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Advances in MR imaging for cervical spondylotic myelopathy

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Abstract

Purpose

To outline the pathogenesis of cervical spondylotic myelopathy (CSM), the correlative abnormalities observed on standard magnetic resonance imaging (MRI), the biological implications and current status of diffusion tensor imaging (DTI), and MR spectroscopy (MRS) as clinical tools, and future directions of MR technology in the management of CSM patients.

Methods

A systematic review of the pathogenesis and current state-of-the-art in MR imaging technology for CSM was performed.

Results

CSM is caused by progressive, degenerative, vertebral column abnormalities that result in spinal cord damage related to both primary mechanical and secondary biological injuries. The T2 signal change on conventional MRI is most commonly associated with neurological deficits, but tends not to be a sensitive predictor of recovery of function. DTI and MRS show altered microstructure and biochemistry that reflect patient-specific pathogenesis.

Conclusion

Advanced imaging techniques, including DTI and MRS, show higher sensitivity to microstructural and biochemical changes within the cord, and may aid in management of CSM patients.

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References

  1. Song T, Chen WJ, Yang B, Zhao HP, Huang JW, Cai MJ, Dong TF, Li TS (2011) Diffusion tensor imaging in the cervical spinal cord. Eur Spine J 20:422–428

    Article  PubMed Central  PubMed  Google Scholar 

  2. Demir A, Ries M, Moonen CT, Vital JM, Dehais J, Arne P, Caille JM, Dousset V (2003) Diffusion-weighted MR imaging with apparent diffusion coefficient and apparent diffusion tensor maps in cervical spondylotic myelopathy. Radiology 229:37–43

    Article  PubMed  Google Scholar 

  3. Facon D, Ozanne A, Fillard P, Lepeintre JF, Tournoux-Facon C, Ducreux D (2005) MR diffusion tensor imaging and fiber tracking in spinal cord compression. AJNR Am J Neuroradiol 26:1587–1594

    PubMed  Google Scholar 

  4. Hernandez E, Mackay AL, MacMillan EL, Madler B, Li DK, Dvorak MF, Cordova T, Ramirez-Manzanares A, Laule C (2009) Diffusion tensor imaging of subjects with cervical spondylotic myelopathy: use of the eigenvalues as indicators of spinal stenosis. Proc Intl Soc Mag Reson Med 17:1309

    Google Scholar 

  5. Jones JG, Cen SY, Lebel RM, Hsieh PC, Law M (2012) Diffusion tensor imaging correlates with the clinical assessment of disease severity in cervical spondylotic myelopathy and predicts outcome following surgery. AJNR Am J Neuroradiol 34:471–478

    Article  PubMed  Google Scholar 

  6. Holly LT, Freitas B, McArthur DL, Salamon N (2009) Proton magnetic resonance spectroscopy to evaluate spinal cord axonal injury in cervical spondylotic myelopathy. J Neurosurg Spine 10:194–200

    Article  PubMed  Google Scholar 

  7. Fehlings MG, Skaf G (1998) A review of the pathophysiology of cervical spondylotic myelopathy with insights for potential novel mechanisms drawn from traumatic spinal cord injury. Spine (Phila Pa 1976) 23:2730–2737

    Article  CAS  Google Scholar 

  8. Fujiwara K, Yonenobu K, Ebara S, Yamashita K, Ono K (1989) The prognosis of surgery for cervical compression myelopathy. An analysis of the factors involved. J Bone Joint Surg Br 71:393–398

    CAS  PubMed  Google Scholar 

  9. Henderson FC, Geddes JF, Vaccaro AR, Woodard E, Berry KJ, Benzel EC (2005) Stretch-associated injury in cervical spondylotic myelopathy: new concept and review. Neurosurgery 56:1101–1113 (discussion 1101–1113)

    PubMed  Google Scholar 

  10. Kim DH, Vaccaro AR, Henderson FC, Benzel EC (2003) Molecular biology of cervical myelopathy and spinal cord injury: role of oligodendrocyte apoptosis. Spine J 3:510–519

    Article  PubMed  Google Scholar 

  11. Yamaura I, Yone K, Nakahara S, Nagamine T, Baba H, Uchida K, Komiya S (2002) Mechanism of destructive pathologic changes in the spinal cord under chronic mechanical compression. Spine (Phila Pa 1976) 27:21–26

