Abstract
Objectives
Although magnetic resonance is widely spread to assess qualitatively disc morphology, a simple method to determine reliably intervertebral disc status is still lacking. Shear wave elastography is a novel technique that allows quantitative evaluation of soft-tissues’ mechanical properties. The aim of this study was to assess preliminary the feasibility and reliability of mechanical characterization of cervical intervertebral discs by elastography and to provide first reference values for asymptomatic subjects.
Methods
Elastographic measurements were performed to determine shear wave speed (SWS) in C6-C7 or C7-T1 disc of 47 subjects; repeatability and inter-operator reproducibility were assessed.
Results
Global average shear wave speed (SWS) was 3.0 ± 0.4 m/s; measurement repeatability and inter-user reproducibility were 7 and 10 %, respectively. SWS was correlated with both subject’s age (p = 1.3 × 10−5) and body mass index (p = 0.008).
Conclusions
Shear wave elastography in intervertebral discs proved reliable and allowed stratification of subjects according to age and BMI. Applications could be relevant, for instance, in early detection of disc degeneration or in follow-up after trauma; these results open the way to larger cohort studies to define the place of this technique in routine intervertebral disc assessment.
Key Points
• A simple method to obtain objectively intervertebral disc status is still lacking
• Shear wave elastography was applied in vivo to assess intervertebral discs
• Elastography showed promising results in biomechanical disc evaluation
• Elastography could be relevant in clinical routine for intervertebral disc assessment
Similar content being viewed by others
References
Andersson GB (1999) Epidemiological features of chronic low-back pain. Lancet 354:581–585
Ehrlich GE (2003) Low back pain. Bull World Health Organ 81:671–676
Murray CJ, Vos T, Lozano R et al (2012) Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2197–2223
Endean A, Palmer KT, Coggon D (2011) Potential of magnetic resonance imaging findings to refine case definition for mechanical low back pain in epidemiological studies: a systematic review. Spine 36:160–169
Cheung KM, Karppinen J, Chan D et al (2009) Prevalence and pattern of lumbar magnetic resonance imaging changes in a population study of one thousand forty-three individuals. Spine 34:934–940
Jacobs B, Ghelman B, Marchisello P (1990) Coexistence of cervical and lumbar disc disease. Spine 15:1261–1264
Matsumoto M, Okada E, Toyama Y, Fujiwara H, Momoshima S, Takahata T (2013) Tandem age-related lumbar and cervical intervertebral disc changes in asymptomatic subjects. Eur Spine J 22:708–713
Teraguchi M, Yoshimura N, Hashizume H et al (2014) Prevalence and distribution of intervertebral disc degeneration over the entire spine in a population-based cohort: the Wakayama Spine Study. Osteoarthr Cartilage 22:104–110
Humzah MD, Soames RW (1988) Human intervertebral disc: Structure and function. Anat Rec 220:337–356
Kurowski P, Kubo A (1986) The Relationship of degeneration of the intervertebral disc to mechanical loading conditions on lumbar vertebrae. Spine 11:726–731
Ruberté LM, Natarajan RN, Andersson GBJ (2009) Influence of single-level lumbar degenerative disc disease on the behavior of the adjacent segments—A finite element model study. J Biomech 42:341–348
Rohlmann A, Zander T, Schmidt H, Wilke H-J, Bergmann G (2006) Analysis of the influence of disc degeneration on the mechanical behaviour of a lumbar motion segment using the finite element method. J Biomech 39:2484–2490
Tanaka N, An HS, Lim T-H, Fujiwara A, Jeon C-H, Haughton VM (2001) The relationship between disc degeneration and flexibility of the lumbar spine. Spine J 1:47–56
Lafage V, Dubousset J, Lavaste F, Skalli W (2004) 3D finite element simulation of Cotrel-Dubousset correction. Comput Aided Surg: Off J Int Soc Comput Aided Surg 9:17–25
Lafon Y, Lafage V, Dubousset J, Skalli W (2009) Intraoperative three-dimensional correction during rod rotation technique. Spine 34:512–519
Aubin CE, Labelle H, Chevrefils C, Desroches G, Clin J, Eng AB (2008) Preoperative planning simulator for spinal deformity surgeries. Spine 33:2143–2152
Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IKY, Bishop PB (1990) Preliminary Evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 15:411–415
Benneker L, Heini P, Anderson S, Alini M, Ito K (2005) Correlation of radiographic and MRI parameters to morphological and biochemical assessment of intervertebral disc degeneration. Eur Spine J 14:27–35
Watanabe A, Benneker LM, Boesch C, Watanabe T, Obata T, Anderson SE (2007) Classification of intervertebral disk degeneration with axial T2 mapping. Am J Roentgenol 189:936–942
Schneiderman G, Flannigan B, Kingston S, Thomas J, Dillin WH, Watkins RG (1987) Magnetic resonance imaging in the diagnosis of disc degeneration: correlation with discography. Spine 12:276–281
Campana S, Charpail E, de Guise JA, Rillardon L, Skalli W, Mitton D (2011) Relationships between viscoelastic properties of lumbar intervertebral disc and degeneration grade assessed by MRI. J Mech Behav Biomed Mater 4:593–599
Mwale F, Demers CN, Michalek AJ et al (2008) Evaluation of quantitative magnetic resonance imaging, biochemical and mechanical properties of trypsin-treated intervertebral discs under physiological compression loading. J Magn Reson Imaging 27:563–573
Périé D, Iatridis JC, Demers CN et al (2006) Assessment of compressive modulus, hydraulic permeability and matrix content of trypsin-treated nucleus pulposus using quantitative MRI. J Biomech 39:1392–1400
Recuerda M, Perie D, Gilbert G, Beaudoin G (2012) Assessment of mechanical properties of isolated bovine intervertebral discs from multi-parametric magnetic resonance imaging. BMC Musculoskelet Disord 13:195
Cortes DH, Magland JF, Wright AC, Elliott DM (2014) The shear modulus of the nucleus pulposus measured using magnetic resonance elastography: A potential biomarker for intervertebral disc degeneration. Magnet Reson Med 72:211–219
Tanter M, Bercoff J, Athanasiou A et al (2008) Quantitative assessment of breast lesion viscoelasticity: initial clinical results using supersonic shear imaging. Ultrasound Med Biol 34:1373–1386
Athanasiou A, Tardivon A, Tanter M et al (2010) Breast lesions: quantitative elastography with supersonic shear imaging–preliminary results. Radiology 256:297–303
Cosgrove D, Berg W, Doré C et al (2012) Shear wave elastography for breast masses is highly reproducible. Eur Radiol 22:1023–1032
Ferraioli G, Tinelli C, Dal Bello B, Zicchetti M, Filice G, Filice C (2012) Accuracy of real-time shear wave elastography for assessing liver fibrosis in chronic hepatitis C: a pilot study. Hepatology 56:2125–2133
Bavu É, Gennisson J-L, Couade M et al (2011) Noninvasive in vivo liver fibrosis evaluation using supersonic shear imaging: a clinical study on 113 hepatitis C virus patients. Ultrasound Med Biol 37:1361–1373
Correas JM, Tissier AM, Khairoune A, Khoury G, Eiss D, Helenon O (2013) Ultrasound elastography of the prostate: state of the art. Diagn Interv Imaging 94:551–560
Vergari C, Rouch P, Dubois G et al (2014) Intervertebral disc characterization by shear wave elastography: an in-vitro preliminary study. Proc Inst Mech Eng H 228:607–615
Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 51:396–409
Sarvazyan AP, Rudenko OV, Swanson SD, Fowlkes JB, Emelianov SY (1998) Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med Biol 24:1419–1435
Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:402–410
Keyes DC, Compere EL (1932) The normal and pathological physiology of the nucleus pulposus of the intervertebral disc. An anatomical, clinical, and experimental study. J Bone Joint Surg 14:897–938
Iatridis JC, Weidenbaum M, Setton LA, Mow VC (1996) Is the nucleus pulposus a solid or a fluid? Mechanical behaviors of the nucleus pulposus of the human intervertebral disc. Spine 21:1174–1184
Royer D, Gennisson JL, Deffieux T, Tanter M (2011) On the elasticity of transverse isotropic soft tissues (L). J Acoust Soc Am 129:2757–2760
Cohen J (1988) Statistical power analysis for the behavioral science. Lawrence Erlbaum Associates, Hillsdale
Lee J, Koh D, Ong CN (1989) Statistical evaluation of agreement between two methods for measuring a quantitative variable. Comput Biol Med 19:61–70
