A novel approach with "skeletonised MTR" measures tract-specific microstructural changes in early primary-progressive MS

Human Brain Mapping

Volumn 35, Issue 2, 2014, Pages 723-733

  Bodini, Benedetta ^a   Cercignani, Mara ^b,c   Toosy, Ahmed ^a   Stefano, Nicola De ^d   Miller, David H ^a   Thompson, Alan J ^a   Ciccarelli, Olga ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^d UNIVERSITY OF SIENA   (Italy)

Author keywords

Magnetization transfer imaging; Primary progressive multiple sclerosis; Tract based spatial statistics

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; FEMALE; FOLLOW UP; FRACTIONAL ANISOTROPY; HUMAN; MALE; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PYRAMIDAL TRACT; WHITE MATTER;

MAGNETIZATION TRANSFER IMAGING; PRIMARY-PROGRESSIVE MULTIPLE SCLEROSIS; TRACT-BASED SPATIAL STATISTICS;

ADULT; ANISOTROPY; BRAIN; BRAIN MAPPING; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; PYRAMIDAL TRACTS; STATISTICS AS TOPIC;

EID: 84892476169     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22196     Document Type: Article

References (68)

1. Ashburner J, Friston KJ (2005): Unified segmentation. Neuroimage 26:839-851.
2. Audoin B, Davies G, Rashid W, Fisniku L, Thompson AJ, Miller DH (2007): Voxel-based analysis of grey matter magnetization transfer ratio maps in early relapsing remitting multiple sclerosis. Mult Scler 13:483-489.
3. Barker GJ, Tofts PS, Gass A (1996): An interleaved sequence for accurate and reproducible clinical measurement of magnetization transfer ratio. Magn Reson Imaging 14:403-411.
4. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O (2009): Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: An in vivo study with TBSS and VBM. Hum Brain Mapp 30:2852-2861.
5. Bodini B, Cercignani M, Khaleeli Z, Miller DH, Ron M, Penny S, Thompson AJ, Ciccarelli O (2012): Corpus callosum damage predicts disability progression and cognitive dysfunction in primary-progressive MS after five years. Hum Brain Mapp doi: 10.1002/hbm.21499. [Epub ahead of print]
6. Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M (2008): Callosal contributions to simultaneous bimanual finger movements. J Neurosci 28:3227-3233.
7. Cader S, Johansen-Berg H, Wylezinska M, Palace J, Behrens TE, Smith S, Matthews PM (2007): Discordant white matter N-acetylasparate and diffusion MRI measures suggest that chronic metabolic dysfunction contributes to axonal pathology in multiple sclerosis. Neuroimage 36:19-27.
8. Catani M, Jones DK, Donato R, Ffytche DH (2003): Occipito-temporal connections in the human brain. Brain 126 (Pt 9):2093-2107.
9. Chen JT, Kuhlmann T, Jansen GH, Collins DL, Atkins HL, Freedman MS, O'Connor PW, Arnold DL (2007): Voxel-based analysis of the evolution of magnetization transfer ratio to quantify remyelination and demyelination with histopathological validation in a multiple sclerosis lesion. Neuroimage 36:1152-1158.
10. Chen JT, Collins DL, Atkins HL, Freedman MS, Arnold DL (2008): Magnetization transfer ratio evolution with demyelination and remyelination in multiple sclerosis lesions. Ann Neurol 63:254-262.
11. Cutter GR, Baier ML, Rudick RA, Cookfair DL, Fischer JS, Petkau J, Syndulko K, Weinshenker BG, Antel JP, Confavreux C, Ellison GW, Lublin F, Miller AE, Rao SM, Reingold S, Thompson A, Willoughby E (1999): Development of a multiple sclerosis functional composite as a clinical trial outcome measure. Brain 122 (Pt 5):871-882.
12. Dalby RB, Frandsen J, Chakravarty MM, Ahdidan J, Sorensen L, Rosenberg R, Videbech P, Ostergaard L (2010): Depression severity is correlated to the integrity of white matter fiber tracts in late-onset major depression. Psychiatr Res 184:38-48.
