Early fiber number ratio is a surrogate of corticospinal tract integrity and predicts motor recovery after stroke

Stroke

Volumn 47, Issue 4, 2016, Pages 1053-1059

  Bigourdan, Antoine ^a,b   Munsch, Fanny ^a,b,c   Coupé, Pierrick ^a,d   Guttmann, Charles R G ^a,e   Sagnier, Sharmila ^b   Renou, Pauline ^b   Debruxelles, Sabrina ^b   Poli, Mathilde ^b   Dousset, Vincent ^a,b,c   Sibon, Igor ^a,b,f   Tourdias, Thomas ^a,b,c  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

^c INSTITUT FRANÇOIS MAGENDIE   (France)

^d UNIVERSITÉ BORDEAUX 1   (France)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f UMR 5287   (France)

Author keywords

cWallerian degeneration; Diffusion tensor imaging; Magnetic resonance imaging; Stroke; Stroke volume

Indexed keywords

ADULT; AGE; AGED; ARTICLE; BRAIN ISCHEMIA; CONVALESCENCE; CORTICOSPINAL TRACT INTEGRITY; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; FEMALE; FOLLOW UP; HEART STROKE VOLUME; HUMAN; IMAGE PROCESSING; IMAGE QUALITY; INITIAL FIBER NUMBER RATIO; MAJOR CLINICAL STUDY; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NERVOUS SYSTEM PARAMETERS; NUCLEAR MAGNETIC RESONANCE SCANNER; OUTCOME ASSESSMENT; PREDICTION; PREDICTIVE VALUE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PYRAMIDAL TRACT; RANKIN SCALE; SENSITIVITY AND SPECIFICITY; MIDDLE AGED; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROGNOSIS; SEVERITY OF ILLNESS INDEX; STROKE;

AGED; BRAIN ISCHEMIA; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR ACTIVITY; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; SEVERITY OF ILLNESS INDEX; STROKE;

EID: 84961230898     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.115.011576     Document Type: Article

References (41)

1. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation. 2015;131:e29-e322. doi: 10.1161/CIR.0000000000000152.
2. Weimar C, König IR, Kraywinkel K, Ziegler A, Diener HC; German Stroke Study Collaboration. Age and National Institutes of Health Stroke Scale Score within 6 hours after onset are accurate predictors of outcome after cerebral ischemia: development and external validation of prognostic models. Stroke. 2004;35:158-162. doi: 10.1161/01.STR.0000106761.94985.8B.
3. Saposnik G, Guzik AK, Reeves M, Ovbiagele B, Johnston SC. Stroke Prognostication using Age and NIH Stroke Scale: SPAN-100. Neurology. 2013;80:21-28. doi: 10.1212/WNL.0b013e31827b1ace.
4. Prabhakaran S, Zarahn E, Riley C, Speizer A, Chong JY, Lazar RM, et al. Inter-individual variability in the capacity for motor recovery after ischemic stroke. Neurorehabil Neural Repair. 2008;22:64-71. doi: 10.1177/1545968307305302.
5. Winters C, van Wegen EE, Daffertshofer A, Kwakkel G. Generalizability of the Proportional Recovery Model for the Upper Extremity After an Ischemic Stroke. Neurorehabil Neural Repair. 2015;29:614-622. doi: 10.1177/1545968314562115.
6. Stinear C. Prediction of recovery of motor function after stroke. Lancet Neurol. 2010;9:1228-1232. doi: 10.1016/S1474-4422(10)70247-7.
7. Vogt G, Laage R, Shuaib A, Schneider A; VISTA Collaboration. Initial lesion volume is an independent predictor of clinical stroke outcome at day 90: an analysis of the Virtual International Stroke Trials Archive (VISTA) database. Stroke. 2012;43:1266-1272. doi: 10.1161/STROKEAHA.111.646570.
8. Johnston KC, Wagner DP, Wang XQ, Newman GC, Thijs V, Sen S, et al; GAIN, Citicoline, and ASAP Investigators. Validation of an acute isch-emic stroke model: does diffusion-weighted imaging lesion volume offer a clinically signifcant improvement in prediction of outcome? Stroke. 2007;38:1820-1825. doi: 10.1161/STROKEAHA.106.479154.
9. Puig J, Pedraza S, Blasco G, Daunis-I-Estadella J, Prados F, Remollo S, et al. Acute damage to the posterior limb of the internal capsule on diffusion tensor tractography as an early imaging predictor of motor outcome after stroke. AJNR Am J Neuroradiol. 2011;32:857-863. doi: 10.3174/ajnr.A2400.
10. Byblow WD, Stinear CM, Barber PA, Petoe MA, Ackerley SJ. Proportional recovery after stroke depends on corticomotor integrity. Ann Neurol. 2015;78:848-859. doi: 10.1002/ana.24472.
11. Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A. Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol. 2008;7:715-727. doi: 10.1016/S1474-4422(08)70163-7.
12. Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Röther J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage. 2004;22:1767-1774. doi: 10.1016/j.neuroimage.2004.03.041.
13. Liang Z, Zeng J, Liu S, Ling X, Xu A, Yu J, et al. A prospective study of secondary degeneration following subcortical infarction using diffusion tensor imaging. J Neurol Neurosurg Psychiatry. 2007;78:581-586. doi: 10.1136/jnnp.2006.099077.
14. Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. Structural integrity of corticospinal motor fbers predicts motor impairment in chronic stroke. Neurology. 2010;74:280-287. doi: 10.1212/WNL.0b013e3181ccc6d9.
15. Puig J, Blasco G, Daunis-I-Estadella J, Thomalla G, Castellanos M, Figueras J, et al. Decreased corticospinal tract fractional anisotropy predicts long-term motor outcome after stroke. Stroke. 2013;44:2016-2018. doi: 10.1161/STROKEAHA.111.000382.
16. Feng W, Wang J, Chhatbar PY, Doughty C, Landsittel D, Lioutas VA, et al. Corticospinal tract lesion load: an imaging biomarker for stroke motor outcomes. Ann Neurol. 2015;78:860-870. doi: 10.1002/ana.24510.
17. Puig J, Pedraza S, Blasco G, Daunis-I-Estadella J, Prats A, Prados F, et al. Wallerian degeneration in the corticospinal tract evaluated by diffusion tensor imaging correlates with motor defcit 30 days after middle cerebral artery ischemic stroke. AJNR Am J Neuroradiol. 2010;31:1324-1330. doi: 10.3174/ajnr.A2038.
18. DeVetten G, Coutts SB, Hill MD, Goyal M, Eesa M, O'Brien B, et al; MONITOR and VISION study groups. Acute corticospinal tract Wallerian degeneration is associated with stroke outcome. Stroke. 2010;41:751-756. doi: 10.1161/STROKEAHA.109.573287.
