Advertisement

Journal of Neural Transmission

, Volume 122, Issue 10, pp 1465–1473 | Cite as

Putaminal alteration in multiple sclerosis patients with spinal cord lesions

  • Hilga Zimmermann
  • Hans O. Rolfsnes
  • Swantje Montag
  • Janine Wilting
  • Amgad Droby
  • Eva Reuter
  • Joachim Gawehn
  • Frauke Zipp
  • Adriane Gröger
Neurology and Preclinical Neurological Studies - Original Article

Abstract

Typical multiple sclerosis (MS) lesions occur in the brain as well as in the spinal cord. However, two extreme magnetic resonance imaging phenotypes appear occasionally: those with predominantly spinal cord lesions (MS + SL) and those with cerebral lesions and no detectable spinal lesions (MS + CL). We assessed whether morphological differences can be found between these two extreme phenotypes. We examined 19 patients with MS + SL, 18 with MS + CL and 20 controls. All subjects were examined using magnetic resonance imaging, including anatomical and diffusion tensor imaging sequences. Voxel-based morphologic and regions of interest-based analyses and tract-based spatial statistics were performed. Patients also underwent neuropsychological testing. Demographic, clinical and neuropsychological characteristics did not differ between MS + SL and MS + CL patients. Patients with MS + SL showed significantly larger putamen volumes than those with MS + CL which correlated negatively with disability. Compared to controls, only MS + CL revealed clear cortical and deep gray matter atrophy, which correlated with cerebral lesion volume. Additionally, extensive white matter microstructural damage was found only in MS + CL compared to MS + SL and controls in the tract-based spatial statistics. Higher putamen volumes in MS + SL could suggest compensatory mechanisms in this area responsible for motor control. Widely reduced fractional anisotropy values in MS + CL were caused by higher cerebral lesion volume and thus presumably stronger demyelination, which subsequently leads to higher global gray matter atrophy.

Keywords

Multiple sclerosis VBM TBSS Putamen 

Notes

Acknowledgments

This study was supported by the Ministry of Science and Education/German Competence Network for Multiple Sclerosis (BMBF/KKNMS, B7.3 to FZ).