13. Damoiseaux JS, Smith SM, Witter MP, Sanz-Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Zarei M, Rombouts SA (2009): White matter tract integrity in aging and Alzheimer's disease. Hum Brain Mapp 30:1051-1059.
14. De Stefano N, Battaglini M, Stromillo ML, Zipoli V, Bartolozzi ML, Guidi L, Siracusa G, Portaccio E, Giorgio A, Sorbi S, Federico A, Amato MP (2006): Brain damage as detected by magnetization transfer imaging is less pronounced in benign than in early relapsing multiple sclerosis. Brain 129 (Pt 8):2008-2016.
15. de Zeeuw P, Mandl RC, Hulshoff Pol HE, van EH, Durston S (2012): Decreased frontostriatal microstructural organization in attention deficit/hyperactivity disorder. Hum Brain Mapp 33:1941-1951.
16. Dehmeshki J, Silver NC, Leary SM, Tofts PS, Thompson AJ, Miller DH (2001): Magnetisation transfer ratio histogram analysis of primary progressive and other multiple sclerosis subgroups. J Neurol Sci 185:11-17.
17. Dehmeshki J, Chard DT, Leary SM, Watt HC, Silver NC, Tofts PS, Thompson AJ, Miller DH (2003): The normal appearing grey matter in primary progressive multiple sclerosis: A magnetisation transfer imaging study. J Neurol 250:67-74.
18. Deloire-Grassin MS, Brochet B, Quesson B, Delalande C, Dousset V, Canioni P, Petry KG (2000): In vivo evaluation of remyelination in rat brain by magnetization transfer imaging. J Neurol Sci 178:10-16.
19. Dwyer M, Bergsland N, Hussein S, Durfee J, Wack D, Zivadinov R (2009): A sensitive, noise-resistant method for identifying focal demyelination and remyelination in patients with multiple sclerosis via voxel-wise changes in magnetization transfer ratio. J Neurol Sci 282:86-95.
20. Filippi M (1999): Magnetization transfer imaging to monitor the evolution of individual multiple sclerosis lesions. Neurology 53 (5, Suppl 3):S18-S22.
21. Filippi M, Agosta F (2010): Imaging biomarkers in multiple sclerosis. J Magn Reson Imaging 31:770-788.
22. Filippi M, Rocca MA, Martino G, Horsfield MA, Comi G (1998): Magnetization transfer changes in the normal appearing white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann Neurol 43:809-814.
23. Filippi M, Iannucci G, Tortorella C, Minicucci L, Horsfield MA, Colombo B, Sormani MP, Comi G (1999): Comparison of MS clinical phenotypes using conventional and magnetization transfer MRI. Neurology 52:588-594.
24. Filippi M, Inglese M, Rovaris M, Sormani MP, Horsfield P, Iannucci PG, Colombo B, Comi G (2000): Magnetization transfer imaging to monitor the evolution of MS: A 1-year follow-up study. Neurology 55:940-946.
25. Focke NK, Yogarajah M, Bonelli SB, Bartlett PA, Symms MR, Duncan JS (2008): Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Neuroimage 40:728-737.
26. Giorgio A, Watkins KE, Douaud G, James AC, James S, De SN, Matthews PM, Smith SM, Johansen-Berg H (2008): Changes in white matter microstructure during adolescence. Neuroimage 39:52-61.
27. Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De SN, Johansen-Berg H (2010): Age-related changes in grey and white matter structure throughout adulthood. Neuroimage 51:943-951.
28. Johansen-Berg H, Della-Maggiore V, Behrens TE, Smith SM, Paus T (2007): Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage 36 (Suppl 2):T16-T21.
29. Jones DK, Horsfield MA, Simmons A (1999): Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 42:515-525.
30. Kern KC, Sarcona J, Montag M, Giesser BS, Sicotte NL (2011): Corpus callosal diffusivity predicts motor impairment in relapsing-remitting multiple sclerosis: A TBSS and tractography study. Neuroimage 55:1169-1177.
