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Clinical determination of bone quality: Is ultrasound an answer?

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Summary

Progress in clinical characterization of bone relies on developing a means to clinically assessall of the important determinants of bone quality, specifically, the intrinsic material properties of a bone (stiffness and brittleness) versus the macroscopic structural properties [apparent mass density (g/cc), structural shape and distribution of cortical mass, trabecular architecture, extent of unrepaired microdamage, and defects associated with the accelerated remodeling in early menopause]. Ultrasound devices currently measure parameters related to either of only two basic properties: bone ultrasound attenuation (BUA) or the apparent velocity of wave propagation (AVU). Theory and repeated corroboration in the laboratory have shown that the velocity of sound in solids such as bone has a quantitative relationship to the elastic modulus (or stiffness) and mass density. Although no comparable physical model exists for BUA, growingin vitro andin vivo empirical evidence shows a relationship to stiffness and mass density as well. Therefore, the question of ultrasound's ability to provide additional, clinically useful information about bone quality reduces to this:Does bone quality depend significantly on bone stiffness and does stiffness depend on factors other than bone mass alone? Clinical study results provide mounting evidence of ultrasound's abilities. (1) Numerous studies compare either velocity or BUA with BMC or BMD. The correlation coefficients vary widely between studies, even when repeated by the same investigators and laboratories. Two studies demonstrated this by comparing groups of subjects who are indistinguishable by BMD at the lumbar spine, but whose mean AVU readings are significantly different. (2) Multiple studies of AVU and BUA by different investigators have shown the ability of ultrasound to distinguish, as effectively as BMC or BMD, women with osteoporotic vertebral crush deformities from normal women. Prospective studies have shown that AVU and BUA each indicated risk of future osteoporotic fractures. In a population-based, randomized, cross-sectional study of men and women, AVU discriminated between groups of subjects who had suffered low trauma fractures versus those free of fracture. Such repeated clinical evidence of the ability of BUA and AVU to detect bone fragility provides mounting evidence that ultrasound measures a clinically relevant property of bone quality in addition to and distinct from bone mass.

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Abbreviations

AVU:

Apparent velocity of ultrasound transmission (meters/second) measured at the patella over the frequency range of 150–300 KHz [5, 6]

BMC:

Bone mineral content, expressed in grams, obtained from a bone densitometer without normalizing for the area or volume over which the measurement was made

BMD:

BMC obtained by normalizing for width (grams/cm), area (grams/cm2) or volume (grams/cc) over which the measurement was made

BUA:

Bone ultrasound attenuation (decibels/megahertz [db/MHz]) is the amount of ultrasound intensity lost during transmission through bone, derived from the slope of the approximately linear dependence of the attenuation coefficient on frequencies between 300 and 600 KHz [7, 8]

DPA:

Dual photon absorptiometry measurement of BMC or areal BMD based on attenuation of X-rays emitted by a radioactive isotope at two different energy levels

DXA:

Dual energy X-ray absorptiometry measurement of BMC or areal BMD based on attenuation of X-rays produced by an X-ray tube, measured at two different energy levels

SPA:

Single photon absorptiometry measurement of BMC or grams/cm based on attenuation of X-rays emitted by a radioactive isotope at a single energy level

QCT:

Quantitative X-ray computed tomography measurement of BMC or volumetric BMD over a user-specifiable region of interest

References

  1. Heaney RP, Avioli LV, Chesnut CH III, Lappe J, Recker RR, Brandenburger GH (1987) Osteoporotic bone fragility: detection by ultrasound transmission velocity. JAMA 261:2986–2990

    Google Scholar 

  2. Brandenburger GH, Avioli LV, Chesnut CH, Heaney RP, Lappe J, McDougall SW, Olson CL, Recker RR, Turner C (1990) Methods for reproducible in vivo apparent velocity in cancellous bone. In: McAvoy BF, (ed) Proc 1990 IEEE Ultrasonics Symposium, IEEE Press, NY, pp 1359–1361

    Google Scholar 

  3. Langton CM, Palmer SB, Porter RW (1984) The measurement of broadband ultrasonic attenuation in cancellous bone. Eng Med 13:89–91

    Google Scholar 

  4. Palmer SB, Langton CM (eds) (1987) Ultrasonic studies of bone. IOP Publishing, LTD Bristol, UK

    Google Scholar 

  5. Heaney RP (1989) Osteoporotic fracture space: an hypothesis. Bone Miner 6:1–13

    Google Scholar 

  6. Einhorn TA (in press) Bone integrity: the bottom line. Calcif Tissue Int

  7. Doherty WP, Bovill EG, Wilson EL (1974) Evaluation of the use of resonant frequencies to characterize physical properties of human long bones. J Biomech 7:559–561

