High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure:​ a review by the Canadian Bone Strength Working Group

Cheung, Angela M.<sup>1</sup>; Adachi, Jonathan D.<sup>2</sup>; Hanley, David A.<sup>3</sup>; Kendler, David L.<sup>4</sup>; Davison, K. Shawn<sup>5</sup>; Josse, Robert<sup>6</sup>; Brown, Jacques P.<sup>7</sup>; Ste-Marie, Louis-Georges<sup>8</sup>; Kremer, Richard<sup>9</sup>; Erlandson, Marta C.<sup>6,10</sup>; Dian, Larry<sup>4</sup>; Burghardt, Andrew J.<sup>11</sup>; Boyd, Steven K.<sup>12</sup>

Year	Entry
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.
2006	Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, .Peterson JM, Melton LJ III. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. January 2006;21(1):124-131.
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.
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.
2010	Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res. May 2010;25(5):983-993.
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.
2011	Varga P, Dall’Ara E, Pahr DH, Pretterklieber M, Zysset PK. Validation of an HR-pQCT-based homogenized finite element approach using mechanical testing of ultra-distal radius sections. Biomech Model Mechanobiol. July 2011;10(4):431-444.
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.
2008	Vico L, Zouch M, Amirouche A, Frère D, Laroche N, Koller B, Laib A, Thomas T, Alexandre C. High‐resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res. November 2008;23(11):1741-1750.
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.
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.
2009	Dalzell N, Kaptoge S, Morris N, Berthier A, Koller B, Braak L, van Rietbergen B, Reeve J. Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT. Osteoporos Int. October 2009;20(10):1683-1694.
2008	MacNeil JA, Boyd SK. Improved reproducibility of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. July 2008;30(6):792-799.
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.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
2012	Rizzoli R, Chapurlat RD, Laroche J-M, Krieg MA, Thomas T, Frieling I, Boutroy S, Laib A, Bock O, Felsenberg D. Effects of strontium ranelate and alendronate on bone microstructure in women with osteoporosis. Osteoporos Int. January 2012;23(1):305-315.
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.
2010	Melton LJ III, Christen D, Riggs BL, Achenbach SJ, Müller R, van Lenthe GH, Amin S, Atkinson EJ, Khosla S. Assessing forearm fracture risk in postmenopausal women. Osteoporos Int. July 2010;21(7):1161-1169.
1999	Laib A, Rüegsegger P. Comparison of structure extraction methods for in vivo trabecular bone measurements. Comput Vis Image Understand. March–April 1999;23(2):69-74.
2007	Sornay‐Rendu E, Boutroy S, Munoz F, Delmas PD. Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res. March 2007;22(3):425-433.
2010	Liu XS, Zhang XH, Sekhon KK, Adams MF, McMahon DJ, Bilezikian JP, Shane E, Guo XE. High-resolution peripheral quantitative computed tomography can assess microstructural and mechanical properties of human distal tibial bone. J Bone Miner Res. April 2010;25(4):746-756.
2011	Szulc P, Boutroy S, Vilayphiou N, Chaitou A, Delmas PD, Chapurlat R. Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res. June 2011;26(6):1358-1367.
2005	Watts NB, Geusens P, Barton IP, Felsenberg D. Relationship between changes in BMD and nonvertebral fracture incidence associated with risedronate: reduction in risk of nonvertebral fracture is not related to change in BMD. J Bone Miner Res. December 2005;20(12):2097-2104.
2009	Varga P, Baumbach S, Pahr D, Zysset PK. Validation of an anatomy specific finite element model of Colles’ fracture. J Biomech. August 7, 2009;42(11):1726-1731.
2010	Zebaze RMD, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. May 15, 2010;375(9727):1729-1736.
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.
2009	Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ III, Riggs BL, Amin S, Müller R, Khosla S. Bone structure at the distal radius during adolescent growth. J Bone Miner Res. June 2009;24(6):1033-1042.
2011	Vilayphiou N, Boutroy S, Szulc P, 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 men. J Bone Miner Res. May 2011;26(5):965-973.
1999	Ettinger B, Black DM, Mitlak BH, Knickerbocker RK, Nickelsen T, Genant HK, Christiansen C, Delmas PD, Zanchetta JR, Stakkestad J, Glüer CC, Krueger K, Cohen FJ, Eckert S, Ensrud KE, Avioli LV, Lips P, Cummings SR; Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. JAMA. August 18, 1999;282(7):637-645.
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.
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.