31. Khaleeli Z, Cercignani M, Audoin B, Ciccarelli O, Miller DH, Thompson AJ (2007a): Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 37:253-261.
32. Khaleeli Z, Sastre-Garriga J, Ciccarelli O, Miller DH, Thompson AJ (2007b): Magnetisation transfer ratio in the normal appearing white matter predicts progression of disability over 1 year in early primary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 78:1076-1082.
33. Khaleeli Z, Altmann DR, Cercignani M, Ciccarelli O, Miller DH, Thompson AJ (2008): Magnetization transfer ratio in gray matter: A potential surrogate marker for progression in early primary progressive multiple sclerosis. Arch Neurol 65:1454-1459.
34. Koch G, Cercignani M, Pecchioli C, Versace V, Oliveri M, Caltagirone C, Rothwell J, Bozzali M (2010): In vivo definition of parieto-motor connections involved in planning of grasping movements. Neuroimage 51:300-312.
35. Kurtzke JF (1983): Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology 33:1444-1452.
36. Larson EB, Burnison DS, Brown WS (2002): Callosal function in multiple sclerosis: Bimanual motor coordination. Cortex 38:201-214.
37. Leary SM, Silver NC, Stevenson VL, Barker GJ, Miller DH, Thompson AJ (1999): Magnetisation transfer of normal appearing white matter in primary progressive multiple sclerosis. Mult Scler 5:313-316.
38. Lin F, Yu C, Jiang T, Li K, Chan P (2007): Diffusion tensor tractography-based group mapping of the pyramidal tract in relapsing-remitting multiple sclerosis patients. AJNR Am J Neuroradiol 28:278-282.
39. Lin X, Tench CR, Morgan PS, Constantinescu CS (2008): Use of combined conventional and quantitative MRI to quantify pathology related to cognitive impairment in multiple sclerosis. J Neurol Neurosurg Psychiatry 79:437-441.
40. Moll NM, Rietsch AM, Thomas S, Ransohoff AJ, Lee JC, Fox R, Chang A, Ransohoff RM, Fisher E (2011): Multiple sclerosis normal-appearing white matter: Pathology-imaging correlations. Ann Neurol 70:764-773.
41. Mori S, Wakana S, Nagae-Poetscher LM, van Zijl PC (2005):MRI Atlas of Human Brain Matter.Amsterdam, The Netherlands:Elsevier.
42. Nguyen D, Vargas MI, Khaw N, Seeck M, Delavelle J, Lovblad KO, Haller S (2011): Diffusion tensor imaging analysis with tract-based spatial statistics of the white matter abnormalities after epilepsy surgery. Epilepsy Res [Epub ahead of print].
43. Pagani E, Filippi M, Rocca MA, Horsfield MA (2005): A method for obtaining tract-specific diffusion tensor MRI measurements in the presence of disease: Application to patients with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage 26:258-265.
44. Plummer D (1992): DispImage: A display and analysis tool for medical images. Rev Neuroradiol 5:489-495.
45. Raz E, Cercignani M, Sbardella E, Totaro P, Pozzilli C, Bozzali M, Pantano P (2010): Gray- and white-matter changes 1 year after first clinical episode of multiple sclerosis: MR imaging. Radiology 257:448-454.
46. Reich DS, Smith SA, Jones CK, Zackowski KM, van Zijl PC, Calabresi PA, Mori S (2006): Quantitative characterization of the corticospinal tract at 3T. AJNR Am J Neuroradiol 27:2168-2178.
47. Reich DS, Smith SA, Zackowski KM, Gordon-Lipkin EM, Jones CK, Farrell JA, Mori S, van Zijl PC, Calabresi PA (2007): Multiparametric magnetic resonance imaging analysis of the corticospinal tract in multiple sclerosis. Neuroimage 38:271-279.
48. Ropele S, Fazekas F (2009): Magnetization transfer MR imaging in multiple sclerosis. Neuroimaging Clin N Am 19:27-36.