    Google Scholar 

  8. Jurist JM (1970) In vivo determination of the elastic response of bone I. Method of ulnar resonant frequency determination. Phys Med Biol 15:417–426

    Google Scholar 

  9. Jurist JM (1970) In vivo determination of the elastic response of bone 11. Ulnar resonant frequency in osteoporotic, diabetic and normal subjects. Phys Med Biol 15:427–434

    Google Scholar 

  10. Spiegl PV, Jurist JM (1975) Prediction of ulnar resonant frequency. J Biomech 8:213–217

    Google Scholar 

  11. Saba S, Lakes RS (1977) The effect of soft tissue on wave propagation and vibration tests for determining the in vivo properties of bone. J Biomech 10:393–401

    Google Scholar 

  12. Rosenstein AD (1990) Method and apparatus for determining osseous implant fixation integrity. PCT Patent WO 90/06720

  13. Fujita T, Fukase M, Yoshimoto Y, Tsutsumi M, Fukami T, Imai Y, Sakaguchi K, Abe T, Sawai M, Seo I, Yaguchi T, Enomoto S, Droke DM, Avioli LV (1983) Basic and clinical evaluation of the measurement of bone resonant frequency. Calcif Tissue Int 35:153–158

    Google Scholar 

  14. Fäh D, Stüssi E (1988) Phase velocity measurement of flexural waves in human tibia. J Biomech 21:975–983

    Google Scholar 

  15. Steele CR, Zhou L-J, Guido D, Marcus R, Heinrichs WL, Cheema C (1988) Noninvasive determination of ulnar stiffness from mechanical response-in vivo comparison of stiffness and bone mineral content in humans. J Biomech Eng 110:87–96

    Google Scholar 

  16. McCabe F, Zhou L-J, Steele CR, Marcus R (1991) Noninvasive assessment of ulnar bending stiffness in women. J Bone Miner Res 6:53–59

    Google Scholar 

  17. Geusens P, Nijs J, Van der Peere G, Van Audekercke R, Lowfet G, Goovaerts S, Barbier A, Lacheretz F, Remandet B, Jiang Y, Dequeker J (1992) Longitudinal effect of tiludronate on bone mineral density resonant frequency, and strength in monkeys. J Bone Miner Res 7:599–609

    Google Scholar 

  18. Baran DT, Kelly AM, Karellas A, Gionet M, Price M, Leahey D, Steuterman S, McSherry B, Roche J (1988) Ultrasound attenuation of the os calcis in women with osteoporosis and hip fractures. Calcif Tissue Int 43:138–142

    Google Scholar 

  19. McCloskey EV, Murray SA, Miller C, Charlesworth D, Tindale W, O'Doherty DP, Bickerstaff DR, Hamdy NAT, Kanis JA (1990) Broadband ultrasound attenuation in the os calcis: relationship to bone mineral at other sites. Clin Sci 78:227–233

    Google Scholar 

  20. Agren M, Karellas A, Leahey, Marks S, Baran D (1991) Ultrasound attenuation of the calcaneous: a sensitive and specific discriminator of osteopenia in postmenopausal women. Calcif Tissue Int 48:240–244

    Google Scholar 

  21. Zagzebski JA, Rossman PJ, Mesina C, Mazess RB, Madsen EL (1991) Ultrasound measurement of the os calcis. Calcif Tissue Int 49:107–111

    Google Scholar 

  22. Abendschein WF, Hyatt GW (1970) Ultrasonics and selected physical properties of bone. Clin Orthop Rel Res 69:294–301

    Google Scholar 

  23. Ashman RB, Cowin JD, Van Buskirk WC, Rice JC (1984) A continuous wave technique for the measurement of the elastic properties of cortical bone. J Biomech 17:349–361

    Google Scholar 

  24. Ashman RB, Rosina G, Cowin SC, Fontenot MG (1985) The bone tissue of the canine mandible is elastically isotropic. J Biomech 18:717–721

    Google Scholar 

  25. Ashman RB, Corin JD, Turner CH (1987) Elastic properties of cancellous bone: measurement by ultrasonic technique. J Biomech 20:979–986

    Google Scholar 

  26. Ashman RB, Rho JY (1988) Elastic modulus of trabecular bone material. J Biomech 21:177–181

    Google Scholar 

  27. Ashman RB, Rho JY, Turner CH (1989) Anatomical variation of orthotropic elastic moduli of the proximal human tibia. J Biomech 22:895–900

    Google Scholar 

  28. Antich P, Anderson JA, Ashman RB, Dowdey JE, Gonzales J, Murry RC, Zerwekh JE, Pak CYC (1991) Measurement of mechanical properties of bone material in vitro by ultrasound reflection: methodology and comparison with ultrasound transmission. J Bone Miner Res 6:417–426

