Two Decades of High-Resolution Peripheral Quantitative Computed Tomography: Present and Future Clinical Perspectives

Abstract

Twenty years have passed since the introduction of high-resolution peripheral quantitative computed tomography (HR-pQCT) to assess human bone microarchitecture. During that time, the technique has emerged as an important research tool used by clinicians and scientists to learn about the pathophysiology of bone adaptation in the context of osteoporosis and many other bone-affected conditions. Its rich three-dimensional data is well suited for precise longitudinal monitoring of bone microarchitecture and associated patient-specific estimated bone strength.

However, uptake of HR-pQCT as a clinical diagnostic tool has been limited, in part due to challenges such as availability, regulatory approvals, and demonstrated cost effectiveness. New research suggests fracture risk assessment using HR-pQCT is comparable with current standards based on traditional bone densitometry, but its contribution to clinical care is best suited to two areas: (1) leveraging microarchitectural information to assist in treatment decisions for the large subset of patients who lie in the so-called gray zone by current fracture risk assessment, and (2) longitudinal monitoring that establishes highly refined trajectories of bone adaptation and can inform decisions to initiate treatment, monitor treatment effects, and inform cessation.

Keywords

bone microarchitecture - fracture risk assessment - osteoporosis - osteoarthritis - high-resolution peripheral quantitative computed tomography

Publikationsverlauf

Artikel online veröffentlicht:
15. Oktober 2024

• References

• 1 Rüegsegger P, Elsasser U, Anliker M, Gnehm H, Kind H, Prader A. Quantification of bone mineralization using computed tomography. Radiology 1976; 121 (01) 93-97
• 2 Dambacher MA, Neff M, Kissling R, Qin L. Highly precise peripheral quantitative computed tomography for the evaluation of bone density, loss of bone density and structures. Consequences for prophylaxis and treatment. Drugs Aging 1998; 12 (Suppl. 01) 15-24
• 3 Dambacher MA, Kranich M, Schacht E, Neff M. Can the fast bone loss in osteoporotic and osteopenic patients be stopped with active vitamin D metabolites?. Calcif Tissue Int 1997; 60 (01) 115-118
• 4 Zanetti M, Romero J, Dambacher MA, Hodler J. Osteonecrosis diagnosed on MR images of the knee. Relationship to reduced bone mineral density determined by high resolution peripheral quantitative CT. Acta Radiol 2003; 44 (05) 525-531
• 5 Tran DM, Vilayphiou N, Koller B. Clinical in vivo assessment of bone microarchitecture with CT scanners: an enduring challenge. J Bone Miner Res 2020; 35 (02) 415-416
• 6 Cheung AM, Adachi JD, Hanley DA. et al. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep 2013; 11 (02) 136-146
• 7 Nishiyama KK, Shane E. Clinical imaging of bone microarchitecture with HR-pQCT. Curr Osteoporos Rep 2013; 11 (02) 147-155
• 8 Lespessailles E, Ibrahim-Nasser N, Toumi H, Chapurlat R. Contribution of high resolution peripheral quantitative CT to the management of bone and joint diseases. Joint Bone Spine 2018; 85 (03) 301-306
• 9 Ohs N, Collins CJ, Atkins PR. Validation of HR-pQCT against micro-CT for morphometric and biomechanical analyses: a review. Bone Rep 2020; 13: 100711
• 10 Boyd SK. High-resolution peripheral quantitative computed tomography in rheumatic diseases: a new option for knee osteoarthritis. Radiol Clin North Am
• 11 van den Bergh JP, Szulc P, Cheung AM, Bouxsein M, Engelke K, Chapurlat R. The clinical application of high-resolution peripheral computed tomography (HR-pQCT) in adults: state of the art and future directions. Osteoporos Int 2021; 32 (08) 1465-1485
