Abstract
This study aims to introduce the protocol for ultrasonic backscatter measurements of musculoskeletal properties based on a novel ultrasonic backscatter bone diagnostic (UBBD) instrument. Dual-energy X-ray absorptiometry (DXA) can be adopted to measure bone mineral density (BMD) in the hip, spine, legs and the whole body. The muscle and fat mass in the legs and the whole body can be also calculated by DXA body composition analysis. Based on the proposed protocol for backscatter measurements by UBBD, ultrasonic backscatter signals can be measured in vivo, deriving three backscatter parameters [apparent integral backscatter (AIB), backscatter signal peak amplitude (BSPA) and the corresponding arrival time (BSPT)]. AIB may provide important diagnostic information about bone properties. BSPA and BSPT may be important indicators of muscle and fat properties. The standardized backscatter measurement protocol of the UBBD instrument may have the potential to evaluate musculoskeletal characteristics, providing help for promoting the application of the backscatter technique in the clinical diagnosis of musculoskeletal disorders (MSDs), such as osteoporosis and muscular atrophy.
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Data, materials and code availability
They were available upon reasonable request to the corresponding authors.
Abbreviations
- MSDs:
-
Musculoskeletal disorders
- DXA:
-
Dual-energy X-ray absorptiometry
- BMD:
-
Bone mineral density
- UBBD:
-
Ultrasonic backscatter bone diagnostic instrument
- AIB:
-
Apparent integral backscatter
- BSPA :
-
Backscatter signal peak amplitude
- BSPT :
-
Backscatter signal peak arrival time
- QUS:
-
Quantitative ultrasound
- SOI:
-
Signal of interest
- ROI:
-
Region of interest
- BMI:
-
Body mass index
- RW:
-
Reflected wave
References
Almohimeed I, Ono Y (2020) Ultrasound measurement of skeletal muscle contractile parameters using flexible and wearable single-element ultrasonic sensor. Sensors 20(13):3616. https://doi.org/10.3390/s20133616
Amin VR (1989) Ultrasonic attenuation estimation for tissue characterization. Theses and dissertations of Iowa State University. https://doi.org/10.31274/rtd-180813-8099
Bevan S (2015) Economic impact of musculoskeletal disorders (MSDs) on work in Europe. Best Pract Res Clin Rheumatol 29(3):356–373. https://doi.org/10.1016/j.berh.2015.08.002
Bhattacharya A (2014) Costs of occupational musculoskeletal disorders (MSDs) in the United States. Int J Ind Ergon 44(3):448–454. https://doi.org/10.1016/j.ergon.2014.01.008
Bi D, Dai Z, Liu D, Wu F, Liu C, Li Y, Li B, Li Z, Li Y, Ta D (2021) Ultrasonic backscatter measurements of human cortical and trabecular bone densities in a head-down bed rest study. Ultrasound Med Biol 47(8):2404–2415. https://doi.org/10.1016/j.ultrasmedbio.2021.04.002
Bi D, Shi L, Liu C et al (2022) Ultrasonic through-transmission measurements of human musculoskeletal and fat properties. Ultrasound Med Biol 49:1–9. https://doi.org/10.1016/j.ultrasmedbio.2022.09.007
Bushberg JT, Seibert JA, Leidholdt EM et al (2011) The essential physics of medical imaging, 3rd edn. Lippincott Williams & Wilkins, Philadelphia
Chaffai S, Peyrin F, Nuzzo S et al (2002) Ultrasonic characterization of human cancellous bone using transmission and backscatter measurements: relationships to density and microstructure. Bone 30(1):229–237. https://doi.org/10.1016/S8756-3282(01)00650-0
Chanda A, McClain S (2019) Mechanical modeling of healthy and diseased calcaneal fat pad surrogates. Biomimetics 4(1):1. https://doi.org/10.3390/biomimetics4010001
Compston JE, McClung MR, Leslie WD (2019) Osteoporosis. Lancet 393(10169):364–376. https://doi.org/10.1016/S0140-6736(18)32112-3
Fontes-Pereira A, Rosa P, Barboza T et al (2018) Monitoring bone changes due to calcium, magnesium, and phosphorus loss in rat femurs using quantitative ultrasound. Sci Rep 8(1):1–9. https://doi.org/10.1038/s41598-018-30327-7
