Relationships of Ultrasonic Backscatter With Bone Densities and Microstructure in Bovine Cancellous Bone

This study was designed to investigate the associations among ultrasonic backscatter, bone densities, and microstructure in bovine cancellous bone. Ultrasonic backscatter measurements were performed on 33 bovine cancellous bone specimens with a 2.25-MHz transducer. Ultrasonic apparent backscatter parameters (“apparent” means not compensating for ultrasonic attenuation and diffraction) were calculated with optimal signals of interest. The results showed that ultrasonic backscatter was significantly related to bone densities and microstructure (<inline-formula> <tex-math notation="LaTeX">$R^{2} = 0.17$ </tex-math></inline-formula>–0.88 and <inline-formula> <tex-math notation="LaTeX">$p < 0.05$ </tex-math></inline-formula>). After adjusting the correlations by bone mineral density (BMD), the bone apparent density (BAD) and some trabecular structural features still contributed significantly to the adjusted correlations, with moderate additional variance explained (<inline-formula> <tex-math notation="LaTeX">$\Delta R^{2} = 9.7$ </tex-math></inline-formula>% at best). Multiple linear regressions revealed that both BAD and trabecular structure contributed significantly and independently to the prediction of ultrasound backscatter (adjusted <inline-formula> <tex-math notation="LaTeX">$R^{2} = 0.75$ </tex-math></inline-formula>–0.89 and <inline-formula> <tex-math notation="LaTeX">$p < 0.05$ </tex-math></inline-formula>), explaining an additional 14% of the variance at most, compared with that of BMD measurements alone. The results proved that ultrasonic backscatter was primarily determined by BAD, not BMD, but the combination of bone structure and densities could achieve encouragingly better performances (89% of the variance explained at best) in predicting backscatter properties. This study demonstrated that ultrasonic apparent backscatter might provide additional density and structural features unrelated to current BMD measurement. Therefore, we suggest that ultrasonic backscatter measurement could play a more important role in cancellous bone evaluation.

[1]  P. Chieng,et al.  Prevalence of Osteoporosis and Low Bone Mass in Older Chinese Population Based on Bone Mineral Density at Multiple Skeletal Sites , 2016, Scientific Reports.

[2]  F. Peyrin,et al.  Prediction of backscatter coefficient in trabecular bones using a numerical model of three-dimensional microstructure. , 2003, The Journal of the Acoustical Society of America.

[3]  Rachid Jennane,et al.  Biomedical Signal Processing and Control , 2013 .

[4]  Juha Töyräs,et al.  Ultrasound backscatter imaging provides frequency-dependent information on structure, composition and mechanical properties of human trabecular bone. , 2009, Ultrasound in medicine & biology.

[5]  Brian S Garra,et al.  Measurements of ultrasonic backscattered spectral centroid shift from spine in vivo: methodology and preliminary results. , 2009, Ultrasound in medicine & biology.

[6]  A. Hosokawa Numerical analysis of ultrasound backscattered waves in cancellous bone using a finite-difference time-domain method: isolation of the backscattered waves from various ranges of bone depths , 2015, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[7]  D. Keedy,et al.  Ultrasonic characterization of human cancellous bone in vitro using three different apparent backscatter parameters in the frequency range 0.6-15.0 mhz , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[8]  S. Chatterjee,et al.  Influential Observations, High Leverage Points, and Outliers in Linear Regression , 1986 .

[9]  S. L. Bridal,et al.  Singular spectrum analysis applied to backscattered ultrasound signals from in vitro human cancellous bone specimens , 2004, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[10]  Francesco Conversano,et al.  Major osteoporotic fragility fractures: Risk factor updates and societal impact. , 2016, World journal of orthopedics.

[11]  G. Berger,et al.  Absolute backscatter coefficient over a wide range of frequencies in a tissue-mimicking phantom containing two populations of scatterers , 1996, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[12]  Tina M. Willson,et al.  The clinical epidemiology of male osteoporosis: a review of the recent literature , 2015, Clinical epidemiology.

[13]  S. Kaste,et al.  Ultrasonic characterization of cancellous bone using apparent integrated backscatter , 2006, Physics in medicine and biology.

