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Ipsilateral hemiparesis in lateral medullary infarction: Clinical investigation of the lesion location on magnetic resonance imaging
Journal of the Neurological Sciences 365 (2016) 40–45
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Ipsilateral hemiparesis in lateral medullary infarction: Clinical investigation of the lesion location on magnetic resonance imaging Masahiro Uemura a, Hiroaki Naritomi a, Hisakazu Uno a, Arisa Umesaki a, Kotaro Miyashita a,⁎, Kazunori Toyoda b, Kazuo Minematsu b, Kazuyuki Nagatsuka a a b
Department of Neurology, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan Department of Cerebrovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan
a r t i c l e
i n f o
Article history: Received 27 May 2015 Received in revised form 29 March 2016 Accepted 5 April 2016 Available online 10 April 2016 Keywords: Cerebral infarction Lateral medullary infarction Magnetic resonance imaging Opalski's syndrome Ipsilateral hemiparesis Pyramidal tract
a b s t r a c t Background: In 1946, Opalski reported two cases of Wallenberg syndrome with ipsilateral hemiparesis (IH). His hypothesis seems to be based on the view that IH is caused by post-decussating pyramidal tract damage. Afterwards, other researchers proposed a different hypothesis that ipsilateral sensory symptoms of limbs (ISSL) or ipsilateral limb ataxia (ILA) caused by lateral medullary infarction (LMI) might lead to ipsilateral motor weakness. The present study is aimed to clarify whether IH in LMI patients is attributable mainly to ISSL/ILA or disruption of ipsilateral post-decussating pyramidal tract. Methods: Thirty-two patients with acute LMI admitted during the last 13 years were divided to IH Group (n = 7) and Non-IH Group (n = 25). Lesion location/distribution on MRI and neurological findings were compared between the two groups. Results: LMI involved the lower medulla in all seven IH patients and 12 of 25 Non-IH patients. The lower medullary lesion extended to the cervico-medullary junction (CMJ) in four of seven IH patients and one of 12 Non-IH patients. Definitive extension to upper cervical cord (UCC) was confirmed in none of the patients. ISSL was found in two IH and three Non-IH patients all showing only superficial sensory impairments. ILA or hypotonia was observed in 57% of IH and 60% of Non-IH patients. Conclusion: IH in LMI appears to be due mainly to post-decussating pyramidal tract damage at the lower medulla instead of ILA or ISSL participation. © 2016 Elsevier B.V. All rights reserved.
1. Introduction In 1946, Opalski reported two cases of Wallenberg syndrome associating with spastic hemiplegia on the same side as the lesion [1,2]. He assumed that Wallenberg syndrome in the two cases could be explained with ischemic lesions in the upper cervical cord (UCC), which might disrupt various neural fibers descending from the medulla, such as trigeminal nerve spinal cord fibers, and damage ipsilateral postdecussating pyramidal tract fibers. Since his original cases were described, several researchers reported patients with lateral medullary infarction (LMI) extending to UCC which caused ipsilateral hemiparesis (IH) and began to call them Opalski's syndrome [3–6]. Later, many others found the association of IH in LMI patients, whose lesions did not reach UCC on MRI, and called them also Opalski's syndrome [7–14]. The majority of them simply assumed that IH might be caused by damage of the ipsilateral post-decussating pyramidal tract at the lower medulla. Brochier et al. and Kim [15,16] were, however, ⁎ Corresponding author at: Department of Neurology, National Cerebral and Cardiovascular Center, 5-7-1 Fujishiro-dai, Suita, Osaka 565-8565, Japan. E-mail address: [email protected] (K. Miyashita).
http://dx.doi.org/10.1016/j.jns.2016.04.006 0022-510X/© 2016 Elsevier B.V. All rights reserved.
suspicious to such a pyramidal tract interruption theory, because many LMI patients with IH show no pyramidal tract sign on neurological examinations and are associated with ipsilateral deep sensory disturbance. Brochier et al. hypothesized that a loss of ipsilateral deep sensation may lead to the disturbance of motor control resulting in ipsilateral limb weakness [15]. Kim similarly hypothesized that IH in LMI patients may result from proprioceptive disturbance combined with spinocerebellar hypotonia/ataxia [16]. Thus, two possible theories have been proposed about the manifestation of ipsilateral motor weakness in LMI. However, previous LMI studies have not focused this particular point. As Opalski's hypothesis is supported by lower lesion location and Kim's hypothesis by symptoms of ISSL and ILA, we retrospectively examined the prevalence of these phenomena in a group of LMI patients with and without IH to test which hypothesis prevails. 2. Materials and methods We conducted a single-center hospital-based retrospective study. This study was approved by the local ethics committee at our center. During the period between June 1998 and July 2011, 68 LMI patients were admitted to our hospital within a week after ictus. In all these
M. Uemura et al. / Journal of the Neurological Sciences 365 (2016) 40–45
patients, LMI lesions were confirmed by diffusion-weighted magnetic resonance imaging (DW-MRI). On admission, detailed neurological examinations were carried out routinely by two or more neurologists, and the findings were recorded on neurological charts. These neurological charts were carefully reviewed retrospectively by two of the authors (M. Uemura and K. Miyashita) to identify the presence of IH, ipsilateral sensory symptoms of limbs (ISSL), ipsilateral limb hypotonia/ataxia (ILA), and pyramidal signs such as pathological reflexes or hyperreflexia. The DW-MRI lesions were also carefully reviewed by three authors (M. Uemura, H. Uno, and K. Miyashita). We excluded patients with the involvement of other lesions which could affect the status of limb weakness such as medial medulla oblongata or cerebellum and without detailed clinical information. The remaining 32 patients were subjected to the study. The 32 patients were divided to two groups, such as one with IH (IH Group, n = 7) and the other without IH (Non-IH Group, n = 25). In the IH Group, the severity of motor weakness for upper and lower limbs was classified into the following three grades according to manual muscle testing scores: 1–2 (severe), 3 (moderate), and 4 (mild). Moreover, we added another grade — very mild weakness (trivial paresis) manifesting only pronation of hand — so-called Barre's sign. Baseline data, including age, gender, and comorbidities (hypertension, diabetes, hyperlipidemia, and atrial fibrillation), were collected for all patients. The diagnosis of stroke subtype was based on the criteria of the trial of Org 10172 in Acute Stroke Treatment (TOAST) [17]. The vertebral arteries (VAs) were evaluated by Doppler ultrasonography and MRA in all patients. Conventional angiography was additionally done in 26 patients. VA dissection was diagnosed on the basis of the following: (1) double-lumen sign or intimal flap in MRA or cerebral angiography, (2) characteristic chronological changes in angiography, or (3) intramural hematoma on T1-weighted MRI, as described in previous reports [18,19]. Diffusion-weighted imaging (DWI), fluid-attenuated inversion recovery (FLAIR) imaging, and time-of-flight magnetic resonance angiography (MRA) were routinely performed at 1.5 T (Magnetom Sonata or Magnetom Vision, Siemens Medical Solutions, Erlangen, Germany). DWI images were obtained using the following parameters: repetition time/echo time, 4000/100 ms; matrix, 128 × 128; field of view, 23 cm; section thickness, 4 mm; intersection gap, 2 mm; and b values, 0 and 1000 s/mm2. 3. Theory and calculation Lesion distribution on MRI, including DWI, was evaluated in coronal and axial directions. In the vertical evaluation, medullary regions were divided into upper, middle, lower areas and cervico-medullary junction (CMJ), according to the classification of Bassetti et al. [20]. The extension of LMI lesion to UCC was also carefully evaluated. Lesions in the upper, middle, lower medulla and CMJ were drawn schematically as shaded zones on stereotyped figures, for each patient, to assess regions potentially responsible for IH manifestation. Statistical analyses were performed using the Student's t-test, Fisher exact test or Pearson's chisquare test in JMP®9.0.0. P-value b 0.05 was considered to be significant. 4. Results Clinical profiles of two groups including age, gender, comorbidities, association of ILA or ISSL, and levels of involved medullary lesions are shown in Table 1. On DWI, the lower medulla was involved in all IH patients (100%) but only in 12 of 25 Non-IH patients (48%). The involvement of the lower medulla was significantly more common in the IH Group than in the Non-IH Group (P = 0.025). The lower medullary lesions reached CMJ in four of the seven IH patients (57%) and only in one of the 12 Non-IH patients (8%). The incidence of CMJ involvement was significantly higher in the IH Group compared with the Non-IH Group (P = 0.004). In none of 32 patients, definitive extension of LMI
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Table 1 Basic characteristics of LMI patients with IH and without IH.
Age Sex (male) Etiology DA LAA CES SVD Und Risk factors HT DM DL AF Smoking Level of involved lesions Upper medulla Middle medulla Lower medulla CMJ Neurological findings in ipsilateral to the lesion ISSL ILA
LMI with IH
LMI without IH
n=7
n = 25
p
58.6 ± 15.5 4 (57.1)
56.9 ± 13.4 21 (84.0)
0.78 0.16
4 (57.1) 3 (42.9) 0 0 0
11 (44.0) 9 (36.0) 0 1 (4.0) 4 (16.0)
0.64
5 (71.4) 4 (57.1) 1 (14.3) 0 4 (57.1)
17 (68.0) 2 (8.0) 10 (40.0) 1 (4.0) 13 (52.0)
1.0 *0.01 0.37 1.0 1.0
0 3 (42.9) 7 (100) 4 (57.1)
7 (28.0) 19 (76.0) 12 (48.0) 1 (4.0)
0.30 0.17 *0.025 *0.004
2 (28.6) 4 (57.1)
3 (12.0) 15 (60.0)
0.30 1.0
DA = dissecting artery, LAA = large artery atherosclerosis, CES = cardiogenic or aortogenic embolism, SVD = small vessel disease, Und = undetermined, HT = hypertension, DM = diabetes mellitus, DL = dyslipidemia, AF = atrial fibrillation, CMJ = cervicomedullary junction, ISSL = ipsilateral sensory symptoms in limb/body, ILA = ipsilateral limb ataxia/ hypotonia. Asterisks indicate statistical significance.
lesions to UCC was identified. ISSL was observed in two of the seven IH patients (28.6%) and three of the 25 Non-IH patients (12.0%). ILA was found in four of the seven IH patients (57%) and 15 of the 25 Non-IH patients (60%). There was no significant difference in the incidence of ISSL association and ILA association between the two groups. Fig. 1 summarizes neurological findings, such as the severity of motor weakness, the presence or absence of ISSL or ILA and MRI findings in each IH patient. In all the seven IH patients, the severity of motor weakness was mild both for the upper and lower limbs. None of them had pyramidal tract signs such as pathological reflexes or hyperreflexia, although not indicated in Fig. 1. Monoparesis, cruciate hemiparesis, or contralateral hemiparesis was not observed. It should be, however, noted that two patients (Cases 1 and 2) had crural dominant hemiparesis evidenced by trivial weakness in the upper limb and mild weakness in the lower limb. The lower medullary lesions in these two IH patients were somewhat smaller than those in the other five IH patients and reached the most lateral area of CMJ. In the other five IH patients, the severity of weakness was the same in the upper and lower limbs. In two of these five IH patients (Cases 3 and 4) also, the lower medullary lesions reached CMJ. Two IH patients (Cases 4 and 5) had ISSL. In these two IH patients, however, the type of ISSL was numbness and not deep sensory impairment. In Case 4, numbness was detected in the ipsilateral upper and lower limbs. In Case 5, numbness was detected only in the ipsilateral hand, while motor weakness was observed in the ipsilateral upper and lower limbs. ILA was observed in 4 of 7 IH patients (Cases 3, 4, 6 and 7). Fig. 2 displays the presence or absence of ISSL/ILA and MRI findings in each Non-IH patient. LMI lesions involved the lower medulla in 12 patients (Cases 8–19) and reached CMJ in one patient (Case 15). In the three Non-IH patients with ISSL (Cases 14, 15, and 22), the type of ISSL was all numbness without deep sensory impairments. Two of them (Cases 14 and 15) had lower medullary lesions, whereas the remainder (Case 22) had no lesions in the lower medulla. Fifteen of the 25 Non-IH patients had ILA. The incidence of ILA association was the same whether the lesions involved the lower medulla (8/13, 62%) or not involved the lower medulla (7/12, 58%).
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Fig. 1. Neurological findings and schematic view and MRI of LMI with IH.
5. Discussion In this retrospective study, we evaluated 32 LMI patients, seven of whom had IH. ISSL was found in two of seven IH patients, although it
was a superficial sensory disturbance unlikely relating with motor weakness in both patients. None of our LMI patients had ipsilateral deep sensory impairment. ILA was observed rather commonly both in IH and Non-IH patients and was not closely related with IH manifestation.