Freemont AJ (2009) The cellular pathobiology of the degenerate intervertebral disc and discogenic back pain. Rheumatology (Oxford) 48:5–10
Pettersson K, Hildingsson C, Toolanen G, Fagerlund M, Bjornebrink J (1997) Disc pathology after whiplash injury. A prospective magnetic resonance imaging and clinical investigation. Spine 22:283–287, discussion 288
Ishihara H, Kanamori M, Kawaguchi Y, Nakamura H, Kimura T (2004) Adjacent segment disease after anterior cervical interbody fusion. Spine J 4:624–628
Stradiotti P, Curti A, Castellazzi G, Zerbi A (2009) Metal-related artifacts in instrumented spine. Techniques for reducing artifacts in CT and MRI: state of the art. Eur Spine J 18:102–108
Jensen MC, Brant-Zawadzki MN, Obuchowski N, Modic MT, Malkasian D, Ross JS (1994) Magnetic resonance imaging of the lumbar spine in people without back pain. New Engl J Med 331:69–73
Skrzypiec D, Pollintine P, Przybyla A, Dolan P, Adams M (2007) The internal mechanical properties of cervical intervertebral discs as revealed by stress profilometry. Eur Spine J 16:1701–1709
Kot BC, Zhang ZJ, Lee AW, Leung VY, Fu SN (2012) Elastic modulus of muscle and tendon with shear wave ultrasound elastography: variations with different technical settings. PLoS One 7:e44348
Lacourpaille L, Hug F, Bouillard K, Hogrel J-Y, Nordez A (2012) Supersonic shear imaging provides a reliable measurement of resting muscle shear elastic modulus. Physiol Meas 33:N19
Mun HS, Choi SH, Kook SH, Choi Y, Jeong WK, Kim Y (2013) Validation of intra- and interobserver reproducibility of shearwave elastography: Phantom study. Ultrasonics 53:1039–1043
Lehto IJ, Tertti MO, Komu ME, Paajanen HEK, Tuominen J, Kormano MJ (1994) Age-related MRI changes at 0.1 T in cervical discs in asymptomatic subjects. Neuroradiology 36:49–53
Scher AT (1990) Premature onset of degenerative disease of the cervical spine in rugby players. S Afr Med J 77:557–558
Jager HJ, Gordon-Harris L, Mehring UM, Goetz GF, Mathias KD (1997) Degenerative change in the cervical spine and load-carrying on the head. Skeletal Radiol 26:475–481
Ebara S, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M (1996) Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine 21:452–461
Acaroglu ER, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M (1995) Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine 20:2690–2701
Liuke M, Solovieva S, Lamminen A et al (2005) Disc degeneration of the lumbar spine in relation to overweight. Int J Obes (Lond) 29:903–908
Weiler C, Lopez-Ramos M, Mayer HM et al (2011) Histological analysis of surgical lumbar intervertebral disc tissue provides evidence for an association between disc degeneration and increased body mass index. BMC Res Notes 4:497
Acknowledgments
The scientific guarantor of this publication is Prof. Wafa Skalli, Arts et Métiers ParisTech, LBM, 151 bd de l'hôpital, 75013 Paris. Jean-Luc Gennisson is a scientific consultant for SuperSonic Imagine, and Mickael Tanter is cofounder and shareholder of SuperSonic Imagine (Aix-en-Provence, France). The other authors declare no relationships with any companies, whose products or services may be related to the subject matter of the article. The authors are grateful to the ParisTech BiomecAM chair program on subject-specific musculoskeletal modelling for funding (with the support of ParisTech and Yves Cotrel Foundations, Société Générale, Proteor and Covea). No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained (ethical committee approval CPP Ile-de-France VI 6036). Written informed consent was obtained from all subjects (patients) in this study. Some study subjects or cohorts have been previously reported in congress communications. Methodology: prospective, experimental, performed at one institution.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vergari, C., Rouch, P., Dubois, G. et al. Non-invasive biomechanical characterization of intervertebral discs by shear wave ultrasound elastography: a feasibility study. Eur Radiol 24, 3210–3216 (2014). https://doi.org/10.1007/s00330-014-3382-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-014-3382-8