Ultrasound‐Based Estimates of Cortical Bone Thickness and Porosity Are Associated With Nontraumatic Fractures in Postmenopausal Women: A Pilot Study

Recent ultrasound (US) axial transmission techniques exploit the multimode waveguide response of long bones to yield estimates of cortical bone structure characteristics. This pilot cross‐sectional study aimed to evaluate the performance at the one‐third distal radius of a bidirectional axial transmission technique (BDAT) to discriminate between fractured and nonfractured postmenopausal women. Cortical thickness (Ct.Th) and porosity (Ct.Po) estimates were obtained for 201 postmenopausal women: 109 were nonfractured (62.6 ± 7.8 years), 92 with one or more nontraumatic fractures (68.8 ± 9.2 years), 17 with hip fractures (66.1 ± 10.3 years), 32 with vertebral fractures (72.4 ± 7.9 years), and 17 with wrist fractures (67.8 ± 9.6 years). The areal bone mineral density (aBMD) was obtained using DXA at the femur and spine. Femoral aBMD correlated weakly, but significantly with Ct.Th (R = 0.23, p < 0.001) and Ct.Po (R = ‐0.15, p < 0.05). Femoral aBMD and both US parameters were significantly different between the subgroup of all nontraumatic fractures combined and the control group (p < 0.05). The main findings were that (1) Ct.Po was discriminant for all nontraumatic fractures combined (OR = 1.39; area under the receiver operating characteristic curve [AUC] equal to 0.71), for vertebral (OR = 1.96; AUC = 0.84) and wrist fractures (OR = 1.80; AUC = 0.71), whereas Ct.Th was discriminant for hip fractures only (OR = 2.01; AUC = 0.72); there was a significant association (2) between increased Ct.Po and vertebral and wrist fractures when these fractures were not associated with any measured aBMD variables; (3) between increased Ct.Po and all nontraumatic fractures combined independently of aBMD neck; and (4) between decreased Ct.Th and hip fractures independently of aBMD femur. BDAT variables showed comparable performance to that of aBMD neck with all types of fractures (OR = 1.48; AUC = 0.72) and that of aBMD femur with hip fractures (OR = 2.21; AUC = 0.70). If these results are confirmed in prospective studies, cortical BDAT measurements may be considered useful for assessing fracture risk in postmenopausal women. © 2019 American Society for Bone and Mineral Research.

[1]  Hirofumi Taki,et al.  Rapid High-Resolution Wavenumber Extraction from Ultrasonic Guided Waves Using Adaptive Array Signal Processing , 2018 .

[2]  K. Brixen,et al.  Age‐ and Sex‐Related Changes in Bone Microarchitecture and Estimated Strength: A Three‐Year Prospective Study Using HRpQCT , 2016, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[3]  Gangming Luo,et al.  Clinical assessment of the 1/3 radius using a new desktop ultrasonic bone densitometer. , 2013, Ultrasound in medicine & biology.

[4]  Jean-Gabriel Minonzio,et al.  Impact of attenuation on guided mode wavenumber measurement in axial transmission on bone mimicking plates. , 2011, The Journal of the Acoustical Society of America.

[5]  Jussi Timonen,et al.  Assessment of the cortical bone thickness using ultrasonic guided waves: modelling and in vitro study. , 2007, Ultrasound in medicine & biology.

[6]  Jean-Gabriel Minonzio,et al.  In Vivo Characterization of Cortical Bone Using Guided Waves Measured by Axial Transmission , 2016, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[7]  L. Qin,et al.  Value of Measuring Bone Microarchitecture in Fracture Discrimination in Older Women with Recent Hip Fracture: A Case-control Study with HR-pQCT , 2016, Scientific Reports.

[8]  Steven K Boyd,et al.  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 , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[9]  C. Cooper,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. , 2016, Bone.

[10]  Bert Van Rietbergen,et al.  Finite Element Analysis Based on In Vivo HR‐pQCT Images of the Distal Radius Is Associated With Wrist Fracture in Postmenopausal Women , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[11]  Daniel C Bridges,et al.  Microindentation for In Vivo Measurement of Bone Tissue Mechanical Properties in Humans , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[12]  H K Genant,et al.  A new method for quantitative ultrasound measurements at multiple skeletal sites: first results of precision and fracture discrimination. , 2000, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[13]  J. Nyman,et al.  The Role of Matrix Composition in the Mechanical Behavior of Bone , 2018, Current Osteoporosis Reports.

[14]  M. Bouxsein,et al.  Trabecular and Cortical Microstructure and Fragility of the Distal Radius in Women , 2015, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[15]  M. Matsukawa,et al.  Estimation of in vivo cortical bone thickness using ultrasonic waves , 2015, Journal of Medical Ultrasonics.

