Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography

wbldb

Whittier, D. E.^1,2; Boyd, S. K.^1,2; Burghardt, A. J.³; Paccou, J.⁴; Ghasem-Zadeh, A.⁵; Chapurlat, R.^6,7; Engelke, K.^8,9; Bouxsein, M. L.^10,11

Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography

Osteoporos Int. September 2020;31(9):1607-1627

©2020 International Osteoporosis Foundation and National Osteoporosis Foundation

Affiliations

¹McCaig Institute for Bone and Joint Health, Cumming School of Medicine, University of Calgary, Calgary, Canada

²Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, Canada

³Department of Radiology and Biomedical Imaging, University of California, San Francisco, USA

⁴Department of Rheumatology, MABlab UR 4490, CHU Lille, Univ. Lille, Lille, France

⁵Departments of Endocrinology and Medicine, Austin Health, The University of Melbourne, Melbourne, Australia

⁶INSERM UMR 1033, Université de Lyon, Lyon, France

⁷Hôpital Edouard Herriot, Hospice Civils de Lyon, Lyon, France

⁸Department of Medicine 3, FAU University Erlangen-Nürnberg and Universitätsklinikum Erlangen, Erlangen, Germany

⁹Bioclinica, Inc., Hamburg, Germany

¹⁰Center for Advanced Orthopedic Studies, Beth Israel Deaconess Medical Center, Boston, USA

¹¹Harvard Medical School, Boston, USA
Abstract and keywords

Introduction: The application of high-resolution peripheral quantitative computed tomography (HR-pQCT) to assess bone microarchitecture has grown rapidly since its introduction in 2005. As the use of HR-pQCT for clinical research continues to grow, there is an urgent need to form a consensus on imaging and analysis methodologies so that studies can be appropriately compared. In addition, with the recent introduction of the second-generation HrpQCT, which differs from the first-generation HR-pQCT in scan region, resolution, and morphological measurement techniques, there is a need for guidelines on appropriate reporting of results and considerations as the field adopts newer systems.

Methods: A joint working group between the International Osteoporosis Foundation, American Society of Bone and Mineral Research, and European Calcified Tissue Society convened in person and by teleconference over several years to produce the guidelines and recommendations presented in this document.

Results: An overview and discussion is provided for (1) standardized protocol for imaging distal radius and tibia sites using HR-pQCT, with the importance of quality control and operator training discussed; (2) standardized terminology and recommendations on reporting results; (3) factors influencing accuracy and precision error, with considerations for longitudinal and multi-center study designs; and finally (4) comparison between scanner generations and other high-resolution CT systems.

Conclusion: This article addresses the need for standardization of HR-pQCT imaging techniques and terminology, provides guidance on interpretation and reporting of results, and discusses unresolved issues in the field.

Keywords: Bone microarchitecture; Guidelines; High-resolution peripheral quantitative computed tomography; Imaging protocol
Links

DOI: 10.1007/s00198-020-05438-5

PubMed: 32458029

WoS: 000553568300001
History

Received: 2020-03-12

Accepted: 2020-04-23

Online: 2020-05-26

Cited Works (48)