49. Santos AC, Narayanan S, De SN, Tartaglia MC, Francis SJ, Arnaoutelis R, Caramanos Z, Antel JP, Pike GB, Arnold DL (2002): Magnetization transfer can predict clinical evolution in patients with multiple sclerosis. J Neurol 249:662-668.
50. Schmahmann JD, Pandya DN (2007): The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362-377.
51. Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH (2004): Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 56:407-415.
52. Serra L, Cercignani M, Lenzi D, Perri R, Fadda L, Caltagirone C, Macaluso E, Bozzali M (2010): Grey and white matter changes at different stages of Alzheimer's disease. J Alzheimers Dis 19:147-159.
53. Smith SM, Nichols TE (2009): Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
54. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De LM, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De SN, Brady JM, Matthews PM (2004): Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (Suppl 1):S208-S219.
55. 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 31:1487-1505.
56. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005): Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132-140.
57. Stricker NH, Schweinsburg BC, Delano-Wood L, Wierenga CE, Bangen KJ, Haaland KY, Frank LR, Salmon DP, Bondi MW (2009): Decreased white matter integrity in late-myelinating fiber pathways in Alzheimer's disease supports retrogenesis. Neuroimage 45:10-16.
58. Thompson AJ, Montalban X, Barkhof F, Brochet B, Filippi M, Miller DH, Polman CH, Stevenson VL, McDonald WI (2000): Diagnostic criteria for primary progressive multiple sclerosis: A position paper. Ann Neurol 47:831-835.
59. Tofts PS (2003):Quantitative MRI of the Brain: Measuring Changes Caused by Disease.Chichester:Wiley.
60. Tortorella C, Viti B, Bozzali M, Sormani MP, Rizzo G, Gilardi MF, Comi G, Filippi M (2000): A magnetization transfer histogram study of normal-appearing brain tissue in MS. Neurology 54:186-193.
61. Tur C, Khaleeli Z, Ciccarelli O, Altmann DR, Cercignani M, Miller DH, Thompson AJ (2011): Complementary roles of grey matter MTR and T2 lesions in predicting progression in early PPMS. J Neurol Neurosurg Psychiatry 82:423-428.
62. van Waesberghe JH, Kamphorst W, De Groot CJ, van Walderveen MA, Castelijns JA, Ravid R, Nijeholt GJ, van der Valk P, Polman CH, Thompson AJ, Barkhof F (1999): Axonal loss in multiple sclerosis lesions: Magnetic resonance imaging insights into substrates of disability. Ann Neurol 46:747-754.
63. Voogd J (2003): The human cerebellum. J Chem Neuroanat 26:243-252.
64. Vrenken H, Pouwels PJ, Ropele S, Knol DL, Geurts JJ, Polman CH, Barkhof F, Castelijns JA (2007): Magnetization transfer ratio measurement in multiple sclerosis normal-appearing brain tissue: Limited differences with controls but relationships with clinical and MR measures of disease. Mult Scler 13:708-716.
65. Wilson M, Tench CR, Morgan PS, Blumhardt LD (2003): Pyramidal tract mapping by diffusion tensor magnetic resonance imaging in multiple sclerosis: Improving correlations with disability. J Neurol Neurosurg Psychiatry 74:203-207.
66. Wingerchuk DM, Noseworthy JH, Weinshenker BG (1997): Clinical outcome measures and rating scales in multiple sclerosis trials. Mayo Clin Proc 72:1070-1079.
67. Zhang J, Jones M, DeBoy CA, Reich DS, Farrell JA, Hoffman PN, Griffin JW, Sheikh KA, Miller MI, Mori S, Calabresi PA (2009): Diffusion tensor magnetic resonance imaging of Wallerian degeneration in rat spinal cord after dorsal root axotomy. J Neurosci 29:3160-3171.
68. Zivadinov R (2007): Can imaging techniques measure neuroprotection and remyelination in multiple sclerosis?Neurology 68(22, Suppl 3):S72-S82.