References

  1. Barkhof F (2002) The clinico-radiological paradox in multiple sclerosis revisited. Curr Opin Neurol 15(3):239–245CrossRefPubMedGoogle Scholar
  2. Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH (2012) Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol 259(1):139–146CrossRefPubMedGoogle Scholar
  3. Chard DT, Parker GJ, Griffin CM, Thompson AJ, Miller DH (2002) The reproducibility and sensitivity of brain tissue volume measurements derived from an SPM-based segmentation methodology. J Magn Reson Imaging 15(3):259–267CrossRefPubMedGoogle Scholar
  4. Charil A, Zijdenbos AP, Taylor J, Boelman C, Worsley KJ, Evans AC, Dagher A (2003) Statistical mapping analysis of lesion location and neurological disability in multiple sclerosis: application to 452 patient data sets. Neuroimage 19(3):532–544CrossRefPubMedGoogle Scholar
  5. Cohen AB, Neema M, Arora A, Dell’oglio E, Benedict RH, Tauhid S, Goldberg-Zimring D, Chavarro-Nieto C, Ceccarelli A, Klein JP, Stankiewicz JM, Houtchens MK, Buckle GJ, Alsop DC, Guttmann CR, Bakshi R (2012) The relationships among MRI-defined spinal cord involvement, brain involvement, and disability in multiple sclerosis. J Neuroimaging 22(2):122–128PubMedCentralCrossRefPubMedGoogle Scholar
  6. Comi G, Filippi M, Martinelli V, Campi A, Rodegher M, Alberoni M, Sirabian G, Canal N (1995) Brain MRI correlates of cognitive impairment in primary and secondary progressive multiple sclerosis. J Neurol Sci 132(2):222–227CrossRefPubMedGoogle Scholar
  7. Coret F, Bosca I, Landete L, Magraner MJ, Navarre A, Leon JL, Casanova B (2010) Early diffuse demyelinating lesion in the cervical spinal cord predicts a worse prognosis in relapsing-remitting multiple sclerosis. Mult Scler 16(8):935–941CrossRefPubMedGoogle Scholar
  8. Cromwell HC, Hassani OK, Schultz W (2005) Relative reward processing in primate striatum. Exp Brain Res 162(4):520–525CrossRefPubMedGoogle Scholar
  9. Draganski B, Kherif F, Kloppel S, Cook PA, Alexander DC, Parker GJ, Deichmann R, Ashburner J, Frackowiak RS (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28(28):7143–7152CrossRefPubMedGoogle Scholar
  10. Evangelou N, DeLuca GC, Owens T, Esiri MM (2005) Pathological study of spinal cord atrophy in multiple sclerosis suggests limited role of local lesions. Brain 128(Pt 1):29–34. doi: 10.1093/brain/awh323 PubMedGoogle Scholar
  11. Filippi M, Campi A, Colombo B, Pereira C, Martinelli V, Baratti C, Comi G (1996) A spinal cord MRI study of benign and secondary progressive multiple sclerosis. J Neurol 243(7):502–505CrossRefPubMedGoogle Scholar
  12. Fischer JS, Rudick RA, Cutter GR, Reingold SC (1999) The Multiple Sclerosis Functional Composite Measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force. Mult Scler 5(4):244–250CrossRefPubMedGoogle Scholar
  13. Foong J, Rozewicz L, Chong WK, Thompson AJ, Miller DH, Ron MA (2000) A comparison of neuropsychological deficits in primary and secondary progressive multiple sclerosis. J Neurol 247(2):97–101CrossRefPubMedGoogle Scholar
  14. Houtchens MK, Benedict RH, Killiany R, Sharma J, Jaisani Z, Singh B, Weinstock-Guttman B, Guttmann CR, Bakshi R (2007) Thalamic atrophy and cognition in multiple sclerosis. Neurology 69(12):1213–1223CrossRefPubMedGoogle Scholar
  15. Jaeger D, Gilman S, Aldridge JW (1995) Neuronal activity in the striatum and pallidum of primates related to the execution of externally cued reaching movements. Brain Res 694(1–2):111–127CrossRefPubMedGoogle Scholar
  16. Kearney H, Rocca MA, Valsasina P, Balk L, Sastre-Garriga J, Reinhardt J, Ruggieri S, Rovira A, Stippich C, Kappos L, Sprenger T, Tortorella P, Rovaris M, Gasperini C, Montalban X, Geurts JJ, Polman CH, Barkhof F, Filippi M, Altmann DR, Ciccarelli O, Miller DH, Chard DT (2014) Magnetic resonance imaging correlates of physical disability in relapse onset multiple sclerosis of long disease duration. Mult Scler 20(1):72–80PubMedCentralCrossRefPubMedGoogle Scholar
  17. Lin X, Tench CR, Turner B, Blumhardt LD, Constantinescu CS (2003) Spinal cord atrophy and disability in multiple sclerosis over four years: application of a reproducible automated technique in monitoring disease progression in a cohort of the interferon beta-1a (Rebif) treatment trial. J Neurol Neurosurg Psychiatry 74(8):1090–1094PubMedCentralCrossRefPubMedGoogle Scholar
  18. Losseff NA, Webb SL, O’Riordan JI, Page R, Wang L, Barker GJ, Tofts PS, McDonald WI, Miller DH, Thompson AJ (1996) Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain 119(Pt 3):701–708CrossRefPubMedGoogle Scholar
  19. Lycklama a Nijeholt GJ, Castelijns JA, Weerts J, Ader H, van Waesberghe JH, Polman C, Barkhof F (1998) Sagittal MR of multiple sclerosis in the spinal cord: fast versus conventional spin-echo imaging. AJNR Am J Neuroradiol 19(2):355–360PubMedGoogle Scholar