[16]  R. Pereira,et al.  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 , 2017, Osteoporosis International.

[17]  Paul D. Miller,et al.  Bone Mineral Density Thresholds for Pharmacological Intervention to Prevent Fractures , 2004 .

[18]  Françoise Peyrin,et al.  Bone microstructure and elastic tissue properties are reflected in QUS axial transmission measurements. , 2005, Ultrasound in medicine & biology.

[19]  B. van Rietbergen,et al.  Age-related changes in bone strength from HR-pQCT derived microarchitectural parameters with an emphasis on the role of cortical porosity. , 2016, Bone.

[20]  T. Jämsä,et al.  Discrimination of fractures by low-frequency axial transmission ultrasound in postmenopausal females , 2012, Osteoporosis International.

[21]  S. Majumdar,et al.  Microarchitecture and Peripheral BMD are Impaired in Postmenopausal White Women With Fracture Independently of Total Hip T‐Score: An International Multicenter Study , 2016, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  Ego Seeman,et al.  Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study , 2010, The Lancet.

[23]  H. Macdonald,et al.  Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT , 2013, Osteoporosis International.

[24]  Françoise Peyrin,et al.  Change in porosity is the major determinant of the variation of cortical bone elasticity at the millimeter scale in aged women. , 2011, Bone.

[25]  Jean-Gabriel Minonzio,et al.  Multichannel processing for dispersion curves extraction of ultrasonic axial-transmission signals: Comparisons and case studies. , 2016, The Journal of the Acoustical Society of America.

[26]  Piet P. Geusens,et al.  Osteoporosis, frailty and fracture: implications for case finding and therapy , 2012, Nature Reviews Rheumatology.

[27]  Didier Hans,et al.  Quantitative Ultrasound (QUS) in the Management of Osteoporosis and Assessment of Fracture Risk. , 2017, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[28]  T. Otani,et al.  Novel ultrasonic bone densitometry based on two longitudinal waves: significant correlation with pQCT measurement values and age-related changes in trabecular bone density, cortical thickness, and elastic modulus of trabecular bone in a normal Japanese population , 2010, Osteoporosis International.

[29]  J. Jurvelin,et al.  New method for point-of-care osteoporosis screening and diagnostics , 2016, Osteoporosis International.

[30]  Ego Seeman,et al.  Role of cortical bone in bone fragility , 2015, Current opinion in rheumatology.

[31]  Ego Seeman,et al.  Cortical Porosity Identifies Women With Osteopenia at Increased Risk for Forearm Fractures , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[32]  M. Popovtzer,et al.  Quantitative ultrasound of the tibia: a novel approach for assessment of bone status. , 1995, Bone.

[33]  Jean-Gabriel Minonzio,et al.  Predicting bone strength with ultrasonic guided waves , 2017, Scientific Reports.

[34]  Sandra Schorlemmer,et al.  The role of cortical bone and its microstructure in bone strength. , 2006, Age and ageing.

[35]  Maryline Talmant,et al.  Modeling the impact of soft tissue on axial transmission measurements of ultrasonic guided waves in human radius. , 2008, The Journal of the Acoustical Society of America.

[36]  P. Delmas,et al.  Bone quality--the material and structural basis of bone strength and fragility. , 2006, The New England journal of medicine.

[37]  P. Delmas,et al.  Severity of Vertebral Fractures Is Associated With Alterations of Cortical Architecture in Postmenopausal Women , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[38]  M. Talmant,et al.  Guided Waves in Cortical Bone , 2011 .

[39]  C. Cooper,et al.  The impact of fragility fracture and approaches to osteoporosis risk assessment worldwide. , 2017, Bone.

[40]  J. Schousboe,et al.  Prediction of hip osteoporosis by DXA using a novel pulse-echo ultrasound device , 2016, Osteoporosis International.

[41]  G. M. Blake,et al.  Multisite Quantitative Ultrasound: Precision, Age- and Menopause-Related Changes, Fracture Discrimination, and T-score Equivalence with Dual-Energy X-ray Absorptiometry , 2001, Osteoporosis International.

[42]  J. Johnston,et al.  Cortical Bone Porosity: What Is It, Why Is It Important, and How Can We Detect It? , 2016, Current Osteoporosis Reports.

[43]  X. Guo,et al.  Deterioration of trabecular plate-rod and cortical microarchitecture and reduced bone stiffness at distal radius and tibia in postmenopausal women with vertebral fractures. , 2016, Bone.

[44]  P. Campistron,et al.  Development of a new ultrasonic technique for bone and biomaterials in vitro characterization. , 2002, Journal of biomedical materials research.

[45]  E. Bossy,et al.  In vivo performance evaluation of bi-directional ultrasonic axial transmission for cortical bone assessment. , 2009, Ultrasound in medicine & biology.

