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Microstructural Status of Ipsilesional and Contralesional Corticospinal Tract Correlates with Motor Skill in Chronic Stroke Patients

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Microstructural Status of Ipsilesional and Contralesional Corticospinal Tract Correlates with Motor Skill in Chronic Stroke Patients r Human Brain Mapping 30:3461–3474 (2009) r Microstructural Status of Ipsilesional and Contralesional Corticospinal Tract Correlates with Motor Skill in Chronic Stroke Patients Judith D. Schaechter,1,2* Zachary P. Fricker,1,2 Katherine L. Perdue,1,2 Karl G. Helmer,1,2 Mark G. Vangel,1,2 Douglas N. Greve,1,2 and Nikos Makris1,3 1MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts 2Department of Radiology, Harvard Medical School, Boston, Massachusetts 3Department of Neurology and Psychiatry, Harvard Medical School, Boston, Massachusetts r r Abstract: Greater loss in structural integrity of the ipsilesional corticospinal tract (CST) is associated with poorer motor outcome in patients with hemiparetic stroke. Animal models of stroke have demonstrated that structural remodeling of white matter in the ipsilesional and contralesional hemispheres is associated with improved motor recovery. Accordingly, motor recovery in patients with stroke may relate to the relative strength of CST degeneration and remodeling. This study examined the relationship between microstructural status of brain white matter tracts, indexed by the fractional anisotropy (FA) metric derived from diffusion tensor imaging (DTI) data, and motor skill of the stroke-affected hand in patients with chronic stroke. Voxel- wise analysis revealed that motor skill significantly and positively correlated with FA of the ipsilesional and contralesional CST in the patients. Additional voxelwise analyses showed that patients with poorer motor skill had reduced FA of bilateral CST compared to normal control subjects, whereas patients with better motor skill had elevated FA of bilateral CST compared to controls. These findings were confirmed using a DTI-tractography method applied to the CST in both hemispheres. The results of this study suggest that the level of motor skill recovery achieved in patients with hemiparetic stroke relates to microstructural status of the CST in both the ipsilesional and contralesional hemispheres, which may reflect the net effect of degener- ation and remodeling of bilateral CST. Hum Brain Mapp 30:3461–3474, 2009. VC 2009 Wiley-Liss, Inc. Key words: diffusion tensor imaging; anisotropy; stroke recovery; hemiparesis; tractography; white matter r r INTRODUCTION typically occurs over the subsequent weeks to months, yet is variable among stroke survivors. Motor recovery has Stroke commonly causes acute, contralateral loss of been shown to relate to reorganization of activity in the motor function. Poststroke recovery of this lost function ipsilesional and contralesional sensorimotor cortices [Dij- Additional Supporting Information may be found in the online Building 149, Room 2301; Charlestown, MA 02129.. version of this article. E-mail: [email protected] Contract grant sponsor: National Institutes of Health/NICHD; Received for publication 23 October 2009; Revised 2 January 2009; Contract grant number: K23-HD044425; Contract grant sponsor: National Accepted 7 February 2009 Institutes of Health/NCRR; Contract grant number: P41-RR14075; DOI: 10.1002/hbm.20770 Contract grant sponsor: National Institutes of Health/NIBIB; Contract Published online 15 April 2009 in Wiley InterScience (www. grant number: R01-EB002066; Contract grant sponsor: MIND Institute. interscience.wiley.com). *Correspondence to: Judith D. Schaechter, MGH/MIT/HMS Athi- noula A. Martinos Center for Biomedical Imaging, 13th Street, VC 2009 Wiley-Liss, Inc. r Schaechter et al. r khuizen et al., 2001; Jaillard et al., 2005; Ward et al., 2003]. between motor outcome in patients with chronic stroke Accumulating evidence from studies in animal models of and microstructural status of brain white matter tracts as stroke suggest that structural remodeling of white matter measured by FA. of the ipsilesional and contralesional hemispheres also To meet this aim, we employed a recently developed plays a role in motor recovery [Brus-Ramer et al., 2007; method called Tract-Based Spatial Statistics (TBSS) that Carmichael and Chesselet, 2002; Dancause et al., 2005; Liu optimally aligns major white matter tracts across subjects, et al., 2008; Stroemer et al., 1995]. Little is known about thereby allowing for valid voxelwise analyses of FA of all the relationship between white matter structure of the sen- major white matter tracts [Smith et al., 2006]. In addition, sorimotor network and motor recovery in patients with we focused on evaluating FA of the ipsilesional and con- stroke. tralesional CST using tractography. As the majority of The relatively recent development of diffusion tensor research aimed at understanding the neural underpinnings imaging (DTI), a noninvasive magnetic resonance imaging of motor outcome in patients with stroke has focused on (MRI) technology that measures the random motion of reorganization of gray matter activity, this study widens water molecules in brain tissue, enables examination of the lens of inquiry