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Osteoporosis International

Published in:

01-04-2014 | Original Article

Locally measured microstructural parameters are better associated with vertebral strength than whole bone density

Authors: J. Hazrati Marangalou, F. Eckstein, V. Kuhn, K. Ito, M. Cataldi, F. Taddei, B. van Rietbergen

Published in: Osteoporosis International | Issue 4/2014

Abstract

Summary

Whole vertebrae areal and volumetric bone mineral density (BMD) measurements are not ideal predictors of vertebral fractures. We introduce a technique which enables quantification of bone microstructural parameters at precisely defined anatomical locations. Results show that local assessment of bone volume fraction at the optimal location can substantially improve the prediction of vertebral strength.

Introduction

Whole vertebrae areal and volumetric BMD measurements are not ideal predictors of vertebral osteoporotic fractures. Recent studies have shown that sampling bone microstructural parameters in smaller regions may permit better predictions. In such studies, however, the sampling location is described only in general anatomical terms. Here, we introduce a technique that enables the quantification of bone volume fraction and microstructural parameters at precisely defined anatomical locations. Specific goals of this study were to investigate at what anatomical location within the vertebrae local bone volume fraction best predicts vertebral-body strength, whether this prediction can be improved by adding microstructural parameters and to explore if this approach could better predict vertebral-body strength than whole bone volume fraction and finite element (FE) analyses.

Methods

Eighteen T12 vertebrae were scanned in a micro-computed tomography (CT) system and FE meshes were made using a mesh-morphing tool. For each element, bone microstructural parameters were measured and correlated with vertebral compressive strength as measured experimentally. Whole bone volume fraction and FE-predicted vertebral strength were also compared to the experimental measurements.

Results

A significant association between local bone volume fraction measured at a specific central region and vertebral-body strength was found that could explain up to 90 % of the variation. When including all microstructural parameters in the regression, the predictive value of local measurements could be increased to 98 %. Whole bone volume fraction could explain only 64 % and FE analyses 76 % of the variation in bone strength.

Conclusions

A local assessment of volume fraction at the optimal location can substantially improve the prediction of bone strength. Local assessment of other microstructural parameters may further improve this prediction but is not clinically feasible using current technology.

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Riggs BL, Melton Iii LJ (1995) The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone 17:S505–S511CrossRef

Grigoryan M, Guermazi A, Roemer F, Delmas P, Genant H (2003) Recognizing and reporting osteoporotic vertebral fractures. Eur Spine J 12:S104–S112PubMedCentralPubMedCrossRef

Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle M-F, Audran M (2000) Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res 15:13–19PubMedCrossRef

Bultink IEM, Lems WF, Kostense PJ, Dijkmans BAC, Voskuyl AE (2005) Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum 52:2044–2050PubMedCrossRef

Bolotin HH (2007) DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodeling. Bone 41:138–154PubMedCrossRef

Kanis J, Borgstrom F, Laet C, Johansson H, Johnell O, Jonsson B, Oden A, Zethraeus N, Pfleger B, Khaltaev N (2005) Assessment of fracture risk. Osteoporos Int 16:581–589PubMedCrossRef

Siris ES, Chen Y, Abbot TA et al (2004) Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med 164:1108–1112PubMedCrossRef

Lochmüller E-M, Müller R, Kuhn V, Lill CA, Eckstein F (2003) Can novel clinical densitometric techniques replace or improve DXA in predicting bone strength in osteoporosis at the hip and other skeletal sites? J Bone Miner Res 18:906–912PubMedCrossRef

Perilli E, Briggs AM, Kantor S, Codrington J, Wark JD, Parkinson IH, Fazzalari NL (2012) Failure strength of human vertebrae: prediction using bone mineral density measured by DXA and bone volume by micro-CT. Bone 50:1416–1425PubMedCrossRef

10.

Briggs A, Perilli E, Parkinson I, Kantor S, Wrigley T, Fazzalari N, Wark J (2012) Measurement of subregional vertebral bone mineral density in vitro using lateral projection dual-energy X-ray absorptiometry: validation with peripheral quantitative computed tomography. J Bone Miner Metab 30:222–231PubMedCrossRef

11.

Mulder L, van Rietbergen B, Noordhoek NJ, Ito K (2012) Determination of vertebral and femoral trabecular morphology and stiffness using a flat-panel C-arm-based CT approach. Bone 50:200–208PubMedCrossRef

12.

Duan Y, Parfitt AM, Seeman E (1999) Vertebral bone mass, size, and volumetric density in women with spinal fractures. J Bone Miner Res 14:1796–1802PubMedCrossRef

13.

Seeman E, Duan Y, Fong C, Edmonds J (2001) Fracture Site-Specific Deficits in Bone Size and Volumetric Density in Men with Spine or Hip Fractures. J Bone Miner Res 16:120–127PubMedCrossRef

14.