M. Uemura et al. / Journal of the Neurological Sciences 365 (2016) 40–45
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Fig. 2. Neurological findings and schematic view and MRI of LMI without IH.
There are two different hypotheses concerning the contributory factors for IH manifestation in LMI patients. One is the hypothesis that IH is caused by ipsilateral post-decussating pyramidal tract. Pyramidal tract fibers are generally believed to finish decussating completely at the level of the UCC. Recent studies using diffusion tensor imaging techniques suggest that the pyramidal tract decussates at the level sufficiently higher than CMJ [12,21] and that the post-deccusating pyramidal tract can be interrupted by lesions in the lower lateral medulla. Li and Wang demonstrated pyramidal tract fibers using diffusion tensor tractography in an LMI patient with IH [12]. In this patient, a lower medullary lesion definitively damaged the ipsilateral pyramidal tract below the level of decussation. It is of interest that hyper-reflexia or pathologic reflexes were not observed in the case reported by Li and Wang. In our
seven IH patients also, pathologic reflexes or hyperreflexia were not observed. Yet, the lack of pathologic reflexes or hyperreflexia does not seem to exclude the possibility of pyramidal tract damage. In a study by Isaza et al., pathologic reflexes had low sensitivity in detecting pyramidal tract disturbance in acute phase of stroke [22]. Tsuda et al. [23] and Liu et al. [24] reported cases of ipsilateral crural monoparesis caused by LMI. Pandy et al. reported a LMI case in which ipsilateral weakness was more marked in the lower limb than in the upper limb [13]. In the present study, two of seven IH patients showed crural dominant hemiparesis. In contrast, ipsilateral brachial monoparesis due to LMI was described only by Kim [16]. Ipsilateral brachial dominant hemiparesis due to LMI has never been reported previously. Thus, in LMI patients with IH, the lower limb appears to be
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more extensively impaired as compared with the upper limb, if the upper and lower limb weakness is uneven in manner. Such an uneven weakness of upper and lower limbs is likely to be related with laminar pattern of pyramidal tract fibers running in the medulla. Lower limb pyramidal tract fibers are known to run more lateral to the upper limb pyramidal tract fibers [25]. Therefore, lateral medullary infarction, if it is small in size, may damage only the lower limb fibers definitively and the upper limb fibers scarcely. In our two IH patients showing ipsilateral crural-dominant hemiparesis, LMI lesions in the lower medulla/ CMJ were somewhat smaller than those in the other five IH patients and located in the most lateral areas. The fact strongly suggests that the ipsilateral crural-dominant hemiparesis in these two patients is caused by interruption of ipsilateral post-decussating pyramidal tract fibers in the lower medulla and/or CMJ; the lower limb fibers running in the most lateral areas are more severely impaired than the upper limb fibers running in the more medial areas. Then a question may be raised here as to how the ipsilateral brachial monoparesis is manifested in the LMI patients reported by Kim. Kim described two LMI patients who had sensory impairment only in the ipsilateral hand, and motor weakness also only in the ipsilateral hand [16]. When a laminar manner of upper/lower limb-fiber passage is considered, such a hand monoparesis may be better explained by sensory impairment, as suggested by Kim, than by post-decussating pyramidal tract damage. The other hypothesis was proposed by Brochier et al. [15] in 1991 and later by Kim in 2001 [16]. In 1991, Brochier et al. reported a LMI patient whose lesion extended from the middle medulla to CMJ [15]. This patient had ipsilateral brachiocrural hemiparesis, decreased deep tendon reflexes, flexor plantar responses, and severe profound hypesthesia in the ipsilateral body including the upper and lower limbs. According to their interpretation, the LMI lesion at CMJ is located in the dorsomedial area and does not seem to involve the post-decussating pyramidal tract. Therefore, they considered ipsilateral profound hypesthesia to be the cause of motor control impairment resulting in ipsilateral limb weakness. In 2001, Kim reported 12 LMI patients with ISSL, all of whom had lesions involving the lower medulla [16]. Seven of them had IH. In all these seven IH patients, the degree of weakness was mild, and no pyramidal tract sign, such as hyperreflexia or pathologic reflexes, was identified. Four of seven IH patients had ipsilateral profound hypesthesia including vibration and position sense impairments. On the basis of such findings, Kim proposed a hypothesis that the involvement of lemniscal fibers together with fibers in the cerebellar tract may induce abnormal sensory-motor feedback resulting in mild weakness or loss of movement control. Limb ataxia is usually caused by damage of the inferior cerebellar peduncles, spinocerebellar tract, or the cerebellum itself. In general, muscle tone of affected limbs is decreased in patients with cerebellar ataxia. Limb hypotonia likely masks the presence of hyperreflexia. Therefore, the cerebellar ataxia/hypotonia may be indistinguishable from limb paresis caused by pyramidal tract damage, particularly in patients showing no pyramidal tract signs.
