Advertisement

Medical & Biological Engineering & Computing

, Volume 57, Issue 4, pp 795–805 | Cite as

A novel technique with reduced computed tomography exposure to predict vertebral compression fracture: a finite element study based on rat vertebrae

  • Giovanni F. Solitro
  • Florian Mainnemare
  • Farid AmiroucheEmail author
  • Ankit Mehta
Original Article

Abstract

Vertebral compression fractures are a significant clinical issue with an annual incidence of approximately 750,000 cases in the USA alone. Mechanical properties of vertebrae are successfully evaluated through finite element (FE) models based on vertebrae CT. However, clinical drawbacks associated to radiation transmission encouraged to explore the possibility to use selected or reduced portions of the vertebra. The objective of our study was to develop a new procedure to predict vertebral compression fracture from sub-volumes. We reconstructed rat vertebras from micro-CT of thoracic and lumbar groups. Each vertebra was partitioned into three sub-volumes of different axial thickness. FE simulating compression tests were performed on each model to evaluate their failure load and stiffness. Using a power function, a high correlation was found for stiffness and strength. The sub-volume with three fifths thickness had a failure load of 180.7 ± 19.2 N for thoracic and of 209.5 ± 27.4 N for the lumbar vertebra. These values were not significantly different from the values found for the entire vertebra (p > 0.05). Based on our findings, failure loads and stiffnesses obtained with reduced CT scans can be successfully used to predict full vertebral failure. This sub-region analysis and power relationship suggests that one can limit radiation exposure to patients when bone characterization is needed.

Graphical abstract

Estimated mechanical properties in relation to the extent of the computed tomography reconstruction

Keywords

Fractures Compression Compressive strength Thoracic vertebrae Lumbar vertebrae Rats 

Notes

Funding information

The work was partially supported by the Aurelio M. Caccomo Family Foundation. F. Mainnemare’s abroad research was fully funded by Fren ch Ecole Normale Supérieur Paris-Saclay.