[14]  Katsunori Mizuno,et al.  The relationship between ultrasonic backscatter and trabecular anisotropic microstructure in cancellous bone , 2014 .

[15]  Ying Li,et al.  An Ultrasonic Backscatter Instrument for Cancellous Bone Evaluation in Neonates , 2015 .

[16]  C. Langton,et al.  Bone volume fraction and structural parameters for estimation of mechanical stiffness and failure load of human cancellous bone samples; in-vitro comparison of ultrasound transit time spectroscopy and X-ray μCT. , 2018, Bone.

[17]  B. Hoffmeister Frequency dependence of apparent ultrasonic backscatter from human cancellous bone , 2011, Physics in medicine and biology.

[18]  Yi-Xian Qin,et al.  Prediction of trabecular bone principal structural orientation using quantitative ultrasound scanning. , 2012, Journal of biomechanics.

[19]  D. Ta,et al.  Analysis of apparent integrated backscatter coefficient and backscattered spectral centroid shift in Calcaneus in vivo for the ultrasonic evaluation of osteoporosis. , 2014, Ultrasound in medicine & biology.

[20]  Weiqi Wang,et al.  Analysis of frequency dependence of ultrasonic backscatter coefficient in cancellous bone. , 2008, The Journal of the Acoustical Society of America.

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

[22]  B. Hoffmeister,et al.  Effect of intervening tissues on ultrasonic backscatter measurements of bone: An in vitro study. , 2015, The Journal of the Acoustical Society of America.

[23]  Rachid Harba,et al.  Anisotropy changes in post-menopausal osteoporosis: characterization by a new index applied to trabecular bone radiographic images , 2005, Osteoporosis International.

[24]  R. Nuti,et al.  Treatment needs and current options for postmenopausal osteoporosis , 2016, Expert opinion on pharmacotherapy.

[25]  F. Padilla,et al.  Femur ultrasound (FemUS)—first clinical results on hip fracture discrimination and estimation of femoral BMD , 2010, Osteoporosis International.

[26]  C. Langton,et al.  The measurement of broadband ultrasonic attenuation in cancellous bone. , 1984, Engineering in medicine.

[27]  G. Breart,et al.  Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study , 1996, The Lancet.

[28]  A. Moayyeri,et al.  Predictive ability of heel quantitative ultrasound for incident fractures: an individual-level meta-analysis , 2015, Osteoporosis International.

[29]  TOR Hildebrand,et al.  Quantification of Bone Microarchitecture with the Structure Model Index. , 1997, Computer methods in biomechanics and biomedical engineering.

[30]  Pascal Laugier,et al.  Estimation of Trabecular Thickness Using Ultrasonic Backcatter , 2006, Ultrasonic imaging.

[31]  D. Ta,et al.  Signal of Interest Selection Standard for Ultrasonic Backscatter in Cancellous Bone Evaluation. , 2015, Ultrasound in medicine & biology.

[32]  N. Otsu A threshold selection method from gray level histograms , 1979 .

[33]  P. Laugier,et al.  Influence of the precision of spectral backscatter measurements on the estimation of scatterers size in cancellous bone. , 2004, Ultrasonics.

[34]  K. Wear,et al.  Characterization of trabecular bone using the backscattered spectral centroid shift , 2003, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[35]  Juha Töyräs,et al.  Ultrasonic characterization of human trabecular bone microstructure , 2006, Physics in medicine and biology.

[36]  D. Cocchi,et al.  New understanding and treatments for osteoporosis , 2012, Endocrine.

[37]  D. Ta,et al.  Measurement of the Human Calcaneus In Vivo Using Ultrasonic Backscatter Spectral Centroid Shift , 2016, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[38]  K. Il Lee,et al.  Frequency-dependent attenuation and backscatter coefficients in bovine trabecular bone from 0.2 to 1.2 MHz. , 2012, The Journal of the Acoustical Society of America.

[39]  J Töyräs,et al.  Spatial variation of acoustic properties is related with mechanical properties of trabecular bone , 2007, Physics in medicine and biology.

[40]  A. Laib,et al.  The dependence of ultrasonic backscatter on trabecular thickness in human calcaneus: theoretical and experimental results , 2003, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[41]  C. M. Langton,et al.  The role of ultrasound in the assessment of osteoporosis: A review , 2005, Osteoporosis International.