Despite the hypothesis of Brochier and Kim, ipsilateral sensory impairment does not seem to be the major contributive factor of IH manifestation in LMI patients for the following reasons. In the present study, ISSL was found in two of seven IH patients. ISSL was, however, not deep sensory impairment, which might cause motor control disturbance, in both patients. While deep sensory impairment in limbs might be connected with motor control impairment in the same limbs, superficial sensory impairment is unlikely to be related with motor control. The fact that none of our seven IH patients have deep sensory impairment appears to indicate small role of sensory impairment in IH manifestation. In the study of Kim [16], two LMI patients with IH had ISSL only in the ipsilateral upper limb and no sensory impairment in the ipsilateral lower limb. Nevertheless, one of them had motor weakness both in the ipsilateral upper and lower limbs. Such dissociation between sensory and motor symptom distribution also suggests that the sensory impairment may not be the major factor causing IH. Ipsilateral deep sensory impairment is caused by interruption of ipsilateral lemniscal fibers, which can result from medullary damage at any level, such as upper or middle medullary lesions. On the other hand, IH in LMI patients is observed only in patients with LMI lesions in the lower medulla/CMJ. Provided ISSL plays a major role in IH manifestation in LMI patients, IH is likely to be found more commonly in LMI patients whose lesions are restricted to the upper and/or middle medulla. Table 2 summarizes neurological findings in previously published 10 case reports of LMI with IH, lesions of which did not extend to the UCC. Ipsilateral sensory impairment was observed only in four of the ten cases [7,12,13,15]. In addition, it is unclear whether ISSL in these four cases is deep sensory impairment in type and whether its distribution is the same as the paretic distribution. The fact also supports the view that the role of ISSL in IH manifestation may be very small. Our results and previous reports suggest that ISSL may be rather a confounding factor instead of a contributing factor for IH manifestation. The participation of ISSL should be considered, only if deep sensory impairment coexists with mild motor weakness in the upper and/or lower limb and if IH is hardly explained with the damage of ipsilateral post-decussating pyramidal tract. Similarly, limb ataxia and/or hypotonia may not be the major cause of IH manifestation for the following reasons. As shown in Table 2, only four of the 10 patients in the previously published LMI case reports had ILA [11–13,24]. In the present study, four of seven IH patients had ILA. However, ILA was found also in 15 of the 25 Non-IH patients, seven of whom had no lesion in the lower medulla or CMJ. Our results suggest that ILA is not specific to the lower medulla/CMJ region and is unlikely to play a major role in IH manifestation. The present study has several limitations. The study is based on a retrospective analysis of LMI patients admitted during the last 13-year period. The slice conditions in MRI were, therefore, not completely the same in these patients. In addition, the slice condition in our MRI methods, such as section thickness 4 mm and intersection gap 2 mm
Table 2 Ipsilateral motor, sensory, and ataxic symptoms in previously reported LMI cases of IH. Case reports
Liu et al. [24] Tsuda et al. [23] Kimura et al. [8] Igarashi et al. [11] Parathan et al. [14] Pandey et al. [13] Brochier et al. [15] Li et al. [12] Montaner et al. [7] Dhamoon et al. [9]
Limb palsy Upper limb
Lower limb
− − + + + Mild + Mild + +
Mild Mild + + + Severe + Mild + +
Note: Cases associating with upper cervical cord lesions are not included. N.D = not described.
Sensory disturbance
Ataxia/hypotonia
Hyper-reflexia
Pathologic Reflexes
− − − − − + + + + N.D
+ − N.D + − + − + − N.D
N.D − N.D +bilateral N.D + − − N.D −
N.D + N.D − + + − − N.D +bilateral
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for DWI, was not sufficiently sensitive to display the exact point of postdecussating pyramidal tract damage occurring at the narrow space between the pyramidal decussation and CMJ. As a consequence, the lesion location and size in patients with IH were not sufficiently distinguished from those in patients without IH. In Figs. 1 and 2, lower medullary lesions in some IH patients are very similar to those in several Non-IH patients. This strange similarity is attributable to such a resolution problem of our MRI methods. Furthermore, in spite of our careful attention using coronal MRI, the possibility of LMI lesions extending to the cervical cord in some patients may not be completely excluded. Thus, the present study is not considered excellent with regards to the anatomical accuracy of the LMI lesion. More detailed prospective study using 3.0 Tesla MRI or diffusion tensor imaging is needed to confirm the location of post-decussating pyramidal tract pathway in the lower brainstem. 6. Conclusion IH in LMI is mainly due to post-decussating pyramidal tract damage at the lower medulla instead of ILA or ISSL participation. Conflict of Interest There are no conflicts of interest to declare. Acknowledgment None. References [1] A. Opalski, Un nouveau syndrome sousbulbaire: syndrome partiel de l'artère vertébro-spinale postérieur, Paris Med. 1 (1946) 214–220. [2] H.S. Schutta, The trouble with eponyms, Arch. Neurol. 62 (2005) 1784–1785 (author reply 5). [3] H.Y. Kim, S.H. Koh, K.Y. Lee, Y.J. Lee, S.H. Kim, J. Kim, et al., Opalski's syndrome with cerebellar infarction, J. Clin. Neurol. 2 (2006) 276–278. [4] J. Garcia-Garcia, O. Ayo-Martin, T. Segura, Lateral medullary syndrome and ipsilateral hemiplegia (Opalski syndrome) due to left vertebral artery dissection, Arch. Neurol. 66 (2009) 1574–1575. [5] C. Gil Polo, A. Castrillo Sanz, R. Gutierrez Rios, A. Mendoza Rodriguez, Opalski syndrome: a variant of lateral-medullary syndrome, Neurologia 28 (2013) 382–384.