References

  1. 1.
    Balooch G, Yao W, Ager JW, Balooch M, Nalla RK, Porter AE, Ritchie RO, Lane NE (2007) The aminobisphosphonate risedronate preserves localized mineral and material properties of bone in the presence of glucocorticoids. Arthritis Rheum 56:3726–3737.  https://doi.org/10.1002/art.22976 CrossRefGoogle Scholar
  2. 2.
    Blanchard R, Dejaco A, Bongaers E, Hellmich C (2013) Intravoxel bone micromechanics for microCT-based finite element simulations. J Biomech 46:2710–2721.  https://doi.org/10.1016/j.jbiomech.2013.06.036 CrossRefGoogle Scholar
  3. 3.
    Bouxsein ML, Seeman E (2009) Quantifying the material and structural determinants of bone strength. Best Pract Res Clin Rheumatol 23:741–753.  https://doi.org/10.1016/j.berh.2009.09.008 CrossRefGoogle Scholar
  4. 4.
    Boyd SK, Szabo E, Ammann P (2011) Increased bone strength is associated with improved bone microarchitecture in intact female rats treated with strontium ranelate: a finite element analysis study. Bone 48:1109–1116.  https://doi.org/10.1016/j.bone.2011.01.004 CrossRefGoogle Scholar
  5. 5.
    Brenner DJ, Elliston CD (2004) Estimated radiation risks potentially associated with full-body CT screening. Radiology 232:735–738.  https://doi.org/10.1148/radiol.2323031095
  6. 6.
    Brixen K, Chapurlat R, Cheung AM, Keaveny TM, Fuerst T, Engelke K, Recker R, Dardzinski B, Verbruggen N, Ather S, Rosenberg E, De Papp AE (2013) Bone density, turnover, and estimated strength in postmenopausal women treated with odanacatib: a randomized trial. J Clin Endocrinol Metab 98:571–580.  https://doi.org/10.1210/jc.2012-2972 CrossRefGoogle Scholar
  7. 7.
    Brouwers JEM, Lambers FM, Van Rietbergen B, Ito K, Huiskes R (2009) Comparison of bone loss induced by ovariectomy and neurectomy in rats analyzed by in vivo micro-CT. J Orthop Res 27:1521–1527.  https://doi.org/10.1002/jor.20913 CrossRefGoogle Scholar
  8. 8.
    Burkhart TA, Andrews DM, Dunning CE (2013) Finite element modeling mesh quality, energy balance and validation methods: a review with recommendations associated with the modeling of bone tissue. J Biomech 46:1477–1488.  https://doi.org/10.1016/j.jbiomech.2013.03.022 CrossRefGoogle Scholar
  9. 9.
    Chevalier Y, Pahr D, Zysset PK (2009) The role of cortical shell and trabecular fabric in finite element analysis of the human vertebral body. J Biomech Eng 131:111003.  https://doi.org/10.1115/1.3212097 CrossRefGoogle Scholar
  10. 10.
    Colloca M, Blanchard R, Hellmich C, Ito K, van Rietbergen B (2014) A multiscale analytical approach for bone remodeling simulations: linking scales from collagen to trabeculae. Bone 64:303–313.  https://doi.org/10.1016/j.bone.2014.03.050 CrossRefGoogle Scholar
  11. 11.
    Crawford RP, Cann CE, Keaveny TM (2003) Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone 33:744–750.  https://doi.org/10.1016/S8756-3282(03)00210-2 CrossRefGoogle Scholar
  12. 12.
    Crawley EO, Evans WD, Owen GM (1988) A theoretical analysis of the accuracy of single-energy CT bone-mineral measurements. Phys Med 33:1113–1127.  https://doi.org/10.1088/0031-9155/33/10/002 Google Scholar
  13. 13.
    Dall’Ara E, Karl C, Mazza G, Franzoso G, Vena P, Pretterklieber M, Pahr D, Zysset P (2013) Tissue properties of the human vertebral body sub-structures evaluated by means of microindentation. J Mech Behav Biomed Mater 25:23–32.  https://doi.org/10.1016/j.jmbbm.2013.04.020 CrossRefGoogle Scholar
  14. 14.
    Diamant I, Shahar R, Masharawi Y, Gefen A (2007) A method for patient-specific evaluation of vertebral cancellous bone strength: in vitro validation. Clin Biomech 22:282–291.  https://doi.org/10.1016/j.clinbiomech.2006.10.005 CrossRefGoogle Scholar
  15. 15.
    Easley SK, Jekir MG, Burghardt AJ, Li M, Keaveny TM (2009) Contribution of the intra-specimen variations in tissue mineralization to PTH- and raloxifene-induced changes in stiffness of rat vertebrae. Bone 46:1162–1169.  https://doi.org/10.1016/j.bone.2009.12.009 CrossRefGoogle Scholar
  16. 16.
    Giambini H, Qin X, Dragomir-Daescu D, An K-N, Nassr A (2015) Specimen-specific vertebral fracture modeling: a feasibility study using the extended finite element method. Med Biol Eng Comput 54:583–593.  https://doi.org/10.1007/s11517-015-1348-x CrossRefGoogle Scholar
  17. 17.
    Hausleiter J, Meyer T, Hermann F (2009) Estimated radiation dose associated with cardiac CT angiography. Jama 301Google Scholar
  18. 18.
    Hellmich C, Kober C, Erdmann B (2008) Micromechanics-based conversion of CT data into anisotropic elasticity tensors, applied to FE simulations of a mandible. Ann Biomed Eng 36:108–122.  https://doi.org/10.1007/s10439-007-9393-8 CrossRefGoogle Scholar