• 12 Mikolajewicz N, Bishop N, Burghardt AJ. et al. HR-pQCT measures of bone microarchitecture predict fracture: systematic review and meta-analysis. J Bone Miner Res 2020; 35 (03) 446-459
• 13 Whittier DE, Boyd SK, Burghardt AJ. et al. Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int 2020; 31 (09) 1607-1627
• 14 Whittier DE, Mudryk AN, Vandergaag ID, Burt LA, Boyd SK. Optimizing HR-pQCT workflow: a comparison of bias and precision error for quantitative bone analysis. Osteoporos Int 2020; 31 (03) 567-576
• 15 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 2017; 97: 43-48
• 16 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 2005; 90 (12) 6508-6515
• 17 Gabel L, Liphardt AM, Hulme PA. et al. Pre-flight exercise and bone metabolism predict unloading-induced bone loss due to spaceflight. Br J Sports Med 2022; 56 (04) 196-203
• 18 Klose-Jensen R, Tse JJ, Keller KK. et al. High-resolution peripheral quantitative computed tomography for bone evaluation in inflammatory rheumatic disease. Front Med (Lausanne) 2020; 7: 337
• 19 Manske SL, Brunet SC, Finzel S. et al; The SPECTRA Collaboration OMERACT Working Group. The SPECTRA Collaboration OMERACT Working Group: Construct validity of joint space outcomes with high-resolution peripheral quantitative computed tomography. J Rheumatol 2019; 46 (10) 1369-1373
• 20 Kroker A, Besler BA, Bhatla JL. et al. Longitudinal effects of acute anterior cruciate ligament tears on peri-articular bone in human knees within the first year of injury. J Orthop Res 2019; 37 (11) 2325-2336
• 21 Shiraishi K, Chiba K, Okazaki N. et al. In vivo analysis of subchondral trabecular bone in patients with osteoarthritis of the knee using second-generation high-resolution peripheral quantitative computed tomography (HR-pQCT). Bone 2020; 132: 115155
• 22 Sada K, Chiba K, Kajiyama S. et al. Bone mineral density and microstructure of the elbow in baseball pitchers: an analysis by second-generation HR-pQCT. J Clin Densitom 2020; 23 (02) 322-328
• 23 Stürznickel J, Schmidt FN, Schäfer HS. et al. Bone microarchitecture of the distal fibula assessed by HR-pQCT. Bone 2021; 151: 116057
• 24 Rogers JA, Jones G, Cook J. et al. Chronic plantar heel pain modifies associations of ankle plantarflexor strength and body mass index with calcaneal bone density and microarchitecture. PLoS One 2021; 16 (12) e0260925
• 25 Hildebrand KN, Sidhu K, Gabel L, Besler BA, Burt LA, Boyd SK. The assessment of skeletal muscle and cortical bone by second-generation HR-pQCT at the tibial midshaft. J Clin Densitom 2021; 24 (03) 465-473
• 26 Erlandson MC, Wong AKO, Szabo E. et al. Muscle and myotendinous tissue properties at the distal tibia as assessed by high-resolution peripheral quantitative computed tomography. J Clin Densitom 2017; 20 (02) 226-232
• 27 Patsch JM, Zulliger MA, Vilayphou N. et al. Quantification of lower leg arterial calcifications by high-resolution peripheral quantitative computed tomography. Bone 2014; 58: 42-47
• 28 Paccou J, Edwards MH, Patsch JM. et al. Lower leg arterial calcification assessed by high-resolution peripheral quantitative computed tomography is associated with bone microstructure abnormalities in women. Osteoporos Int 2016; 27 (11) 3279-3287
• 29 Chiba K, Burghardt AJ, Osaki M, Majumdar S. Three-dimensional analysis of subchondral cysts in hip osteoarthritis: an ex vivo HR-pQCT study. Bone 2014; 66: 140-145
• 30 Boyd SK. Site-specific variation of bone micro-architecture in the distal radius and tibia. J Clin Densitom 2008; 11 (03) 424-430
• 31 Agarwal S, Rosete F, Zhang C. et al. In vivo assessment of bone structure and estimated bone strength by first- and second-generation HR-pQCT. Osteoporos Int 2016; 27 (10) 2955-2966
• 32 Bugbird AR, Klassen RE, Bruce OL, Burt LA, Edwards WB, Boyd SK. Fixed and relative positioning of scans for high resolution peripheral quantitative computed tomography. J Clin Densitom 2024; 27 (01) 101462