  20. Mühlau M, Buck D, Forschler A, Boucard CC, Arsic M, Schmidt P, Gaser C, Berthele A, Hoshi M, Jochim A, Kronsbein H, Zimmer C, Hemmer B, Ilg R (2013) White-matter lesions drive deep gray-matter atrophy in early multiple sclerosis: support from structural MRI. Mult Scler 19(11):1485–1492CrossRefPubMedGoogle Scholar
  21. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69(2):292–302PubMedCentralCrossRefPubMedGoogle Scholar
  22. Popescu V, Agosta F, Hulst HE, Sluimer IC, Knol DL, Sormani MP, Enzinger C, Ropele S, Alonso J, Sastre-Garriga J, Rovira A, Montalban X, Bodini B, Ciccarelli O, Khaleeli Z, Chard DT, Matthews L, Palace J, Giorgio A, De Stefano N, Eisele P, Gass A, Polman CH, Uitdehaag BM, Messina MJ, Comi G, Filippi M, Barkhof F, Vrenken H (2013) Brain atrophy and lesion load predict long term disability in multiple sclerosis. J Neurol Neurosurg Psychiatry 84(10):1082–1091CrossRefPubMedGoogle Scholar
  23. Reetz K, Gaser C, Klein C, Hagenah J, Buchel C, Gottschalk S, Pramstaller PP, Siebner HR, Binkofski F (2009) Structural findings in the basal ganglia in genetically determined and idiopathic Parkinson’s disease. Mov Disord 24(1):99–103CrossRefPubMedGoogle Scholar
  24. Rovaris M, Judica E, Sastre-Garriga J, Rovira A, Sormani MP, Benedetti B, Korteweg T, De Stefano N, Khaleeli Z, Montalban X, Barkhof F, Miller DH, Polman C, Thompson AJ, Filippi M (2008) Large-scale, multicentre, quantitative MRI study of brain and cord damage in primary progressive multiple sclerosis. Mult Scler 14(4):455–464CrossRefPubMedGoogle Scholar
  25. Roxburgh RH, Seaman SR, Masterman T, Hensiek AE, Sawcer SJ, Vukusic S, Achiti I, Confavreux C, Coustans M, le Page E, Edan G, McDonnell GV, Hawkins S, Trojano M, Liguori M, Cocco E, Marrosu MG, Tesser F, Leone MA, Weber A, Zipp F, Miterski B, Epplen JT, Oturai A, Sorensen PS, Celius EG, Lara NT, Montalban X, Villoslada P, Silva AM, Marta M, Leite I, Dubois B, Rubio J, Butzkueven H, Kilpatrick T, Mycko MP, Selmaj KW, Rio ME, Sa M, Salemi G, Savettieri G, Hillert J, Compston DA (2005) Multiple Sclerosis Severity Score: using disability and disease duration to rate disease severity. Neurology 64(7):1144–1151CrossRefPubMedGoogle Scholar
  26. Rudick RA, Fisher E, Lee JC, Simon J, Jacobs L (1999) Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 53(8):1698–1704CrossRefPubMedGoogle Scholar
  27. Sastre-Garriga J, Ingle GT, Chard DT, Cercignani M, Ramio-Torrenta L, Miller DH, Thompson AJ (2005) Grey and white matter volume changes in early primary progressive multiple sclerosis: a longitudinal study. Brain 128(Pt 6):1454–1460CrossRefPubMedGoogle Scholar
  28. Schmidt P, Gaser C, Arsic M, Buck D, Forschler A, Berthele A, Hoshi M, Ilg R, Schmid VJ, Zimmer C, Hemmer B, Mühlau M (2012) An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage 59(4):3774–3783CrossRefPubMedGoogle Scholar
  29. Shu SY, Song C, Wu Y, Mo L, Guo Z, Liu SH, Bao X (2009) Learning and memory deficits caused by a lesion in the medial area of the left putamen in the human brain. CNS Spectr 14(9):473–476PubMedGoogle Scholar
  30. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44(1):83–98CrossRefPubMedGoogle Scholar
  31. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31(4):1487–1505CrossRefPubMedGoogle Scholar
  32. Sombekke MH, Wattjes MP, Balk LJ, Nielsen JM, Vrenken H, Uitdehaag BM, Polman CH, Barkhof F (2013) Spinal cord lesions in patients with clinically isolated syndrome: a powerful tool in diagnosis and prognosis. Neurology 80(1):69–75CrossRefPubMedGoogle Scholar
  33. Stevenson VL, Moseley IF, Phatouros CC, MacManus D, Thompson AJ, Miller DH (1998) Improved imaging of the spinal cord in multiple sclerosis using three-dimensional fast spin echo. Neuroradiology 40(7):416–419CrossRefPubMedGoogle Scholar
  34. Ueda Y, Kimura M (2003) Encoding of direction and combination of movements by primate putamen neurons. Eur J Neurosci 18(4):980–994CrossRefPubMedGoogle Scholar
  35. Vukusic S, Confavreux C (2003) Primary and secondary progressive multiple sclerosis. J Neurol Sci 206(2):153–155CrossRefPubMedGoogle Scholar
  36. Weinshenker BG, Bass B, Rice GP, Noseworthy J, Carriere W, Baskerville J, Ebers GC (1989) The natural history of multiple sclerosis: a geographically based study. I. Clinical course and disability. Brain 112(Pt 1):133–146CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Hilga Zimmermann
    • 1
  • Hans O. Rolfsnes
    • 1
  • Swantje Montag
    • 1
  • Janine Wilting
    • 1
  • Amgad Droby
    • 1
  • Eva Reuter
    • 1
  • Joachim Gawehn
    • 2
  • Frauke Zipp
    • 1
  • Adriane Gröger
    • 1
  1. 1.Department of Neurology and Neuroimaging Center (NIC) of the Focus Program Translational Neuroscience (FTN)University Medical Center of the Johannes Gutenberg-University MainzMainzGermany
  2. 2.Institute of NeuroradiologyUniversity Medical Center of the Johannes Gutenberg-University MainzMainzGermany

Personalised recommendations