Yoganandan N, Pintar FA, Stemper BD, Baisden JL, Aktay R, Shender BS, Paskoff G, Laud P (2006) Trabecular bone density of male human cervical and lumbar vertebrae. Bone 39:336–344PubMedCrossRef

15.

Lang TF, Li J, Harris ST, Genant HK (1999) Assessment of vertebral bone mineral density using volumetric quantitative CT. J Comput Assist Tomogr 23

16.

Tabensky AD, Deluca V, Briganti E, Seeman E, Williams J (1996) Bone mass, areal, and volumetric bone density are equally accurate, sensitive, and specific surrogates of the breaking strength of the vertebral body: an in vitro study. J Bone Miner Res 11:1981–1988PubMedCrossRef

17.

Lochmüller EM, Bürklein D, Kuhn V, Glaser C, Müller R, Glüer CC, Eckstein F (2002) Mechanical strength of the thoracolumbar spine in the elderly: prediction from in situ dual-energy X-ray absorptiometry, quantitative computed tomography (QCT), upper and lower limb peripheral QCT, and quantitative ultrasound. Bone 31:77–84PubMedCrossRef

18.

Banse X, Devogelaer JP, Munting E, Delloye C, Cornu O, Grynpas M (2001) Inhomogeneity of human vertebral cancellous bone: systematic density and structure patterns inside the vertebral body. Bone 28:563–571PubMedCrossRef

19.

Stauber M, Müller R (2006) Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos Int 17:616–626PubMedCrossRef

20.

Parkinson IH, Badiei A, Stauber M, Codrington J, Müller R, Fazzalari NL (2012) Vertebral body bone strength: the contribution of individual trabecular element morphology. Osteoporos Int 23:1957–1965PubMedCrossRef

21.

Gong H, Zhang M, Qin L, Lee KKH, Guo X, Shi SQ (2006) Regional variations in microstructural properties of vertebral trabeculae with structural groups. Spine 31:24–32PubMedCrossRef

22.

Briggs AM, Perilli E, Parkinson IH, Wrigley TV, Fazzalari NL, Kantor S, Wark JD (2010) Novel assessment of subregional bone mineral density using DXA and pQCT and subregional microarchitecture using micro-CT in whole human vertebrae: applications, methods, and correspondence between technologies. J Clin Densitom 13:161–174PubMedCrossRef

23.

Lochmüller EM, Pöschl K, Würstlin L, Matsuura M, Müller R, Link TM, Eckstein F (2008) Does thoracic or lumbar spine bone architecture predict vertebral failure strength more accurately than density? Osteoporos Int 19:537–545PubMedCrossRef

24.

Grassi L, Hraiech N, Schileo E, Ansaloni M, Rochette M, Viceconti M (2011) Evaluation of the generality and accuracy of a new mesh morphing procedure for the human femur. Med Eng Phys 33:112–120PubMedCrossRef

25.

Harrigan TP, Jasty M, Mann RW, Harris WH (1988) Limitations of the continuum assumption in cancellous bone. J Biomech 21:269–275PubMedCrossRef

26.

Zysset PK, Curnier A (1995) An alternative model for anisotropic elasticity based on fabric tensors. Mech Mater 21:243–250CrossRef

27.

Charlebois M, Jirasek M, Zysset PK (2010) A nonlocal constitutive model for trabecular bone softening in compression. Biomech Model Mechanobiol 9:597–611PubMedCrossRef

28.

Imai K, Ohnishi I, Bessho M, Nakamura K (2006) Nonlinear finite element model predicts vertebral bone strength and fracture site. Spine 31

29.

Kopperdahl DL, Roberts AD, Keaveny TM (1999) Localized damage in vertebral bone is most detrimental in regions of high strain energy density. J Biomech Eng 121:622–628PubMedCrossRef

30.

Moro M, Hecker AT, Bouxsein ML, Myers ER (1995) Failure load of thoracic vertebrae correlates with lumbar bone mineral density measured by DXA. Calcif Tissue Int 56:206–209PubMedCrossRef

31.

Hulme PA, Boyd SK, Ferguson SJ (2007) Regional variation in vertebral bone morphology and its contribution to vertebral fracture strength. Bone 41:946–957PubMedCrossRef

32.

Edmondston SJ, Singer KP, Day RE, Breidahl PD, Price RI (1994) In vitro relationships between vertebral body density, size, and compressive strength the elderly thoracolumbar spine. Clin Biomech 9:180–186CrossRef

33.

Cheng XG, Nicholson PHF, Boonen S, Lowet G, Brys P, Aerssens J, van der Perre G, Dequeker J (1997) Prediction of vertebral strength in vitro by spinal bone densitometry and calcaneal ultrasound. J Bone Miner Res 12:1721–1728PubMedCrossRef

34.

Ebbesen EN, Thomsen JS, Beck-Nielsen H, Nepper-Rasmussen HJ, Mosekilde L (1999) Lumbar vertebral body compressive strength evaluated by dual-energy X-ray absorptiometry, quantitative computed tomography, and ashing. Bone 25:713–724PubMedCrossRef

35.