Year	Entry
2010	Wang Q, Wang X-F, Iuliano-Burns S, Ghasem-Zadeh A, Zebaze R, Seeman E. Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty. J Bone Miner Res. July 2010;25(7):1521-1526.
2012	Pauchard Y, Liphardt A-M, Macdonald HM, Hanley DA, Boyd SK. Quality control for bone quality parameters affected by subject motion in high-resolution peripheral quantitative computed tomography. Bone. June 2012;50(6):1304-1310.
2018	Whittier DE, Manske SL, Kiel DP, Bouxsein M, Boyd SK. Harmonizing finite element modelling for non-invasive strength estimation by high-resolution peripheral quantitative computed tomography. J Biomech. October 26, 2018;80:63-71.
2008	MacNeil JA, Boyd SK. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone. June 2008;42(6):1203-1213.
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.
2002	Pistoia W, van Rietbergen B, Lochmüller E-M, Lill CA, Eckstein F, Rüegsegger P. Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone. June 2002;30(6):842-848.
2017	Tsai JN, Nishiyama KK, Lin D, Yuan A, Lee H, Bouxsein ML, Leder BZ. Effects of denosumab and teriparatide transitions on bone microarchitecture and estimated strength: the DATA-Switch HR-pQCT study. J Bone Miner Res. October 2017;32(10):2001-2009.
2004	Pistoia W, van Rietbergen B, Lochmüller E-M, Lill CA, Eckstein F, Rüegsegger P. Image-based micro-finite-element modeling for improved distal radius strength diagnosis: moving from "bench" to "bedside". J Clin Densitom. Summer 2004;7(2):153-160.
2019	Burt LA, Billington EO, Rose MS, Raymond DA, Hanley DA, Boyd SK. Effect of high-dose vitamin D supplementation on volumetric bone density and bone strength: a randomized clinical trial. JAMA. August 27, 2019;322(8):736-745.
2015	van Rietbergen B, Ito K. A survey of micro-finite element analysis for clinical assessment of bone strength: the first decade. J Biomech. March 18, 2015;48(5):832-841.
1998	Laib A, Häuselmann HJ, Rüegsegger P. In vivo high resolution 3D-QCT of the human forearm. Technol Health Care. 1998;6(5-6):329-337.
2010	Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. September 2010;47(3):519-528.
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.
2013	Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res. February 2013;28(2):313-324.
2012	Engelke K, Stampa B, Timm W, Dardzinski B, de Papp AE, Genant HK, Fuerst T. Short-term in vivo precision of BMD and parameters of trabecular architecture at the distal forearm and tibia. Osteoporos Int. August 2012;23(8):2151-2158.
1974	Whitehouse WJ. The quantitative morphology of anisotropic trabecular bone. J Microsc (Oxford). July 1974;101:153-168.
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.
2017	Kroker A, Zhu Y, Manske SL, Barber R, Mohtadi N, Boyd SK. Quantitative in vivo assessment of bone microarchitecture in the human knee using HR-pQCT. Bone. April 2017;97:43-48.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
2014	Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat J-B, Boutroy S. Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone. June 2014;63:147-157.
2008	Boyd SK. Site-specific variation of bone micro-architecture in the distal radius and tibia. J Clin Densitom. July–September 2008;11(3):424-430.
2012	Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S. Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone. January 2012;50(1):111-118.
2011	Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK. Age‐related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population‐based HT‐pQCT study. J Bone Miner Res. January 2011;26(1):50-62.
2018	Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu C-T, Boyd SK, McLean RR, Broe KE, Kiel DP, Bouxsein ML. Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT study. J Bone Miner Res. January 2018;33(1):54-62.
2017	Bonaretti S, Majumdar S, Lang TF, Khosla S, Burghardt AJ. The comparability of HR-pQCT bone measurements is improved by scanning anatomically standardized regions. Osteoporos Int. July 2017;28(7):2115-2128.
2010	Seeman E, Delmas PD, Hanley DA, Sellmeyer D, Cheung AM, Shane E, Kearns A, Thomas T, Boyd SK, Boutroy S, Bogado C, Majumdar S, Fan M, Libanati C, Zanchetta J. Microarchitectural deterioration of cortical and trabecular bone: differing effects of denosumab and alendronate. J Bone Miner Res. August 2010;25(8):1886-1894.