    Article  Google Scholar 

  12. Baptiste DC, Fehlings MG (2006) Pathophysiology of cervical myelopathy. Spine J 6:190S–197S

    Article  PubMed  Google Scholar 

  13. Wada E, Yonenobu K, Suzuki S, Kanazawa A, Ochi T (1999) Can intramedullary signal change on magnetic resonance imaging predict surgical outcome in cervical spondylotic myelopathy? Spine (Phila Pa 1976) 24:455–461 (discussion 462)

    Article  CAS  Google Scholar 

  14. Matsuda Y, Miyazaki K, Tada K, Yasuda A, Nakayama T, Murakami H, Matsuo M (1991) Increased MR signal intensity due to cervical myelopathy. Analysis of 29 surgical cases. J Neurosurg 74:887–892

    Article  CAS  PubMed  Google Scholar 

  15. Mehalic TF, Pezzuti RT, Applebaum BI (1990) Magnetic resonance imaging and cervical spondylotic myelopathy. Neurosurgery 26:217–226 (discussion 217–226)

    Article  CAS  PubMed  Google Scholar 

  16. Yukawa Y, Kato F, Yoshihara H, Yanase M, Ito K (2007) MR T2 image classification in cervical compression myelopathy: predictor of surgical outcomes. Spine (Phila Pa 1976) 32:1675–1678 (discussion 1679)

    Article  Google Scholar 

  17. Kadanka Z, Bednarik J, Vohanka S, Vlach O, Stejskal L, Chaloupka R, Filipovicova D, Surelova D, Adamova B, Novotny O, Nemec M, Smrcka V, Urbanek I (2000) Conservative treatment versus surgery in spondylotic cervical myelopathy: a prospective randomised study. Eur Spine J 9:538–544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Mummaneni PV, Kaiser MG, Matz PG, Anderson PA, Groff M, Heary R, Holly L, Ryken T, Choudhri T, Vresilovic E, Resnick D (2009) Preoperative patient selection with magnetic resonance imaging, computed tomography, and electroencephalography: does the test predict outcome after cervical surgery? J Neurosurg Spine 11:119–129

    Article  PubMed  Google Scholar 

  19. Mastronardi L, Elsawaf A, Roperto R, Bozzao A, Caroli M, Ferrante M, Ferrante L (2007) Prognostic relevance of the postoperative evolution of intramedullary spinal cord changes in signal intensity on magnetic resonance imaging after anterior decompression for cervical spondylotic myelopathy. J Neurosurg Spine 7:615–622

    Article  PubMed  Google Scholar 

  20. Park YS, Nakase H, Kawaguchi S, Sakaki T, Nikaido Y, Morimoto T (2006) Predictors of outcome of surgery for cervical compressive myelopathy: retrospective analysis and prospective study. Neurol Med Chir (Tokyo) 46:231–239

    Article  Google Scholar 

  21. Ito T, Oyanagi K, Takahashi H, Takahashi HE, Ikuta F (1996) Cervical spondylotic myelopathy. Clinicopathologic study on the progression pattern and thin myelinated fibers of the lesions of seven patients examined during complete autopsy. Spine (Phila Pa 1976) 21:827–833

    Article  CAS  Google Scholar 

  22. Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254

    Article  CAS  PubMed  Google Scholar 

  23. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8:333–344

    Article  CAS  PubMed  Google Scholar 

  25. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219

    Article  CAS  PubMed  Google Scholar 

  26. Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906

    Article  CAS  PubMed  Google Scholar 

  27. Ellingson BM, Ulmer JL, Schmit BD (2007) Gray and white matter delineation in the human spinal cord using diffusion tensor imaging and fuzzy logic. Acad Radiol 14:847–858

    Article  PubMed  Google Scholar 

  28. Ennis DB, Kindlmann G (2006) Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magn Reson Med 55:136–146

    Article  PubMed  Google Scholar 

  29. Ford JC, Hackney DB (1997) Numerical model for calculation of apparent diffusion coefficients (ADC) in permeable cylinders—comparison with measured ADC in spinal cord white matter. Magn Reson Med 37:387–394

    Article  CAS  PubMed  Google Scholar 

  30. Ford JC, Hackney DB, Lavi E, Phillips M, Patel U (1998) Dependence of apparent diffusion coefficients on axonal spacing, membrane permeability, and diffusion time in spinal cord white matter. J Magn Reson Imaging 8:775–782