Hakulinen MA, Töyräs J, Saarakkala S et al (2004) Ability of ultrasound backscattering to predict mechanical properties of bovine trabecular bone. Ultrasound Med Biol 30(7):919–927. https://doi.org/10.1016/j.ultrasmedbio.2004.04.006
Hakulinen MA, Day JS, Töyräs J et al (2005) 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. Phys Med Biol 50(8):1629–1642. https://doi.org/10.1088/0031-9155/50/8/001
Hassen A, Wilson DE, Willham RL et al (1998) Evaluation of ultrasound measurements of fat thickness and longissimus muscle area in feedlot cattle: assessment of accuracy and repeatability. Can J Anim Sci 78(3):277–285. https://doi.org/10.4141/A97-102
Hoffmeister BK (2011) Frequency dependence of apparent ultrasonic backscatter from human cancellous bone. Phys Med Biol 56(3):667. https://doi.org/10.1088/0031-9155/56/3/009
Hoffmeister BK, Johnson DP, Janeski JA et al (2008) Ultrasonic characterization of human cancellous bone in vitro using three different apparent backscatter parameters in the frequency range 0.6–15.0 MHz. IEEE Trans Ultrason Ferroelect Freq Contr 55(7):1442–1452. https://doi.org/10.1109/tuffc.2008.819
Hoffmeister BK, Holt AP, Kaste SC (2011) Effect of the cortex on ultrasonic backscatter measurements of cancellous bone. Phys Med Biol 56(19):6243–6255. https://doi.org/10.1088/0031-9155/56/19/006
Hoffmeister BK, Wilson AR, Gilbert MJ et al (2012) A backscatter difference technique for ultrasonic bone assessment. J Acous Soc Am 132(6):4069–4076. https://doi.org/10.1121/1.4763992
Hoffmeister BK, Mcpherson JA, Smathers MR et al (2015) Ultrasonic backscatter from cancellous bone: the apparent backscatter transfer function. IEEE Trans Ultrason Ferroelect Freq Contr 62(12):2115–2125. https://doi.org/10.1109/tuffc.2015.007299
Hoffmeister BK, Viano AM, Huang J et al (2018) Ultrasonic backscatter difference measurements of cancellous bone from the human femur: relation to bone mineral density and microstructure. J Acous Soc Am 143(6):3642–3653. https://doi.org/10.1121/1.5043385
Hoffmeister BK, Gray AJ, Sharp PC et al (2020) Ultrasonic bone assessment using the backscatter amplitude decay constant. Ultrasound Med Biol 46(9):2412–2423. https://doi.org/10.1016/j.ultrasmedbio.2020.04.029
Hoffmeister BK, Delahunt SI, Downey KL et al (2022) In vivo comparison of backscatter techniques for ultrasonic bone assessment at the femoral neck. Ultrasound Med Biol 48(6):997–1009. https://doi.org/10.1016/j.ultrasmedbio.2022.01.017
Ishida Y, Carroll JF, Pollock ML et al (1992) Reliability of B-mode ultrasound for the measurement of body fat and muscle thickness. Amer J Hum Biol 4:511–520. https://doi.org/10.1002/ajhb.1310040410
Jiang Y, Liu C, Li R et al (2014) Analysis of apparent integrated backscatter coefficient and backscattered spectral centroid shift in calcaneus in vivo for the ultrasonic evaluation of osteoporosis. Ultrasound Med Biol 40(6):1307–1317. https://doi.org/10.1016/j.ultrasmedbio.2013.12.024
Karjalainen JP, Riekkinen O, Töyräs J et al (2008) Ultrasonic assessment of cortical bone thickness in vitro and in vivo. IEEE Trans Ultrason Ferroelect Freq Contr 55(10):2191–2197. https://doi.org/10.1109/tuffc.918
Karjalainen JP, Töyräs J, Riekkinen O et al (2009) Ultrasound backscatter imaging provides frequency-dependent information on structure, composition and mechanical properties of human trabecular bone. Ultrasound Med Biol 35(8):1376–1384. https://doi.org/10.1016/j.ultrasmedbio.2009.03.011
Lee KI (2020) Relationships of the ultrasonic backscatter measurements with the bone mineral density and the microarchitectural parameters in bovine trabecular bone in vitro. J Acoust Soc Am 148(1):EL51–EL57. https://doi.org/10.1121/10.0001605