2017	Ghasem-Zadeh A, Burghardt A, Wang X-F, Iuliano S, Bonaretti S, Bui M, Zebaze R, Seeman E. Quantifying sex, race, and age specific differences in bone microstructure requires measurement of anatomically equivalent regions. Bone. August 2017;101:206-213.
2010	Vilayphiou N, Boutroy S, Sornay-rendu E, Van rietbergen B, Munoz F, Delmas PD, Chapurlat R. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in postmenopausal women. Bone. April 2010;46(4):1030-1037.
2015	Manske SL, Zhu Y, Sandino C, Boyd SK. Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone. October 2015;79:213-221.
2017	Manske SL, Davison EM, Burt LA, Raymond DA, Boyd SK. The estimation of second-generation HR-pQCT from first-generation -pQCT using in vivo cross-calibration. J Bone Miner Res. July 2017;32(7):1514-1524.
2013	Christen D, Melton LJ III, Zwahlen A, Amin S, Khosla S, Müller R. Improved fracture risk assessment based on nonlinear micro-finite element simulations from HRpQCT images at the distal radius. J Bone Miner Res. December 2013;28(12):2601-2608.
2008	Liu XS, Sajda P, Saha PK, Wehrli FW, Bevill G, Keaveny TM, Guo XE. Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res. February 2008;23(2):223-235.
2010	Varga P, Pahr DH, Baumbach S, Zysset PK. HR-pQCT based FE analysis of the most distal radius section provides an improved prediction of Colles' fracture load in vitro. Bone. November 2010;47(5):982-988.
2014	Hansen S, Shanbhogue V, Folkestad L, Nielsen MMF, Brixen K. Bone microarchitecture and estimated strength in 499 adult Danish women and men: a cross-sectional, population-based high-resolution peripheral quantitative computed tomographic study on peak bone structure. Calcif Tiss Int. March 2014;94(3):269-281.
2013	Zebaze R, Ghasem-Zadeh A, Mbala A, Seeman E. A new method of segmentation of compact-appearing, transitional and trabecular compartments and quantification of cortical porosity from high resolution peripheral quantitative computed tomographic images. Bone. May 2013;54(1):8-20.
2011	Mueller TL, Christen D, Sandercott S, Boyd SK, van Rietbergen B, Eckstein F, Lochmüller E-M, Müller R, van Lenthe GH. Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. Bone. June 1, 2011;48(6):1232-1238.
2018	Chiba K, Okazaki N, Kurogi A, Isobe Y, Yonekura A, Tomita M, Osaki M. Precision of second-generation high-resolution peripheral quantitative computed tomography: intra- and intertester reproducibilities and factors involved in the reproducibility of cortical porosity. J Clin Densitom. April–June 2018;21(2):295-302.
1999	Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.
2007	Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone. October 2007;41(4):505-515.
2010	Bacchetta J, Boutroy S, Vilayphiou N, Juillard L, Guebre-Egziabher F, Rognant N, Sornay-Rendu E, Szulc P, Laville M, Delmas PD, Fouque D, Chapurlat R. Early impairment of trabecular microarchitecture assessed with HR-pQCT in patients with stage II-IV chronic kidney disease. J Bone Miner Res. April 2010;25(4):849-857.
2016	Burt LA, Liang Z, Sajobi TT, Hanley DA, Boyd SK. Sex‐ and site‐specific normative data curves for HR‐pQCT. J Bone Miner Res. 2016;31(11):2041-2047.
1995	van Rietbergen B, Weinans H, Huiskes R, Odgaard A. A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. J Biomech. January 1995;28(1):69-81.
2013	Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.
2010	Nishiyama KK, Macdonald HM, Buie HR, Hanley DA, Boyd SK. Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J Bone Miner Res. April 2010;25(4):882-890.
2017	Gabel L, Macdonald HM, McKay HA. Sex differences and growth‐related adaptations in bone microarchitecture, geometry, density, and strength from childhood to early adulthood: a mixed longitudinal HR‐pQCT study. J Bone Miner Res. February 2017;32(2):250-263.
2011	Sode M, Burghardt AJ, Pialat J-B, Link TM, Majumdar S. Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone. June 1, 2011;48(6):1291-1297.
1993	Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.
1995	Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57(1):289-300.

