Investigating axonal damage in multiple sclerosis by diffusion tensor spectroscopy

Journal of Neuroscience

Volumn 32, Issue 19, 2012, Pages 6665-6669

  Wood, Emily T ^a,b   Ronen, Itamar ^c   Techawiboonwong, Aranee ^d   Jones, Craig K ^b,e   Barker, Peter B ^b,e   Calabresi, Peter ^b   Harrison, Daniel ^b   Reich, Daniel S ^a,b,f  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MAHIDOL UNIVERSITY   (Thailand)

^e KENNEDY KRIEGER INSTITUTE   (United States)

^f JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N ACETYLASPARTIC ACID;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; CROSS-SECTIONAL STUDY; DIFFUSION; DIFFUSION TENSOR IMAGING; DIFFUSION TENSOR SPECTROSCOPY; DISEASE SEVERITY; FEMALE; HUMAN; MALE; MULTIPLE SCLEROSIS; NERVE FIBER DEGENERATION; NEUROPATHY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PILOT STUDY; PRIORITY JOURNAL; WHITE MATTER;

ADULT; ASPARTIC ACID; AXONS; DIFFUSION MAGNETIC RESONANCE IMAGING; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; INTRACELLULAR FLUID; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; YOUNG ADULT;

EID: 84860691656     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0044-12.2012     Document Type: Article

References (44)