• 33 Gabel L, Kent K, Hosseinitabatabaei S. et al. Recommendations for high-resolution peripheral quantitative computed tomography assessment of bone density, microarchitecture, and strength in pediatric populations. Curr Osteoporos Rep 2023; 21 (05) 609-623
• 34 Keen CE, Whittier DE, Firminger CR, Edwards WB, Boyd SK. Validation of bone density and microarchitecture measurements of the load-bearing femur in the human knee obtained using in vivo HR-pQCT protocol. J Clin Densitom 2021; 24 (04) 651-657
• 35 Yamada S, Chiba K, Okazaki N. et al. Correlation between vertebral bone microstructure and estimated strength in elderly women: an ex-vivo HR-pQCT study of cadaveric spine. Bone 2019; 120: 459-464
• 36 Michalak GJ, Walker R, Boyd SK. Concurrent assessment of cartilage morphology and bone microarchitecture in the human knee using contrast-enhanced HR-pQCT imaging. J Clin Densitom 2019; 22 (01) 74-85
• 37 Mueller TL, Basler SE, Müller R, van Lenthe GH. Time-lapsed imaging of implant fixation failure in human femoral heads. Med Eng Phys 2013; 35 (05) 636-643
• 38 Rolvien T, Friesecke C, Butscheidt S, Gehrke T, Hahn M, Püschel K. A novel, multi-level approach to assess allograft incorporation in revision total hip arthroplasty. Sci Rep 2020; 10 (01) 15226
• 39 Trope GD, Ghasem-Zadeh A, Anderson GA, Mackie EJ, Whitton RC. Can high-resolution peripheral quantitative computed tomography imaging of subchondral and cortical bone predict condylar fracture in thoroughbred racehorses?. Equine Vet J 2015; 47 (04) 428-432
• 40 Krause M, Oheim R, Catala-Lehnen P. et al. Metaphyseal bone formation induced by a new injectable β-TCP-based bone substitute: a controlled study in rabbits. J Biomater Appl 2014; 28 (06) 859-868
• 41 Sode M, Burghardt AJ, Pialat JB, Link TM, Majumdar S. Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone 2011; 48 (06) 1291-1297
• 42 Pauchard Y, Liphardt AM, Macdonald HM, Hanley DA, Boyd SK. Quality control for bone quality parameters affected by subject motion in high-resolution peripheral quantitative computed tomography. Bone 2012; 50 (06) 1304-1310
• 43 Pauchard Y, Ayres FJ, Boyd SK. Automated quantification of three-dimensional subject motion to monitor image quality in high-resolution peripheral quantitative computed tomography. Phys Med Biol 2011; 56 (20) 6523-6543
• 44 Benedikt S, Zelger P, Horling L. et al. Deep convolutional neural networks provide motion grading for high-resolution peripheral quantitative computed tomography of the scaphoid. Diagnostics (Basel) 2024; 14 (05) 568
• 45 Walle M, Eggemann D, Atkins PR. et al. Motion grading of high-resolution quantitative computed tomography supported by deep convolutional neural networks. Bone 2023; 166: 116607
• 46 Brunet SC, Kuczynski MT, Bhatla JL. et al. The utility of multi-stack alignment and 3D longitudinal image registration to assess bone remodeling in rheumatoid arthritis patients from second generation HR-pQCT scans. BMC Med Imaging 2020; 20 (01) 36
• 47 Whittier DE, Walle M, Schenk D. et al. A multi-stack registration technique to improve measurement accuracy and precision across longitudinal HR-pQCT scans. Bone 2023; 176: 116893
• 48 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 2007; 41 (04) 505-515
• 49 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 2010; 47 (03) 519-528
• 50 Valentinitsch A, Patsch JM, Deutschmann J. et al. Automated threshold-independent cortex segmentation by 3D-texture analysis of HR-pQCT scans. Bone 2012; 51 (03) 480-487
• 51 Neeteson NJ, Besler BA, Whittier DE, Boyd SK. Automatic segmentation of trabecular and cortical compartments in HR-pQCT images using an embedding-predicting U-Net and morphological post-processing. Sci Rep 2023; 13 (01) 252