Cited By (52)

Year	Entry
2021	Ghasem-Zadeh A, Galea MP, Nunn A, Panisset M, Wang X-F, Iuliano S, Boyd SK, Forwood MR, Seeman E. Heterogeneity in microstructural deterioration following spinal cord injury. Bone. January 2021;142:115778.
2021	Lalayiannis AD, Fewtrell M, Biassoni L, Silva S, Goodman N, Shroff R, Crabtree NJ. Studying bone mineral density in young people: the complexity of choosing a pQCT reference database. Bone. February 2021;143:115713.
2021	Whittier DE, Burt LA, Boyd SK. A new approach for quantifying localized bone loss by measuring void spaces. Bone. February 2021;143:115785.
2021	Chiba K, Yamada S, Yoda I, Era M, Yokota K, Okazaki N, Ota S, Isobe Y, Miyazaki S, Tashiro S, Nakashima S, Morimoto S, Sato S, Tsukazaki T, Watanabe T, Enomoto H, Yabe Y, Yonekura A, Tomita M, Ito M, Osaki M. Effects of monthly intravenous ibandronate on bone mineral density and microstructure in patients with primary osteoporosis after teriparatide treatment: the MONUMENT study. Bone. March 2021;144:115770.
2021	Miller T, Ying MTC, Hung VWY, Tsang CSL, Ouyang H, Chung RCK, Qin L, Pang MYC. Determinants of estimated failure load in the distal radius after stroke: an HR-pQCT study. Bone. March 2021;144:115831.
2021	Mikolajewicz N, Zimmermann EA, Rummler M, Hosseinitabatabaei S, Julien C, Glorieux FH, Rauch F, Willie BM. Multisite longitudinal calibration of HR-pQCT scanners and precision in osteogenesis imperfecta. Bone. June 2021;147:115880.
2021	Fuggle NR, Westbury LD, Bevilacqua G, Titcombe P, Ó. Breasail M, Harvey NC, Dennison EM, Cooper C, Ward KA. Level and change in bone microarchitectural parameters and their relationship with previous fracture and established bone mineral density loci. Bone. June 2021;147:115937.
2021	Ohs N, Collins CJ, Tourolle DC, Atkins PR, Schroeder BJ, Blauth M, Christen P, Müller R. Automated segmentation of fractured distal radii by 3D geodesic active contouring of in vivo HR-pQCT images. Bone. June 2021;147:115930.
2021	Okazaki N, Chiba K, Burghardt AJ, Kondo C, Doi M, Yokota K, Yonekura A, Tomita M, Osaki M. Differences in bone mineral density and morphometry measurements by fixed versus relative offset methods in high-resolution peripheral quantitative computed tomography. Bone. August 2021;149:115973.
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.
2022	Revel M, Bermond F, Duboeuf F, Mitton D, Follet H. Influence of loading conditions in finite element analysis assessed by HR–pQCT on ex vivo fracture prediction. Bone. January 2022;154:116206.
2022	Doi M, Chiba K, Okazaki N, Kondo C, Yamada S, Yokota K, Yonekura A, Tomita M, Osaki M. Bone microstructure in healthy men measured by HR-pQCT: age-related changes and their relationships with DXA parameters and biochemical markers. Bone. January 2022;154:116252.
2022	Ghasem-Zadeh A, Bui M, Seeman E, Boyd SK, Iuliano S, Jaipurwala R, Mount PF, Toussaint ND, Chiang C. Bone microarchitecture and estimated failure load are deteriorated whether patients with chronic kidney disease have normal bone mineral density, osteopenia or osteoporosis. Bone. January 2022;154:116260.
2022	Gaffney-Stomberg E, Hughes JM, Guerriere KI, Staab JS, Cable SJ, Bouxsein ML, McClung JP. Once daily calcium (1000 mg) and vitamin D (1000 IU) supplementation during military training prevents increases in biochemical markers of bone resorption but does not affect tibial microarchitecture in Army recruits. Bone. February 2022;155:116269.