Li Y, Li B, Xu F et al (2018) Ultrasonic backscatter measurements at the calcaneus: an in vivo study. Measurement 122:128–134. https://doi.org/10.1016/j.measurement.2018.02.071
Li Y, Li B, Li Y et al (2019) The ability of ultrasonic backscatter parametric imaging to characterize bovine trabecular bone. Ultrason Imaging 41(5):271–289. https://doi.org/10.1177/0161734619862190
Lima RM, De Oliveira RJ, Raposo R et al (2019) Stages of sarcopenia, bone mineral density, and the prevalence of osteoporosis in older women. Arch Osteoporosis 14(1). https://doi.org/10.1007/s11657-019-0591-4
Liu C, Han H, Ta D et al (2013) Effect of selected signals of interest on ultrasonic backscattering measurement in cancellous bones. Sci China Phys Mech Astron 56(7):1310–1316. https://doi.org/10.1007/s11433-013-5113-6
Liu C, Ta D, Hu B et al (2014) The analysis and compensation of cortical thickness effect on ultrasonic backscatter signals in cancellous bone. J Appl Phys 116(12):124903. https://doi.org/10.1063/1.4896258
Liu C, Tang T, Xu F et al (2015) Signal of interest selection standard for ultrasonic backscatter in cancellous bone evaluation. Ultrasound Med Biol 41(10):2714–2721. https://doi.org/10.1016/j.ultrasmedbio.2015.06.005
Liu C, Zhang R, Li Y et al (2015b) An ultrasonic backscatter instrument for cancellous bone evaluation in neonates. Engineering 1(3):336–343. https://doi.org/10.15302/j-eng-2015079
Liu C, Xu F, Ta D et al (2016) Measurement of the human calcaneus in vivo using ultrasonic backscatter spectral centroid shift. J Ultrasound Med 35(10):2197–2208. https://doi.org/10.7863/ultra.15.03030
Liu C, Li B, Diwu Q et al (2018) Relationships of ultrasonic backscatter with bone densities and microstructure in bovine cancellous bone. IEEE Trans Ultrason Ferroelect Freq Contr 65(12):2311–2321. https://doi.org/10.1109/TUFFC.2018.2872084
Liu C, Li B, Li Y et al (2020) Ultrasonic backscatter difference measurement of bone health in preterm and term newborns. Ultrasound Med Biol 46(2):305–314. https://doi.org/10.1016/j.ultrasmedbio.2019.10.021
Lunar G (2009) GE Medical Systems Lunar: Lunar enCORE Safety and Specification Manual. https://www.gehealthcare.com/-/media/20fc07d1369e4d15acae5732090559db.pdf?la=en-us 1–57
Mao W, Du Y, Liu C et al (2019) Ultrasonic backscatter technique for assessing and monitoring neonatal cancellous bone status in vivo. IEEE Access 7:157417–157426. https://doi.org/10.1109/ACCESS.2019.2949748
Mao W, Du Y, Liu C et al (2020) A combined ultrasonic backscatter parameter for bone status evaluation in neonates. Comput Math Methods Med 2020:3187268. https://doi.org/10.1155/2020/3187268
Matsukawa M (2019) Bone ultrasound. Jpn J Appl Phys 58(SG):SG0802.0801-SG0802.0808. https://doi.org/10.7567/1347-4065/ab0dfa
Padilla F, Jenson F, Bousson V et al (2008) Relationships of trabecular bone structure with quantitative ultrasound parameters: in vitro study on human proximal femur using transmission and backscatter measurements. Bone 42(6):1193–1202. https://doi.org/10.1016/j.bone.2007.10.024
Pahor M, Manini T, Cesari M (2009) Sarcopenia: clinical evaluation, biological markers and other evaluation tools. J Nutr Health Aging 13(8):724–728. https://doi.org/10.1007/s12603-009-0204-9
Pineau JC, Bouslah M (2020) Prediction of body fat in male athletes from ultrasound and anthropometric measurements versus DXA. J Sports Med Phys Fitness 60(2):251–256. https://doi.org/10.23736/s0022-4707.19.09985-7
Pineau J-C, Filliard JR, Bocquet M (2009) Ultrasound techniques applied to body fat measurement in male and female athletes. J Athl Train 44(2):142–147. https://doi.org/10.4085/1062-6050-44.2.142
Rodríguez M, Medina BR, Jiménez E et al (2014) The levels of bone mineralization are influenced by body composition in children and adolescents. Nutr Hosp 30(4):763–768. https://doi.org/10.3305/nh.2014.30.4.7683