• 52 Nishiyama KK, Pauchard Y, Nikkel LE. et al. Longitudinal HR-pQCT and image registration detects endocortical bone loss in kidney transplantation patients. J Bone Miner Res 2015; 30 (03) 554-561
• 53 Boyd SK, Szabo E, Ammann P. Increased bone strength is associated with improved bone microarchitecture in intact female rats treated with strontium ranelate: a finite element analysis study. Bone 2011; 48 (05) 1109-1116
• 54 Sadoughi S, Subramanian A, Ramil G, Burghardt AJ, Kazakia GJ. A Laplace-Hamming binarization approach for second-generation HR-pQCT rescues fine feature segmentation. J Bone Miner Res 2023; 38 (07) 1006-1014
• 55 Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc 1997; 185 (01) 67-75
• 56 Manske SL, Zhu Y, Sandino C, Boyd SK. Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone 2015; 79: 213-221
• 57 Manske SL, Davison EM, Burt LA, Raymond DA, Boyd SK. The estimation of second-generation HR-pQCT from first-generation HR-pQCT using in vivo cross-calibration. J Bone Miner Res 2017; 32 (07) 1514-1524
• 58 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 1995; 28 (01) 69-81
• 59 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 2008; 42 (06) 1203-1213
• 60 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 2018; 80: 63-71
• 61 Arias-Moreno AJ, Hosseini HS, Bevers M, Ito K, Zysset P, van Rietbergen B. Validation of distal radius failure load predictions by homogenized- and micro-finite element analyses based on second-generation high-resolution peripheral quantitative CT images. Osteoporos Int 2019; 30 (07) 1433-1443
• 62 Varga P, Baumbach S, Pahr D, Zysset PK. Validation of an anatomy specific finite element model of Colles' fracture. J Biomech 2009; 42 (11) 1726-1731
• 63 Samelson EJ, Broe KE, Xu H. et al. Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the Bone Microarchitecture International Consortium (BoMIC): a prospective study. Lancet Diabetes Endocrinol 2019; 7 (01) 34-43
• 64 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 2010; 25 (04) 882-890
• 65 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 2013; 54 (01) 8-20
• 66 Jorgenson BL, Buie HR, McErlain DD, Sandino C, Boyd SK. A comparison of methods for in vivo assessment of cortical porosity in the human appendicular skeleton. Bone 2015; 73: 167-175
• 67 Liu XS, Cohen A, Shane E. et al. 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 2010; 25 (07) 1496-1505
• 68 Liu XS, Stein EM, Zhou B. et al. 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 2012; 27 (02) 263-272
• 69 Whittier DE, Burt LA, Boyd SK. A new approach for quantifying localized bone loss by measuring void spaces. Bone 2021; 143: 115785
• 70 Whittier DE, Samelson EJ, Hannan MT. et al. Bone microarchitecture phenotypes identified in older adults are associated with different levels of osteoporotic fracture risk. J Bone Miner Res 2022; 37: 428-439
• 71 Edwards MH, Robinson DE, Ward KA. et al. Cluster analysis of bone microarchitecture from high resolution peripheral quantitative computed tomography demonstrates two separate phenotypes associated with high fracture risk in men and women. Bone 2016; 88: 131-137
• 72 Whittier DE, Manske SL, Billington E. et al. Hip fractures in older adults are associated with the low density bone phenotype and heterogeneous deterioration of bone microarchitecture. J Bone Miner Res 2022; 37 (10) 1963-1972
• 73 Walle M, Whittier DE, Schenk D. et al. Precision of bone mechanoregulation assessment in humans using longitudinal high-resolution peripheral quantitative computed tomography in vivo. Bone 2023; 172: 116780
• 74 Warden SJ, Liu Z, Fuchs RK, van Rietbergen B, Moe SM. Reference data and calculators for second-generation HR-pQCT measures of the radius and tibia at anatomically standardized regions in White adults. Osteoporos Int 2022; 33 (04) 791-806