2000	Black DM, Thompson DE, Bauer DC, Ensrud K, Musliner T, Hochberg MC, Nevitt MC, Suryawanshi S, Cummings SR; FIT Research Group. Fracture risk reduction with alendronate in women with osteoporosis: the fracture intervention trial. J Clin Endocrinol Metab. November 2000;85(11):4118-4124.
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.
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.
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.
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.
2009	Sornay-Rendu E, Cabrera-Bravo J-L, Boutroy S, Munoz F, Delmas PD. Severity of vertebral fractures is associated with alterations of cortical architecture in postmenopausal women. J Bone Miner Res. April 2009;24(4):737-743.
2007	Burghardt AJ, Kazakia GJ, Majumdar S. A local adaptive threshold strategy for high resolution peripheral quantitative computed tomography of trabecular bone. Ann Biomed Eng. October 2007;235(10):1678-1686.
2010	Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE. Individual trabeculae segmentation (ITS)–based morphological analysis of high‐resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res. July 2010;25(7):1496-1505.
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.
2012	Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE. Individual trabecula segmentation (ITS)‐based morphological analyses and microfinite element analysis of HR‐pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res. February 2012;27(2):263-272.
2010	Liu XS, Cohen A, Shane E, Yin PT, Stein EM, Rogers H, Kokolus SL, McMahon DJ, Lappe JM, Recker RR, Lang T, Guo XE. Bone density, geometry, microstructure, and stiffness: relationships between peripheral and central skeletal sites assessed by DXA, HR‐pQCT, and cQCT in premenopausal women. J Bone Miner Res. October 2010;25(10):2229-2238.
2011	Macdonald HM, Nishiyama KK, Hanley DA, Boyd SK. Changes in trabecular and cortical bone microarchitecture at peripheral sites associated with 18 months of teriparatide therapy in postmenopausal women with osteoporosis. Osteoporos Int. January 2011;22(1):357-362.
2010	Stein EM, Liu XS, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Zhang C, Yin PT, Cosman F, Nieves J, Guo XE, Shane E. Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res. December 2010;25(12):2572-2581.

Year	Entry
2019	Silva AMH, Boyd SK, Manske SL, Alves JM, de Carvalho J. Assessment of the elastic properties of human vertebral trabecular bone using computational mechanical tests and x-ray microtomograph: a subvolume analysis. Biomed Phys Eng Express. July 2019;5(4):045031.
2020	Fuusager G, Milandt N, Shanbhogue VV, Hermann AP, Schou AJ, Christesen HT. Lower estimated bone strength and impaired bone microarchitecture in children with type 1 diabetes. BMJ Open Diabetes Res Care. January 2020;8(1):e001384.
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	Li Y, Tseng W-J, de Bakker CMJ, Zhao H, Chung R, Liu XS. Peak trabecular bone microstructure predicts rate of estrogen-deficiency-induced bone loss in rats. Bone. April 2021;145:115862.
2021	Shalof H, Dimitri P, Shuweihdi F, Offiah AC. Which skeletal imaging modality is best for assessing bone health in children and young adults compared to DXA? a systematic review and meta-analysis. Bone. September 2021;150:116013.
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	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.
2020	de Bakker CMJ, Burt LA, Gabel L, Hanley DA, Boyd SK. Associations between breastfeeding history and early postmenopausal bone loss. Calcif Tiss Int. March 2020;106(3):264-273.
2016	Hunt HB, Donnelly E. Bone quality assessment techniques: geometric, compositional, and mechanical characterization from macroscale to nanoscale. Clin Rev Bone Miner Metab. September 2016;14(3):133-149.
2020	Armamento‐Villareal R, Aguirre L, Waters DL, Napoli N, Qualls C, Villareal DT. Effect of aerobic or resistance exercise, or both, on bone mineral density and bone metabolism in obese older adults while dieting: a randomized controlled trial. J Bone Miner Res. March 2020;35(3):430-439.
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.
2023	Ng C-A, Gandham A, Mesinovic J, Owen PJ, Ebeling PR, Scott D. Effects of moderate- to high-impact exercise training on bone structure across the lifespan: a systematic review and meta-analysis of randomized controlled trials. J Bone Miner Res. November 2023;38(11):1612-1634.
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.
2020	Chirvi S, Pintar FA, Yoganandan N, Stemper B, Kleinberger M. Trabecular bone mineral density correlations using QCT: central and peripheral human skeleton. J Mech Behav Biomed Mater. December 2020;112:104076.
2020	Ng C-A, McMillan LB, Beck B, Humbert L, Ebeling PR, Scott D. Associations between physical activity and bone structure in older adults: does the use of self-reported versus objective assessments of physical activity influence the relationship? Osteoporos Int. March 2020;31(3):493-503.
