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1 0 Wallerian Degeneration of the Pyramidal Tract in Capsular Infarction Studied by Magnetic Resonance Imaging Jesiis Pujol, MD, Josep L. Marti-Vilalta, MD, Carme Junqu6, PhD, Pere Vendrell, PhD, Juan Fernandez, MD, and Antoni Capdevila, MD Using magnetic resonance imaging, we studied 2 patients with ischemic infarction of the internal capsule. Magnetic resonance imaging detected wallerian degeneration of the pyramidal tract below the capsular lesion in 11 patients (.8%); all 11 had clinical evidence of pyramidal tract damage. In six additional patients magnetic resonance imaging findings, present only on axial slices, were considered to indicate possible wallerian degeneration. When motor deficit was associated with posterior limb lesions, magnetic resonance imaging detected wallerian degeneration of the pyramidal tract in 78.6% (11) of 1 patients. (Stroke 1990^1:0-09) Magnetic resonance imaging (MR!) provides excellent visualization of anterograde (wallerian) degeneration in the human brain. 1-2 Prolongation of the Tl and T2 relaxation times permits visualization of a band of signal abnormality topographically limited to the impaired tract distal to the pathway disruption; the band traces the course of the degenerated pathways. The correlation between such bands and wallerian degeneration has been histopathologically confirmed by autopsy. 1 The usefulness of MRI in visualizing wallerian degeneration has been demonstrated in both experimental and clinical studies. Jolesz et al 3 reported an experimental work using magnetic resonance spectroscopy of rat sciatic nerves. A series of patients 1 and several case reports showing MRI evidence of wallerian degeneration in the human brain have been reported. However, there have been no systematic studies using a uniform sample of clinically similar patients with lesions of the same size and location. The sensitivity of MRI in demonstrating wallerian degeneration is not yet known, and its relation with the clinical status of the patient has not been investigated. We report the occurrence on MRI of changes suggestive of wallerian degeneration of the pyramidal From the Department of Neurology, Sta. Creu i St Pau Hospital, Autonomous University of Barcelona (J.P., J.L.M-V., P.V., J.F.), the Department of Psychiatry and Clinical Psychobiology, University of Barcelona (CJ.), and the Magnetic Resonance Center of Barcelona (A.C.), Barcelona, Spain. Address for correspondence: Dr. Jesus Pujol, Department of Neurology, Sta. Creu i St. Pau Hospital, Av. St A.M. Claret, 167, 0802 Barcelona, Spain. Received June 26, 1989; accepted October 10, tract in patients with chronic ischemic lesions of the internal capsule, and we correlate the extent of MRI findings of wallerian degeneration with the severity of clinical signs of pyramidal tract involvement. Subjects and Methods We selected 2 subjects from among 3 patients with clinical and MRI findings compatible with deep ischemic infarction and the absence of cortical lesions. These 2 subjects include all patients who had a lesion on MRI involving the internal capsule and clinical findings compatible with a lesion in this location. There were 17 men and seven women with a mean age of 6. (range -77) years. Each patient had superconductive MRI during the chronic stage of the disease, >3 months after the initial insult. We performed a thorough neurologic evaluation during both the acute and the chronic stages of the disease. Pyramidal tract signs were evaluated as none (normal examination), mild (mild hemiparesis, but muscles still capable of contracting against resistance, with or without hyperreflexia or Babinski's sign), or moderate-severe (moderate to severe hemiparesis, muscles incapable of contracting against resistance, and positive hyperreflexia or Babinski's sign). MRI was carried out with a 1.-T magnetic resonance imager (General Electric, Milwaukee, Wisconsin) 3-36 (mean±sd 13.33± 12.37) months after the stroke. All T2-weighted images were obtained using a multiecho spin-echo pulse sequence with a repetition time of 2,000 msec and echo times of 0 msec for the axial planes and 90 msec for the coronal planes. Tl-weighted images for the sagittal planes were obtained with a repetition time of 00 msec and an
2 echo time of 30 msec. In all 2 subjects we obtained 1 contiguous -mm-thick slices for each plane. We analyzed T2-weighted images in the axial and coronal projections, and we related the features of the capsular lesions to location and contour. We also analyzed the pyramidal tract signal abnormalities below the lesion. A subject was considered to have MRI abnormalities suggestive of wallerian degeneration when 1) coronal images showed a band of abnormal signal intensity topographically limited to the pyramidal tract below the lesion, extending through the internal capsule and midbrain, and reaching the pons or medulla, and 2) several axial slices showed focal abnormal signal intensity confined to the site of the pyramidal tract, corresponding to the level of abnormal signal intensity seen on coronal slices. The MRI study was considered to indicate possible wallerian