by investigating the influence of micro- white matter microstructure in vivo. Fractional anisotropy structural status of white matter. (FA) is a metric derived from DTI data that quantifies the extent to which water diffusion is directionally restricted, and is influenced by a number of factors including axonal myelination, diameter, density, and orientational coher- MATERIALS AND METHODS ence [Beaulieu, 2002; Takahashi et al., 2002]. FA is cur- Subjects rently the most commonly used metric to reflect microstructural status of white matter. During the first Ten patients with chronic stroke, former in-patients in few weeks after stroke in patients who go on to recover hospitals within the Greater Boston area, were enrolled relatively little motor function, the ipsilesional corticospi- (Table I). These patients fulfilled the following inclusion nal tract (CST) undergoes progressive decline in FA due criteria: (1) first-ever ischemic stroke incurred 6 to loss of axonal integrity that leads to Wallerian degen- months earlier; (2) acute unilateral loss of hand strength eration [Moller et al., 2007; Watanabe et al., 2001]. In ani- to 4 on the Medical Research Council (MRC) scale (0– mals recovering from experimentally-induced stroke, FA 5, 5 ¼ normal) [Medical Research Council, 1976] lasting of perilesional white matter declines during the first few 48 h, based on physician notes entered into the medi- days poststroke [van der Zijden et al., 2008], yet rises cal record of the initial hospitalization within 24 h af- during subsequent weeks [Ding et al., 2008; Jiang et al., ter stroke; and (3) at the time of study enrollment, the 2006; van der Zijden et al., 2008]. The rise in FA of per- stroke-affected hand had sufficient motor skill to permit ilesional white matter has been shown to colocalize with measurement of manual dexterity and index finger tap- histological evidence of white matter reorganization [Ding ping speed. Exclusion criteria were as follows: (1) prior et al., 2008; Jiang et al., 2006], increased angiogenesis and or subsequent symptomatic stroke; (2) language or cog- local cerebral blood flow [Ding et al., 2008], and en- nitive deficit that would impair cooperation with study hanced neural connectivity with perilesional sensorimotor procedures; (3) other disorder that impaired motor func- cortex based on manganese-enhanced MRI [van der Zij- tion of the stroke-affected hand; and (4) contraindication den et al., 2008]. Treatment of animals poststroke with to MRI. All patients had received and completed post- certain cell-based or pharmacological agents enhances the stroke physical rehabilitation. No patient had switched rise in perilesional FA in association with improved handedness from before the stroke to the time of study motor recovery [Ding et al., 2008; Jiang et al., 2006]. Ana- enrollment based on the Edinburgh Inventory [Oldfield, tomical tracing studies in animals with experimental 1971]. stroke have also shown that contralesional corticofugal Ten healthy adults with no history of stroke and a axons sprout to make new connections with nuclei dener- normal neurological examination were also enrolled. vated due to stroke, and that this form of axonal remod- These subjects were well matched to the patients with eling is enhanced by certain poststroke treatments in stroke for handedness (controls and patients: 9 right association with improved motor recovery [Andrews hand dominant, 1 left hand dominant), age (controls: 60 et al., 2008; Carmichael and Chesselet, 2002; Chen et al., Æ 10 years; patients: 59 Æ 11 years), and gender (con- 2002; Lee et al., 2004; Liu et al., 2008; Ramic et al., 2006]. trols: 3 females; patients: 4 females). This matching was In patients with chronic stroke, a progressive increase in done because handedness [Buchel et al., 2004], age FA of normal-appearing, whole-brain white matter has [Pfefferbaum et al., 2000], and gender [Hsu et al., 2008] been observed (from 3–6 to 24 months poststroke) [Wang may affect FA of white matter in the sensorimotor et al., 2006]. Together, these findings suggest that struc- network. tural changes of ipsilesional and contralesional white All subjects provided written informed consent in ac- matter occur after stroke and relate to motor recovery. cordance with the Human Subjects Committee of the Part- In this study, we sought to examine the relationship ners Institutional Review Board. r 3462 r r DTI and Motor Skill in Stroke Patients r TABLE I. Patient characteristics Time Acute UL Dominant Stroke-affected Age post-stroke (hand) Patient hand hand (yr) Gender (yr) MRC score Lesion location 1 R L 52 M 0.5 3 R CR, BG, temporal lobe 2 R R 47 M 3.9 0 (0) L CR, BG, IC, inferior frontal lobe 3 R R 41 F 5.9 0–3 (0) L medial temporal lobe, PLIC 4 R R 69 M 1.6 4 L CR, BG, temporal lobe 5 R L 76 F 2 1 (0) R CR, temporal lobe 6 R R 62 F 1.2 3–4þ (3þ)LCR 7 R L 48 F 1.7 0 (0) R frontal and parietal lobe white matter 8 L R 60 M 5.8 0–3 (0) L CR, BG 9 R R 61 M 2.2 0 (0) L frontal lobe, parietal lobe 10 R L 69 M 1.2 1–3 (1) R BG, IC Summary 9R/1L 6R/4L 59 Æ 11 4F/6M 2.6 Æ 1.9 M, male; F, female; R, right; L, left; UL, upper limb; IC, internal capsule; PLIC, posterior limb of IC; BG, basal ganglia; CR, corona radi- ata.
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