    Article  CAS  PubMed  Google Scholar 

  31. Nilsson M, Latt J, Stahlberg F, van Westen D, Hagslatt H (2012) The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study. NMR Biomed 25:795–805

    Article  PubMed  Google Scholar 

  32. Benae JL, Ellingson BM, Kurpad SN, Kocak M, Wang MC (2009) Diffusion tensor MR imaging in degenerative cervical stenosis. In: Congress of Neurological Surgeons Annual Meeting. New Orleans, LA

  33. Mamata H, Jolesz FA, Maier SE (2005) Apparent diffusion coefficient and fractional anisotropy in spinal cord: age and cervical spondylosis-related changes. J Magn Reson Imaging 22:38–43

    Article  PubMed  Google Scholar 

  34. Uda T, Takami T, Tsuyuguchi N, Sakamoto S, Yamagata T, Ikeda H, Nagata T, Ohata K (2012) Assessment of cervical spondylotic myelopathy using diffusion tensor MRI parameter at 3.0 tesla. Spine (Phila Pa 1976) 38:407–414

    Article  Google Scholar 

  35. Hori M, Fukunaga I, Masutani Y, Nakanishi A, Shimoji K, Kamagata K, Asahi K, Hamasaki N, Suzuki Y, Aoki S (2012) New diffusion metrics for spondylotic myelopathy at an early clinical stage. Eur Radiol 22:1797–1802

    Article  PubMed Central  PubMed  Google Scholar 

  36. Kara B, Celik A, Karadereler S, Ulusoy L, Ganiyusufoglu K, Onat L, Mutlu A, Ornek I, Sirvanci M, Hamzaoglu A (2011) The role of DTI in early detection of cervical spondylotic myelopathy: a preliminary study with 3-T MRI. Neuroradiology 53:609–616

    Article  PubMed  Google Scholar 

  37. Kerkovsky M, Bednarik J, Dusek L, Sprlakova-Pukova A, Urbanek I, Mechl M, Valek V, Kadanka Z (2012) Magnetic resonance diffusion tensor imaging in patients with cervical spondylotic spinal cord compression: correlations between clinical and electrophysiological findings. Spine (Phila Pa 1976) 37:48–56

    Article  Google Scholar 

  38. Budzik JF, Balbi V, Le Thuc V, Duhamel A, Assaker R, Cotten A (2011) Diffusion tensor imaging and fibre tracking in cervical spondylotic myelopathy. Eur Radiol 21:426–433

    Article  PubMed  Google Scholar 

  39. Hori M, Okubo T, Aoki S, Kumagai H, Araki T (2006) Line scan diffusion tensor MRI at low magnetic field strength: feasibility study of cervical spondylotic myelopathy in an early clinical stage. J Magn Reson Imaging 23:183–188

    Article  PubMed  Google Scholar 

  40. Lindberg PG, Feydy A, Sanchez K, Rannou F, Maier MA (2011) Measures of spinal canal stenosis and relationship to spinal cord structure in patients with cervical spondylosis. J Neuroradiol 39:236–242

    Article  PubMed  Google Scholar 

  41. Lee JW, Kim JH, Park JB, Park KW, Yeom JS, Lee GY, Kang HS (2011) Diffusion tensor imaging and fiber tractography in cervical compressive myelopathy: preliminary results. Skeletal Radiol 40:1543–1551

    Article  PubMed  Google Scholar 

  42. Xiangshui M, Xiangjun C, Xiaoming Z, Qingshi Z, Yi C, Chuanqiang Q, Xiangxing M, Chuanfu L, Jinwen H (2010) 3 T magnetic resonance diffusion tensor imaging and fibre tracking in cervical myelopathy. Clin Radiol 65:465–473

    Article  CAS  PubMed  Google Scholar 

  43. Sato T, Horikoshi T, Watanabe A, Uchida M, Ishigame K, Araki T, Kinouchi H (2012) Evaluation of cervical myelopathy using apparent diffusion coefficient measured by diffusion-weighted imaging. AJNR Am J Neuroradiol 33:388–392

    Article  CAS  PubMed  Google Scholar 

  44. Aota Y, Niwa T, Uesugi M, Yamashita T, Inoue T, Saito T (2008) The correlation of diffusion-weighted magnetic resonance imaging in cervical compression myelopathy with neurologic and radiologic severity. Spine (Phila Pa 1976) 33:814–820

