Quantitative magnetic resonance of postmortem multiple sclerosis brain before and after fixation

Magnetic Resonance in Medicine

Volumn 59, Issue 2, 2008, Pages 268-277

  Schmierer, Klaus ^a   Wheeler Kingshott, Claudia A M ^a   Tozer, Daniel J ^a   Boulby, Phil A ^a   Parkes, Harold G ^a   Yousry, Tarek A ^a   Scaravilli, Francesco ^a   Barker, Gareth J ^b   Tofts, Paul S ^a,c   Miller, David H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

Author keywords

Diffusion; Fixation; Magnetization transfer; Multiple sclerosis; Postmortem

Indexed keywords

DIFFUSION; NITROGEN FIXATION;

FRACTIONAL ANISOTROPY; MAGNETIZATION TRANSFER; MULTIPLE SCLEROSIS; POSTMORTEM; PROTON FRACTION; QUANTITATIVE MAGNETIC RESONANCES; RADIAL DIFFUSIVITY; STUDENT'S T TESTS;

MAGNETIC RESONANCE;

FORMALDEHYDE; MYELIN;

ANISOTROPY; ARTICLE; CADAVER; CONTROLLED STUDY; DIFFUSION; DIFFUSION TENSOR IMAGING; GLIOSIS; HISTOPATHOLOGIC SKIN REACTION; HUMAN; HUMAN TISSUE; MULTIPLE SCLEROSIS; NERVE FIBER; NUCLEAR MAGNETIC RESONANCE IMAGING; QUANTITATIVE ANALYSIS; TISSUE FIXATION; WHITE MATTER;

EID: 38949200241     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.21487     Document Type: Article

References (68)