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[6] D.M. Hermann, H.H. Jung, C.L. Bassetti, Lateral medullary infarct with alternating and dissociated sensorimotor deficits: Opalski's syndrome revisited, Eur. J. Neurol. 16 (2009) e72–e74. [7] J. Montaner, J. Alvarez-Sabin, Opalski's syndrome, J. Neurol. Neurosurg. Psychiatry 67 (1999) 688–689. [8] Y. Kimura, H. Hashimoto, M. Tagaya, Y. Abe, H. Etani, Ipsilateral hemiplegia in a lateral medullary infarct–Opalski's syndrome, J. Neuroimaging 13 (2003) 83–84. [9] S.K. Dhamoon, J. Iqbal, G.H. Collins, Ipsilateral hemiplegia and the Wallenberg syndrome, Arch. Neurol. 41 (1984) 179–180. [10] L. Milandre, P. Lucchini, R. Khalil, Lateral bulbar infarctions. Distribution, etiology and prognosis in 40 cases diagnosed by MRI, Rev. Neurol. (Paris) 151 (1995) 714–721. [11] O. Igarashi, N. Ogura, T. Kiyozuka, K. Kawabe, H. Iguchi, M. Maruyama, et al., Lateral lower medullary infarction, Arch. Neurol. 61 (2004) 1609. [12] X. Li, Y. Wang, Lateral medullary infarction with ipsilateral hemiparesis, lemniscal sensation loss and hypoglossal nerve palsy, Neurol. Sci. 35 (2014) 633–634. [13] S. Pandey, A. Batla, Opalski's syndrome: a rare variant of lateral medullary syndrome, J. Neurosci. Rural Pract. 4 (2013) 102–104. [14] K. Parathan, R. Kannan, P. Chitrambalam, S.K. Aiyappan, N. Deepthi, A rare variant of Wallenberg's syndrome: Opalski syndrome, J. Clin. Diagn. Res. 8 (2014) MD05–MD06. [15] T. Brochier, M. Ceccaldi, L. Milandre, M. Brouchon, Dorsolateral infarction of the lower medulla: Clinical-MRI study, Neurology 52 (1999) 190–193. [16] J.S. Kim, Sensory symptoms in ipsilateral limbs/body due to lateral medullary infarction, Neurology 57 (2001) 1230–1234. [17] H.P. Adams Jr., B.H. Bendixen, L.J. Kappelle, J. Biller, B.B. Love, D.L. Gordon, et al., Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in acute stroke treatment, Stroke 24 (1993) 35–41. [18] H. Ohkuma, S. Suzuki, T. Kikkawa, N. Shimamura, Neuroradiologic and clinical features of arterial dissection of the anterior cerebral artery, AJNR Am. J. Neuroradiol. 24 (2003) 691–699. [19] T. Hosoya, M. Adachi, K. Yamaguchi, T. Haku, T. Kayama, T. Kato, Clinical and neuroradiological features of intracranial vertebrobasilar artery dissection, Stroke 30 (1999) 1083–1090. [20] C. Bassetti, J. Bogousslavsky, H. Mattle, A. Bernasconi, Medial medullary stroke: report of seven patients and review of the literature, Neurology 48 (1997) 882–890. [21] S. Nakamura, M. Kitami, Y. Furukawa, Opalski syndrome: ipsilateral hemiplegia due to a lateral-medullary infarction, Neurology 75 (2010) 1658. [22] S.P. Isaza Jaramillo, C.S. Uribe Uribe, F.A. Garcia Jimenez, W. Cornejo-Ochoa, J.F. Alvarez Restrepo, G.C. Roman, Accuracy of the Babinski sign in the identification of pyramidal tract dysfunction, J. Neurol. Sci. 343 (2014) 66–68. [23] H. Tsuda, K. Tanaka, S. Kishida, Pure motor monoparesis in the leg due to a lateral medullary infarction, Case Rep. Med. 2012 (2012) 1–3. [24] C.Y. Liu, F.C. Chang, H.H. Hu, L.C. Hsu, Ipsilateral crural monoparesis in lateral medullary infarction due to vertebral artery dissection, Eur. J. Neurol. 13 (2006) e8–e9. [25] S. Vulliemoz, O. Raineteau, D. Jabaudon, Reaching beyond the midline: why are human brains cross wired? Lancet Neurol. 4 (2005) 87–99.
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Ipsilateral hemiparesis in lateral medullary infarction: Clinical investigation of the lesion location on magnetic resonance imaging Masahiro Uemura a, Hiroaki Naritomi a, Hisakazu Uno a, Arisa Umesaki a, Kotaro Miyashita a,⁎, Kazunori Toyoda b, Kazuo Minematsu b, Kazuyuki Nagatsuka a a b
Department of Neurology, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan Department of Cerebrovascular Medicine, National Cerebral and Cardiovascular Center, Suita, Osaka, Japan
a r t i c l e
i n f o
Article history: Received 27 May 2015 Received in revised form 29 March 2016 Accepted 5 April 2016 Available online 10 April 2016 Keywords: Cerebral infarction Lateral medullary infarction Magnetic resonance imaging Opalski's syndrome Ipsilateral hemiparesis Pyramidal tract
a b s t r a c t Background: In 1946, Opalski reported two cases of Wallenberg syndrome with ipsilateral hemiparesis (IH). His hypothesis seems to be based on the view that IH is caused by post-decussating pyramidal tract damage. Afterwards, other researchers proposed a different hypothesis that ipsilateral sensory symptoms of limbs (ISSL) or ipsilateral limb ataxia (ILA) caused by lateral medullary infarction (LMI) might lead to ipsilateral motor weakness. The present study is aimed to clarify whether IH in LMI patients is attributable mainly to ISSL/ILA or disruption of ipsilateral post-decussating pyramidal tract. Methods: Thirty-two patients with acute LMI admitted during the last 13 years were divided to IH Group (n = 7) and Non-IH Group (n = 25). Lesion location/distribution on MRI and neurological findings were compared between the two groups. Results: LMI involved the lower medulla in all seven IH patients and 12 of 25 Non-IH patients. The lower medullary lesion extended to the cervico-medullary junction (CMJ) in four of seven IH patients and one of 12 Non-IH patients. Definitive extension to upper cervical cord (UCC) was confirmed in none of the patients. ISSL was found in two IH and three Non-IH patients all showing only superficial sensory impairments. ILA or hypotonia was observed in 57% of IH and 60% of Non-IH patients. Conclusion: IH in LMI appears to be due mainly to post-decussating pyramidal tract damage at the lower medulla instead of ILA or ISSL participation. © 2016 Elsevier B.V. All rights reserved.
1. Introduction In 1946, Opalski reported two cases of Wallenberg syndrome associating with spastic hemiplegia on the same side as the lesion [1,2]. He assumed that Wallenberg syndrome in the two cases could be explained with ischemic lesions in the upper cervical cord (UCC), which might disrupt various neural fibers descending from the medulla, such as trigeminal nerve spinal cord fibers, and damage ipsilateral postdecussating pyramidal tract fibers. Since his original cases were described, several researchers reported patients with lateral medullary infarction (LMI) extending to UCC which caused ipsilateral hemiparesis (IH) and began to call them Opalski's syndrome [3–6]. Later, many others found the association of IH in LMI patients, whose lesions did not reach UCC on MRI, and called them also Opalski's syndrome [7–14]. The majority of them simply assumed that IH might be caused by damage of the ipsilateral post-decussating pyramidal tract at the lower medulla. Brochier et al. and Kim [15,16] were, however, ⁎ Corresponding author at: Department of Neurology, National Cerebral and Cardiovascular Center, 5-7-1 Fujishiro-dai, Suita, Osaka 565-8565, Japan. E-mail address: [email protected] (K. Miyashita).
http://dx.doi.org/10.1016/j.jns.2016.04.006 0022-510X/© 2016 Elsevier B.V. All rights reserved.
