Blood-Brain Barrier Permeability of Normal Appearing White Matter in Relapsing-Remitting Multiple Sclerosis

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lund, Henrik ^a   Krakauer, Martin ^b   Skimminge, Arnold ^a   Sellebjerg, Finn ^b   Garde, Ellen ^a   Siebner, Hartwig R ^a   Paulson, Olaf B ^a,b   Hesse, Dan ^b   Hanson, Lars G ^a,c  

^a Mental Health Services CPH   (Denmark)

^b Rigshospitalet   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM PENTETATE;

ADULT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN REGION; BRAIN SIZE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPANDED DISABILITY STATUS SCALE; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT ASSESSMENT; QUANTITATIVE ANALYSIS; WHITE MATTER;

EID: 84874140558     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056375     Document Type: Article

References (49)

1. Holman DW, Klein RS, Ransohoff RM, ((2011)) The blood-brain barrier, chemokines and multiple sclerosis. Biochim Biophys Acta 1812: 220-30.
2. Hemmer B, Archelos JJ, Hartung H-P, (2002) New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 3: 291-301.
3. Filippi M, Rocca MA, Barkhof F, Brück W, Chen J, et al. (2012) Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 11: 349-360.
4. Larochelle C, Alvarez JI, Prat A, (2011) How do immune cells overcome the blood-brain barrier in multiple sclerosis? FEBS Lett 585: 3770-80.
5. Grossman RI, Gonzalez-Scarano F, Atlas SW, Galetta S, Silberberg DH, (1986) Multiple sclerosis: gadolinium enhancement in MR imaging. Radiology 161: 721-5.
6. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, et al. (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann.Neurol. 50: 121-127.
7. Rovaris M, Rocca MA, Barkhof F, Calabrese M, De Stefano N, et al. (2011) Relationship between brain MRI lesion load and short-term disease evolution in non-disabling MS: a large-scale, multicentre study. Mult Scler 17: 319-26.
8. Comi G, Rovaris M, Falautano M, Santuccio G, Martinelli V, et al. (1999) A multiparametric MRI study of frontal lobe dementia in multiple sclerosis. J.Neurol.Sci. 171: 135-144.
9. Filippi M, Tortorella C, Rovaris M, Bozzali M, Possa F, et al. (2000) Changes in the normal appearing brain tissue and cognitive impairment in multiple sclerosis. J.Neurol.Neurosurg.Psychiatry 68: 157-161.
10. Zivadinov R, De Masi R, Nasuelli D, Bragadin LM, Ukmar M, et al. (2001) MRI techniques and cognitive impairment in the early phase of relapsing-remitting multiple sclerosis. Neuroradiology 43: 272-278.
11. Barkhof F, (1999) MRI in multiple sclerosis: correlation with expanded disability status scale (EDSS). Mult Scler 5: 283-6.
12. Filippi M, Iannucci G, Cercignani M, Assunta Rocca M, Pratesi A, et al. (2000) A quantitative study of water diffusion in multiple sclerosis lesions and normal-appearing white matter using echo-planar imaging. Arch Neurol 57: 1017-21.
13. Sarchielli P, Presciutti O, Pelliccioli GP, Tarducci R, Gobbi G, et al. (1999) Absolute quantification of brain metabolites by proton magnetic resonance spectroscopy in normal-appearing white matter of multiple sclerosis patients. Brain 122 (Pt 3): 513-521.
14. Davies GR, Altmann DR, Hadjiprocopis A, Rashid W, Chard DT, et al. (2005) Increasing normal-appearing grey and white matter magnetisation transfer ratio abnormality in early relapsing-remitting multiple sclerosis. J.Neurol. 252: 1037-1044.
15. Allen IV, McKeown SR, (1979) A histological, histochemical and biochemical study of the macroscopically normal white matter in multiple sclerosis. J Neurol Sci 41: 81-91.
16. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, et al. (2005) Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 128: 2705-12.
17. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, et al. (2009) The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132: 1175-89.
18. Lund H, Jønsson A, Andresen J, Rostrup E, Paulson OB, et al. (2012) Cognitive deficits in multiple sclerosis: correlations with T2 changes in normal appearing brain tissue. Acta Neurol Scand 125: 338-44.
19. Iannucci G, Tortorella C, Rovaris M, Sormani MP, Comi G, et al. (2000) Prognostic value of MR and magnetization transfer imaging findings in patients with clinically isolated syndromes suggestive of multiple sclerosis at presentation. AJNR Am J Neuroradiol 21: 1034-8.
20. Schmierer K, Altmann DR, Kassim N, Kitzler H, Kerskens CM, et al. (2004) Progressive change in primary progressive multiple sclerosis normal-appearing white matter: a serial diffusion magnetic resonance imaging study. Mult.Scler 10: 182-187.
21. Vos CMP, Geurts JJG, Montagne L, van Haastert ES, Bo L, et al. (2005) Blood-brain barrier alterations in both focal and diffuse abnormalities on postmortem MRI in multiple sclerosis. Neurobiol.Dis. 20: 953-960.