    Article  Google Scholar 

  45. Tsuchiya K, Katase S, Fujikawa A, Hachiya J, Kanazawa H, Yodo K (2003) Diffusion-weighted MRI of the cervical spinal cord using a single-shot fast spin-echo technique: findings in normal subjects and in myelomalacia. Neuroradiology 45:90–94

    CAS  PubMed  Google Scholar 

  46. Wang W, Qin W, Hao N, Wang Y, Zong G (2012) Diffusion tensor imaging in spinal cord compression. Acta Radiol 53:921–928

    Article  PubMed  Google Scholar 

  47. Cheung MM, Li DT, Hui ES, Fan S, Ding AY, Hu Y, Wu EX (2009) In vivo diffusion tensor imaging of chronic spinal cord compression in rat model. Conf Proc IEEE Eng Med Biol Soc 2009:2715–2718

    PubMed  Google Scholar 

  48. Ellingson BM, Ulmer JL, Kurpad SN, Schmit BD (2008) Diffusion tensor MR imaging in chronic spinal cord injury. AJNR Am J Neuroradiol 29:1976–1982

    Article  CAS  PubMed  Google Scholar 

  49. Deo AA, Grill RJ, Hasan KM, Narayana PA (2006) In vivo serial diffusion tensor imaging of experimental spinal cord injury. J Neurosci Res 83:801–810

    Article  CAS  PubMed  Google Scholar 

  50. Harkey HL, al-Mefty O, Marawi I, Peeler DF, Haines DE, Alexander LF (1995) Experimental chronic compressive cervical myelopathy: effects of decompression. J Neurosurg 83:336–341

    Article  CAS  PubMed  Google Scholar 

  51. Bennett MH, McCallum JE (1977) Experimental decompression of spinal cord. Surg Neurol 8:63–67

    CAS  PubMed  Google Scholar 

  52. DeGirolami U, Zivin JA (1982) Neuropathology of experimental spinal cord ischemia in the rabbit. J Neuropathol Exp Neurol 41:129–149

    Article  CAS  PubMed  Google Scholar 

  53. Gooding MR, Wilson CB, Hoff JT (1975) Experimental cervical myelopathy. Effects of ischemia and compression of the canine cervical spinal cord. J Neurosurg 43:9–17

    Article  CAS  PubMed  Google Scholar 

  54. Hukuda S, Wilson CB (1972) Experimental cervical myelopathy: effects of compression and ischemia on the canine cervical cord. J Neurosurg 37:631–652

    Article  CAS  PubMed  Google Scholar 

  55. Wilson CB, Bertan V, Norrell HA Jr, Hukuda S (1969) Experimental cervical myelopathy. II. Acute ischemic myelopathy. Arch Neurol 21:571–589

    Article  CAS  PubMed  Google Scholar 

  56. Jones J, Lerner A, Kim PE, Law M, Hsieh PC (2011) Diffusion tensor imaging in the assessment of ossification of the posterior longitudinal ligament: a report on preliminary results in 3 cases and review of the literature. Neurosurg Focus 30:E14

    Article  PubMed  Google Scholar 

  57. Cui JL, Wen CY, Hu Y, Mak KC, Mak KH, Luk KD (2011) Orientation entropy analysis of diffusion tensor in healthy and myelopathic spinal cord. Neuroimage 58:1028–1033

    Article  PubMed  Google Scholar 

  58. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632

    Article  CAS  PubMed  Google Scholar 

  59. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269

    Article  CAS  PubMed  Google Scholar 

  60. Blamire AM, Cader S, Lee M, Palace J, Matthews PM (2007) Axonal damage in the spinal cord of multiple sclerosis patients detected by magnetic resonance spectroscopy. Magn Reson Med 58:880–885

    Article  CAS  PubMed  Google Scholar 

  61. Kendi AT, Tan FU, Kendi M, Yilmaz S, Huvaj S, Tellioglu S (2004) MR spectroscopy of cervical spinal cord in patients with multiple sclerosis. Neuroradiology 46:764–769

    Article  PubMed  Google Scholar 

  62. Cooke FJ, Blamire AM, Manners DN, Styles P, Rajagopalan B (2004) Quantitative proton magnetic resonance spectroscopy of the cervical spinal cord. Magn Reson Med 51:1122–1128