[42]  I. Kiviranta,et al.  Prediction of density and mechanical properties of human trabecular bone in vitro by using ultrasound transmission and backscattering measurements at 0.2–6.7 MHz frequency range , 2005, Physics in medicine and biology.

[43]  F Peyrin,et al.  Relationships of trabecular bone structure with quantitative ultrasound parameters: in vitro study on human proximal femur using transmission and backscatter measurements. , 2008, Bone.

[44]  F. Blyth,et al.  Managing osteoporosis with FRAX® in Australia: proposed new treatment thresholds from the 45&Up Study cohort. , 2014, Bone.

[45]  K. Wear,et al.  Relationships of ultrasonic backscatter with ultrasonic attenuation, sound speed and bone mineral density in human calcaneus. , 2000, Ultrasound in medicine & biology.

[46]  D. Deligianni,et al.  Influence of microarchitecture alterations on ultrasonic backscattering in an experimental simulation of bovine cancellous bone aging. , 2008, The Journal of the Acoustical Society of America.

[47]  J. Litniewski,et al.  Statistics of the envelope of ultrasonic backscatter from human trabecular bone. , 2011, The Journal of the Acoustical Society of America.

[48]  J. P. Karjalainen,et al.  Multi-site bone ultrasound measurements in elderly women with and without previous hip fractures , 2012, Osteoporosis International.

[49]  J. Rho,et al.  Low-megahertz ultrasonic properties of bovine cancellous bone. , 2000, Bone.

[50]  J. Currey,et al.  Prediction of mechanical properties of the human calcaneus by broadband ultrasonic attenuation. , 1996, Bone.

[51]  Lorenz C. Hofbauer Osteoporosis: now and the future , 2013 .

[52]  J Töyräs,et al.  Ultrasound backscatter measurements of intact human proximal femurs--relationships of ultrasound parameters with tissue structure and mineral density. , 2014, Bone.

[53]  L. Le,et al.  The analysis and compensation of cortical thickness effect on ultrasonic backscatter signals in cancellous bone , 2014 .

[54]  M. Dreher,et al.  Relationships of quantitative ultrasound parameters with cancellous bone microstructure in human calcaneus in vitro. , 2012, The Journal of the Acoustical Society of America.

[55]  S. Majumdar,et al.  Ultrasound Velocity of Trabecular Cubes Reflects Mainly Bone Density and Elasticity , 2014, Calcified Tissue International.

[56]  K. Wear,et al.  Ultrasonic scattering from cancellous bone: A review , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[57]  Srinidhi Nagaraja,et al.  Relationships among ultrasonic and mechanical properties of cancellous bone in human calcaneus in vitro. , 2017, Bone.

[58]  B. Garra,et al.  Assessment of bone density using ultrasonic backscatter. , 1998, Ultrasound in medicine & biology.

[59]  Ralph Müller,et al.  Guidelines for assessment of bone microstructure in rodents using micro–computed tomography , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[60]  Dean Ta,et al.  Effect of selected signals of interest on ultrasonic backscattering measurement in cancellous bones , 2013 .

[61]  P. Andreopoulou,et al.  Management of postmenopausal osteoporosis. , 2015, Annual review of medicine.

[62]  F Peyrin,et al.  Ultrasonic characterization of human cancellous bone using transmission and backscatter measurements: relationships to density and microstructure. , 2002, Bone.

[63]  B. Hoffmeister,et al.  Ultrasonic backscatter from cancellous bone: the apparent backscatter transfer function , 2015, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[64]  Reinhard Barkmann,et al.  Association of Five Quantitative Ultrasound Devices and Bone Densitometry With Osteoporotic Vertebral Fractures in a Population‐Based Sample: The OPUS Study , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[65]  Himadri S. Gupta,et al.  Structure and mechanical quality of the collagen–mineral nano-composite in bone , 2004 .

[66]  Weiqi Wang,et al.  Simplified inverse filter tracking algorithm for estimating the mean trabecular bone spacing , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[67]  Xulei Tang,et al.  High prevalence of vitamin D deficiency among middle-aged and elderly individuals in northwestern China: its relationship to osteoporosis and lifestyle factors. , 2015, Bone.