1. Miller DH. Biomarkers and surrogate outcomes in neurodegenerative disease: lessons from multiple sclerosis. NeuroRx 2004;1:284-294.
2. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, Lublin FD, Metz LM, McFarland HF, O'Connor PW, Sandberg-Wollheim M, Thompson AJ, Weinshenker BG, Wolinsky JS. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann Neurol 2005;58:840-846.
3. Kappos L, Moeri D, Radue EW, Schoetzau A, Schweikert K, Barkhof F, Miller D, Guttmann CR, Weiner HL, Gasperini C, Filippi M. Predictive value of gadolinium-enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis. Lancet 1999;353:964-969.
4. Brex PA, Ciccarelli O, O'Riordan JI, Sailer M, Thompson AJ, Miller DH. A longitudinal study of abnormalities on MRI and disability from multiple sclerosis. N Engl J Med 2002;346:158-164.
5. Hawkins CP, Munro PM, Mackenzie F, Kesselring J, Tofts PS, Du Boulay EP, Landon DN, McDonald WI. Duration and selectivity of blood-brain barrier breakdown in chronic relapsing experimental allergic encephalomyelitis studied by gadolinium-DTPA and protein markers. Brain 1990;113:365-378.
6. Katz D, Taubenberger JK, Cannella B, McFarlin DE, Raine CS, McFarland HF. Correlation between magnetic resonance imaging findings and lesion development in chronic, active multiple sclerosis. Ann Neurol 1993;34:661-669.
7. Moore GRW. MRI-clinical correlations: more than inflammation alone - what can MRI contribute to improve the understanding of pathological processes in MS? J Neurol Sci 2003;206:175-179.
8. Tofts PS, editor. Quantitative MRI of the brain: measuring changes caused by disease. 1st edition. Chichester: Wiley; 2003.
9. van Walderveen MAA, Kamphorst W, Scheltens P, van Waesberghe JH, Ravid R, Valk J, Polman CH, Barkhof F. Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis. Neurology 1998;50:1282-1288.
10. van Waesberghe JH, Kamphorst W, de Groot CJ, van Walderveen MAA, Castelijns JA, Ravid R, Nijeholt GJ, van der Valk P, Polman CH, Thompson AJ, Barkhof F. Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann Neurol 1999;46:747-754.
11. Moore GRW, Leung E, MacKay AL, Vavasour IM, Whittall KP, Cover KS, Li DK, Hashimoto SA, Oger J, Sprinkle TJ, Paty DW. A pathology-MRI study of the short-T2 component in formalin-fixed multiple sclerosis brain. Neurology 2000;55:1506-1510.
12. Barkhof F, Brück W, de Groot CJ, Bergers E, Hülshof S, Geurts J, Polman CH, van der Valk P. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurol 2003;60:1073-1081.
13. Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 2004;56:407-415.
14. Fox R, Holtman R, Lee JC, Tkach J, Phillips M, Fisher E. Diffusion tensor measurements in post-mortem brain. In: Proceedings of the 13th Annual Meeting of ISMRM, Miami Beach, FL, USA 2005 (Abstract 139).
15. Schmierer K, Wheeler-Kingshott CAM, Scaravilli F, Boulby PA, Miller DH. Diffusion tensor indices and their histological correlates in post mortem multiple sclerosis brain. In: Proceedings of the 13th Annual Meeting of ISMRM, Miami Beach, FL, USA 2005 (Abstract 70).
16. Bö L, Geurts JJ, Ravid R, Barkhof F. Magnetic resonance imaging as a tool to examine the neuropathology of multiple sclerosis. Neuropathol Appl Neurobiol 2004;30:106-117.
17. Newcombe J, Hawkins CP, Henderson CL, Patel HA, Woodroofe MN, Hayes GM, Cuzner ML, MacManus D, Du Boulay EP, McDonald WI. Histopathology of multiple sclerosis lesions detected by magnetic resonance imaging in unfixed postmortem central nervous system tissue. Brain 1991;114:1013-1023.
18. Schmierer K, Scaravilli F, Barker GJ, MacManus DG, Miller DH. Stereotactic co-registration of magnetic resonance imaging and histopathology in post-mortem multiple sclerosis brain. Neuropath Appl Neurobiol 2003;29:596-601.
19. Sun SW, Neil JJ, Song SK. Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med 2003;50:743-748.
20. Nijeholt GJ, Bergers E, Kamphorst W, Bot J, Nicolay K, Castelijns JA, van Waesberghe JH, Ravid R, Polman CH, Barkhof F. Post-mortem high-resolution MRI of the spinal cord in multiple sclerosis: a correlative study with conventional MRI, histopathology and clinical phenotype. Brain 2001;124:154-166.