[46]  P. Laugier,et al.  Bone cortical thickness and porosity assessment using ultrasound guided waves: An ex vivo validation study. , 2018, Bone.

[47]  N. Kuriyama,et al.  Decreased cortical thickness, as estimated by a newly developed ultrasound device, as a risk for vertebral fracture in type 2 diabetes mellitus patients with eGFR of less than 60 mL/min/1.73 m2 , 2014, Osteoporosis International.

[48]  E. Seeman,et al.  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. , 2013, Bone.

[49]  J. Kanis,et al.  A precise method for the assessment of tibial ultrasound velocity , 2005, Osteoporosis International.

[50]  Françoise Peyrin,et al.  An In Vitro Study of the Ultrasonic Axial Transmission Technique at the Radius: 1‐MHz Velocity Measurements Are Sensitive to Both Mineralization and Intracortical Porosity , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[51]  H Follet,et al.  Genetic algorithms-based inversion of multimode guided waves for cortical bone characterization , 2016, Physics in medicine and biology.

[52]  Jean-Gabriel Minonzio,et al.  Guided wave phase velocity measurement using multi-emitter and multi-receiver arrays in the axial transmission configuration. , 2010, The Journal of the Acoustical Society of America.

[53]  Jean-Gabriel Minonzio,et al.  Accurate measurement of guided modes in a plate using a bidirectional approach. , 2014, The Journal of the Acoustical Society of America.

[54]  Cathleen S. Colón-Emeric,et al.  Meta-analysis: Excess Mortality After Hip Fracture Among Older Women and Men , 2010, Annals of Internal Medicine.

[55]  Jean-Gabriel Minonzio,et al.  Combined estimation of thickness and velocities using ultrasound guided waves: a pioneering study on in vitro cortical bone samples , 2014, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[56]  R. Shigdel,et al.  Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures. , 2015, Bone.

[57]  Laurence Vico,et al.  High‐Resolution pQCT Analysis at the Distal Radius and Tibia Discriminates Patients With Recent Wrist and Femoral Neck Fractures , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[58]  Yuanyuan Wang,et al.  Measurement of the dispersion and attenuation of cylindrical ultrasonic guided waves in long bone. , 2009, Ultrasound in medicine & biology.

[59]  K. Saag,et al.  Which fractures are most attributable to osteoporosis? , 2011, Journal of clinical epidemiology.

[60]  M. Sacchi,et al.  Imaging ultrasonic dispersive guided wave energy in long bones using linear radon transform. , 2014, Ultrasound in medicine & biology.

[61]  Mauricio D. Sacchi,et al.  Computing dispersion curves of elastic/viscoelastic transversely-isotropic bone plates coupled with soft tissue and marrow using semi-analytical finite element (SAFE) method , 2017, Comput. Biol. Medicine.

[62]  G. H. van Lenthe,et al.  Assessing forearm fracture risk in postmenopausal women , 2010, Osteoporosis International.

[63]  Tommi Kärkkäinen,et al.  Guided ultrasonic waves in long bones: modelling, experiment and in vivo application. , 2002, Physiological measurement.

[64]  Piet Geusens,et al.  Clinical fractures beyond low BMD , 2011 .

[65]  Jacques P. Brown,et al.  Multisite quantitative ultrasound for the prediction of fractures over 5 years of follow‐up: The Canadian Multicentre Osteoporosis Study , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[66]  B. L. Riggs,et al.  Relationship of age to bone microstructure independent of areal bone mineral density , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[67]  E. Lespessailles,et al.  Low-trauma fractures without osteoporosis , 2017, Osteoporosis International.

[68]  P. Moilanen,et al.  Ultrasonic guided waves in bone , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[69]  J. Timonen,et al.  Association between low-frequency ultrasound and hip fractures - comparison with DXA-based BMD , 2014, BMC Musculoskeletal Disorders.

[70]  O. Johnell,et al.  Ten Year Probabilities of Osteoporotic Fractures According to BMD and Diagnostic Thresholds , 2001, Osteoporosis International.

[71]  F. Patat,et al.  Bidirectional axial transmission can improve accuracy and precision of ultrasonic velocity measurement in cortical bone: a validation on test materials , 2004, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[72]  R. Chapurlat,et al.  Bone Microarchitecture Assessed by HR‐pQCT as Predictor of Fracture Risk in Postmenopausal Women: The OFELY Study , 2017, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[73]  M. Rapoport,et al.  Reference Database for Bone Speed of Sound Measurement by a Novel Quantitative Multi-site Ultrasound Device , 2000, Osteoporosis International.

[74]  S. Naili,et al.  Analytical methods to determine the effective mesoscopic and macroscopic elastic properties of cortical bone , 2011, Biomechanics and Modeling in Mechanobiology.