1. Bammer R, Augustin M, Strasser-Fuchs S, Seifert T, Kapeller P, Stollberger R, Ebner F, Hartung HP, Fazekas F (2000) Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magn Reson Med 44:583-591.
2. Budde MD, Frank JA (2010) Neurite beading is sufficient to decrease the apparent diffusion coefficient after ischemic stroke. Proc Natl Acad Sci U S A 107:14472-14477.
3. Budde MD, Xie M, Cross AH, Song SK (2009) Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyeli-tis spinal cord: a quantitative pixelwise analysis. J Neurosci 29:2805-2813.
4. 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.
5. Carass A, Cuzzocreo J, Wheeler MB, Bazin PL, Resnick SM, Prince JL (2011) Simple paradigm for extra-cerebral tissue removal: algorithm and analysis. Neuroimage 56:1982-1992.
6. Ciccarelli O, Toosy AT, De Stefano N, Wheeler-Kingshott CA, Miller DH, Thompson AJ (2010) Assessing neuronal metabolism in vivo by modeling imaging measures. J Neurosci 30:15030-15033.
7. Davie CA, Hawkins CP, Barker GJ, Brennan A, Tofts PS, Miller DH, McDonald WI (1994) Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 117:49-58.
8. DeBoy CA, Zhang J, Dike S, Shats I, Jones M, Reich DS, Mori S, Nguyen T, Rothstein B, Miller RH, Griffin JT, Kerr DA, Calabresi PA (2007) High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 130:2199-2210.
9. Ellegood J, Hanstock CC, Beaulieu C (2006) Diffusion tensor spectroscopy (DTS) of human brain. Magn Reson Med 55:1-8.
10. Filippi M, Bozzali M, Rovaris M, Gonen O, Kesavadas C, Ghezzi A, Martinelli V, Grossman RI, Scotti G, Comi G, Falini A (2003) Evidence for widespread axonal damage at the earliest clinical stage of multiple sclerosis. Brain 126:433-437.
11. Fu L, Matthews PM, De Stefano N, Worsley KJ, Narayanan S, Francis GS, Antel JP, Wolfson C, Arnold DL (1998) Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 121:103-113.
12. Gonen O, Catalaa I, Babb JS, Ge Y, Mannon LJ, Kolson DL, Grossman RI (2000) Total brain N-acetylaspartate: a new measure of disease load in MS. Neurology 54:15-19.
13. Haga KK, Khor YP, Farrall A, Wardlaw JM (2009) A systematic review of brain metabolite changes, measured with 1H magnetic resonance spec-troscopy, in healthy aging. Neurobiol Aging 30:353-363.
14. Inglese M, Ge Y, Filippi M, Falini A, Grossman RI, Gonen O (2004) Indirect evidence for early widespread gray matter involvement in relapsing-remitting multiple sclerosis. Neuroimage 21:1825-1829.
15. Kan HE, Techawiboonwong A, van Osch MJ, Versluis MJ, Deelchand DK, Henry PG, Marjańska M, van Buchem MA, Webb AG, Ronen I (2011) Differences in apparent diffusion coefficients of brain metabolites between grey and white matter in the human brain measured at 7 T. Magn Reson Med 67:1203-1209.
16. Kroenke CD, Ackerman JJ, Yablonskiy DA (2004) Onthe nature ofthe NAA diffusion attenuated MR signal in the central nervous system. Magn Reson Med 52:1052-1059.
17. Kutzelnigg A, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Berg-mann M, Schmidbauer M, Parisi JE, Lassmann H (2005) Cortical demy-elination and diffuse white matter injury in multiple sclerosis. Brain 128:2705-2712.
18. Landman BA, Farrell JA, Smith SA, Reich DS, Calabresi PA, van Zijl PC (2010) Complex geometric models of diffusion and relaxation in healthy and damaged white matter. NMR Biomed 23:152-162.
19. Mahad DJ, Ziabreva I, Campbell G, Lax N, White K, Hanson PS, Lassmann H, Turnbull DM (2009) Mitochondrial changes within axons in multiple sclerosis. Brain 132:1161-1174.
20. McAuliffe MJ, Lalonde FM, McGarry D, Gandler W, Csaky K, Trus BL (2001) Medical image processing, analysis and visualization in clinical research. In: 14th IEEE Symposium on Computer-Based Medical Sys tems, pp 381-386.
21. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AM (2007) N-acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol 81:89-131.
22. Naismith RT, Xu J, Tutlam NT, Lancia S, Trinkaus K, Song SK, Cross AH (2012) Diffusion tensor imaging in acute optic neuropathies: predictor of clinical outcomes. Arch Neurol 69:65-71.
23. Oh J, Pelletier D, Nelson SJ (2004) Corpus callosum axonal injury in multiple sclerosis measured by proton magnetic resonance spectroscopic imaging. Arch Neurol 61:1081-1086.
24. Ozturk A, Smith SA, Gordon-Lipkin EM, Harrison DM, Shiee N, Pham DL, Caffo BS, Calabresi PA, Reich DS (2010) MRI of the corpus callosum in multiple sclerosis: association with disability. Mult Scler 16:166-177.
25. Pham DL, Prince JL (1999) Adaptive fuzzy segmentation of magnetic resonance images. IEEE Trans Med Imaging 18:737-752.
26. Posse S, Cuenod CA, LeBihan D (1993) Human brain: proton diffusion MR spectroscopy. Radiology 188:719-725.
27. Provencher SW (1993) Estimationof metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672-679.
28. Reich DS, Ozturk A, Calabresi PA, Mori S (2010) Automated vs conventional tractography in multiple sclerosis: variability and correlation with disability. Neuroimage 49:3047-3056.
29. Riccitelli G, Rocca MA, Forn C, Colombo B, Comi G, Filippi M (2011) Voxel-wise assessment of the regional distribution of damage in the brains of patients with multiple sclerosis and fatigue. Am J Neuroradiol 32:874-879.
30. Rigotti DJ, Gonen O, Grossman RI, Babb JS, Falini A, Benedetti B, Filippi M (2011) Global N-acetylaspartate declines even in benign multiple sclerosis. Am J Neuroradiol 32:204-209.
31. Sajja BR, Narayana PA, Wolinsky JS, Ahn CW, PROMiSe Trial MRSI Group (2008) Longitudinal magnetic resonance spectroscopic imaging of primary progressive multiple sclerosis patients treated with glatiramer acetate: multicenter study. Mult Scler 14:73-80.
32. Simmons ML, Frondoza CG, Coyle JT (1991) Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience 45:37-45.
33. Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
34. Tallantyre EC, Bø L, Al-Rawashdeh O, Owens T, Polman CH, Lowe JS, Evan-gelou N (2010) Clinico-pathological evidence that axonal loss underlies disability in progressive multiple sclerosis. Mult Scler 16:406-411.
35. Teunissen CE, Iacobaeus E, Khademi M, Brundin L, Norgren N, Koel-Simmelink MJA, Schepens M, Bouwman F, Twaalfhoven HA, Blom HJ, Jakobs C, Dijkstra CD (2009) Combination of CSF N-acetylaspartate and neurofilaments in multiple sclerosis. Neurology 72:1322-1329.
36. Trapp BD, Nave KA (2008) Multiple sclerosis: an immune or neurodegen-erative disorder? Annu Rev Neurosci 31:247-269.
37. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mörk S, Böø L (1998) Axonal transection in the lesions of multiple sclerosis. N Engl J Med 338:278-285.
38. Upadhyay J, Hallock K, Erb K, Kim DS, Ronen I (2007) Diffusion properties of NAA in human corpus callosum as studied with diffusion tensor spec-troscopy. Magn Reson Med 58:1045-1053.
39. Upadhyay J, Hallock K, Ducros M, Kim DS, Ronen I (2008) Diffusion tensor spectroscopy and imaging of the arcuate fasciculus. Neuroimage 39:1-9.
40. van Zijl PCM, Davis D, Moonen CTW (1994) Diffusion spectroscopy in living systems. In: NMR in physiology and biomedicine (Gillies RJ, ed), pp 185-198. San Diego: Academic.
41. Visser F, Zwanenburg JJ, Hoogduin JM, Luijten PR (2010) High-resolution magnetization-prepared 3D-FLAIR imaging at 7.0 Tesla. Magn Reson Med 64:194-202.
42. Wattjes MP, Harzheim M, Lutterbey GG, Klotz L, Schild HH, Träber F (2007) Axonal damage but no increased glial cell activity in the normal-appearing white matterofpatients with clinically isolated syndromes suggestive of multiple sclerosis using high-field magnetic resonance spectroscopy. Am J Neuroradiol 28:1517-1522.
43. Werring DJ, Clark CA, Barker GJ, Thompson AJ, Miller DH (1999) Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology 52:1626-1632.
44. Xie M, Tobin JE, Budde MD, Chen CI, Trinkaus K, Cross AH, McDaniel DP, Song SK, Armstrong RC (2010) Rostrocaudal analysis of corpus callosum demyelination and axon damage across disease stages refines diffusion tensor imaging correlations with pathological features. J Neuropathol Exp Neurol 69:704 -716.