21. Bot JC, Blezer EL, Kamphorst W, Lycklama ANG, Ader HJ, Castelijns JA, Ig KN, Bergers E, Ravid R, Polman C, Barkhof F. The spinal cord in multiple sclerosis: relationship of high-spatial-resolution quantitative MR imaging findings to histopathologic results. Radiology 2004;233:531-540.
22. Lublin FD, Reingold SC. Denning the clinical course of multiple sclerosis: results of an international survey. Neurology 1996;46:907-911.
23. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983;33:1444-1452.
24. Boulby PA, Rugg-Gunn F. T2: the transverse relaxation time. In: Tofts PS, editor. Quantitative MRI of the brain: measuring changes caused by disease. Chichester: John Wiley & Sons; 2003. p 143-201.
25. Parker GJM, Barker GJ, Tofts PS. Accurate multislice gradient echo T(1) measurement in the presence of non-ideal RF pulse shape and RF field nonuniformity. Magn Reson Med 2001;45:838-845.
26. Barker GJ, Tofts PS, Gass A. An interleaved sequence for accurate and reproducible clinical measurement of magnetization transfer ratio. Magn Reson Imaging 1996;14:403-411.
27. Davies GR, Tozer DJ, Cercignani M, Ramani A, Dalton CM, Thompson AJ, Barker GJ, Tofts PS, Miller DH. Estimation of the macromolecular proton fraction and bound pool T2 in multiple sclerosis. Mult Scler 2004;10:607-613.
28. Henkelman RM, Huang X, Xiang QS, Stanisz GJ, Swanson SD, Bronskill MJ. Quantitative interpretation of magnetization transfer. Magn Reson Med 1993; 29:759-766.
29. Ramani A, Dalton C, Miller DH, Tofts PS, Barker GJ. Precise estimate of fundamental in-vivo MT parameters in human brain in clinically feasible times. Magn Reson Imaging 2002;20:721-731.
30. Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 1996;36:893-906.
31. Basser PJ, Pierpaoli C. A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 1998;39:928-934.
32. Basser PJ. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 1995;8:333-344.
33. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med 2000;44:625-632.
34. Xue R, van Zijl PC, Crain BJ, Solaiyappan M, Mori S. In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn Reson Med 1999;42:1123-1127.
35. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002;17:1429-1436.
36. Plummer DL. Dispimage: a display and analysis tool for medical images. Rev Neuroradiol 1992;5:489-495.
37. Grimaud J, Lai M, Thorpe J, Adeleine P, Wang L, Barker GJ, Plummer DL, Tofts PS, McDonald WI, Miller DH. Quantification of MRI lesion load in multiple sclerosis: a comparison of three computer-assisted techniques. Magn Reson Imaging 1996;14:495-505.
38. Prineas JW, McDonald WI, Franklin RJM. Demyelinating diseases. In: Graham DI, Lantos PC, editors. Greenfield's neuropathology. 7th edition. London: Arnold; 2002. p 471-550.
39. Brück W, Kuhlmann T, Stadelmann C. Remyelination in multiple sclerosis. J Neurol Sci 2003;206:181-185.
40. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Bö L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338:278-285.
41. van der Valk P, de Groot CJ. Staging of multiple sclerosis (MS) lesions: pathology of the time frame of MS. Neuropathol Appl Neurobiol 2000;26:2-10.
42. Yong-Hing CJ, Obenaus A, Stryker R, Tong K, Sarty GE. Magnetic resonance imaging and mathematical modelling of progressive formalin fixation of the human brain. Magn Reson Med 2005;54:324-332.
43. Fox CH, Johnson FB, Whiting J, Roller PP. Formaldehyde fixation. J Histochem Cytochem 1985;33:845-853.
44. Hopwood D. Fixation and fixatives. In: Bancroft JD, Stevens A, editors. Theory and practice of histological techniques. 4th edition. New York: Churchill Livingstone; 1996. p 23-45.
45. Mouritzen Dam A. Shrinkage of the brain during histological procedures with fixation in formaldehyde solutions of different concentrations. J Hirnforsch 1979;20:115-119.
46. Nagara H, Inoue T, Koga T, Kitaguchi T, Tateishi J, Goto I. Formalin fixed brains are useful for magnetic resonance imaging (MRI) study. J Neurol Sci 1987;81:67-77.
