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MRI imaging of the spinal cord in multiple sclerosis

PART OF MS Alumni FEATURE
MRI imaging of the spinal cord in multiple sclerosis
  • Neurology

Lucia Moiola Scientific Institute San Raffaele, Milan, Italy

Spinal cord (SC) lesions are a common finding in multiple sclerosis (MS) patients, and are less frequent in healthy aging and in patients affected by other neurologic disorders. At post-mortem analysis, SC lesions are present in up to 86% of patients with MS1, while, using magnetic resonance imaging (MRI), asymptomatic SC lesions have been described in up to 30-40% of patients presenting with a clinically isolated syndrome (CIS) and in about 90% of patients with definite MS 2. For these reasons, spinal MRI is a powerful tool in the diagnosis of MS and SC lesions have been incorporated in the MS diagnostic criteria since 2001. 3-5 Moreover, the 2010 update to Mc Donald criteria , established a central role of SC lesions that have now the same importance as brain lesions at MRI scan. Recently, Sombekke et al. 6 showed that the presence of SC lesions facilitates the diagnosis of MS and is associated with a higher risk of conversion to definite MS (odds ratio: 14.4; 95% confidence interval: 2.6–80.0) and with a shorter time to conversion to MS (hazard ratio: 51.4; 95% confidence interval: 5.5–476.3), especially in patients presenting with first symptoms non originating from the spinal cord who do not fulfil brain MRI criteria. These findings support the recommendation to perform a spinal cord MRI scan also in patients with nonspinal CIS suggestive of MS.

Nowadays MRI techniques allow to easily scan the entire spinal cord with an high resolution; among these, sagittal dual-echo sequences are commonly used 2 with conventional spin echo (CSE) and fast spin echo (FSE)/turbo spin echo (TSE) sequences showing similar sensitivities 7, 8. Dual echo T2-weighted MRI should be applied because of the ability to detect spinal cord lesions limiting the high signal intensity of the cerebro-spinal fluid (CSF) which appears isointense to normal spinal cord. So doing, SC lesions slightly hyperintense to CSF can be found out.

 Several studies 7, 9 suggested that fast short-tau inversion recovery (STIR) sequences allow the detection of up to 66% more lesions than FSE/TSE sequences, whereas the results provided by fast-fluid attenuated inversion recovery (FLAIR) sequences in imaging the cord are unsatisfactory 10 and FLAIR technique is considered not suitable for spinal cord imaging.

MRI features of SC lesions in MS

MS cord lesions are more frequently observed in the cervical region, are usually peripheral, limited to two vertebral segments in length or less and occupy less than half the cross-sectional area (CSA) of the cord. Acute lesions may be associated with cord swelling 11. Localized cord atrophy is typically absent 2 and “black holes” (T1-hypointense lesions) are rarely seen in the spinal cord, possibly because of its compact tissue organization 12. In patient with relapsing-remitting MS (RRMS), multiple, focal lesions are usually detected 13, 14, whereas, in patients with primary progressive (PP) and secondary progressive (SP) MS, spinal cord abnormalities tend to be extensive and confluent 13, 15. In PPMS patients, the cord abnormalities may be more conspicuous than brain abnormalities 16. Gadolinium (Gd)-enhancing lesions are less frequently seen in the spinal cord than in the brain 14, 17, but they are more often associated with new clinical symptoms 14.

Nonconventional MRI techniques

Despite the spinal cord is an eloquent area commonly affected in MS, the correlation between the extent of cord abnormalities and clinical disability are conflicting, both in cross-sectional and longitudinal studies. For this reason, other MRI measures have been investigated to improve the so called “clinico-radiological paradox in MS”.

Atrophy of the spinal cord is frequently seen in MS patients, especially in those with the progressive forms of the disease 16, 18, 19, possibly due to axonal degeneration. In particular, the spinal cord CSA seems to correlate better with clinical disability than the extent of focal lesions 18, 20. Recently, a new semi-automatic method 21, which allows segmentation of long portions of the cord, has been implemented. Using such an approach, Rocca et al. 22 found that cord CSA differs significantly among the main MS clinical phenotypes and is correlated with the Expanded Disability Status Scale (EDSS) 23 score in RRMS, SPMS and PPMS. Using a voxel-based analisys, Valsasina et al., 24 showed that RRMS patients had a few clusters of regional atrophy mainly located in the posterior and lateral columns, while SPMS patients had a more diffuse cord atrophy, which was significantly correlated with EDSS score. In another study, including all the main MS clinical phenotypes, Rocca et al. 25 described cord atrophy in PPMS but not in CIS patients compared to healthy controls as well as clusters of cord atrophy in benign form of MS (BMS) vs. RRMS, and in SPMS vs. RRMS, BMS and PPMS. In progressive MS, regional cord atrophy was correlated with clinical disability and impairment in the pyramidal system. Finally, the analysis of T2 lesion probability maps showed that SPMS, RRMS and PPMS had an higher probability of having spinal cord lesions.