    Google Scholar 

  29. Floriani LP, Debefoise NT, Hyatt GW (1967) Mechanical properties of healing bone by the use of ultrasound. Surg Forum Orthop Surg 18:468–470

    Google Scholar 

  30. Yoon HS, Katz JL (1979) Ultrasonic properties and microtexture of human cortical bone. In: Linzer M (ed) Ultrasonic tissue characterization II, NBS Spec Publ 525, US Govt Printing Office, Wash DC, pp 189–196

    Google Scholar 

  31. Barger JE (1979) Attenuation and dispersion of ultrasound in cancellous bone. In: Linzer M (ed) Ultrasonic tissue characterization II, NBS Spec Publ 525, US Govt Printing Office, Wash DC, pp 197–201

    Google Scholar 

  32. Lees S, Klopholz DZ (1992) Sonic velocity and attenuation in wet compact cow femur for the frequency range 5 to 100 MHz. Ultrasound Med Biol 18:303–308

    Google Scholar 

  33. Craven JD, Costantini M (1973) A new technique for the qualitative assessment of cortical bone using an ultrasonic pulse echo method—an in vivo study. In: Frame B, Parfitt AM, Duncan MB (eds) Clinical aspects of metabolic bone disease. Excerpta Medica, Amsterdam, pp 48–49

    Google Scholar 

  34. Greenfield MA, Craven JD, Huddleston A, Kehrer ML, Wishko D, Stern R (1981) Measurement of the velocity of ultrasound in human cortical bone in vivo. Radiology 138:701–710

    Google Scholar 

  35. Anast GT, Fields T, Siegel IM (1958) Ultrasonic technique for the evaluation of bone fractures. Am J Phys Med 37:157–159

    Google Scholar 

  36. Abendschein WF, Hyatt GW (1972) Ultrasonics and physical properties of healing bone. J Trauma 12:297–301

    Google Scholar 

  37. Brown SA, Mayor MB (1976) Ultrasonic assessment of early callus formation. Biomed Eng 124–136

  38. Gerlanc M, Haddad D, Hyatt GW, Langloh JT, St. Hilaire P (1975) Ultrasonic study of normal and fractured bone. Clin Orthop Rel Res 3:175–180

    Google Scholar 

  39. Kaufman JJ, Chiabrera, Hatem M, Hakim NZ, Figueiredo M, Nasser P, Lattuga S, Pilla AA, Siffert RS (1990) A neural network approach for bone fracture healing assessment. IEEE Eng Med Biol 9:23–30

    Google Scholar 

  40. Cunningham JL, Kenwright J, Kershaw CJ (1991) Biomechanical measurement of fracture healing. J Med Eng Tech 14:92–101

    Google Scholar 

  41. Sonstegard DA, Mattews LS (1976) Sonic diagnosis of bone fracture healing—a preliminary study. J Biomech 9:689–694

    Google Scholar 

  42. Bonfield W, Tully AE (1982) Ultrasonic analysis of the Young's modulus of cortical bone. J Biomed Eng 4:23–27

    Google Scholar 

  43. Lees S, Davidson CL (1979) A theory relating sonic velocity to mineral content in bone. In: Linzer M (ed) Ultrasonic tissue characterization II. NBS Spec Publ 525, US Govt Printing Office, Wash DC, pp 179–187

    Google Scholar 

  44. Porter RW, Miller CG, Grainger D, Palmer SB (1990) Prediction of hip fracture in elderly women: a prospective study. Br Med 7:638–641

    Google Scholar 

  45. Resch H, Pietschmann P, Bernecker P, Krexner E, Willvonseder R (1990) Broadband ultrasound attenuation: a new diagnostic method in osteoporosis. AJR 155:825–828

    Google Scholar 

  46. Camporeale A, Cepollaro C, Zacchei F, Montagnani, Agnusdei D, Gennari C (1990) Ultrasound transmission velocity in normal and osteoporotic postmenopausal women. In: Christiansen C, Overgaard K (eds) Osteoporosis 1990. Osteopress ApS, Copenhagen, pp 670–672

    Google Scholar 

  47. Fujii Y, Goto B, Keiichi T, Fujita T (in press) Ultrasound transmission as a sensitive indicator of bone change in Japanese women in the perimenopausal period. Bone Miner

  48. Collier RJ, Donarski RJ (1987) Non-invasive method of measuring resonant frequency of a human tibia in vivo, parts 1–2. J Biomed Eng 9:321–331

    Google Scholar 

  49. Jeffcott LB, McCartney RN (1985) Ultrasound as a tool for assessment of bone quality in the horse. Vet Rec 116:337–342