suspicious to such a pyramidal tract interruption theory, because many LMI patients with IH show no pyramidal tract sign on neurological examinations and are associated with ipsilateral deep sensory disturbance. Brochier et al. hypothesized that a loss of ipsilateral deep sensation may lead to the disturbance of motor control resulting in ipsilateral limb weakness [15]. Kim similarly hypothesized that IH in LMI patients may result from proprioceptive disturbance combined with spinocerebellar hypotonia/ataxia [16]. Thus, two possible theories have been proposed about the manifestation of ipsilateral motor weakness in LMI. However, previous LMI studies have not focused this particular point. As Opalski's hypothesis is supported by lower lesion location and Kim's hypothesis by symptoms of ISSL and ILA, we retrospectively examined the prevalence of these phenomena in a group of LMI patients with and without IH to test which hypothesis prevails. 2. Materials and methods We conducted a single-center hospital-based retrospective study. This study was approved by the local ethics committee at our center. During the period between June 1998 and July 2011, 68 LMI patients were admitted to our hospital within a week after ictus. In all these
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patients, LMI lesions were confirmed by diffusion-weighted magnetic resonance imaging (DW-MRI). On admission, detailed neurological examinations were carried out routinely by two or more neurologists, and the findings were recorded on neurological charts. These neurological charts were carefully reviewed retrospectively by two of the authors (M. Uemura and K. Miyashita) to identify the presence of IH, ipsilateral sensory symptoms of limbs (ISSL), ipsilateral limb hypotonia/ataxia (ILA), and pyramidal signs such as pathological reflexes or hyperreflexia. The DW-MRI lesions were also carefully reviewed by three authors (M. Uemura, H. Uno, and K. Miyashita). We excluded patients with the involvement of other lesions which could affect the status of limb weakness such as medial medulla oblongata or cerebellum and without detailed clinical information. The remaining 32 patients were subjected to the study. The 32 patients were divided to two groups, such as one with IH (IH Group, n = 7) and the other without IH (Non-IH Group, n = 25). In the IH Group, the severity of motor weakness for upper and lower limbs was classified into the following three grades according to manual muscle testing scores: 1–2 (severe), 3 (moderate), and 4 (mild). Moreover, we added another grade — very mild weakness (trivial paresis) manifesting only pronation of hand — so-called Barre's sign. Baseline data, including age, gender, and comorbidities (hypertension, diabetes, hyperlipidemia, and atrial fibrillation), were collected for all patients. The diagnosis of stroke subtype was based on the criteria of the trial of Org 10172 in Acute Stroke Treatment (TOAST) [17]. The vertebral arteries (VAs) were evaluated by Doppler ultrasonography and MRA in all patients. Conventional angiography was additionally done in 26 patients. VA dissection was diagnosed on the basis of the following: (1) double-lumen sign or intimal flap in MRA or cerebral angiography, (2) characteristic chronological changes in angiography, or (3) intramural hematoma on T1-weighted MRI, as described in previous reports [18,19]. Diffusion-weighted imaging (DWI), fluid-attenuated inversion recovery (FLAIR) imaging, and time-of-flight magnetic resonance angiography (MRA) were routinely performed at 1.5 T (Magnetom Sonata or Magnetom Vision, Siemens Medical Solutions, Erlangen, Germany). DWI images were obtained using the following parameters: repetition time/echo time, 4000/100 ms; matrix, 128 × 128; field of view, 23 cm; section thickness, 4 mm; intersection gap, 2 mm; and b values, 0 and 1000 s/mm2. 3. Theory and calculation Lesion distribution on MRI, including DWI, was evaluated in coronal and axial directions. In the vertical evaluation, medullary regions were divided into upper, middle, lower areas and cervico-medullary junction (CMJ), according to the classification of Bassetti et al. [20]. The extension of LMI lesion to UCC was also carefully evaluated. Lesions in the upper, middle, lower medulla and CMJ were drawn schematically as shaded zones on stereotyped figures, for each patient, to assess regions potentially responsible for IH manifestation. Statistical analyses were performed using the Student's t-test, Fisher exact test or Pearson's chisquare test in JMP®9.0.0. P-value b 0.05 was considered to be significant. 4. Results Clinical profiles of two groups including age, gender, comorbidities, association of ILA or ISSL, and levels of involved medullary lesions are shown in Table 1. On DWI, the lower medulla was involved in all IH patients (100%) but only in 12 of 25 Non-IH patients (48%). The involvement of the lower medulla was significantly more common in the IH Group than in the Non-IH Group (P = 0.025). The lower medullary lesions reached CMJ in four of the seven IH patients (57%) and only in one of the 12 Non-IH patients (8%). The incidence of CMJ involvement was significantly higher in the IH Group compared with the Non-IH Group (P = 0.004). In none of 32 patients, definitive extension of LMI
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Table 1 Basic characteristics of LMI patients with IH and without IH.
Age Sex (male) Etiology DA LAA CES SVD Und Risk factors HT DM DL AF Smoking Level of involved lesions Upper medulla Middle medulla Lower medulla CMJ Neurological findings in ipsilateral to the lesion ISSL ILA
LMI with IH
LMI without IH
n=7
n = 25
p
58.6 ± 15.5 4 (57.1)
56.9 ± 13.4 21 (84.0)
0.78 0.16
4 (57.1) 3 (42.9) 0 0 0
11 (44.0) 9 (36.0) 0 1 (4.0) 4 (16.0)
0.64
5 (71.4) 4 (57.1) 1 (14.3) 0 4 (57.1)
17 (68.0) 2 (8.0) 10 (40.0) 1 (4.0) 13 (52.0)
1.0 *0.01 0.37 1.0 1.0
0 3 (42.9) 7 (100) 4 (57.1)
7 (28.0) 19 (76.0) 12 (48.0) 1 (4.0)
0.30 0.17 *0.025 *0.004
2 (28.6) 4 (57.1)
3 (12.0) 15 (60.0)
0.30 1.0
DA = dissecting artery, LAA = large artery atherosclerosis, CES = cardiogenic or aortogenic embolism, SVD = small vessel disease, Und = undetermined, HT = hypertension, DM = diabetes mellitus, DL = dyslipidemia, AF = atrial fibrillation, CMJ = cervicomedullary junction, ISSL = ipsilateral sensory symptoms in limb/body, ILA = ipsilateral limb ataxia/ hypotonia. Asterisks indicate statistical significance.