47. Macchi G, Cioffi RP. An in vivo and post mortem MRI study in multiple sclerosis with pathological correlation. Ital J Neurol Sci 1992;13(Suppl 14):97-103.
48. Blamire AM, Rowe JG, Styles P, McDonald B. Optimising imaging parameters for post mortem MR imaging of the human brain. Acta Radiol 1999;40:593-597.
49. Bossart EL, Inglis BA, Silver XS, Mareci TH. The effect of fixative solutions in magnetic resonance imaging. In: Proceedings of the 7th Annual Meeting of ISMRM, Philadelphia, PA, USA, 1999 (Abstract 1928).
50. Tozer DJ, Davies GR, Altmann DR, Miller DH, Tofts PS. Correlation of apparent myelin measures obtained in multiple sclerosis patients and controls from magnetization transfer and multicompartmental T2 analysis. Magn Reson Med 2005;53:1415-1422.
51. Tofts PS, Steens SCA, van Buchem MA. MT: Magnetization transfer. In: Tofts PS, editor. Quantitative MRI of the brain: measuring changes caused by disease. Chichester: John Wiley & Sons; 2003. p 257-298.
52. Sled JG, Pike GB. Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med 2001;46:923-931.
53. Ciccarelli O, Werring DJ, Wheeler-Kingshott CA, Barker GJ, Parker GJ, Thompson AJ, Miller DH. Investigation of MS normal-appearing brain using diffusion tensor MRI with clinical correlations. Neurology 2001;56:926-933.
54. Le Bihan D, Turner R, Douek P, Patronas N. Diffusion MR imaging: clinical applications. AJR Am J Roentgenol 1992;159:591-599.
55. Lee VM, Burdett NG, Carpenter TA, Herrod NJ, James MF, Hall LD. Magnetic resonance imaging of the common marmoset head. Altern Lab Anim 1998;26:343-356.
56. Wheeler-Kingshott CAM, Schmierer K, Ciccarelli O, Boulby PA, Parker GJM, Miller DH. Diffusion tensor imaging of post-mortem brain (fresh and fixed) on a clinical scanner. In: Proceedings of the 11th Annual Meeting of ISMRM, Toronto, Ontario, Canada, 2003 (Abstract 422).
57. Jones DK, Horsfield MA, Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 1999;42:515-525.
58. Whittall KP, MacKay AL, Li DK. Are mono-exponential fits to a few echoes sufficient to determine T2 relaxation for in vivo human brain? Magn Reson Med 1999;41:1255-1257.
59. MacKay A, Whittall K, Adler J, Li D, Paty D, Graeb D. In vivo visualization of myelin water in brain by magnetic resonance. Magn Reson Med 1994;31:673-677.
60. Laule C, Leung E, Lis DK, Traboulsee AL, Paty DW, MacKay AL, Moore GRW. Myelin water imaging in multiple sclerosis: quantitative correlations with histopathology. Mult Scler 2006;12:747-753.
61. Odrobina EE, Lam TY, Pun T, Midha R, Stanisz GJ. MR properties of excised neural tissue following experimentally induced demyelination. NMR Biomed 2005;18:277-284.
62. Stanisz GJ, Kecojevic A, Bronskill MJ, Henkelman RM. Characterizing white matter with magnetization transfer and T(2). Magn Reson Med 1999;42:1128-1136.
63. Henkelman RM, Stanisz GJ, Graham SJ. Magnetization transfer in MRI: a review. NMR Biomed 2001;14:57-64.
64. Berry I, Barker GJ, Barkhof F, Campi A, Dousset V, Franconi JM, Gass A, Schreiber W, Miller DH, Tofts PS. A multicenter measurement of magnetization hansfer ratio in normal white matter. J Magn Reson Imaging 1999;9:441-446.
65. Tofts PS, Steens SC, Cercignani M, Admiraal-Behloul F, Hofman PA, van Osch MJ, Teeuwisse WM, Tozer DJ, Van Waesberghe JH, Yeung R, Barker GJ, van Buchem MA. Sources of variation in multi-centre brain MTR histogram studies: body-coil transmission eliminates inter-centre differences. MAGMA 2006;19:209-222.
66. Vavasour IM, Whittall KP, Li DK, MacKay AL. Different magnetization transfer effects exhibited by the short and long T(2) components in human brain. Magn Reson Med 2000;44:860-866.
67. Stanisz GJ, Webb S, Munro CA, Pun T, Midha R. MR properties of excised neural tissue following experimentally induced inflammation. Magn Reson Med 2004;51:473-479.
68. Mottershead J, Schmierer K, Clemence M, Thornton J, Scaravilli F, Barker G, Tofts P, Newcombe J, Cuzner M, Ordidge R, McDonald W, Miller D. High field MRI correlates of myelin content and axonal density in multiple sclerosis: a post-mortem study of the spinal cord. J Neurol 2003;250:1293-1301.