• 75 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
• 76 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 2020; 35 (11) 2151-2158
• 77 Kemp TD, de Bakker CMJ, Gabel L. et al. Longitudinal bone microarchitectural changes are best detected using image registration. Osteoporos Int 2020; 31 (10) 1995-2005
• 78 Boyd SK, Moser S, Kuhn M. et al. Evaluation of three-dimensional image registration methodologies for in vivo micro-computed tomography. Ann Biomed Eng 2006; 34 (10) 1587-1599
• 79 Hosseinitabatabaei S, Mikolajewicz N, Zimmermann EA. et al. 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 2022; 37 (05) 908-924
• 80 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 2019; 322 (08) 736-745
• 81 Burt LA, Gabel L, Billington EO, Hanley DA, Boyd SK. Response to high-dose vitamin d supplementation is specific to imaging modality and skeletal site. JBMR Plus 2022; 6 (05) e10615
• 82 Mikolajewicz N, Zimmermann EA, Rummler M. et al. Multisite longitudinal calibration of HR-pQCT scanners and precision in osteogenesis imperfecta. Bone 2021; 147: 115880
• 83 Burghardt AJ, Pialat JB, Kazakia GJ. et al. Multicenter precision of cortical and trabecular bone quality measures assessed by high-resolution peripheral quantitative computed tomography. J Bone Miner Res 2013; 28 (03) 524-536
• 84 Lewiecki EM, Binkley N. DXA: 30 years and counting: Introduction to the 30th anniversary issue. Bone 2017; 104: 1-3
• 85 Miller PD. The history of bone densitometry. Bone 2017; 104: 4-6
• 86 Miller PD, Bonnick SL, Rosen C. Society for Clinical Densitometry. Guidelines for the clinical utilization of bone mass measurement in the adult population. Calcif Tissue Int 1995; 57 (04) 251-252
• 87 Miller PD, Bonnick SL, Rosen CJ. Consensus of an international panel on the clinical utility of bone mass measurements in the detection of low bone mass in the adult population. Calcif Tissue Int 1996; 58 (04) 207-214
• 88 Miller PD, Bonnick SL, Rosen CJ. et al; The Society for Clinical Densitometry. Clinical utility of bone mass measurements in adults: consensus of an international panel. Semin Arthritis Rheum 1996; 25 (06) 361-372
• 89 Genant HK, Wu CY, van Kuijk C, Nevitt MC. Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 1993; 8 (09) 1137-1148
• 90 Beck TJ, Ruff CB, Warden KE, Scott Jr WW, Rao GU. Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol 1990; 25 (01) 6-18
• 91 Harvey NC, Glüer CC, Binkley N. et al. Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 2015; 78: 216-224
• 92 Glüer CC. 30 years of DXA technology innovations. Bone 2017; 104: 7-12
• 93 Wainwright SA, Marshall LM, Ensrud KE. et al; Study of Osteoporotic Fractures Research Group. Hip fracture in women without osteoporosis. J Clin Endocrinol Metab 2005; 90 (05) 2787-2793
• 94 Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E. FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int 2008; 19 (04) 385-397
• 95 Bolland MJ, Siu AT, Mason BH. et al. Evaluation of the FRAX and Garvan fracture risk calculators in older women. J Bone Miner Res 2011; 26 (02) 420-427
• 96 Hippisley-Cox J, Coupland C. Derivation and validation of updated QFracture algorithm to predict risk of osteoporotic fracture in primary care in the United Kingdom: prospective open cohort study. BMJ 2012; 344: e3427
• 97 Leslie WD, Berger C, Langsetmo L. et al; Canadian Multicentre Osteoporosis Study Research Group. Construction and validation of a simplified fracture risk assessment tool for Canadian women and men: results from the CaMos and Manitoba cohorts. Osteoporos Int 2011; 22 (06) 1873-1883
• 98 Morin SN, Feldman S, Funnell L. et al; Osteoporosis Canada 2023 Guideline Update Group. Clinical practice guideline for management of osteoporosis and fracture prevention in Canada: 2023 update. CMAJ 2023; 195 (39) E1333-E1348