2021	Ng C-A, McMillan LB, Humbert L, Ebeling PR, Scott D. Feasibility, safety and effectiveness of a pilot 16-week home-based, impact exercise intervention in postmenopausal women with low bone mineral density. Osteoporos Int. May 2021;32(5):893-905.
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.
2022	Bott KN. Effects of Exogenous Lipopolysaccharide Exposure on Bone Outcomes in Rodent Models [PhD thesis]. Brock University; 2022.
2019	Ó Breasail M. The Quantification of Pregnancy-Induced Bone Mineral Mobilisation in the Maternal Appendicular Skeleton With Novel Peripheral Quantitative Computed Tomography (pQCT) Techniques [PhD thesis]. Cambridge, UK: University of Cambridge; 2019.
2015	Zhou B. Bone Quality Assessment Using High Resolution Peripheral Quantitative Computed Tomography (HR-PQCT) [PhD thesis]. Columbia University; 2015.
2018	Hunt HB. Characterization of Material Properties, Microarchitecture, and Mechanics of Bone from Subjects With Type 2 Diabetes Mellitus [PhD thesis]. Ithaca, NY: Cornell University; December 2018.
2019	Du J. Mechanical Adaptation of Human Trabecular Bone: Experimental and Computational Study [PhD thesis]. Loughborough University; 2019.
2021	Schwarzenberg PM. Development and Validation of Virtual Mechanical Testing of Bone Fracture Healing [PhD thesis]. Lehigh University; August 2021.
2022	Ng CATT. Getting the Jump on Healthy Bones: The Skeletal Effects of Impact Physical Activity Across the Lifespan [PhD thesis]. Monash University; 2022.
2017	Draghici AE. Rescuing Osteoporotic Bone in Individuals With Spinal Cord Injury [PhD thesis]. Northeastern University; April 2017.
2018	Metcalf LM. HR-PQCT Scanning of the Human Calcaneus: Early Development and Validation of Assessment of Calcaneal Trabecular Microstructure [PhD thesis]. University of Sheffield; March 2018.
2015	Tan VPS. Effects of a School-Based Physical Activity Intervention on Adolescent Bone Strength, Structure and Density: The Health Promoting Secondary Schools (HPSS) Bone Health Study [PhD thesis]. Vancouver, BC: University of British Columbia; June 2015.
2017	Gabel LEC. Bone Strength Accrual Across Adolescent Growth and the Influences of Physical Activity and Sedentary Time [PhD thesis]. Vancouver, BC: University of British Columbia; April 2017.
2018	George JK. Using Finite Element Models Under Multiple Loading Conditions to Improve the Association Between Radius and Tibia Microarchitecture and Prevalent Osteoporotic Vertebral Fracture [Master's thesis]. Calgary, AB: University of Calgary; May 2018.
2019	Kroker AM. The Progression of Bone Microarchitecture Changes Following an Acute Knee Injury in Young Adults [PhD thesis]. Calgary, AB: University of Calgary; March 2019.
2021	Kemp TD. An Inverse Interface Evolution Problem to Identify Participant-Specific Bone Microarchitecture Adaptation [Master's thesis]. Calgary, AB: University of Calgary; May 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.
2023	Kaketsis D. Investigating Bone Remodelling in Knee Osteoarthritis Using HR-PQCT Imaging [Master's thesis]. Calgary, AB: University of Calgary; May 2023.
2023	Austermann K. Effects of Nutritive Antioxidants on Bone During Immobility [PhD thesis]. Rheinische Friedrich-Wilhelms-Universität Bonn; 2023.
2021	Li Y. Adaptation of Maternal Skeletal Mechano-Responsiveness, Osteocyte Microenvironment, and Bone Marrow Adipocytes in Response to Reproduction and Lactation [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2021.
2018	Hosseini Kalajahi SM. Addressing Partial Volume Artifacts With Quantitative Computed Tomography-Based Finite Element Modeling of the Human Proximal Tibia [Master's thesis]. University of Saskatchewan; April 2018.
2020	Bunyamin ATO. Predicting Off-Axis Bone Strength of the Distal Radius Using High-Resolution Peripheral Quantitative Computed Tomography Based Finite Element Modeling [Master's thesis]. University of Saskatchewan; March 2020.
2020	Hiebert B. The Development of a Cortical Bone Turnover Model: Parathyroid Hormone Effects in the Rabbit [Master's thesis]. University of Saskatchewan; July 2020.
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.