degeneration if the abnormal signal intensity at the pyramidal tract was seen only on axial slices and there were no abnormalities on coronal images; in this instance it was not possible to exclude a focal ischemic or infarcted region. Results The clinical features of the 2 subjects with capsular lesions and their MRIfindings are shown in Table 1. Eleven (.8%) had signal intensity abnormalities at the site of the pyramidal tract, suggesting anterograde or wallerian degeneration. In three of these 11 patients, T2-weighted coronal images revealed increased signal intensity extending from the primary capsular lesion down to the internal capsule below the lesion, the midbrain, pons, and medulla (Figure 1). In the remaining eight patients, the band of increased signal intensity arising from the capsular lesion reached the pons (Figure 2). In all 11 patients, MRI demonstrated focal abnormal signal intensity confined to the site of the pyramidal tract on axial slices, corresponding to the level of abnormal signal intensity on coronal slices. All 11 patients with images suggestive of wallerian degeneration had a lesion involving the posterior limb of the internal capsule, with a well-demarcated contour. In addition, ah 1 11 patients had clinical evidence of pyramidal tract involvement (moderate-severe in six patients and mild in the other five). Wallerian degeneration was catalogued as possible in six of the 2 patients with capsular lesions. On axial slices, all six of these patients had signal intensity abnormalities confined to the site of the pyramidal tract ipsilateral to the capsular lesion, but no band of increased signal intensity was seen on coronal slices (Figure 3). In two patients the capsular lesion was well-demarcated and located in the posterior limb; the remaining four patients had 6 patchy, poorly defined lesions. Clinical signs of pyramidal tract involvement were moderate-severe in one patient and mild in four; the neurologic examination was normal in the other patient. Seven patients had no MRI evidence of wallerian degeneration. In five of these patients, the capsular Pujol et al Wallerian Degeneration and MRI 0 lesion was well demarcated; the lesion was located in the posterior limb in one patient, in the genu in another, and in the thalamocapsular region in the other three (the lesion extended more into the thalamus than into the capsule). Two patients had a diffuse, poorly defined lesion. Among these seven patients, one had moderate-severe clinical signs of pyramidal tract involvement, two had mild signs, and four had no signs. Overall, 11 (78.6%) of the 1 patients with motor deficit and a well-demarcated lesion in the posterior limb of the internal capsule showed MRI findings of pyramidal tract degeneration. Discussion We investigated MRI changes suggestive of wallerian degeneration in a homogeneous series of 2 patients. All patients were in the chronic stage of ischemic infarction of the internal capsule. In all 2 patients MRI was performed ^3 months after the acute event. In all 2 patients the current clinical diagnosis could be directly explained by the lesion seen on MRI. To our knowledge there are no previous reports studying wallerian degeneration using a sample similar to that reported here. We found that.8% of patients with a capsular lesion have MRI findings compatible with wallerian degeneration of the pyramidal tract. Since the MRI signal abnormalities are confined to the site of the pyramidal tract, it is unlikely that such abnormalities represent changes other than degenerative alterations of this tract. Therefore, when a hyperintense band is seen in the axial and coronal slices and the band traces the anatomic course of the pyramidal tract, degeneration of this pathway can be inferred. The degree of evidence depends on the length of the band. In three patients the entire pyramidal tract, from the capsular lesion to the medulla, was seen to be involved; in the other eight patients the indication of degenerative changes reached the pons. The distribution of these changes does not correspond to any vascular region; furthermore, we do not know of any nondegenerative pathologic changes showing images that may be misinterpreted as those reported here. In six patients MRI was considered to indicate possible wallerian degeneration. In these six patients signal abnormalities were seen only in the axial slices, and we cannot exclude the possibility of a focal ischemic or infarcted region. However, the signal abnormalities seen in these patients, especially at the pontine level, were similar to those observed in patients with definite wallerian degeneration, and the signal abnormalities were confined to the site of the pyramidal tract. No patient had a history of repeated stroke. According to our results, degenerative changes of the pyramidal tract are closely related to clinical signs of pyramidal deficit. Marked clinical signs of pyramidal tract involvement were observed in all patients with MRI indications of wallerian degeneration. Conversely, when a patient with a capsular lesion