    Article  CAS  PubMed  Google Scholar 

  63. Yu WR, Baptiste DC, Liu T, Odrobina E, Stanisz GJ, Fehlings MG (2009) Molecular mechanisms of spinal cord dysfunction and cell death in the spinal hyperostotic mouse: implications for the pathophysiology of human cervical spondylotic myelopathy. Neurobiol Dis 33:149–163

    Article  CAS  PubMed  Google Scholar 

  64. Tobias CA, Han SS, Shumsky JS, Kim D, Tumolo M, Dhoot NO, Wheatley MA, Fischer I, Tessler A, Murray M (2005) Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression. J Neurotrauma 22:138–156

    Article  PubMed  Google Scholar 

  65. Xu K, Uchida K, Nakajima H, Kobayashi S, Baba H (2006) Targeted retrograde transfection of adenovirus vector carrying brain-derived neurotrophic factor gene prevents loss of mouse (twy/twy) anterior horn neurons in vivo sustaining mechanical compression. Spine (Phila Pa 1976) 31:1867–1874

    Article  Google Scholar 

  66. Holly LT, Blaskiewicz D, Wu A, Feng C, Ying Z, Gomez-Pinilla F (2012) Dietary therapy to promote neuroprotection in chronic spinal cord injury. J Neurosurg Spine 17:134–140

    Article  PubMed Central  PubMed  Google Scholar 

  67. Ellingson BM, Schmit BD, Gourab K, Sieber-Blum M, Hu YF, Schmainda KM (2009) Diffusion heterogeneity tensor MRI (Alpha-DTI): mathematics and initial applications in spinal cord regeneration after trauma. Biomed Sci Instrum 45:167–172

    Google Scholar 

  68. Nossin-Manor R, Duvdevani R, Cohen Y (2002) q-Space high b value diffusion MRI of hemi-crush in rat spinal cord: evidence for spontaneous regeneration. Magn Reson Imaging 20:231–241

    Article  PubMed  Google Scholar 

  69. Assaf Y, Mayk A, Eliash S, Speiser Z, Cohen Y (2003) Hypertension and neuronal degeneration in excised rat spinal cord studied by high-b value q-space diffusion magnetic resonance imaging. Exp Neurol 184:726–736

    Article  PubMed  Google Scholar 

  70. Biton IE, Mayk A, Assaf Y, Cohen Y (2004) Structural changes in glutamate cell swelling followed by multiparametric q-space diffusion MR of excised rat spinal cord. Magn Reson Imaging 22:661–672

    Article  CAS  PubMed  Google Scholar 

  71. Nossin-Manor R, Duvdevani R, Cohen Y (2007) Spatial and temporal damage evolution after hemi-crush injury in rat spinal cord obtained by high b-value q-space diffusion magnetic resonance imaging. J Neurotrauma 24:481–491

    Article  PubMed  Google Scholar 

  72. van Zijl PC, Yadav NN (2011) Chemical exchange saturation transfer (CEST): what is in a name and what isn’t? Magn Reson Med 65:927–948

    Article  PubMed Central  PubMed  Google Scholar 

  73. Ng MC, Hua J, Hu Y, Luk KD, Lam EY (2009) Magnetization transfer (MT) asymmetry around the water resonance in human cervical spinal cord. J Magn Reson Imaging 29:523–528

    Article  PubMed  Google Scholar 

  74. Wilhelm MJ, Ong HH, Wehrli SL, Li C, Tsai PH, Hackney DB, Wehrli FW (2012) Direct magnetic resonance detection of myelin and prospects for quantitative imaging of myelin density. Proc Natl Acad Sci USA 109:9605–9610

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Cohen-Adad J, El Mendili MM, Lehericy S, Pradat PF, Blancho S, Rossignol S, Benali H (2011) Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI. Neuroimage 55:1024–1033

    Article  CAS  PubMed  Google Scholar 

  76. Stroman PW (2005) Magnetic resonance imaging of neuronal function in the spinal cord: spinal FMRI. Clin Med Res 3:146–156

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

Research support: NIH 1R21NS065419-01A1 and 1R01NS078494-01A1.

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Correspondence to Langston T. Holly.

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Ellingson, B.M., Salamon, N. & Holly, L.T. Advances in MR imaging for cervical spondylotic myelopathy. Eur Spine J 24 (Suppl 2), 197–208 (2015). https://doi.org/10.1007/s00586-013-2915-1

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  • DOI: https://doi.org/10.1007/s00586-013-2915-1

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