2022	Chiba K, Okazaki N, Kurogi A, Watanabe T, Mori A, Suzuki N, Adachi K, Era M, Yokota K, Inoue T, Yabe Y, Furukawa K, Kondo C, Tsuda K, Ota S, Isobe Y, Miyazaki S, Morimoto S, Sato S, Nakashima S, Tashiro S, Yonekura A, Tomita M, Osaki M. Randomized controlled trial of daily teriparatide, weekly high-dose teriparatide, or bisphosphonate in patients with postmenopausal osteoporosis: the TERABIT study. Bone. July 2022;160:116416.
2022	Hepp N, Folkestad L, Møllebæk S, Frederiksen AL, Duno M, Jørgensen NR, Hermann AP, Jensen J-EB. Bone-microarchitecture and bone-strength in a sample of adults with hypophosphatasia and a matched reference population assessed by HR-pQCT and impact microindentation. Bone. July 2022;160:116420.
2022	Uppuganti S, Ketsiri T, Zhang Y, Does MD, Nyman JS. HR-pQCT parameters of the distal radius correlate with the bending strength of the radial diaphysis. Bone. August 2022;161:116429.
2022	Singhal V, Huynh C, Nimmala S, Mitchell DM, Pedreira CC, Bader A, Flanders K, Zheng J, Bouxsein ML, Misra M, Bredella MA. Load-to-strength ratio at the radius is higher in adolescent and young adult females with obesity compared to normal-weight controls. Bone. November 1, 2022;164:116515.
2023	Walle M, Eggemann D, Atkins PR, Kendall JJ, Stock K, Müller R, Collins CJ. Motion grading of high-resolution quantitative computed tomography supported by deep convolutional neural networks. Bone. January 2023;166:116607.
2023	Singhal V, Kaur S, Haidar LA, Lee H, Bredella MA, Misra M. Differences in bone accrual over one year in young girls with obesity compared to normal weight controls. Bone. July 2023;172:116757.
2023	Walle M, Whittier DE, Schenk D, Atkins PR, Blauth M, Zysset P, Lippuner K, Müller R, Collins CJ. Precision of bone mechanoregulation assessment in humans using longitudinal high-resolution peripheral quantitative computed tomography in vivo. Bone. July 2023;172:116780.
2023	Bevers MSAM, Heyer FL, Wyers CE, van Rietbergen B, Geusens PPMM, Janzing HMJ, Lambers Heerspink O, Poeze M, van den Bergh JP. The contribution of lower-mineralized tissue to the healing of distal radius fractures assessed using HR-pQCT. Bone. October 2023;175:116859.
2023	Whittier DE, Walle M, Schenk D, Atkins PR, Collins CJ, Zysset P, Lippuner K, Müller R. A multi-stack registration technique to improve measurement accuracy and precision across longitudinal HR-pQCT scans. Bone. November 2023;176:116893.
2023	Yadav RN, Oravec DJ, Morrison CK, Bevins NB, Rao SD, Yeni YN. Digital wrist tomosynthesis (DWT)-based finite element analysis of ultra-distal radius differentiates patients with and without a history of osteoporotic fracture. Bone. December 2023;177:116901.
2020	Whittier DE, Burt LA, Hanley DA, Boyd SK. Sex‐ and site‐specific reference data for bone microarchitecture in adults measured using second‐generation HR‐pQCT. J Bone Miner Res. November 2020;35(11):2151-2158.
2021	Dietrich K, Fiedler IAK, Kurzyukova A, López‐Delgado AC, McGowan LM, Geurtzen K, Hammond CL, Busse B, Knopf F. Skeletal biology and disease modeling in zebrafish. J Bone Miner Res. March 2021;36(3):436-458.