19. Maraka S, Jiang Q, Jafari-Khouzani K, Li L, Malik S, Hamidian H, et al. Degree of corticospinal tract damage correlates with motor function after stroke. Ann Clin Transl Neurol. 2014;1:891-899. doi: 10.1002/acn3.132.
20. Møller M, Frandsen J, Andersen G, Gjedde A, Vestergaard-Poulsen P, Østergaard L. Dynamic changes in corticospinal tracts after stroke detected by fbretracking. J Neurol Neurosurg Psychiatry. 2007;78:587-592. doi: 10.1136/jnnp.2006.100248.
21. Zhang M, Lin Q, Lu J, Rong D, Zhao Z, Ma Q, et al. Pontine infarction: diffusion-tensor imaging of motor pathways-a longitudinal study. Radiology. 2015;274:841-850. doi: 10.1148/radiol.14140373.
22. Gladstone DJ, Danells CJ, Black SE. The fugl-meyer assessment of motor recovery after stroke: a critical review of its measurement properties. Neurorehabil Neural Repair. 2002;16:232-240.
23. Verheyden G, Nieuwboer A, De Wit L, Thijs V, Dobbelaere J, Devos H, et al. Time course of trunk, arm, leg, and functional recovery after ischemic stroke. Neurorehabil Neural Repair. 2008;22:173-179. doi: 10.1177/1545968307305456.
24. Sorensen AG, Wu O, Copen WA, Davis TL, Gonzalez RG, Koroshetz WJ, et al. Human acute cerebral ischemia: detection of changes in water diffusion anisotropy by using MR imaging. Radiology. 1999;212:785-792. doi: 10.1148/radiology.212.3.r99se24785.
25. Manjón JV, Coupé P, Concha L, Buades A, Collins DL, Robles M. Diffusion weighted image denoising using overcomplete local PCA. PLoS One. 2013;8:e73021. doi: 10.1371/journal.pone.0073021.
26. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage. 2011;54:2033-2044. doi: 10.1016/j. neuroimage.2010.09.025.
27. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology. 2004;230:77-87. doi: 10.1148/radiol.2301021640.
28. Sanford J, Moreland J, Swanson LR, Stratford PW, Gowland C. Reliability of the Fugl-Meyer assessment for testing motor performance in patients following stroke. Phys Ther. 1993;73:447-454.
29. Kuhn MJ, Mikulis DJ, Ayoub DM, Kosofsky BE, Davis KR, Taveras JM. Wallerian degeneration after cerebral infarction: evaluation with sequential MR imaging. Radiology. 1989;172:179-182. doi: 10.1148/radiology.172.1.2740501.
30. Thomalla G, Glauche V, Weiller C, Röther J. Time course of wallerian degeneration after ischaemic stroke revealed by diffusion tensor imaging. J Neurol Neurosurg Psychiatry. 2005;76:266-268. doi: 10.1136/jnnp.2004.046375.
31. Iizuka H, Sakatani K, Young W. Corticofugal axonal degeneration in rats after middle cerebral artery occlusion. Stroke. 1989;20:1396-1402.
32. Bhagat YA, Hussain MS, Stobbe RW, Butcher KS, Emery DJ, Shuaib A, et al. Elevations of diffusion anisotropy are associated with hyper-acute stroke: a serial imaging study. Magn Reson Imaging. 2008;26:683-693. doi: 10.1016/j.mri.2008.01.015.
33. Zhu LL, Lindenberg R, Alexander MP, Schlaug G. Lesion load of the corticospinal tract predicts motor impairment in chronic stroke. Stroke. 2010;41:910-915. doi: 10.1161/STROKEAHA.109.577023.
34. Lansberg MG, O'Brien MW, Tong DC, Moseley ME, Albers GW. Evolution of cerebral infarct volume assessed by diffusion-weighted magnetic resonance imaging. Arch Neurol. 2001;58:613-617.
35. Krakauer JW, Marshall RS. The proportional recovery rule for stroke revisited. Ann Neurol. 2015;78:845-847. doi: 10.1002/ana.24537.
36. Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain. 2012;135(pt 8):2527-2535. doi: 10.1093/brain/aws146.
37. Green JB. Brain reorganization after stroke. Top Stroke Rehabil. 2003;10:1-20. doi: 10.1310/H65X-23HW-QL1G-KTNQ.
38. Zeiler SR, Krakauer JW. The interaction between training and plasticity in the poststroke brain. Curr Opin Neurol. 2013;26:609-616. doi: 10.1097/WCO.0000000000000025.
39. Marshall RS, Zarahn E, Alon L, Minzer B, Lazar RM, Krakauer JW. Early imaging correlates of subsequent motor recovery after stroke. Ann Neurol. 2009;65:596-602. doi: 10.1002/ana.21636.
40. Zarahn E, Alon L, Ryan SL, Lazar RM, Vry MS, Weiller C, et al. Prediction of motor recovery using initial impairment and fMRI 48 h poststroke. Cereb Cortex. 2011;21:2712-2721. doi: 10.1093/cercor/bhr047.
41. Lee DH, Park JW, Park SH, Hong C. Have You Ever Seen the Impact of Crossing Fiber in DTI?: Demonstration of the Corticospinal Tract Pathway. PLoS One. 2015;10:e0112045. doi: 10.1371/journal. pone.0112045.