• 99 Curry SJ, Krist AH, Owens DK. et al; US Preventive Services Task Force. Screening for osteoporosis to prevent fractures: US Preventive Services Task Force recommendation statement. JAMA 2018; 319 (24) 2521-2531
• 100 Ensrud KE, Crandall CJ. Osteoporosis. Ann Intern Med 2024; 177 (01) ITC1-ITC16
• 101 Rubin KH, Friis-Holmberg T, Hermann AP, Abrahamsen B, Brixen K. Risk assessment tools to identify women with increased risk of osteoporotic fracture: complexity or simplicity? A systematic review. J Bone Miner Res 2013; 28 (08) 1701-1717
• 102 Beaudoin C, Moore L, Gagné M. et al. Performance of predictive tools to identify individuals at risk of non-traumatic fracture: a systematic review, meta-analysis, and meta-regression. Osteoporos Int 2019; 30 (04) 721-740
• 103 Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone 2007; 41 (01) 138-154
• 104 Kanis JA, Oden A, Johnell O. et al. The use of clinical risk factors enhances the performance of BMD in the prediction of hip and osteoporotic fractures in men and women. Osteoporos Int 2007; 18 (08) 1033-1046
• 105 Curtis EM, Moon RJ, Harvey NC, Cooper C. The impact of fragility fracture and approaches to osteoporosis risk assessment worldwide. Bone 2017; 104: 29-38
• 106 McCloskey EV, Odén A, Harvey NC. et al. A meta-analysis of Trabecular Bone Score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 2016; 31 (05) 940-948
• 107 Shevroja E, Reginster JY, Lamy O. et al. Update on the clinical use of trabecular bone score (TBS) in the management of osteoporosis: results of an expert group meeting organized by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO), and the International Osteoporosis Foundation (IOF) under the auspices of WHO Collaborating Center for Epidemiology of Musculoskeletal Health and Aging. Osteoporos Int 2023; 34 (09) 1501-1529
• 108 Kanis JA, Borgström F, Compston J. et al. SCOPE: a scorecard for osteoporosis in Europe. Arch Osteoporos 2013; 8 (01) 144
• 109 Burt LA, Hanley DA, Boyd SK. Cross-sectional versus longitudinal change in a prospective HR-pQCT study. J Bone Miner Res 2017; 32 (07) 1505-1513
• 110 Liu XS, Cohen A, Shane E. et al. 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 2010; 25 (10) 2229-2238
• 111 Nishi K, Endo D, Hasegawa T. et al. Similarities and differences in bone mineral density between multiple sites in the same individual: an elderly cadaveric study. BioMed Res Int 2022; 2022: 6094663
• 112 Cohen A, Dempster DW, Müller R. et al. Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos Int 2010; 21 (02) 263-273
• 113 Marques ID, Araújo MJ, Graciolli FG. et al. Biopsy vs. peripheral computed tomography to assess bone disease in CKD patients on dialysis: differences and similarities. Osteoporos Int 2017; 28 (05) 1675-1683
• 114 Kroker A, Plett R, Nishiyama KK, McErlain DD, Sandino C, Boyd SK. Distal skeletal tibia assessed by HR-pQCT is highly correlated with femoral and lumbar vertebra failure loads. J Biomech 2017; 59: 43-49
• 115 Whittier DE, Samelson EJ, Hannan MT. et al. A fracture risk assessment tool for high resolution peripheral quantitative computed tomography. J Bone Miner Res 2023; 38 (09) 1234-1244
• 116 Bugbird AR, Whittier DE, Boyd SK. Transferability of bone phenotyping and fracture risk assessment by μFRAC from first-generation high-resolution peripheral quantitative computed tomography to second-generation scan data. J Bone Miner Res 2024; 39 (05) 571-579
• 117 Cook NR. Use and misuse of the receiver operating characteristic curve in risk prediction. Circulation 2007; 115 (07) 928-935
• 118 Donaldson MG, Cawthon PM, Schousboe JT. et al; Study of Osteoporotic Fractures (SOF). Novel methods to evaluate fracture risk models. J Bone Miner Res 2011; 26 (08) 1767-1773