2021	Vilaca T, Paggiosi M, Walsh JS, Selvarajah D, Eastell R. The effects of type 1 diabetes and diabetic peripheral neuropathy on the musculoskeletal system: a case–control study. J Bone Miner Res. June 2021;36(6):1048-1059.
2021	O'Leary TJ, Wardle SL, Gifford RM, Double RL, Reynolds RM, Woods DR, Greeves JP. Tibial macrostructure and microarchitecture adaptations in women during 44 weeks of arduous military training. J Bone Miner Res. July 2021;36(7):1300-1315.
2021	Schmidt C, Stürznickel J, Strahl A, Oheim R, Weiler-Normann C, Sebode M, Barvencik F, Lohse AW, Schinke T, Amling M, Schramm C, Rolvien T. Bone microarchitecture in patients with autoimmune hepatitis. J Bone Miner Res. July 2021;36(7):1316-1325.
2022	Whittier DE, Samelson EJ, Hannan MT, Burt LA, Hanley DA, Biver E, Szulc P, Sornay-Rendu E, Merle B, Chapurlat R, Lespessailles E, Wong AKO, Goltzman D, Khosla S, Ferrari S, Bouxsein ML, Kiel DP, Boyd SK. Bone microarchitecture phenotypes identified in older adults are associated with different levels of osteoporotic fracture risk. J Bone Miner Res. March 2022;37(3):428-439.
2022	Pang Q, Xu Y, Huang L, Li Y, Lin Y, Hou Y, Hung VW, Qi X, Ni X, Li M, Jiang Y, Wang O, Xing X, Qin L, Xia W. Bone geometry, density, microstructure, and biomechanical properties in the distal tibia in patients with primary hypertrophic osteoarthropathy assessed by second-generation high-resolution peripheral quantitative computed tomography. J Bone Miner Res. March 2022;37(3):484-493.
2022	Orwoll ES, Parimi N, Wiedrick J, Lapidus J, Napoli N, Wilkinson JE, Huttenhower C, Langsetmo L, Kiel DP. Analysis of the associations between the human fecal microbiome and bone density, structure, and strength: the Osteoporotic Fractures in Men (mrOS) cohort. J Bone Miner Res. April 2022;37(4):597-607.
2022	Hosseinitabatabaei S, Mikolajewicz N, Zimmermann EA, Rummler M, Steyn B, Julien C, Rauch F, Willie BM. 3D image registration marginally improves the precision of HR-pQCT measurements compared to cross-sectional-area registration in adults with osteogenesis imperfecta. J Bone Miner Res. May 2022;37(5):908-924.
2022	Geusens P, Bevers MSAM, van Rietbergen B, Messina OD, Lespessailles E, Oliveri B, Chapurlat R, Engelke K, Chines A, Huang S, Saag KG, van den Bergh JP. Effect of denosumab compared with risedronate on bone strength in patients initiating or continuing glucocorticoid treatment. J Bone Miner Res. June 2022;37(6):1136-1146.
2022	Stürznickel J, Heider F, Delsmann A, Gödel M, Grünhagen J, Huber TB, Kornak U, Amling M, Oheim R. Clinical spectrum of hereditary hypophosphatemic rickets with hypercalciuria (HHRH). J Bone Miner Res. August 2022;37(8):1580-1591.
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.
2022	Bobillier A, Wagner P, Whittier DE, Ecochard R, Boyd SK, Chapurlat R, Szulc P. Association of vitamin D and parathyroid hormone status with the aging-related decline of bone microarchitecture in older men: the Prospective Structure of Aging Men's Bones (STRAMBO) study. J Bone Miner Res. October 2022;37(10):1903-1914.
2022	Whittier DE, Manske SL, Billington E, Walker RE, Schneider PS, Burt LA, Hanley DA, Boyd SK. Hip fractures in older adults are associated with the low density bone phenotype and heterogeneous deterioration of bone microarchitecture. J Bone Miner Res. October 2022;37(10):1963-1972.