22. Silver NC, Tofts PS, Symms MR, Barker GJ, Thompson AJ, et al. (2001) Quantitative contrast-enhanced magnetic resonance imaging to evaluate blood-brain barrier integrity in multiple sclerosis: a preliminary study. Mult.Scler. 7: 75-82.
23. Topakian R, Barrick TR, Howe FA, Markus HS, (2010) Blood-brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis. J Neurol Neurosurg Psychiatry 81: 192-7.
24. Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, et al. (2003) High field MRI correlates of myelin content and axonal density in multiple sclerosis-a post-mortem study of the spinal cord. J Neurol 250: 1293-301.
25. van Waesberghe JH, Kamphorst W, De Groot CJ, van Walderveen MA, Castelijns JA, et al. (1999) Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann.Neurol. 46: 747-754.
26. Mathiesen HK, Jonsson A, Tscherning T, Hanson LG, Andresen J, et al. (2006) Correlation of global N-acetyl aspartate with cognitive impairment in multiple sclerosis. Arch.Neurol. 63: 533-536.
27. Vaithianathar L, Tench CR, Morgan PS, Lin X, Blumhardt LD, (2002) White matter T(1) relaxation time histograms and cerebral atrophy in multiple sclerosis. J Neurol Sci 197: 45-50c.
28. Vrenken H, Rombouts SA, Pouwels PJ, Barkhof F, (2006) Voxel-based analysis of quantitative T1 maps demonstrates that multiple sclerosis acts throughout the normal-appearing white matter. AJNR Am.J.Neuroradiol. 27: 868-874.
29. van Walderveen MA, van Schijndel RA, Pouwels PJ, Polman CH, Barkhof F, (2003) Multislice T1 relaxation time measurements in the brain using IR-EPI: reproducibility, normal values, and histogram analysis in patients with multiple sclerosis. J.Magn Reson.Imaging 18: 656-664.
30. Parry A, Clare S, Jenkinson M, Smith S, Palace J, et al. (2002) White matter and lesion T1 relaxation times increase in parallel and correlate with disability in multiple sclerosis. J.Neurol. 249: 1279-1286.
31. Calabresi PA, Stone LA, Bash CN, Frank JA, McFarland HF, (1997) Interferon beta results in immediate reduction of contrast-enhanced MRI lesions in multiple sclerosis patients followed by weekly MRI. Neurology 48: 1446-8.
32. Comi G, Filippi M, Wolinsky JS, (2001) European/Canadian multicenter, double-blind, randomized, placebo-controlled study of the effects of glatiramer acetate on magnetic resonance imaging-measured disease activity and burden in patients with relapsing multiple sclerosis. European/Canadian Glatiramer Acetate Study Group. Ann Neurol 49: 290-7.
33. NCBI PubChem. Available: http://pubchem.ncbi.nlm.nih.gov/summary/summary.cgi?cid=55466. Accessed 2013 Jan 16.
34. Claudio L, Raine CS, Brosnan CF (1995) Evidence of persistent blood-brain barrier abnormalities in chronic-progressive multiple sclerosis. Acta Neuropathol 90, 228-38.
35. Kirk J, Plumb J, Mirakhur M, McQuaid S, (2003) Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J.Pathol. 201: 319-327.
36. Evangelou N, Konz D, Esiri MM, Smith S, Palace J, et al. (2000) Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain 123 (Pt 9): 1845-9.
37. Gaitán MI, Shea CD, Evangelou IE, Stone RD, Fenton KM, et al. (2011) Evolution of the blood-brain barrier in newly forming multiple sclerosis lesions. Ann Neurol 70: 22-9.
38. Caravan P, Ellison JJ, McMurry TJ, Lauffer RB, (1999) Gadolinium(III) Chelates as MRI Contrast Agents: Structure, Dynamics, and Applications. Chem Rev 99: 2293-352.
39. Barkhof F, et al. (2002) Whole-brain T1-relaxation time measurements in multiple sclerosis. J.Neurol. 249: 1451-1452.
40. Wansapura JP, Holland SK, Dunn RS, Ball WS, (1999) NMR relaxation times in the human brain at 3.0 tesla. J.Magn Reson.Imaging 9: 531-538.
41. Gold R, Wolinsky JS, Amato MP, Comi G, (2010) Evolving expectations around early management of multiple sclerosis. Ther Adv Neurol Disord 3: 351-67.
42. Kurtzke JF, (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33: 1444-1452.
43. Hanson LG, Lund H, Rostrup E, (2005) Efficient multi-dimensional diffusion measurements at 3 Tesla. Proc Intl Soc Magn Reson Med, #1298.
44. Hanson LG, Topp S, Paulson OB, (1998) Correction for B1 inhomogeneity using EPI-based field maps. Proc Intl Soc Magn Reson Med, #128.
45. Frahm J, Merboldt KD, Hänicke W, Haase A, (1985) Stimulated Echo Imaging. Journal of Magnetic Resonance 64: 81-93.
46. Topp S, Adalsteinsson E, Spielman DM, (1997) Fast Multislice B1-Mapping. Proc Intl Soc Magn Reson Med, #281.
47. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1: S208-19.
48. Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, et al. (2009) Bayesian analysis of neuroimaging data in FSL. Neuroimage 45: S173-86.
49. Evans AC, (1993) 3D statistical neuroanatomical models from 305 MRI volumes. Nuclear Science Symposium and Medical Imaging Conference 3: 1813-1817.