• 119 Pepe MS, Feng Z, Huang Y. et al. Integrating the predictiveness of a marker with its performance as a classifier. Am J Epidemiol 2008; 167 (03) 362-368
• 120 Liew D, Chapurlat RD, Sornay-Rendu E, Lespessailles E, Peng Y, Seeman E. Cost-effectiveness of treatment of women aged 70 years and older with both osteopenia and microstructural deterioration. Bone 2021; 142: 115682
• 121 Poole KES, Chappell DDG, Clark E. et al. PHOENIX (Picking up Hidden Osteoporosis Effectively during Normal CT Imaging without additional X-rays): protocol for a randomised, multicentre feasibility study. BMJ Open 2022; 12 (05) e050343
• 122 Bevers MSAM, Daniels AM, Wyers CE. et al. The feasibility of high-resolution peripheral quantitative computed tomography (HR-pQCT) in patients with suspected scaphoid fractures. J Clin Densitom 2020; 23 (03) 432-442
• 123 Khan A, Weinstein Z, Hanley DA. et al. In vivo bone architecture in Pompe disease using high-resolution peripheral computed tomography. JIMD Rep 2013; 7: 81-88
• 124 Alvarenga JC, Fuller H, Pasoto SG, Pereira RM. Age-related reference curves of volumetric bone density, structure, and biomechanical parameters adjusted for weight and height in a population of healthy women: an HR-pQCT study. Osteoporos Int 2017; 28 (04) 1335-1346
• 125 Alvarenga JC, Caparbo VF, Domiciano DS, Pereira RMR. Age-related reference data of bone microarchitecture, volumetric bone density, and bone strength parameters in a population of healthy Brazilian men: an HR-pQCT study. Osteoporos Int 2022; 33 (06) 1309-1321
• 126 Hansen S, Shanbhogue V, Folkestad L, Nielsen MM, 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 Tissue Int 2014; 94 (03) 269-281
• 127 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 HR-pQCT study. J Bone Miner Res 2011; 26 (01) 50-62
• 128 Zhu TY, Yip BH, Hung VW. et al. Normative standards for HRpQCT parameters in Chinese men and women. J Bone Miner Res 2018; 33 (10) 1889-1899
• 129 Hung VW, Zhu TY, Cheung WH. et al. Age-related differences in volumetric bone mineral density, microarchitecture, and bone strength of distal radius and tibia in Chinese women: a high-resolution pQCT reference database study. Osteoporos Int 2015; 26 (06) 1691-1703
• 130 Khosla S, Melton III LJ, Achenbach SJ, Oberg AL, Riggs BL. Hormonal and biochemical determinants of trabecular microstructure at the ultradistal radius in women and men. J Clin Endocrinol Metab 2006; 91 (03) 885-891
• 131 Dalzell N, Kaptoge S, Morris N. et al. 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 2009; 20 (10) 1683-1694
• 132 Koy EHS, Amouzougan A, Biver E. et al. Reference microarchitectural values measured by HR-pQCT in a Franco-Swiss cohort of young adult women. Osteoporos Int 2022; 33 (03) 703-709
• 133 Stuck AK, Schenk D, Zysset P, Bütikofer L, Mathis A, Lippuner K. Reference values and clinical predictors of bone strength for HR-pQCT-based distal radius and tibia strength assessments in women and men. Osteoporos Int 2020; 31 (10) 1913-1923
• 134 Yu F, Xu Y, Hou Y. et al. Age-, site-, and sex-specific normative centile curves for HR-pQCT-derived microarchitectural and bone strength parameters in a Chinese mainland population. J Bone Miner Res 2020; 35 (11) 2159-2170
• 135 Yokota K, Chiba K, Okazaki N. et al. Deterioration of bone microstructure by aging and menopause in Japanese healthy women: analysis by HR-pQCT. J Bone Miner Metab 2020; 38 (06) 826-838
• 136 Burt LA, Macdonald HM, Hanley DA, Boyd SK. Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch Osteoporos 2014; 9: 183
• 137 Gabel L, Macdonald HM, Nettlefold LA, McKay HA. Sex-, ethnic-, and age-specific centile curves for pQCT- and HR-pQCT-derived measures of bone structure and strength in adolescents and young adults. J Bone Miner Res 2018; 33 (06) 987-1000