lesions to UCC was identified. ISSL was observed in two of the seven IH patients (28.6%) and three of the 25 Non-IH patients (12.0%). ILA was found in four of the seven IH patients (57%) and 15 of the 25 Non-IH patients (60%). There was no significant difference in the incidence of ISSL association and ILA association between the two groups. Fig. 1 summarizes neurological findings, such as the severity of motor weakness, the presence or absence of ISSL or ILA and MRI findings in each IH patient. In all the seven IH patients, the severity of motor weakness was mild both for the upper and lower limbs. None of them had pyramidal tract signs such as pathological reflexes or hyperreflexia, although not indicated in Fig. 1. Monoparesis, cruciate hemiparesis, or contralateral hemiparesis was not observed. It should be, however, noted that two patients (Cases 1 and 2) had crural dominant hemiparesis evidenced by trivial weakness in the upper limb and mild weakness in the lower limb. The lower medullary lesions in these two IH patients were somewhat smaller than those in the other five IH patients and reached the most lateral area of CMJ. In the other five IH patients, the severity of weakness was the same in the upper and lower limbs. In two of these five IH patients (Cases 3 and 4) also, the lower medullary lesions reached CMJ. Two IH patients (Cases 4 and 5) had ISSL. In these two IH patients, however, the type of ISSL was numbness and not deep sensory impairment. In Case 4, numbness was detected in the ipsilateral upper and lower limbs. In Case 5, numbness was detected only in the ipsilateral hand, while motor weakness was observed in the ipsilateral upper and lower limbs. ILA was observed in 4 of 7 IH patients (Cases 3, 4, 6 and 7). Fig. 2 displays the presence or absence of ISSL/ILA and MRI findings in each Non-IH patient. LMI lesions involved the lower medulla in 12 patients (Cases 8–19) and reached CMJ in one patient (Case 15). In the three Non-IH patients with ISSL (Cases 14, 15, and 22), the type of ISSL was all numbness without deep sensory impairments. Two of them (Cases 14 and 15) had lower medullary lesions, whereas the remainder (Case 22) had no lesions in the lower medulla. Fifteen of the 25 Non-IH patients had ILA. The incidence of ILA association was the same whether the lesions involved the lower medulla (8/13, 62%) or not involved the lower medulla (7/12, 58%).
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Fig. 1. Neurological findings and schematic view and MRI of LMI with IH.
5. Discussion In this retrospective study, we evaluated 32 LMI patients, seven of whom had IH. ISSL was found in two of seven IH patients, although it
was a superficial sensory disturbance unlikely relating with motor weakness in both patients. None of our LMI patients had ipsilateral deep sensory impairment. ILA was observed rather commonly both in IH and Non-IH patients and was not closely related with IH manifestation.
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Fig. 2. Neurological findings and schematic view and MRI of LMI without IH.
There are two different hypotheses concerning the contributory factors for IH manifestation in LMI patients. One is the hypothesis that IH is caused by ipsilateral post-decussating pyramidal tract. Pyramidal tract fibers are generally believed to finish decussating completely at the level of the UCC. Recent studies using diffusion tensor imaging techniques suggest that the pyramidal tract decussates at the level sufficiently higher than CMJ [12,21] and that the post-deccusating pyramidal tract can be interrupted by lesions in the lower lateral medulla. Li and Wang demonstrated pyramidal tract fibers using diffusion tensor tractography in an LMI patient with IH [12]. In this patient, a lower medullary lesion definitively damaged the ipsilateral pyramidal tract below the level of decussation. It is of interest that hyper-reflexia or pathologic reflexes were not observed in the case reported by Li and Wang. In our
seven IH patients also, pathologic reflexes or hyperreflexia were not observed. Yet, the lack of pathologic reflexes or hyperreflexia does not seem to exclude the possibility of pyramidal tract damage. In a study by Isaza et al., pathologic reflexes had low sensitivity in detecting pyramidal tract disturbance in acute phase of stroke [22]. Tsuda et al. [23] and Liu et al. [24] reported cases of ipsilateral crural monoparesis caused by LMI. Pandy et al. reported a LMI case in which ipsilateral weakness was more marked in the lower limb than in the upper limb [13]. In the present study, two of seven IH patients showed crural dominant hemiparesis. In contrast, ipsilateral brachial monoparesis due to LMI was described only by Kim [16]. Ipsilateral brachial dominant hemiparesis due to LMI has never been reported previously. Thus, in LMI patients with IH, the lower limb appears to be
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more extensively impaired as compared with the upper limb, if the upper and lower limb weakness is uneven in manner. Such an uneven weakness of upper and lower limbs is likely to be related with laminar pattern of pyramidal tract fibers running in the medulla. Lower limb pyramidal tract fibers are known to run more lateral to the upper limb pyramidal tract fibers [25]. Therefore, lateral medullary infarction, if it is small in size, may damage only the lower limb fibers definitively and the upper limb fibers scarcely. In our two IH patients showing ipsilateral crural-dominant hemiparesis, LMI lesions in the lower medulla/ CMJ were somewhat smaller than those in the other five IH patients and located in the most lateral areas. The fact strongly suggests that the ipsilateral crural-dominant hemiparesis in these two patients is caused by interruption of ipsilateral post-decussating pyramidal tract fibers in the lower medulla and/or CMJ; the lower limb fibers running in the most lateral areas are more severely impaired than the upper limb fibers running in the more medial areas. Then a question may be raised here as to how the ipsilateral brachial monoparesis is manifested in the LMI patients reported by Kim. Kim described two LMI patients who had sensory impairment only in the ipsilateral hand, and motor weakness also only in the ipsilateral hand [16]. When a laminar manner of upper/lower limb-fiber passage is considered, such a hand monoparesis may be better explained by sensory impairment, as suggested by Kim, than by post-decussating pyramidal tract damage. The other hypothesis was proposed by Brochier et al. [15] in 1991 and later by Kim in 2001 [16]. In 1991, Brochier et al. reported a LMI patient whose lesion extended from the middle medulla to CMJ [15]. This patient had ipsilateral brachiocrural hemiparesis, decreased deep tendon reflexes, flexor plantar responses, and severe profound hypesthesia in the ipsilateral body including the upper and lower limbs. According to their interpretation, the LMI lesion at CMJ is located in the dorsomedial area and does not seem to involve the post-decussating pyramidal tract. Therefore, they considered ipsilateral profound hypesthesia to be the cause of motor control impairment resulting in ipsilateral limb weakness. In 2001, Kim reported 12 LMI patients with ISSL, all of whom had lesions involving the lower medulla [16]. Seven of them had IH. In all these seven IH patients, the degree of weakness was mild, and no pyramidal tract sign, such as hyperreflexia or pathologic reflexes, was identified. Four of seven IH patients had ipsilateral profound hypesthesia including vibration and position sense impairments. On the basis of such findings, Kim proposed a hypothesis that the involvement of lemniscal fibers together with fibers in the cerebellar tract may induce abnormal sensory-motor feedback resulting in mild weakness or loss of movement control. Limb ataxia is usually caused by damage of the inferior cerebellar peduncles, spinocerebellar tract, or the cerebellum itself. In general, muscle tone of affected limbs is decreased in patients with cerebellar ataxia. Limb hypotonia likely masks the presence of hyperreflexia. Therefore, the cerebellar ataxia/hypotonia may be indistinguishable from limb paresis caused by pyramidal tract damage, particularly in patients showing no pyramidal tract signs.