Sopher R, Nixon J, McGinnis E et al (2011) The influence of foot posture, support stiffness, heel pad loading and tissue mechanical properties on biomechanical factors associated with a risk of heel ulceration. J Mech Behav Biomed Mater 4(4):572–582. https://doi.org/10.1016/j.jmbbm.2011.01.004
Ta D, Wang W, Huang K et al (2008) Analysis of frequency dependence of ultrasonic backscatter coefficient in cancellous bone. J Acous Soc Am 124(6):4083–4090. https://doi.org/10.1121/1.3001705
Tang T, Liu C, Xu F et al (2016) Correlation between the combination of apparent integrated backscatter-spectral centroid shift and bone mineral density. J Med Ultrason 43(2):167–173. https://doi.org/10.1007/s10396-015-0690-9
Taş S, Bek N, Ruhi Onur M et al (2017) Effects of body mass index on mechanical properties of the plantar fascia and heel pad in asymptomatic participants. Foot Ankle Int 38(7):779–784. https://doi.org/10.1177/1071100717702463
Wagner DR (2013) Ultrasound as a tool to assess body fat. J Obes 2013:1–9. https://doi.org/10.1155/2013/280713
Wear KA (2020) Mechanisms of interaction of ultrasound with cancellous bone: a review. IEEE Trans Ultrason Ferroelect Freq Contr 67(3):454–482. https://doi.org/10.1109/TUFFC.2019.2947755
Wear KA, Armstrong DW (2001) Relationships among calcaneal backscatter, attenuation, sound speed, hip bone mineral density, and age in normal adult women. J Acous Soc Am 110(1):573–578. https://doi.org/10.1121/1.1378343
Wear KA, Garra BS (1998) Assessment of bone density using ultrasonic backscatter. Ultrasound Med Biol 24(5):689–695. https://doi.org/10.1016/S0301-5629(98)00040-4
Wear KA, Laib A (2003) The dependence of ultrasonic backscatter on trabecular thickness in human calcaneus: theoretical and experimental results. IEEE Trans Ultrason Ferroelect Freq Contr 50(8):979–986. https://doi.org/10.1109/TUFFC.2003.1226542
Wear KA, Stuber AP, Reynolds JC (2000) Relationships of ultrasonic backscatter with ultrasonic attenuation, sound speed and bone mineral density in human calcaneus. Ultrasound Med Biol 26(8):1311–1316. https://doi.org/10.1016/S0301-5629(00)00267-2
Wear KA, Nagaraja S, Dreher ML et al (2017) Relationships among ultrasonic and mechanical properties of cancellous bone in human calcaneus in vitro. Bone 103:93–101. https://doi.org/10.1016/j.bone.2017.06.021
Yoshimura N, Muraki S, Iidaka T et al (2019) Prevalence and co-existence of locomotive syndrome, sarcopenia, and frailty: the third survey of Research on Osteoarthritis/Osteoporosis Against Disability (ROAD) study. J Bone Miner Metab 37(6):1058–1066. https://doi.org/10.1007/s00774-019-01012-0
Zhang R, Ta D, Liu C et al (2013) Feasibility of bone assessment with ultrasonic backscatter signals in neonates. Ultrasound Med Biol 39(10):1751–1759. https://doi.org/10.1016/j.ultrasmedbio.2013.03.023
Funding
This study was supported by Shanghai Municipal Science and Technology Major Project (2017SHZDZX01), the National Natural Science Foundation of China (12034005, 12122403, 11827808, 11874289), the China Postdoctoral Science Foundation (2021M690709), the Shanghai Science and Technology Innovation Plan (20S31901300), the Shanghai Rising-Star Program (21QC1400100) and the China Scholarship Council (202106100122).
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All authors contributed to the conception and design of this study. Material preparation and collection were conducted by DB, LS, BL, YL and SW. DB drafted the manuscript. CL, LL, JL and DT revised and commented on the manuscript. All authors read and approved the final manuscript.
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Bi, D., Shi, L., Li, B. et al. The Protocol of Ultrasonic Backscatter Measurements of Musculoskeletal Properties. Phenomics 4, 72–80 (2024). https://doi.org/10.1007/s43657-023-00122-0
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DOI: https://doi.org/10.1007/s43657-023-00122-0