes in the Matrix and Fracture Resistance of Bone [PhD thesis]. Nashville, TN: Vanderbilt University; August 10, 2018.