    Google Scholar 

  50. El Shorafa WM, Feaster JP, Ott EA (1979) Horse metacarpa bone: age, ash content, cortical area and failure stress interrelationships. J Anim Sci 49:979–982

    Google Scholar 

  51. Glade MJ, Luba NK, Schryver HF (1986) Effects of age and diet on the development of mechanical strength by the third metacarpal and metatarsal bone of young horses. J Anim Sci 63:1432–1444

    Google Scholar 

  52. Pratt GW (1980) An in vivo method of ultrasonically evaluating bone strength. Proc 26th Annual Convention of the American Association of Equine Practitioners, AAEP, Golden CO, pp 295–301

  53. Rubin CT, Pratt GW, Porter AL, Lanyon LE, Poss R (1987) The use of ultrasound in vivo to determine acute change in the mechanical properties of bone following intense physical activity. J Biomech 20:723–727

    Google Scholar 

  54. Turner CH, Eich M (1991) Ultrasonic velocity as a predictor of strength in bovine cancellous bone. Calcif Tissue Int 49:116–119

    Google Scholar 

  55. Brandenburger GH, Avioli LV, Chesnut CH, Heaney RP, Lappe J, McDougall SW, Olson CL, Recker RR (1990) Effects of estrogen cessation on bone mass and apparent velocity of ultrasound transmission. In: Christiansen C, Overgaard K (eds) Osteoporosis 1990. Osteopress ApS, Copenhagen, pp 647–649

    Google Scholar 

  56. Brandenburger GH, Avioli LV, Chesnut CH, Davies KM, Heaney RP, Kwon S, Lappe J, McDougall SW, Olson CL, Recker RR (1990) Assessment of spine fracture by apparent velocity of ultrasound transmission. In: Christiansen C, Overgaard K (eds) Osteoporosis 1990. Osteopress ApS, Copenhagen, pp 650–652

    Google Scholar 

  57. McKelvie ML, Palmer SB (1987) The interaction of ultrasound with cancellous bone. In: Palmer SB, Langton CM (eds) Ultrasonic studies of bone. IOP Publishing, LTD Bristol UK, pp 1–13

    Google Scholar 

  58. Glüer CC, Faulkner KG, Engelke K, Black D, Genant HK (1991) Broadband ultrasound attenuation of the heel versus single photon absorptiometry of the heel: Do these techniques measure different entities? (abstract). J Bone Miner Res 6(suppl 1):S169

    Google Scholar 

  59. Mazess RB, Hanson JA, Bonnick SL (1991) Ultrasound measurement of the os calcis (abstract). J Bone Miner Res 6(suppl 1):S167

    Google Scholar 

  60. Kvasnicka HM, Lehmann R, Wapniarz M, Klein K, Allolio B (1992) Bone fragility in comparison to distal forearm bone mineral density in perimenopausal women (abstract). Bone Miner 12(suppl. 1):A413

    Google Scholar 

  61. Poll V, Cooper C, Cawley MID (1986) Broadband ultrasonic attenuation in the os calcis and single photon absorptiometry in the distal forearm: a comparative study. Clin Phys Physiol Meas 7:375–379

    Google Scholar 

  62. Kimmel DB, Heaney RP, Avioli LV, Chesnut CH, Recker RR, Lappe JM, Brandenburger GH (1991) Patellar ultrasound velocity in osteoporotic and normal subjects of equal forearm or spinal bone density (abstract). J Bone Miner Res 6(suppl. 1):S366

    Google Scholar 

  63. Cummings SR, Blake DM, Nevitt MC, Warren SB, Cauley JA, Genant HK, Mascioli SR, Scott JC, Seeley DG, Steiger P, Vogt TM, and the Study Fractures Research Group (1990) Appendicular bone density and age predict hip fracture in women. JAMA 265:665–668

    Google Scholar 

  64. Wasnich RD, Ross PD, Davis JW, Vogel JM (1989) A comparison of single and multi-site MBC measurements for assessment of spine fracture probability. J Nucl Med 30:1166–1171

    Google Scholar 

  65. Stegman MR, Heaney RP, Recker RR, Leist J, Travers-Gustfason (in press) Ultrasound measurement of bone quality of a stratified sample of a rural population (abstract) J Bone Miner Res

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  1. Mallinckrodt Madical, Inc., 675 McDonnell Blvd., 5840, 63134, St. Louis, Missouri, USA

    Gary H. Brandenburger

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Brandenburger, G.H. Clinical determination of bone quality: Is ultrasound an answer?. Calcif Tissue Int 53 (Suppl 1), S151–S156 (1993). https://doi.org/10.1007/BF01673427

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  • DOI: https://doi.org/10.1007/BF01673427

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