Using more sophisticated MR receiver coils and fast imaging techniques, which have led to a more reliable imaging of the cord, other quantitative techniques have been applied to assess the spinal cord damage. Abnormal magnetization transfer (MT) and diffusion tensor (DT) MRI quantities from the cervical cord have been shown in patients with established MS, but not in those with CIS 26. Conventional and DT MRI of the cervical cord was recently obtained from relapse-onset MS patients at baseline and after a mean follow up of 2.4 years 27: baseline cord cross-sectional area and fractional anisotropy (FA) correlated with an increased disability at follow up 27. Using a MT-weighted approach, Zackowsk at al. 28 showed that signal abnormalities in the dorsal and lateral columns of the spinal cord correlate with dysfunctions of vibration sensation and strenght, respectively.

Moreover, spinal cord spectroscopy and diffusion-based tractography allow to detect a reduction in N-Acetyl-aspartate (NAA) and in the structural connectivity in the lateral corticospinal tract (CST) and posterior tracts in  MS patients with a cervical cord relapse , correlating with disability 29.

Finally, an increased functional MRI (fMRI) activation of the cervical cord has been demonstrated in all the major MS clinical phenotypes and has been related to the severity of clinical disability and the extent of tissue damage 30-33.

In conclusion, high-quality MRI imaging of the cervical cord is now feasible. The application of conventional and quantitative MRI techniques to study the spinal cord might improve the diagnosis of MS and our understanding of the structural and functional changes of the central nervous system associated to MS as well as to aging, to other demyelinating disorders, and to degenerative conditions. This might contribute to understand “what is lost”, “what is left”, and functional adaptation responsible for the different clinical patterns of neurological diseases as well as to improve the definition of their pathophysiological mechanisms.

References:

1. Ikuta F, Zimmerman HM. Distribution of plaques in seventy autopsy cases of multiple sclerosis in the United States. Neurology. Jun 1976;26(6 PT 2):26-28.

2. Lycklama G, Thompson A, Filippi M, et al. Spinal-cord MRI in multiple sclerosis. Lancet Neurol. Sep 2003;2(9):555-562.

3. McDonald WI, Compston A, Edan G, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. Jul 2001;50(1):121-127.

4. Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. Feb 2011;69(2):292-302.

5. Polman CH, Reingold SC, Edan G, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol. Dec 2005;58(6):840-846.

6. Sombekke MH, Wattjes MP, Balk LJ, et al. Spinal cord lesions in patients with clinically isolated syndrome: A powerful tool in diagnosis and prognosis. Neurology. Jan 1 2013;80(1):69-75.

7. Hittmair K, Mallek R, Prayer D, Schindler EG, Kollegger H. Spinal cord lesions in patients with multiple sclerosis: comparison of MR pulse sequences. AJNR Am J Neuroradiol. Sep 1996;17(8):1555-1565.

8. Lycklama a Nijeholt GJ, Castelijns JA, Weerts J, et al. Sagittal MR of multiple sclerosis in the spinal cord: fast versus conventional spin-echo imaging. AJNR Am J Neuroradiol. Feb 1998;19(2):355-360.

9. Rocca MA, Mastronardo G, Horsfield MA, et al. Comparison of three MR sequences for the detection of cervical cord lesions in patients with multiple sclerosis. AJNR Am J Neuroradiol. Oct 1999;20(9):1710-1716.

10. Filippi M, Yousry TA, Alkadhi H, Stehling M, Horsfield MA, Voltz R. Spinal cord MRI in multiple sclerosis with multicoil arrays: a comparison between fast spin echo and fast FLAIR. J Neurol Neurosurg Psychiatry. Dec 1996;61(6):632-635.

11. Thielen KR, Miller GM. Multiple sclerosis of the spinal cord: magnetic resonance appearance. J Comput Assist Tomogr. May-Jun 1996;20(3):434-438.

12. Gass A, Filippi M, Rodegher ME, Schwartz A, Comi G, Hennerici MG. Characteristics of chronic MS lesions in the cerebrum, brainstem, spinal cord, and optic nerve on T1-weighted MRI. Neurology. Feb 1998;50(2):548-550.

13. Tartaglino LM, Friedman DP, Flanders AE, Lublin FD, Knobler RL, Liem M. Multiple sclerosis in the spinal cord: MR appearance and correlation with clinical parameters. Radiology. Jun 1995;195(3):725-732.