3 6" TABLE 1. Clinical Characteristics and Magnetic Resonance Imaging Findings in 2 Patients With Internal Capsule Lesions Pt/sex/age Acute-stage clinical syndromes Chronic pyramidal tract signs l/f/77 Sensorimotor stroke M-S 2/M/67 Pure motor hemiparesis M-S 3/M/66 Pure motor hemiparesis M-S /M/66 Hemiparesis+dysarthria Mild /M/61 Sensorimotor stroke Mild 6/M/70 Pure motor hemiparesis M-S 7/M/76 Pure motor hemiparesis M-S 8/M/66 Pure motor hemiparesis M-S 9/M/71 Sensorimotor deficit+hemianopsia Mild 10/F/61 Sensorimotor stroke Mild ll/m/ Hemiparesis+dysphonia-dysarthria-dysphagia Mild 12/F/67 Sensorimotor stroke Mild 13/M/6 Sensorimotor stroke Mild 1/M/66 Sensorimotor stroke None 1/F/8 Pure motor hemiparesis M-S 16/F/77 Sensorimotor stroke Mild 17/F/71 Pure motor hemiparesis Mild 18/M/67 Pure motor hemiparesis None 19/M/76 Atypical hemiparesthesia None 20/M/61 Pure motor hemiparesis M-S 21/M/6 Sensorimotor stroke Mild 22/F/61 Pure motor hemiparesis Mild 23/M/61 Pure sensory stroke None 2/M/62 Pure sensory stroke None Magnetic resonance imaging Time after onset Capsular lesion Location Definition Caudal extent Genu Thalamocapsular Thalamocapsular Thalamocapsular Wallerian degeneration Pt, patient; F, female; M, male; age in years; time after onset in months; M-S, moderate-severe; caudal extent, most caudal level in which wallerian degeneration was seen in coronal plane. Medulla Medulla Medulla Coronal slice Axial slice -
4 Pujol e! al Wallerian Degeneration and MRI 07 FIGURE 1. Magnetic resonance images fivm patient with lesion of internal capsule. Top: Coronal T2-weighted image demonstrates long band of increased signal extending from capsular infarct to medulla.(arrows). Bottom: Axial slices from same patient show focal signal intensity confined to site of pyramidal tract (arrows) at midbrain-diencephalon junction (left) and atpontine level (right). does not have signs of pyramidal deficit, the probability of showing indications of wallerian degeneration on MRI is low. In all the patients in whom definite wallerian degeneration was demonstrated, there was a welldemarcated ischemic lesion in the posterior limb of the internal capsule. Therefore, when motor deficit on clinical examination coexists with posterior limb capsular lesion on MRI, the probability of finding indications of wallerian degeneration is high. In our
5 G Stroke Vol 21, No 3, March 1990 FIGURE 2. Coronal T2-weighted magnetic resonance image shows band of increased signal intensity extending from internal capsule to pons (arrows). series, 78.6% of patients with both conditions had evidence of wallerian degeneration on MRI. However, three patients with a well-demarcated lesion and motor deficit had no MRI findings suggestive of wallerian degeneration. Based on histopathologic data concerning the time course of axonal degeneration following pathway disruption, we believe that our timing of postinfarction MRI was optimal to detect signal changes. Axons begin to degenerate soon after the pathway is interrupted, but the myelin sheath may remain intact for up to 2 days. Myelin begins to break down into simpler lipids only after 100 days. 6 According to this, degenerative changes may be seen on MRI more clearly 3 months after the stroke. Even though 21 patients had MRI performed during the acute stage of their disease for clinical purposes, we did not analyze these initial images because they were obtained with different parameters. However, none of these early images showed signal abnormalities suggesting wallerian degeneration. We conclude that in patients with capsular infarction, high-field (1. -T) MRI can depict wallerian degeneration of the pyramidal tract with great sensitivity, particularly if there is a well-demarcated lesion in the posterior limb and when the patient presents clinically with some degree of pyramidal tract deficit. Acknowledgments The authors gratefully acknowledge the assistance of Dr. J. Dalmau and Dr. J. Krol in the preparation of this manuscript. FIGURE 3. Magnetic resonance images from patient with lesion of internal capsule. Left: Coronal T2-weighted image shows capsular infarct (arrow). Right: Axial slice from same patient demonstrates signal abnormalities topographically limited to location of pyramidal tract at pontine level (arrow).
6 Pujol et al Wallerian Degeneration and MRI 09 References 1. Kuhn MJ, Johnson KA, Davis KR: Wallerian degeneration: Evaluation with MR imaging. Radiology 1988;168: Cobb SR, Mehringer CM: Wallerian degeneration in a patient with Schilder disease: MR imaging demonstration. Radiology 1987;162: Jolesz FA, Polak JF, Ruenzel PW, Adams DF: Wallerian degeneration demonstrated by magnetic resonance: Spectroscopic measurements on peripheral nerve. Radiology 198; 12:8-87. DeWitt LD, Kistler JP, Miller DC, Richardson EP Jr, Buonanno FS: NMR-neuropathologic correlation in stroke. Stroke 1987;18: Sussman NM, Scanlon MD, Garfinkle MD, Canallan M, O'Connor MJ, Harner RN: Magnetic resonance imaging after corpus callosotomy. Neurology 1987;37: Adams JH (ed): Greenfield's Neuropathology, ed. New York, John Wiley & Sons, 198, pp 1-17 KEY WORDS cerebral infarction magnetic resonance imaging nerve degeneration pyramidal tracts
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