  19. 19.
    Henninger HB, Reese SP, Anderson a E, Weiss J a (2010) Validation of computational models in biomechanics. Proc Inst Mech Eng H 224:801–812.  https://doi.org/10.1243/09544119JEIM649 CrossRefGoogle Scholar
  20. 20.
    Imai K, Ohnishi I, Yamamoto S, Nakamura K (2008) In vivo assessment of lumbar vertebral strength in elderly women using computed tomography-based nonlinear finite element model. Spine (Phila. Pa 1976) (33):27–32.  https://doi.org/10.1097/BRS.0b013e31815e3993
  21. 21.
    Ito M, Akifumi A, Ae N, Aoyagi K, Uetani M, Kuniaki A, Ae H, Kawase M (2005) Effects of risedronate on trabecular microstructure and biomechanical properties in ovariectomized rat tibia. doi: https://doi.org/10.1007/s00198-004-1802-3
  22. 22.
    Ito M, Nakayama K, Konaka A, Sakata K, Ikeda K, Maruyama T (2006) Effects of a prostaglandin EP4 agonist, ONO-4819, and risedronate on trabecular microstructure and bone strength in mature ovariectomized rats. Bone 39:453–459.  https://doi.org/10.1016/j.bone.2006.02.054 CrossRefGoogle Scholar
  23. 23.
    Johnell O, Kanis JA (2004) An estimate of the worldwide prevalence, mortality and disability associated with hip fracture. Osteoporos Int 15:897–902.  https://doi.org/10.1007/s00198-004-1627-0 CrossRefGoogle Scholar
  24. 24.
    Kinney JH, Haupt DL, Balooch M, Ladd AJC, Ryaby JT, Lane NE (2000) Three-dimensional morphometry of the L6 vertebra in the ovariectomized rat model of osteoporosis: biomechanical implications. J Bone Miner Res 15:1981–1991.  https://doi.org/10.1359/jbmr.2000.15.10.1981 CrossRefGoogle Scholar
  25. 25.
    Kuefner MA, Grudzenski S, Hamann J, Achenbach S, Lell M, Anders K, Schwab SA, Häberle L, Löbrich M, Uder M (2010) Effect of CT scan protocols on x-ray-induced DNA double-strand breaks in blood lymphocytes of patients undergoing coronary CT angiography. Eur Radiol 20:2917–2924.  https://doi.org/10.1007/s00330-010-1873-9 CrossRefGoogle Scholar
  26. 26.
    Ladd AJC, Kinney JH (1998) Numerical errors and uncertainties in finite-element modeling of trabecular bone. J Biomech 31:941–945.  https://doi.org/10.1016/S0021-9290(98)00108-0 CrossRefGoogle Scholar
  27. 27.
    Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF (2005) Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res 21:466–476.  https://doi.org/10.1359/JBMR.051103 CrossRefGoogle Scholar
  28. 28.
    Li H, Zhang H, Tang Z, Hu G (2008) Micro-computed tomography for small animal imaging: technological details. Prog Nat Sci 18:513–521.  https://doi.org/10.1016/j.pnsc.2008.01.002 CrossRefGoogle Scholar
  29. 29.
    Linet MS, Slovis TL, Miller DL, Kleinerman R, Lee C, Rajaraman P, Gonzalez AB De 2012 Cancer Risks Associated With External Radiation From Diagnostic Imaging Procedures 62, 75–100. doi: https://doi.org/10.3322/caac.21132
  30. 30.
    Mazess RB, Barden HS, Drinka PJ, Bauwens SF, Orwoll ES, Bell NH (1990) Influence of age and body weight on spine and femur bone mineral density in U.S white men. J Bone Miner Res 5:645–652.  https://doi.org/10.1002/jbmr.5650050614 CrossRefGoogle Scholar
  31. 31.
    McNamara LM, Ederveen AGH, Lyons CG, Price C, Schaffler MB, Weinans H, Prendergast PJ (2006) Strength of cancellous bone trabecular tissue from normal, ovariectomized and drug-treated rats over the course of ageing. Bone 39:392–400.  https://doi.org/10.1016/j.bone.2006.02.070 CrossRefGoogle Scholar
  32. 32.
    Melton LJ, Kallmes DF (2006) Epidemiology of vertebral fractures: implications for vertebral augmentation. Acad Radiol 13:538–545.  https://doi.org/10.1016/j.acra.2006.01.005 CrossRefGoogle Scholar
  33. 33.
    Müller R, Kampschulte M, El Khassawna T, Schlewitz G, Hürter B, Böcker W, Bobeth M, Langheinrich AC, Heiss C, Deutsch A, Cuniberti G (2014) Change of mechanical vertebrae properties due to progressive osteoporosis: combined biomechanical and finite-element analysis within a rat model. Med. Biol. Eng. Comput. 52:405–414.  https://doi.org/10.1007/s11517-014-1140-3 CrossRefGoogle Scholar
  34. 34.
    Notomi T, Okimoto N, Okazaki Y, Nakamura T, Suzuki M (2003) Tower climbing exercise started 3 months after ovariectomy recovers bone strength of the femur and lumbar vertebrae in aged osteopenic rats. J Bone Miner Res 18:140–149.  https://doi.org/10.1359/jbmr.2003.18.1.140 CrossRefGoogle Scholar
  35. 35.
    Nyman JS, Uppuganti S, Makowski AJ, Rowland BJ, Merkel AR, Sterling JA, Bredbenner TL, Perrien DS (2015) Predicting mouse vertebra strength with micro-computed tomography-derived finite element analysis. BoneKEy Rep 4:664.  https://doi.org/10.1038/bonekey.2015.31 CrossRefGoogle Scholar