14. Thorpe JW, Kidd D, Moseley IF, et al. Serial gadolinium-enhanced MRI of the brain and spinal cord in early relapsing-remitting multiple sclerosis. Neurology. Feb 1996;46(2):373-378.

15. Nijeholt GJ, van Walderveen MA, Castelijns JA, et al. Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. Brain. Apr 1998;121 ( Pt 4):687-697.

16. Kidd D, Thorpe JW, Thompson AJ, et al. Spinal cord MRI using multi-array coils and fast spin echo. II. Findings in multiple sclerosis. Neurology. Dec 1993;43(12):2632-2637.

17. Kidd D, Thorpe JW, Kendall BE, et al. MRI dynamics of brain and spinal cord in progressive multiple sclerosis. J Neurol Neurosurg Psychiatry. Jan 1996;60(1):15-19.

18. Losseff NA, Webb SL, O'Riordan JI, et al. Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain. Jun 1996;119 ( Pt 3):701-708.

19. Stevenson VL, Leary SM, Losseff NA, et al. Spinal cord atrophy and disability in MS: a longitudinal study. Neurology. Jul 1998;51(1):234-238.

20. Lin X, Tench CR, Evangelou N, Jaspan T, Constantinescu CS. Measurement of spinal cord atrophy in multiple sclerosis. J Neuroimaging. Jul 2004;14(3 Suppl):20S-26S.

21. Horsfield MA, Sala S, Neema M, et al. Rapid semi-automatic segmentation of the spinal cord from magnetic resonance images: Application in multiple sclerosis. Neuroimage. Jan 7 2010.

22. Rocca MA, Horsfield MA, Sala S, et al. A multicenter assessment of cervical cord atrophy among MS clinical phenotypes. Neurology. Jun 14 2011;76(24):2096-2102.

23. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. Nov 1983;33(11):1444-1452.

24. Valsasina P, Horsfield MA, Rocca MA, Absinta M, Comi G, Filippi M. Spatial Normalization and Regional Assessment of Cord Atrophy: Voxel-Based Analysis of Cervical Cord 3D T1-Weighted Images. AJNR Am J Neuroradiol. Jun 7 2012.

25. Rocca MA, Valsasina P, Damjanovic D, et al. Voxel-wise mapping of cervical cord damage in multiple sclerosis patients with different clinical phenotypes. j Neurol Neurosurg Psychiatry. 2012.

26. Agosta F, Filippi M. MRI of spinal cord in multiple sclerosis. J Neuroimaging. Apr 2007;17 Suppl 1:46S-49S.

27. Agosta F, Absinta M, Sormani MP, et al. In vivo assessment of cervical cord damage in MS patients: a longitudinal diffusion tensor MRI study. Brain. Aug 2007;130(Pt 8):2211-2219.

28. Zackowski KM, Smith SA, Reich DS, et al. Sensorimotor dysfunction in multiple sclerosis and column-specific magnetization transfer-imaging abnormalities in the spinal cord. Brain. May 2009;132(Pt 5):1200-1209.

29. Ciccarelli O, Wheeler-Kingshott CA, McLean MA, et al. Spinal cord spectroscopy and diffusion-based tractography to assess acute disability in multiple sclerosis. Brain. Aug 2007;130(Pt 8):2220-2231.

30. Agosta F, Valsasina P, Absinta M, Sala S, Caputo D, Filippi M. Primary progressive multiple sclerosis: tactile-associated functional MR activity in the cervical spinal cord. Radiology. Oct 2009;253(1):209-215.

31. Valsasina P, Agosta F, Absinta M, Sala S, Caputo D, Filippi M. Cervical Cord Functional MRI Changes in Relapse-Onset MS Patients. J Neurol Neurosurg Psychiatry. Dec 3 2009.

32. Agosta F, Valsasina P, Rocca MA, et al. Evidence for enhanced functional activity of cervical cord in relapsing multiple sclerosis. Magn Reson Med. May 2008;59(5):1035-1042.

33. Agosta F, Valsasina P, Caputo D, Stroman PW, Filippi M. Tactile-associated recruitment of the cervical cord is altered in patients with multiple sclerosis. Neuroimage. Feb 15 2008;39(4):1542-1548.

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Preceptorship
Milan, Italy
Oct 30 - 31, 2014
Target audience
Clinicians and scientists currently involved in MS and/or NMO management., Radiologists
EACCME®
by Excemed
Neurology

MS Alumni

The MS Alumni programme is an educational initiative of EXCEMED that is intended to provide ongoing support for young physicians and specialists in neurology.