Despite the hypothesis of Brochier and Kim, ipsilateral sensory impairment does not seem to be the major contributive factor of IH manifestation in LMI patients for the following reasons. In the present study, ISSL was found in two of seven IH patients. ISSL was, however, not deep sensory impairment, which might cause motor control disturbance, in both patients. While deep sensory impairment in limbs might be connected with motor control impairment in the same limbs, superficial sensory impairment is unlikely to be related with motor control. The fact that none of our seven IH patients have deep sensory impairment appears to indicate small role of sensory impairment in IH manifestation. In the study of Kim [16], two LMI patients with IH had ISSL only in the ipsilateral upper limb and no sensory impairment in the ipsilateral lower limb. Nevertheless, one of them had motor weakness both in the ipsilateral upper and lower limbs. Such dissociation between sensory and motor symptom distribution also suggests that the sensory impairment may not be the major factor causing IH. Ipsilateral deep sensory impairment is caused by interruption of ipsilateral lemniscal fibers, which can result from medullary damage at any level, such as upper or middle medullary lesions. On the other hand, IH in LMI patients is observed only in patients with LMI lesions in the lower medulla/CMJ. Provided ISSL plays a major role in IH manifestation in LMI patients, IH is likely to be found more commonly in LMI patients whose lesions are restricted to the upper and/or middle medulla. Table 2 summarizes neurological findings in previously published 10 case reports of LMI with IH, lesions of which did not extend to the UCC. Ipsilateral sensory impairment was observed only in four of the ten cases [7,12,13,15]. In addition, it is unclear whether ISSL in these four cases is deep sensory impairment in type and whether its distribution is the same as the paretic distribution. The fact also supports the view that the role of ISSL in IH manifestation may be very small. Our results and previous reports suggest that ISSL may be rather a confounding factor instead of a contributing factor for IH manifestation. The participation of ISSL should be considered, only if deep sensory impairment coexists with mild motor weakness in the upper and/or lower limb and if IH is hardly explained with the damage of ipsilateral post-decussating pyramidal tract. Similarly, limb ataxia and/or hypotonia may not be the major cause of IH manifestation for the following reasons. As shown in Table 2, only four of the 10 patients in the previously published LMI case reports had ILA [11–13,24]. In the present study, four of seven IH patients had ILA. However, ILA was found also in 15 of the 25 Non-IH patients, seven of whom had no lesion in the lower medulla or CMJ. Our results suggest that ILA is not specific to the lower medulla/CMJ region and is unlikely to play a major role in IH manifestation. The present study has several limitations. The study is based on a retrospective analysis of LMI patients admitted during the last 13-year period. The slice conditions in MRI were, therefore, not completely the same in these patients. In addition, the slice condition in our MRI methods, such as section thickness 4 mm and intersection gap 2 mm
Table 2 Ipsilateral motor, sensory, and ataxic symptoms in previously reported LMI cases of IH. Case reports
Liu et al. [24] Tsuda et al. [23] Kimura et al. [8] Igarashi et al. [11] Parathan et al. [14] Pandey et al. [13] Brochier et al. [15] Li et al. [12] Montaner et al. [7] Dhamoon et al. [9]
Limb palsy Upper limb
Lower limb
− − + + + Mild + Mild + +
Mild Mild + + + Severe + Mild + +
Note: Cases associating with upper cervical cord lesions are not included. N.D = not described.
Sensory disturbance
Ataxia/hypotonia
Hyper-reflexia
Pathologic Reflexes
− − − − − + + + + N.D
+ − N.D + − + − + − N.D
N.D − N.D +bilateral N.D + − − N.D −
N.D + N.D − + + − − N.D +bilateral
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for DWI, was not sufficiently sensitive to display the exact point of postdecussating pyramidal tract damage occurring at the narrow space between the pyramidal decussation and CMJ. As a consequence, the lesion location and size in patients with IH were not sufficiently distinguished from those in patients without IH. In Figs. 1 and 2, lower medullary lesions in some IH patients are very similar to those in several Non-IH patients. This strange similarity is attributable to such a resolution problem of our MRI methods. Furthermore, in spite of our careful attention using coronal MRI, the possibility of LMI lesions extending to the cervical cord in some patients may not be completely excluded. Thus, the present study is not considered excellent with regards to the anatomical accuracy of the LMI lesion. More detailed prospective study using 3.0 Tesla MRI or diffusion tensor imaging is needed to confirm the location of post-decussating pyramidal tract pathway in the lower brainstem. 6. Conclusion IH in LMI is mainly due to post-decussating pyramidal tract damage at the lower medulla instead of ILA or ISSL participation. Conflict of Interest There are no conflicts of interest to declare. Acknowledgment None. References [1] A. Opalski, Un nouveau syndrome sousbulbaire: syndrome partiel de l'artère vertébro-spinale postérieur, Paris Med. 1 (1946) 214–220. [2] H.S. Schutta, The trouble with eponyms, Arch. Neurol. 62 (2005) 1784–1785 (author reply 5). [3] H.Y. Kim, S.H. Koh, K.Y. Lee, Y.J. Lee, S.H. Kim, J. Kim, et al., Opalski's syndrome with cerebellar infarction, J. Clin. Neurol. 2 (2006) 276–278. [4] J. Garcia-Garcia, O. Ayo-Martin, T. Segura, Lateral medullary syndrome and ipsilateral hemiplegia (Opalski syndrome) due to left vertebral artery dissection, Arch. Neurol. 66 (2009) 1574–1575. [5] C. Gil Polo, A. Castrillo Sanz, R. Gutierrez Rios, A. Mendoza Rodriguez, Opalski syndrome: a variant of lateral-medullary syndrome, Neurologia 28 (2013) 382–384.
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