Fields AJ, Nawathe S, Eswaran SK, Jekir MG, Adams MF, Papadopoulos P, Keaveny TM (2012) Vertebral fragility and structural redundancy. J Bone Miner Res 27:2152–2158PubMedCentralPubMedCrossRef

36.

Dall’Ara E, Schmidt R, Pahr D, Varga P, Chevalier Y, Patsch J, Kainberger F, Zysset P (2010) A nonlinear finite element model validation study based on a novel experimental technique for inducing anterior wedge-shape fractures in human vertebral bodies in vitro. J Biomech 43:2374–2380PubMedCrossRef

37.

Matsumoto T, Ohnishi I, Bessho M, Imai K, Ohashi S, Nakamura K (2009) Prediction of vertebral strength under loading conditions occurring in activities of daily living using a computed tomography-based nonlinear finite element method. Spine 34

38.

Buckley JM, Loo K, Motherway J (2007) Comparison of quantitative computed tomography-based measures in predicting vertebral compressive strength. Bone 40:767–774PubMedCentralPubMedCrossRef

39.

Crawford RP, Cann CE, Keaveny TM (2003) Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone 33:744–750PubMedCrossRef

40.

Mirzaei M, Zeinali A, Razmjoo A, Nazemi M (2009) On prediction of the strength levels and failure patterns of human vertebrae using quantitative computed tomography (QCT)-based finite element method. J Biomech 42:1584–1591PubMedCrossRef

41.

Dall’Ara E, Varga P, Pahr D, Zysset P (2011) A calibration methodology of QCT BMD for human vertebral body with registered micro-CT images. Med Phys 38:2602–2608PubMedCrossRef

42.

Schmidt C, Priemel M, Kohler T, Weusten A, Müller R, Amling M, Eckstein F (2003) Precision and accuracy of peripheral quantitative computed tomography (pQCT) in the mouse skeleton compared with histology and microcomputed tomography (μCT). J Bone Miner Res 18:1486–1496PubMedCrossRef

43.

Bredella MA, Misra M, Miller KK, Madisch I, Sarwar A, Cheung A, Klibanski A, Gupta R (2008) Distal radius in adolescent girls with anorexia nervosa: trabecular structure analysis with high-resolution flat-panel volume CT1. Radiology 249:938–946PubMedCentralPubMedCrossRef

44.

Walsh CJ, Phan CM, Misra M, Bredella MA, Miller KK, Fazeli PK, Bayraktar HH, Klibanski A, Gupta R (2010) Women with anorexia nervosa: finite element and trabecular structure analysis by using flat-panel volume CT. Radiology 257:167–174PubMedCentralPubMedCrossRef

45.

Cheung A, Bredella M, Al Khalaf MM, Grasruck M, Leidecker C, Gupta R (2009) Reproducibility of trabecular structure analysis using flat-panel volume computed tomography. Skeletal Radiol 38:1003–1008PubMedCrossRef

46.

Gupta R, Grasruck M, Suess C, Bartling S, Schmidt B, Stierstorfer K, Popescu S, Brady T, Flohr T (2006) Ultra-high resolution flat-panel volume CT: fundamental principles, design architecture, and system characterization. Eur Radiol 16:1191–1205PubMedCrossRef

47.

Hazrati Marangalou J, Ito K, van Rietbergen B (2012) A new approach to determine the accuracy of morphology–elasticity relationships in continuum FE analyses of human proximal femur. J Biomech 45:2884–2892PubMedCrossRef

48.

Pahr DH, Zysset PK (2009) A comparison of enhanced continuum FE with micro FE models of human vertebral bodies. J Biomech 42:455–462PubMedCrossRef

49.

Hazrati Marangalou J, Ito K, Cataldi M, Taddei F, van Rietbergen B (2013) A novel approach to estimate trabecular bone anisotropy using a database approach. J Biomech 46:2356–2362PubMedCrossRef

50.

Edmondston SJ, Singer KP, Day RE, Breidahl PD, Price RI (1994) Formalin fixation effects on vertebral bone density and failure mechanics: an in vitro study of human and sheep vertebrae. Clin Biomech 9:175–179CrossRef

51.

Wilke H-J, Krischak S, Claes LE (1996) Formalin fixation strongly influences biomechanical properties of the spine. J Biomech 29:1629–1631PubMedCrossRef

Title: Locally measured microstructural parameters are better associated with vertebral strength than whole bone density
Authors: J. Hazrati Marangalou
F. Eckstein
V. Kuhn
K. Ito
M. Cataldi
F. Taddei
B. van Rietbergen
Publication date: 01-04-2014
Publisher: Springer London
Published in: Osteoporosis International / Issue 4/2014
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI: https://doi.org/10.1007/s00198-013-2591-3

At a glance: The STEP trials

Springer Medicine

Locally measured microstructural parameters are better associated with vertebral strength than whole bone density

Abstract

Summary

Introduction

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Summary

Introduction

Methods

Results

Conclusions

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