2023	Ramchand SK, David NL, Lee H, Bruce M, Bouxsein ML, Tsai JN, Leder BZ. The effect of zoledronic acid on bone microarchitecture and strength after denosumab and teriparatide administration: DATA-HD study extension. J Bone Miner Res. January 2023;38(1):26-34.
2023	Agarwal S, McMahon DJ, Chen J, Brossfield AV, Fernando J, Bilezikian JP, Cusano NE, Rubin MR. The clinical and skeletal effects of long-term therapy of hypoparathyroidism with rhPTH(1-84). J Bone Miner Res. April 2023;38(4):480-492.
2023	Gunsing E, Wagner PP, Whittier DE, Boyd SK, Chapurlat R, Szulc P. Rapid cortical bone loss at the distal radius is associated with higher risk of fracture in older men: the STRAMBO study. J Bone Miner Res. June 2023;38(6):841-850.
2023	Whittier DE, Samelson EJ, Hannan MT, Burt LA, Hanley DA, Biver E, Szulc P, Sornay-Rendu E, Merle B, Chapurlat R, Lespessailles E, Wong AKO, Goltzman D, Khosla S, Ferrari S, Bouxsein ML, Kiel DP, Boyd SK. A fracture risk assessment tool for high resolution peripheral quantitative computed tomography. J Bone Miner Res. September 2023;38(9):1234-1244.
2023	Holling T, Brylka L, Scholz T, Bierhals T, Herget T, Meinecke P, Schinke T, Oheim R, Kutsche K. TMCO3, a putative K+:proton antiporter at the Golgi apparatus, is important for longitudinal growth in mice and humans. J Bone Miner Res. September 2023;38(9):1334-1349.
2022	Schmidt C, Riedel C, Stürznickel J, Mushumba H, Delsmann MM, Ries C, Kleiss S, Bannas P, Beil FT, Amling M, Püschel K, Rolvien T, Hubert J. Investigation of distal femur microarchitecture and factors influencing its deterioration: an ex vivo high-resolution peripheral quantitative computed tomography study. J Orthop Res. September 2022;40(9):2057-2064.
2023	Schlickewei C, Schweizer C, Püschel K, Ondruschka B, Kleinertz H, Barg A, Rolvien T, Stürznickel J. Age-, sex-, and subregion-specific properties of distal fibular microarchitecture and strength: an ex vivo HR-pQCT study. J Orthop Res. February 2023;41(2):355-363.
2021	Du J, Hartley C, Brooke-Wavell K, Paggiosi MA, Walsh JS, Li S, Silberschmidt VV. High-impact exercise stimulated localised adaptation of microarchitecture across distal tibia in postmenopausal women. Osteoporos Int. May 2021;32(5):907-919.
2020	Plett RM. Enhanced Longitudinal Analysis of Bone Strength Estimated by 3D Bone Imaging and the Finite Element Method [Master's thesis]. Calgary, AB: University of Calgary; October 2020.
2021	Whittier DEW. The Assessment of Fragility Fracture Risk Using HR-PQCT as a Novel Tool for Diagnosis of Osteoporosis [PhD thesis]. Calgary, AB: University of Calgary; August 2021.
2022	Mielczarek CB. An Investigation of Local Microarchitecture Topology Changes in Long-Duration Spaceflight [Master's thesis]. Calgary, AB: University of Calgary; November 2022.
2022	Wyatt P. Bone Quality of Elite Winter Endurance Athletes [Master's thesis]. Calgary, AB: University of Calgary; April 2022.
2022	Sales EdS. The Spatio-Temporal Behavior of Basic Multicellular Units in a PTH-Induced Cortical Bone Remodeling Rabbit Model [Master's thesis]. University of Saskatchewan; August 2022.
2021	Kusins J. A Multi-Level Mechanical Assessment of the Shoulder Coupled With Evaluation of Upper Extremity Predictive Finite Element Models [PhD thesis]. University of Western Ontario; 2021.