  36. 36.
    Perrien DS, Akel NS, Edwards PK, Carver AA, Bendre MS, Swain FL, Skinner RA, Hogue WR, Nicks KM, Pierson TM, Suva LJ, Gaddy D (2007) Inhibin A Is an Endocrine Stimulator of Bone Mass and Strength. Endocrinology 148(4):1654–1665. doi: https://doi.org/10.1210/en.2006-0848
  37. 37.
    Pistoia W, van Rietbergen B, Lochmüller E-M, Lill CA, Eckstein F, Rüegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848.  https://doi.org/10.1016/S8756-3282(02)00736-6 CrossRefGoogle Scholar
  38. 38.
    Rincón-Kohli L, Zysset PK (2009) Multi-axial mechanical properties of human trabecular bone. Biomech Model Mechanobiol 8:195–208.  https://doi.org/10.1007/s10237-008-0128-z CrossRefGoogle Scholar
  39. 39.
    Shane E, Addesso V, Namerow PB, McMahon DJ, Lo S-H, Staron RB, Zucker M, Pardi S, Maybaum S, Mancini D (2004) Alendronate versus calcitriol for the prevention of bone loss after cardiac transplantation. N Engl J Med 350:767–776.  https://doi.org/10.1056/NEJMoa035617 CrossRefGoogle Scholar
  40. 40.
    Silverman SL (1992) The clinical consequences of vertebral compression fracture. Bone 13:S27–S31.  https://doi.org/10.1016/9756-3282(92)90193-Z CrossRefGoogle Scholar
  41. 41.
    Spatz JM, Ellman R, Cloutier AM, Louis L, Van Vliet M, Suva LJ, Dwyer D, Stolina M, Ke HZ, Bouxsein ML (2013) Sclerostin antibody inhibits skeletal deterioration due to reduced mechanical loading. J Bone Miner Res 28:865–874.  https://doi.org/10.1002/jbmr.1807 CrossRefGoogle Scholar
  42. 42.
    Thomsen JS, Niklassen AS, Ebbesen EN, Brüel A (2013) Age-related changes of vertical and horizontal lumbar vertebral trabecular 3D bone microstructure is different in women and men. Bone 57:47–55.  https://doi.org/10.1016/j.bone.2013.07.025 CrossRefGoogle Scholar
  43. 43.
    Verhulp E, van Rietbergen B, Müller R, Huiskes R (2008) Indirect determination of trabecular bone effective tissue failure properties using micro-finite element simulations. J Biomech 41:1479–1485.  https://doi.org/10.1016/j.jbiomech.2008.02.032 CrossRefGoogle Scholar
  44. 44.
    Vuong J, Hellmich C (2011) Bone fibrillogenesis and mineralization: quantitative analysis and implications for tissue elasticity. J Theor Biol 287:115–130.  https://doi.org/10.1016/j.jtbi.2011.07.028 CrossRefGoogle Scholar
  45. 45.
    Wagner DW, Lindsey DP, Beaupre GS (2011) Deriving tissue density and elastic modulus from microCT bone scans. Bone 49:931–938.  https://doi.org/10.1016/j.bone.2011.07.021 CrossRefGoogle Scholar
  46. 46.
    Wasnich RD (1996) Vertebral fracture epidemiology. Bone 18:179S–183SCrossRefGoogle Scholar
  47. 47.
    Yao W, Cheng Z, Koester KJ, Ager JW, Balooch M, Pham A, Chefo S, Busse C, Ritchie RO, Lane NE (2007) The degree of bone mineralization is maintained with single intravenous bisphosphonates in aged estrogen-deficient rats and is a strong predictor of bone strength. Bone 41(5):804–812CrossRefGoogle Scholar
  48. 48.
    Yeh JK, Aloia JF, Tierney JM, Sprintz S (2000) Effect of treadmill exercise on vertebral and Tibial bone mineral content and bone mineral density in the aged adult rat : determined by dual energy X-ray absorptiometry 234–238Google Scholar
  49. 49.
    Zeinali A, Hashemi B, Akhlaghpoor S (2010) Noninvasive prediction of vertebral body compressive strength using nonlinear finite element method and an image based technique. Phys Medica 26:88–97.  https://doi.org/10.1016/j.ejmp.2009.08.002 CrossRefGoogle Scholar
  50. 50.
    Zioupos P, Currey J (1998) Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 22:57–66.  https://doi.org/10.1016/S8756-3282(97)00228-7 CrossRefGoogle Scholar
  51. 51.
    Zysset P, Qin L, Lang T, Khosla S, Leslie WD, Shepherd JA, Schousboe JT, Engelke K (2015) Clinical use of quantitative computed tomography-based finite element analysis of the hip and spine in the management of osteoporosis in adults: the 2015 ISCD official positions-part II. J Clin Densitom 18:359–392.  https://doi.org/10.1016/j.jocd.2015.06.011 CrossRefGoogle Scholar

Copyright information

© International Federation for Medical and Biological Engineering 2018

Authors and Affiliations

  1. 1.Department of OrthopaedicsUniversity of Illinois at ChicagoChicagoUSA
  2. 2.Department of Orthopaedic SurgeryLouisiana State University Health Science Center of ShreveportShreveportUSA
  3. 3.Department of Mechanical Engineering, ENS CachanUniversité Paris-SaclayCachanFrance
  4. 4.Department of NeurosurgeryUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations