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Clinical Study of 46 Patients with Lateral Medullary Infarction
Clinical Study of 46 Patients with Lateral Medullary Infarction Katsuhiko Ogawa, MD, Yutaka Suzuki, MD, Minoru Oishi, MD, and Satoshi Kamei, MD
Background: Lateral medullary infarction (LMI) exhibits a variety of clinical features. Various bulbar symptoms can occur in LMI. Methods: Neuroradiologic findings of 46 LMI patients were examined. Their infarcts were categorized into the rostral, middle, and caudal groups and were further subdivided into the anteromedial, anterolateral, lateral (L), and posterior regions. Results: The middle medulla was the most common site (27 patients). Most lesions affected the L region alone (25 patients). Dysarthria and facial palsy occurred significantly more frequently in the rostral group than those in the caudal group. Severe truncal ataxia was significantly more common in the caudal group than that in the rostral group. Twenty-five of the 28 patients with severe truncal ataxia displayed vestibular symptoms; otherwise, the other 3 patients showed absence of vestibular symptoms. Soft palate paralysis occurred at a significantly high frequency in the patients with dysphagia and hoarseness compared with the patients without these 2 symptoms. Segmental sensory disturbance occurred in 5 patients, 4 of whom exhibited atypical patterns. Conclusions: The results of our comparisons between the rostral and caudal groups were consistent with those of previous studies. The presence of severe truncal ataxia without vestibular symptoms in LMI was atypical. An analysis of the bulbar symptoms indicated that the extent to which soft palate paralysis contributed to dysphagia was associated with the severity of ischemia in the nucleus ambiguus. The present study showed variability in clinical features of LMI, which was related to differences in the severity and the extent of ischemia in the lateral medulla. Key Words: Lateral medullary infarction—severe truncal ataxia— sensory disturbance—dysphagia—soft palate paralysis. Ó 2015 Published by Elsevier Inc. on behalf of National Stroke Association
Lateral medullary infarction (LMI) is caused by ischemia in the lateral region of the medulla.1,2 In typical patients of LMI, vertigo, the disturbance of superficial sensation on the ipsilateral side of the face and the contralateral limbs and trunk; Horner sign; truncal ataxia; ipsilateral incoordination of the extremities; and ipsilateral paralysis of the soft palate, larynx, and From the Division of Neurology, Department of Medicine, Nihon University School of Medicine, Tokyo, Japan. Received November 5, 2014; revision received December 16, 2014; accepted January 2, 2015. Address correspondence to Katsuhiko Ogawa, MD, Division of Neurology, Department of Medicine, Nihon University School of Medicine, 30-1 Oyaguchi-kamimachi, Itabashi-ku, Tokyo 173-8610, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 Published by Elsevier Inc. on behalf of National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.01.006
pharynx are observed.1,3,4 However, the clinical features of LMI can vary markedly.5,6 Various types of sensory disturbances are seen in LMI.7 Truncal ataxia in LMI is usually accompanied by vestibular symptoms (vertigo and horizontal or horizontal/torsional unidirectional nystagmus).8–10 Recently, atypical patients of LMI involving isolated lateropulsion8-11 or vestibular symptoms alone12 have been reported. We studied the neurologic characteristics of LMI based on an investigation of the neuroradiologic findings of 46 patients who had experienced LMI.
Patients and Methods Characteristics of the Enrolled Patients and Study Design Forty-six patients who had experienced LMI were enrolled. The patients were diagnosed as having LMI,
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based on their magnetic resonance imaging findings, and all their infarcts were limited to the medulla. Patients whose lesions had spread to parts of the brainstem other than the medulla or the cerebellum were excluded. We reviewed the medical charts of each patient and identified their neurologic findings. Nystagmus was evaluated by the confrontation test. Sensory disturbance was grouped into 4 types: type a: ipsilateral side of the face— contralateral limbs/trunk, type b: contralateral side of the face—limbs/trunk, type c: contralateral limbs/trunk, and type d: ipsilateral side of the face. We divided the infarct locations into the rostral, middle, and caudal groups (Fig 1), and then, subdivided them into the anteromedial, anterolateral (AL), lateral (L), and posterior (P) regions, based on the distribution of each penetrating artery (Figs 1, 2).13,14
Statistical Analysis We compared the frequencies of each neurologic finding between the rostral and caudal groups, using the Fisher exact test. The associations between the presence/the absence of dysphagia and hoarseness and the frequency of soft palate paralysis were also evaluated. Specifically, we classified the patients into 4 groups, based on the presence or absence of dysphagia and hoarseness and then compared the frequency of soft palate paralysis between group 1 (dysphagia and hoarseness were present) and the other 3 groups, using Fisher exact test. Significance was defined as a P value of less than .05.
Results The Locations of the Patients’ Infarcts and their Neurologic Findings The infarcts were located in the rostral medulla in 11 patients (patients 1-11), in the middle medulla in 27 patients (patients 12-38), in the caudal medulla in 6 patients (patients 39-44), and in the middle and caudal medulla in 2 patients (patients 45 and 46). The Rostral Group (Patients 1-11) All the 11 infarcts were located in the L region. At onset, vertigo was present in 5 patients, and 4 patients were
experiencing headaches or neck pain. Five patients exhibited dysphagia, and 7 patients displayed dysarthria. Hoarseness and soft palate paralysis (ipsilateral to the lesion: 3 patients and bilateral: 1 patient) were seen in 4 patients each. Ipsilateral facial paresis was observed in 6 patients. Six patients exhibited nystagmus. Of these, 5 patients (patients 2, 4, and 9-11) demonstrated horizontal or horizontal/torsional gaze-evoked directional nystagmus, and 1 patient (patient 7) displayed horizontal/torsional unidirectional nystagmus. Two patients exhibited severe truncal ataxia (unable to stand or lateropulsion in the standing/sitting position; patients 4 and 9). Vestibular symptoms were present in 1 of these patients (patient 9) and were absent in another patient (patient 4). All 11 patients suffered from superficial sensory disturbance (type a: 3 patients, type b: 4 patients, type c: 2 patients, and type d: 2 patients). Three of the patients demonstrated segmental superficial sensory disturbance (patients 2, 3, and 9). Of these, sensory disturbance was absent from the lower trunk and the lower extremity in 2 patients (patients 2 and 9) and from the upper trunk and the upper extremity in 1 patient (patient 3). The Middle Group (Patients 12-38) The infarcts were located in the L region in 12 patients; the L and P regions in 8 patients; the L, AL, and P regions in 3 patients; the L and AL regions in 2 patients; and the anteromedial, AL, L, and P regions in 2 patients. At onset, vertigo was present in 17 patients, and 14 patients had headaches or neck pain. Of the latter 14 patients, 2 experienced ipsilateral trigeminal pain (patients 20 and 36). Dysphagia occurred in 10 patients, 6 patients demonstrated hoarseness, and soft palate paralysis developed in 12 patients (ipsilateral to the lesion: 10 patients and bilateral: 2 patients). Ipsilateral facial paresis was present in 8 patients. Eighteen patients exhibited nystagmus. Of these, 4 patients (patients 12, 14, 27, and 29) had horizontal or horizontal/torsional gaze-evoked directional nystagmus, and 14 patients demonstrated horizontal or horizontal/torsional unidirectional nystagmus. Severe truncal ataxia with vestibular symptoms was seen in 18 patients. Four patients developed hiccups (patients 16, 26, 31, and 32). One patient (patient 26) experienced respiratory failure. All 27 patients exhibited superficial sensory
Figure 1. Regions of the medulla supplied by each penetrating artery. The medulla is supplied by 4 penetrating arteries, and hence, can be divided into the anteromedial (AM), anterolateral (AL), lateral (L), and posterior (P) regions.
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Figure 2. Arterial supply of the medulla (modified from the original figure by Goto14). The median medullary branch, which diverges from the anterior spinal artery, supplies the anteromedial region. The posterior inferior cerebellar artery, which originates from the vertebral artery, has 3 branches. The medial medullary branch supplies the anterolateral region where the inferior olivary nucleus is located. The lateral medullary branch supplied the lateral region. The dorsal medullary branch supplies the posterior part of the medulla. Abbreviations: F lm, fasciculus longitudinalis medialis; Fo ret, Formatio reticularis; L m, lemniscus medialis; N amb, nucleus ambiguus; N cu, nucleus cuneatus; N dX, nucleus dorsalis nervi vagi; N o, nucleus olivaris; N oad, nucleus olivaris accessorius dorsalis; N oam, nucleus olivaris accessorius medialis; N XII, nucleus nervi hypoglossi; N tspV, nucleus tractus spinalis nervi trigemini; P ci, peduncles cerebellaris inferior; Rx XII, radix nervi hypoglossi; T s, tract solitarius; T spV, tract spinalis nervi trigemini.
disturbance (type a: 13 patients, type b: 4 patients, type c: 7 patients, and type d: 3 patients). In 1 patient (patient 20), the sensory disturbance affected the ophthalmic (V1) and maxillary nerves (V2), and in 2 others, the sensory disturbance exhibited a segmental distribution (patients 16 and 22). Sensory disturbance was absent from the lower trunk and the lower extremity and limited to the upper extremity in 1 patient each (patients 16 and 22, respectively). The Caudal Group (Patients 39-44) The infarcts developed in the L region in 1 patient, the L and P regions in 3 patients, and the L and AL regions in 2 patients. At onset, 4 patients were suffering from vertigo and 5 patients were suffering from neck pain or headaches. One patient complained of ophthalmalgia (patient 44). Ipsilateral soft palate paralysis developed in 2 patients (patients 39 and 42). Five patients exhibited nystagmus. Of these, 1 patient (patient 40) demonstrated horizontal gaze-evoked directional nystagmus, and horizontal or horizontal/torsional unidirectional nystagmus was seen in 4 patients (patients 39 and 41-43). Severe truncal ataxia was observed in all 6 patients, and vestibular symptoms developed in 4 of them (patients 39 and 41-43). One patient noted vestibular symptoms alone (patient 41). Two patients exhibited any nonvestibular symptoms (patients 40 and 44). Three patients experienced superficial sensory disturbance (type a: 2 patients and type c: 1 patient). The Middle 1 Caudal group (Patients 45 and 46) In 1 patient (patient 45), the lesion was located in the L region, whereas the lesion affected both the L and P regions in the other patient (patient 46). Both patients exhibited vertigo and ipsilateral ophthalmalgia at onset and developed hoarseness, ipsilateral facial paresis, ataxia of
the extremities, and severe truncal ataxia. In addition, one of the patients displayed horizontal/torsional unidirectional nystagmus (patient 45). In both patients, the sensory disturbance was classified as type c. A disturbance of vibratory sensation was also observed in 1 patient (patient 46; Tables 1, 2).
Comparison of the Frequencies of Neurologic Findings between the Rostral and Caudal Groups and the Associations between the Presence/Absence of Dysphagia and Hoarseness and the Frequency of Soft Palate Paralysis As shown in Table 3, dysarthria and facial palsy occurred significantly more frequently in the rostral group. In contrast, the incidences of severe truncal ataxia and unidirectional nystagmus were significantly higher in the caudal group. In the analysis shown in Table 4, soft palate paralysis was found to be significantly more common in the patients with both dysphagia and hoarseness (group 1) than those in which dysphagia and hoarseness were both absent (group 4; Tables 3, 4).
Discussion The medulla is divided into 4 regions, based on the distribution of each penetrating artery (Figs 1, 2).13,14 LMI is mainly caused by ischemia in the L region, which is supplied by the lateral medullary branch.14 This region contains the lateral spinothalamic tract, nucleus ambiguus, the spinal tract and nucleus of the trigeminal nerve, the ventral part of the inferior cerebellar peduncle, and the dorsal/ventral spinocerebellar tract (Fig 3).1,14 The AL region is supplied by the medial medullary branch.14 The P region, which is fed by the dorsal medullary branch, contains the vestibular nucleus, the dorsal
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Table 1. Breakdown of 46 patients with lateral medullary infarction
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Continued
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Table 1. (Continued)
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Table 2. Schema of the medullary magnetic resonance imaging findings of the 46 patients
nucleus of the vagus nerve, and the nucleus of the solitary tract (Fig 3).1,14 In this study, a large proportion of the LMI affected the L region only (25 patients). Headache and vertigo are the chief complaints in LMI.2,6 In the present study, many of the patients displayed these symptoms at onset. In LMI, trigeminal pain tends to occur in the ipsilateral periorbital region.15 Fitzek et al16 reported that in patients of LMI, ipsilateral trigeminal pain is associated with lesions affecting the parts of the spinal trigeminal tract in the caudal medulla. Ipsilateral trigeminal pain was observed in 5 patients
(patients 20, 36, and 44-46), and it extended to the orbital region in 4 patients (patients 20 and 44-46). These findings were consistent with those of previous reports.15,16 Three of the previously mentioned patients (patients 44-46) had lesions that affected the caudal medulla; however, the other 2 patients’ lesions were located in the middle medulla (patients 20 and 36). Hiccups are caused by an imbalance between inspiration and expiration.4 In LMI, hiccups are reported to be caused by lesions affecting the dorsal nucleus of the vagus nerve and the nucleus of the solitary tract, which
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Table 3. Comparison of the frequencies of each neurologic finding between the rostral and caudal groups
Vertigo Headache, neck pain Dysphagia Dysarthria Hoarseness Soft palate paralysis Facial palsy Lingual palsy Paresis of the extremities Eye movement disturbance Directional gaze-evoked nystagmus Unidirectional nystagmus Ataxia of the extremities Disturbance of standing and gait Lateropulsion in the standing position or unable to stand Hiccups Horner sign Respiratory failure Sensory disturbance Ipsilateral side of the face—contralateral limbs/trunk Contralateral side of the face—limbs/trunk Contralateral limbs/trunk Ipsilateral side of the face
Rostral (n 5 11)
Caudal (n 5 6)
5 4 5 7 4 4 6 2 0 0 5 1 6 8 2 0 8 0
4 5 0 0 0 2 0 1 1 0 1 4 4 6 6 1 4 0
3 4 2 2
2 0 1 0
P value
.034*
.042*
.027*
.0022*
Based on the Fisher exact test. Significant P value was tagged with *. Significance was defined as a P value of less than .05. Where no P value is given, the difference was not significant.
are located in the P region.4 Park et al4 reported that in patients of LMI involving hiccups, the causative lesions extended from the L to the P region in the middle medulla. In the present study, the 5 patients with hiccups also exhibited vertigo (patients 16, 26, 31, 32, and 42), and 4 of them demonstrated ipsilateral facial sensory disturbance. In 3 of the patients with hiccups, the lesions extended from the L to the P region in the middle medulla (patients 26, 31, and 32). These results were consistent with the findings of previous reports4,17; however, dysphagia occurred in one of the patients, which is atypical. One of the patients experienced respiratory failure (patient 26). The medulla contains the dorsal respiratory group and the rostral ventral respiratory group, which influence the respiratory system.18 The dor-
sal respiratory group is located in the ventrolateral part of the nucleus of the solitary tract,18 and the rostral ventral respiratory group is situated in the ventral part of the nucleus ambiguus.18 Therefore, patients who develop respiratory failure after suffering LMI frequently present with dysphagia and hiccups,6,17 which was also true of our patient (patient 26). The vestibular nucleus is located in the P region (Fig 3) of the rostral to middle medulla and projects into the lower cerebellum via the inferior cerebellar peduncle (the vestibulocerebellar pathway).19 The vestibular pathway consists of the vestibulocerebellar pathway and the vestibular nucleus.19 Impairment of the vestibular pathway results in severe truncal ataxia with vestibular symptoms.20 Many of the patients who exhibited severe
Table 4. The associations between soft palate paralysis and the presence/absence of dysphagia and hoarseness
Group (n) 1 (7) 2 (9) 3 (5) 4 (25) Total
Dysphagia
Hoarseness
1 1 2 2
1 2 1 2
Number of patients with soft palate paralysis, n (%) 6 (85) 4 (44) 1 (20) 8 (32) 19
P value
.145 .071 .026*
Comparison of the frequencies of soft palate paralysis between group 1 and the other groups based on the Fisher exact test. Significant P value was tagged with *. Significance was defined as a P value of less than .05.
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Figure 3. Schema of the middle level of the medulla. The anatomic structure of the middle medulla is shown. Abbreviations: DSCT, dorsal spinocerebellar tract; LVST, lateral vestibulospinal tract; MLF, medial longitudinal fasciculus; VSCT, ventral spinocerebellar tract.
truncal ataxia in the present study also displayed vestibular symptoms (25 patients). Among these patients, 1 patient did not exhibit any nonvestibular symptoms (patient 41). Kim12 reported 3 patients of rostral LMI in whom the patients’ neurologic symptoms mimicked those of labyrinthitis. The latter patients’ infarcts involved the vestibular nuclei and the inferior cerebellar peduncle, which are located in the L and P regions. Infarct of patient 41 also affected the L and P regions, although it was situated in the caudal part of the medulla. In contrast, 3 patients displayed severe truncal ataxia without vestibular symptoms (patients 4, 40, and 44). Ataxia of the extremities was observed in 2 of the patients (patients 4 and 44). Th€ omke et al11 studied patients of LMI involving body lateropulsion without vestibular symptoms and reported that body lateropulsion without ataxia of the extremities was attributed to impairment of the lateral vestibulospinal tract (LVST), whereas body lateropulsion combined with ataxia of the extremities was associated with impairment of the dorsal spinocerebellar tract (DSCT).11 The DSCT conveys unconsciousness proprioceptive signals from the ipsilateral trunk and leg, and such signals pass through the superficial part of the L region (Fig 3).8 The lesions of 2 of the previously mentioned patients (patients 4 and 44) extended into the superficial part of the L region, which suggested that the DSCT had been affected in these patients. The LVST is involved in vestibulospinal postural control and is located in the ventromedial part of the L region (Fig 3).10,11 Lesion of patient 40 extended to the ventromedial part of the L region, and thus, was considered to involve the LVST. Four patterns of sensory disturbance were observed in our study, all of which have been reported previously.6,7,21 Among the 4 types, type a was the most common (18 patients), which was consistent with the findings of previous reports.6,20,21 In 2 of the patients involving sensory disturbance (patients 20 and 34), the patients’ other neurologic findings were mild. The latter 2 patients’ lesions were relatively small and were mainly localized in the superficial part of the L region. Five patients displayed segmental sensory disturbance. Segmental sensory disturbance caused by lower lateral brainstem lesions can be classified into the crossed and unilateral patterns.22 In the crossed pattern, sensory
disturbance is seen on the ipsilateral side of the face and on the contralateral lower trunk and leg,22 whereas in the unilateral pattern, it is observed on contralateral side of the face and on the contralateral upper trunk and arm.22 In our study, 1 patient demonstrated the unilateral pattern (patient 2). This patient’s lesion was considered to involve the medial part of the lateral spinothalamic tract and the ventral trigeminothalamic tract.22 The other 4 patients displayed atypical patterns of sensory disturbances that did not correspond to the previously reported types of segmental sensory disturbance.7,22 LMI can produce bilateral dysfunction of the pharyngeal phase of swallowing, which leads to dysphagia.23 In the medulla, the premotor neurons involved in swallowing are located in the nucleus ambiguus and nucleus of the solitary tract.23 In LMI, dysphagia is mainly caused by lesions involving the parts of the nucleus ambiguus located in the rostral to middle medulla.23,24 Conversely, the section of the nucleus ambiguus in the caudal medulla does not directly influence the pharyngeal muscles.23 The premotor neurons in the nucleus ambiguus are connected with the ipsilateral cranial motor neurons related to swallowing and also project to the nucleus ambiguus on the contralateral side.23 In the present study, dysphagia occurred in the patients whose lesions involved the rostral to middle parts of the medulla. This finding supports the assertion that lesions affecting the nucleus ambiguus, which is involved in swallowing, are chiefly responsible for dysphagia in patients who have experienced LMI.23,24 Hoarseness, which is caused by ipsilateral vocal cord paresis, and soft palate paralysis are the other main symptoms associated with lesions affecting the nucleus ambiguus, which also controls the ipsilateral vocal cord muscles.25 In the present study, hoarseness developed in the rostral and middle groups as a result of dysphagia. In LMI, soft palate paralysis usually occurs on the ipsilateral side to the lesion.23,24 Among the patients examined in the present study, unilateral soft palate paralysis was seen in 15 patients, and bilateral soft palate paralysis developed in 3 patients. Impairment of the projections to the contralateral nucleus ambiguus was considered to have been responsible for the contralateral paralysis seen in the latter 3 patients.23
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Kim investigated the frequencies of neurologic symptoms in patients of LMI involving rostral and caudal lesions. As a result, they reported that dysphagia, dysarthria, and facial palsy occurred significantly more frequently in the rostral group than those in the caudal group, and also found that gait ataxia and headaches were significantly more common in the caudal group than those in the rostral group.6 In our study, dysarthria and facial palsy occurred significantly more often in the rostral group than those in the caudal group. Severe gait ataxia was significantly more common in the caudal group than that in the rostral group. These results were consistent with those of previous reports.6,20 We also analyzed the associations between the presence/the absence of dysphagia and hoarseness and the frequency of soft palate paralysis (Table 4). The incidence of soft palate paralysis was highest in group 1 in which dysphagia and hoarseness were both present, and the soft palate paralysis in this group was considered to have contributed to the patients’ dysphagia. Soft palate paralysis was also seen in group 4 in which dysphagia and hoarseness were both absent. In this group, the soft palate paralysis did not result in dysphagia. It was considered that the contribution of soft palate paralysis to dysphagia depends on the severity of the impairment of the nucleus ambiguus. Patients of facial palsy caused by medullary lesions have been reported in the literature.6,20,26 A section of the corticobulbar tract descends to the rostral medulla and approaches the contralateral facial nucleus after its decussation.26 In LMI, the fibers of the corticobulbar tract can be impaired after their decussation, causing ipsilateral facial palsy. In our patients, facial palsy occurred ipsilaterally, which is consistent with the findings of previous reports.6,20 In conclusion, the present study showed the atypical patterns of segmental sensory disturbance and patients of LMI involving severe truncal ataxia without vestibular symptoms, which suggests that the clinical symptoms of LMI vary markedly. An analysis of the bulbar symptoms of LMI indicated that the extent to which soft palate paralysis contributes to dysphagia depends on how badly the nucleus ambiguus is impaired. The variability in the clinical features of LMI can be explained by the differences in the severity and locations of such lesions.
References 1. Vuilleumier P, Bogousslavsky J, Regli F. Infarction of the lower brainstem: clinical, aetiological and MRItopographical correlations. Brain 1995;118:1013-1025. 2. Sacco RL, Freddo L, Bello JA, et al. Wallenberg’s lateral medullary syndrome: clinical-magnetic resonance imaging correlations. Arch Neurol 1993;50:609-614. 3. Zhang SQ, Liu MY, Wan B, et al. Contralateral body half hypalgesia in a patient with lateral medullary infarction: atypical Wallenberg syndrome. Eur Neurol 2008;59: 211-215.
4. Park MH, Kim BJ, Koh SB, et al. Lesional location of lateral medullary infarction presenting hiccups (singultus). J Neurol Neurosurg Psychiatry 2005;76:95-98. 5. Nowak DA, Topka HR. The clinical variability of Wallenberg’s syndrome. The anatomical correlate of ipsilateral axial lateropulsion. J Neurol 2006;253:507-511. 6. Kim JS. Pure lateral medullary infarction: clinicalradiological correlation of 130 acute, consecutive patients. Brain 2003;126:1864-1872. 7. Kim JS, Lee JH, Lee MC. Patterns of sensory dysfunction in lateral medullary infarction: clinical-MRI correlation. Neurology 1997;49:1557-1563. 8. Maeda K, Saikyo M, Mukose A, et al. Lateropulsion due to a lesion of the dorsal spinocerebellar tract. Intern Med 2005;44:1295-1297. 9. Kim SH, Cho YJ, Cho JH, et al. Isolated lateropulsion by a lesion of the dorsal spinocerebellar tract. Cerebrovasc Dis 2004;18:344-345. 10. Kim HJ, Kwon HM, Huh YE, et al. Ipsilateral axial lateropulsion as an initial symptom of lateral medullary infarction: a case report. J Clin Neurol 2007;3:197-199. 11. Th€ omke F, Marx JJ, Iannetti GD, et al. A topodiagnostic investigation on body lateropulsion in medullary infarcts. Neurology 2005;64:716-718. 12. Kim JS. Vertigo and gait ataxia without usual signs of lateral medullary infarction: a clinical variant related to rostraldorsolateral lesions. Cerebrovasc Dis 2000;10:471-474. 13. Kim K, Lee HS, Jung YH, et al. Mechanism of medullary infarction based on arterial territory involvement. J Clin Neurol 2012;8:116-122. 14. Goto N. Arterial supply of the medulla. Anatomy of brain vessels. Tokyo: Medical Tribune 1986:109-115 [in Japanese]. 15. Ord as CM, Cuadrado NL, Simal P, et al. Wallenberg’s syndrome and symptomatic trigeminal neuralgia. J Headache Pain 2011;12:377-380. 16. Fitzek S, Baumg€ artner U, Fitzek C, et al. Mechanisms and predictors of chronic facial pain in lateral medullary infarction. Ann Neurol 2001;49:493-500. 17. Currier RD, Giles CL, Dejong RN. Some comments on Wallenberg’s lateral medullary syndrome. Neurology 1961;11:778-791. 18. Ezure K, Manabe M, Yamada H. Distribution of medullary respiratory neurons in the rat. Brain Res 1988;455:262-270. 19. Parent A. Carpenter’s human anatomy. 9 ed. Baltimore: Williams & Wilkins 1996:421-468. 20. Kim JS, Lee JH, Suh DC, et al. Spectrum of lateral medullary syndrome: correlation between clinical findings and magnetic resonance imaging 33 subjects. Stroke 1994;25: 1405-1410. 21. Norrving Bo, Cronqvist S. Lateral medullary infarction: prognosis in an unselected series. Neurology 1991;41:244-248. 22. Matsumoto S, Okuda B, Imai T, et al. A sensory level on the trunk in lower lateral brainstem lesions. Neurology 1988;38:1515-1519. 23. Aydogdu I, Ertekin C, Taslaci S, et al. Dysphagia in lateral medullary infarction (Wallenberg’s syndrome): an acute disconnection syndrome in premotor neurons related to swallowing activity? Stroke 2001;32:2081-2087. 24. Kwon M, Le JH, Kim JS. Dysphagia in unilateral medullary infarction: lateral vs medial lesions. Neurology 2005; 65:714-718. 25. Venketasubramanian N, Seshadri R, Chee N. Vocal cord paresis in acute ischemic stroke. Cerebrovasc Dis 1999; 9:157-162. 26. Terao S, Miura N, Takeda A, et al. Course and distribution of facial corticobulbar tract fibres in the lower brain stem. J Neurol Neurosurg Psychiatry 2000;69:262-265.
Background: Lateral medullary infarction (LMI) exhibits a variety of clinical features. Various bulbar symptoms can occur in LMI. Methods: Neuroradiologic findings of 46 LMI patients were examined. Their infarcts were categorized into the rostral, middle, and caudal groups and were further subdivided into the anteromedial, anterolateral, lateral (L), and posterior regions. Results: The middle medulla was the most common site (27 patients). Most lesions affected the L region alone (25 patients). Dysarthria and facial palsy occurred significantly more frequently in the rostral group than those in the caudal group. Severe truncal ataxia was significantly more common in the caudal group than that in the rostral group. Twenty-five of the 28 patients with severe truncal ataxia displayed vestibular symptoms; otherwise, the other 3 patients showed absence of vestibular symptoms. Soft palate paralysis occurred at a significantly high frequency in the patients with dysphagia and hoarseness compared with the patients without these 2 symptoms. Segmental sensory disturbance occurred in 5 patients, 4 of whom exhibited atypical patterns. Conclusions: The results of our comparisons between the rostral and caudal groups were consistent with those of previous studies. The presence of severe truncal ataxia without vestibular symptoms in LMI was atypical. An analysis of the bulbar symptoms indicated that the extent to which soft palate paralysis contributed to dysphagia was associated with the severity of ischemia in the nucleus ambiguus. The present study showed variability in clinical features of LMI, which was related to differences in the severity and the extent of ischemia in the lateral medulla. Key Words: Lateral medullary infarction—severe truncal ataxia— sensory disturbance—dysphagia—soft palate paralysis. Ó 2015 Published by Elsevier Inc. on behalf of National Stroke Association
Lateral medullary infarction (LMI) is caused by ischemia in the lateral region of the medulla.1,2 In typical patients of LMI, vertigo, the disturbance of superficial sensation on the ipsilateral side of the face and the contralateral limbs and trunk; Horner sign; truncal ataxia; ipsilateral incoordination of the extremities; and ipsilateral paralysis of the soft palate, larynx, and From the Division of Neurology, Department of Medicine, Nihon University School of Medicine, Tokyo, Japan. Received November 5, 2014; revision received December 16, 2014; accepted January 2, 2015. Address correspondence to Katsuhiko Ogawa, MD, Division of Neurology, Department of Medicine, Nihon University School of Medicine, 30-1 Oyaguchi-kamimachi, Itabashi-ku, Tokyo 173-8610, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 Published by Elsevier Inc. on behalf of National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.01.006
pharynx are observed.1,3,4 However, the clinical features of LMI can vary markedly.5,6 Various types of sensory disturbances are seen in LMI.7 Truncal ataxia in LMI is usually accompanied by vestibular symptoms (vertigo and horizontal or horizontal/torsional unidirectional nystagmus).8–10 Recently, atypical patients of LMI involving isolated lateropulsion8-11 or vestibular symptoms alone12 have been reported. We studied the neurologic characteristics of LMI based on an investigation of the neuroradiologic findings of 46 patients who had experienced LMI.
Patients and Methods Characteristics of the Enrolled Patients and Study Design Forty-six patients who had experienced LMI were enrolled. The patients were diagnosed as having LMI,
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based on their magnetic resonance imaging findings, and all their infarcts were limited to the medulla. Patients whose lesions had spread to parts of the brainstem other than the medulla or the cerebellum were excluded. We reviewed the medical charts of each patient and identified their neurologic findings. Nystagmus was evaluated by the confrontation test. Sensory disturbance was grouped into 4 types: type a: ipsilateral side of the face— contralateral limbs/trunk, type b: contralateral side of the face—limbs/trunk, type c: contralateral limbs/trunk, and type d: ipsilateral side of the face. We divided the infarct locations into the rostral, middle, and caudal groups (Fig 1), and then, subdivided them into the anteromedial, anterolateral (AL), lateral (L), and posterior (P) regions, based on the distribution of each penetrating artery (Figs 1, 2).13,14
Statistical Analysis We compared the frequencies of each neurologic finding between the rostral and caudal groups, using the Fisher exact test. The associations between the presence/the absence of dysphagia and hoarseness and the frequency of soft palate paralysis were also evaluated. Specifically, we classified the patients into 4 groups, based on the presence or absence of dysphagia and hoarseness and then compared the frequency of soft palate paralysis between group 1 (dysphagia and hoarseness were present) and the other 3 groups, using Fisher exact test. Significance was defined as a P value of less than .05.
Results The Locations of the Patients’ Infarcts and their Neurologic Findings The infarcts were located in the rostral medulla in 11 patients (patients 1-11), in the middle medulla in 27 patients (patients 12-38), in the caudal medulla in 6 patients (patients 39-44), and in the middle and caudal medulla in 2 patients (patients 45 and 46). The Rostral Group (Patients 1-11) All the 11 infarcts were located in the L region. At onset, vertigo was present in 5 patients, and 4 patients were
experiencing headaches or neck pain. Five patients exhibited dysphagia, and 7 patients displayed dysarthria. Hoarseness and soft palate paralysis (ipsilateral to the lesion: 3 patients and bilateral: 1 patient) were seen in 4 patients each. Ipsilateral facial paresis was observed in 6 patients. Six patients exhibited nystagmus. Of these, 5 patients (patients 2, 4, and 9-11) demonstrated horizontal or horizontal/torsional gaze-evoked directional nystagmus, and 1 patient (patient 7) displayed horizontal/torsional unidirectional nystagmus. Two patients exhibited severe truncal ataxia (unable to stand or lateropulsion in the standing/sitting position; patients 4 and 9). Vestibular symptoms were present in 1 of these patients (patient 9) and were absent in another patient (patient 4). All 11 patients suffered from superficial sensory disturbance (type a: 3 patients, type b: 4 patients, type c: 2 patients, and type d: 2 patients). Three of the patients demonstrated segmental superficial sensory disturbance (patients 2, 3, and 9). Of these, sensory disturbance was absent from the lower trunk and the lower extremity in 2 patients (patients 2 and 9) and from the upper trunk and the upper extremity in 1 patient (patient 3). The Middle Group (Patients 12-38) The infarcts were located in the L region in 12 patients; the L and P regions in 8 patients; the L, AL, and P regions in 3 patients; the L and AL regions in 2 patients; and the anteromedial, AL, L, and P regions in 2 patients. At onset, vertigo was present in 17 patients, and 14 patients had headaches or neck pain. Of the latter 14 patients, 2 experienced ipsilateral trigeminal pain (patients 20 and 36). Dysphagia occurred in 10 patients, 6 patients demonstrated hoarseness, and soft palate paralysis developed in 12 patients (ipsilateral to the lesion: 10 patients and bilateral: 2 patients). Ipsilateral facial paresis was present in 8 patients. Eighteen patients exhibited nystagmus. Of these, 4 patients (patients 12, 14, 27, and 29) had horizontal or horizontal/torsional gaze-evoked directional nystagmus, and 14 patients demonstrated horizontal or horizontal/torsional unidirectional nystagmus. Severe truncal ataxia with vestibular symptoms was seen in 18 patients. Four patients developed hiccups (patients 16, 26, 31, and 32). One patient (patient 26) experienced respiratory failure. All 27 patients exhibited superficial sensory
Figure 1. Regions of the medulla supplied by each penetrating artery. The medulla is supplied by 4 penetrating arteries, and hence, can be divided into the anteromedial (AM), anterolateral (AL), lateral (L), and posterior (P) regions.
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Figure 2. Arterial supply of the medulla (modified from the original figure by Goto14). The median medullary branch, which diverges from the anterior spinal artery, supplies the anteromedial region. The posterior inferior cerebellar artery, which originates from the vertebral artery, has 3 branches. The medial medullary branch supplies the anterolateral region where the inferior olivary nucleus is located. The lateral medullary branch supplied the lateral region. The dorsal medullary branch supplies the posterior part of the medulla. Abbreviations: F lm, fasciculus longitudinalis medialis; Fo ret, Formatio reticularis; L m, lemniscus medialis; N amb, nucleus ambiguus; N cu, nucleus cuneatus; N dX, nucleus dorsalis nervi vagi; N o, nucleus olivaris; N oad, nucleus olivaris accessorius dorsalis; N oam, nucleus olivaris accessorius medialis; N XII, nucleus nervi hypoglossi; N tspV, nucleus tractus spinalis nervi trigemini; P ci, peduncles cerebellaris inferior; Rx XII, radix nervi hypoglossi; T s, tract solitarius; T spV, tract spinalis nervi trigemini.
disturbance (type a: 13 patients, type b: 4 patients, type c: 7 patients, and type d: 3 patients). In 1 patient (patient 20), the sensory disturbance affected the ophthalmic (V1) and maxillary nerves (V2), and in 2 others, the sensory disturbance exhibited a segmental distribution (patients 16 and 22). Sensory disturbance was absent from the lower trunk and the lower extremity and limited to the upper extremity in 1 patient each (patients 16 and 22, respectively). The Caudal Group (Patients 39-44) The infarcts developed in the L region in 1 patient, the L and P regions in 3 patients, and the L and AL regions in 2 patients. At onset, 4 patients were suffering from vertigo and 5 patients were suffering from neck pain or headaches. One patient complained of ophthalmalgia (patient 44). Ipsilateral soft palate paralysis developed in 2 patients (patients 39 and 42). Five patients exhibited nystagmus. Of these, 1 patient (patient 40) demonstrated horizontal gaze-evoked directional nystagmus, and horizontal or horizontal/torsional unidirectional nystagmus was seen in 4 patients (patients 39 and 41-43). Severe truncal ataxia was observed in all 6 patients, and vestibular symptoms developed in 4 of them (patients 39 and 41-43). One patient noted vestibular symptoms alone (patient 41). Two patients exhibited any nonvestibular symptoms (patients 40 and 44). Three patients experienced superficial sensory disturbance (type a: 2 patients and type c: 1 patient). The Middle 1 Caudal group (Patients 45 and 46) In 1 patient (patient 45), the lesion was located in the L region, whereas the lesion affected both the L and P regions in the other patient (patient 46). Both patients exhibited vertigo and ipsilateral ophthalmalgia at onset and developed hoarseness, ipsilateral facial paresis, ataxia of
the extremities, and severe truncal ataxia. In addition, one of the patients displayed horizontal/torsional unidirectional nystagmus (patient 45). In both patients, the sensory disturbance was classified as type c. A disturbance of vibratory sensation was also observed in 1 patient (patient 46; Tables 1, 2).
Comparison of the Frequencies of Neurologic Findings between the Rostral and Caudal Groups and the Associations between the Presence/Absence of Dysphagia and Hoarseness and the Frequency of Soft Palate Paralysis As shown in Table 3, dysarthria and facial palsy occurred significantly more frequently in the rostral group. In contrast, the incidences of severe truncal ataxia and unidirectional nystagmus were significantly higher in the caudal group. In the analysis shown in Table 4, soft palate paralysis was found to be significantly more common in the patients with both dysphagia and hoarseness (group 1) than those in which dysphagia and hoarseness were both absent (group 4; Tables 3, 4).
Discussion The medulla is divided into 4 regions, based on the distribution of each penetrating artery (Figs 1, 2).13,14 LMI is mainly caused by ischemia in the L region, which is supplied by the lateral medullary branch.14 This region contains the lateral spinothalamic tract, nucleus ambiguus, the spinal tract and nucleus of the trigeminal nerve, the ventral part of the inferior cerebellar peduncle, and the dorsal/ventral spinocerebellar tract (Fig 3).1,14 The AL region is supplied by the medial medullary branch.14 The P region, which is fed by the dorsal medullary branch, contains the vestibular nucleus, the dorsal
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Table 1. Breakdown of 46 patients with lateral medullary infarction
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Continued
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Table 1. (Continued)
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Table 2. Schema of the medullary magnetic resonance imaging findings of the 46 patients
nucleus of the vagus nerve, and the nucleus of the solitary tract (Fig 3).1,14 In this study, a large proportion of the LMI affected the L region only (25 patients). Headache and vertigo are the chief complaints in LMI.2,6 In the present study, many of the patients displayed these symptoms at onset. In LMI, trigeminal pain tends to occur in the ipsilateral periorbital region.15 Fitzek et al16 reported that in patients of LMI, ipsilateral trigeminal pain is associated with lesions affecting the parts of the spinal trigeminal tract in the caudal medulla. Ipsilateral trigeminal pain was observed in 5 patients
(patients 20, 36, and 44-46), and it extended to the orbital region in 4 patients (patients 20 and 44-46). These findings were consistent with those of previous reports.15,16 Three of the previously mentioned patients (patients 44-46) had lesions that affected the caudal medulla; however, the other 2 patients’ lesions were located in the middle medulla (patients 20 and 36). Hiccups are caused by an imbalance between inspiration and expiration.4 In LMI, hiccups are reported to be caused by lesions affecting the dorsal nucleus of the vagus nerve and the nucleus of the solitary tract, which
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Table 3. Comparison of the frequencies of each neurologic finding between the rostral and caudal groups
Vertigo Headache, neck pain Dysphagia Dysarthria Hoarseness Soft palate paralysis Facial palsy Lingual palsy Paresis of the extremities Eye movement disturbance Directional gaze-evoked nystagmus Unidirectional nystagmus Ataxia of the extremities Disturbance of standing and gait Lateropulsion in the standing position or unable to stand Hiccups Horner sign Respiratory failure Sensory disturbance Ipsilateral side of the face—contralateral limbs/trunk Contralateral side of the face—limbs/trunk Contralateral limbs/trunk Ipsilateral side of the face
Rostral (n 5 11)
Caudal (n 5 6)
5 4 5 7 4 4 6 2 0 0 5 1 6 8 2 0 8 0
4 5 0 0 0 2 0 1 1 0 1 4 4 6 6 1 4 0
3 4 2 2
2 0 1 0
P value
.034*
.042*
.027*
.0022*
Based on the Fisher exact test. Significant P value was tagged with *. Significance was defined as a P value of less than .05. Where no P value is given, the difference was not significant.
are located in the P region.4 Park et al4 reported that in patients of LMI involving hiccups, the causative lesions extended from the L to the P region in the middle medulla. In the present study, the 5 patients with hiccups also exhibited vertigo (patients 16, 26, 31, 32, and 42), and 4 of them demonstrated ipsilateral facial sensory disturbance. In 3 of the patients with hiccups, the lesions extended from the L to the P region in the middle medulla (patients 26, 31, and 32). These results were consistent with the findings of previous reports4,17; however, dysphagia occurred in one of the patients, which is atypical. One of the patients experienced respiratory failure (patient 26). The medulla contains the dorsal respiratory group and the rostral ventral respiratory group, which influence the respiratory system.18 The dor-
sal respiratory group is located in the ventrolateral part of the nucleus of the solitary tract,18 and the rostral ventral respiratory group is situated in the ventral part of the nucleus ambiguus.18 Therefore, patients who develop respiratory failure after suffering LMI frequently present with dysphagia and hiccups,6,17 which was also true of our patient (patient 26). The vestibular nucleus is located in the P region (Fig 3) of the rostral to middle medulla and projects into the lower cerebellum via the inferior cerebellar peduncle (the vestibulocerebellar pathway).19 The vestibular pathway consists of the vestibulocerebellar pathway and the vestibular nucleus.19 Impairment of the vestibular pathway results in severe truncal ataxia with vestibular symptoms.20 Many of the patients who exhibited severe
Table 4. The associations between soft palate paralysis and the presence/absence of dysphagia and hoarseness
Group (n) 1 (7) 2 (9) 3 (5) 4 (25) Total
Dysphagia
Hoarseness
1 1 2 2
1 2 1 2
Number of patients with soft palate paralysis, n (%) 6 (85) 4 (44) 1 (20) 8 (32) 19
P value
.145 .071 .026*
Comparison of the frequencies of soft palate paralysis between group 1 and the other groups based on the Fisher exact test. Significant P value was tagged with *. Significance was defined as a P value of less than .05.
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Figure 3. Schema of the middle level of the medulla. The anatomic structure of the middle medulla is shown. Abbreviations: DSCT, dorsal spinocerebellar tract; LVST, lateral vestibulospinal tract; MLF, medial longitudinal fasciculus; VSCT, ventral spinocerebellar tract.
truncal ataxia in the present study also displayed vestibular symptoms (25 patients). Among these patients, 1 patient did not exhibit any nonvestibular symptoms (patient 41). Kim12 reported 3 patients of rostral LMI in whom the patients’ neurologic symptoms mimicked those of labyrinthitis. The latter patients’ infarcts involved the vestibular nuclei and the inferior cerebellar peduncle, which are located in the L and P regions. Infarct of patient 41 also affected the L and P regions, although it was situated in the caudal part of the medulla. In contrast, 3 patients displayed severe truncal ataxia without vestibular symptoms (patients 4, 40, and 44). Ataxia of the extremities was observed in 2 of the patients (patients 4 and 44). Th€ omke et al11 studied patients of LMI involving body lateropulsion without vestibular symptoms and reported that body lateropulsion without ataxia of the extremities was attributed to impairment of the lateral vestibulospinal tract (LVST), whereas body lateropulsion combined with ataxia of the extremities was associated with impairment of the dorsal spinocerebellar tract (DSCT).11 The DSCT conveys unconsciousness proprioceptive signals from the ipsilateral trunk and leg, and such signals pass through the superficial part of the L region (Fig 3).8 The lesions of 2 of the previously mentioned patients (patients 4 and 44) extended into the superficial part of the L region, which suggested that the DSCT had been affected in these patients. The LVST is involved in vestibulospinal postural control and is located in the ventromedial part of the L region (Fig 3).10,11 Lesion of patient 40 extended to the ventromedial part of the L region, and thus, was considered to involve the LVST. Four patterns of sensory disturbance were observed in our study, all of which have been reported previously.6,7,21 Among the 4 types, type a was the most common (18 patients), which was consistent with the findings of previous reports.6,20,21 In 2 of the patients involving sensory disturbance (patients 20 and 34), the patients’ other neurologic findings were mild. The latter 2 patients’ lesions were relatively small and were mainly localized in the superficial part of the L region. Five patients displayed segmental sensory disturbance. Segmental sensory disturbance caused by lower lateral brainstem lesions can be classified into the crossed and unilateral patterns.22 In the crossed pattern, sensory
disturbance is seen on the ipsilateral side of the face and on the contralateral lower trunk and leg,22 whereas in the unilateral pattern, it is observed on contralateral side of the face and on the contralateral upper trunk and arm.22 In our study, 1 patient demonstrated the unilateral pattern (patient 2). This patient’s lesion was considered to involve the medial part of the lateral spinothalamic tract and the ventral trigeminothalamic tract.22 The other 4 patients displayed atypical patterns of sensory disturbances that did not correspond to the previously reported types of segmental sensory disturbance.7,22 LMI can produce bilateral dysfunction of the pharyngeal phase of swallowing, which leads to dysphagia.23 In the medulla, the premotor neurons involved in swallowing are located in the nucleus ambiguus and nucleus of the solitary tract.23 In LMI, dysphagia is mainly caused by lesions involving the parts of the nucleus ambiguus located in the rostral to middle medulla.23,24 Conversely, the section of the nucleus ambiguus in the caudal medulla does not directly influence the pharyngeal muscles.23 The premotor neurons in the nucleus ambiguus are connected with the ipsilateral cranial motor neurons related to swallowing and also project to the nucleus ambiguus on the contralateral side.23 In the present study, dysphagia occurred in the patients whose lesions involved the rostral to middle parts of the medulla. This finding supports the assertion that lesions affecting the nucleus ambiguus, which is involved in swallowing, are chiefly responsible for dysphagia in patients who have experienced LMI.23,24 Hoarseness, which is caused by ipsilateral vocal cord paresis, and soft palate paralysis are the other main symptoms associated with lesions affecting the nucleus ambiguus, which also controls the ipsilateral vocal cord muscles.25 In the present study, hoarseness developed in the rostral and middle groups as a result of dysphagia. In LMI, soft palate paralysis usually occurs on the ipsilateral side to the lesion.23,24 Among the patients examined in the present study, unilateral soft palate paralysis was seen in 15 patients, and bilateral soft palate paralysis developed in 3 patients. Impairment of the projections to the contralateral nucleus ambiguus was considered to have been responsible for the contralateral paralysis seen in the latter 3 patients.23
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Kim investigated the frequencies of neurologic symptoms in patients of LMI involving rostral and caudal lesions. As a result, they reported that dysphagia, dysarthria, and facial palsy occurred significantly more frequently in the rostral group than those in the caudal group, and also found that gait ataxia and headaches were significantly more common in the caudal group than those in the rostral group.6 In our study, dysarthria and facial palsy occurred significantly more often in the rostral group than those in the caudal group. Severe gait ataxia was significantly more common in the caudal group than that in the rostral group. These results were consistent with those of previous reports.6,20 We also analyzed the associations between the presence/the absence of dysphagia and hoarseness and the frequency of soft palate paralysis (Table 4). The incidence of soft palate paralysis was highest in group 1 in which dysphagia and hoarseness were both present, and the soft palate paralysis in this group was considered to have contributed to the patients’ dysphagia. Soft palate paralysis was also seen in group 4 in which dysphagia and hoarseness were both absent. In this group, the soft palate paralysis did not result in dysphagia. It was considered that the contribution of soft palate paralysis to dysphagia depends on the severity of the impairment of the nucleus ambiguus. Patients of facial palsy caused by medullary lesions have been reported in the literature.6,20,26 A section of the corticobulbar tract descends to the rostral medulla and approaches the contralateral facial nucleus after its decussation.26 In LMI, the fibers of the corticobulbar tract can be impaired after their decussation, causing ipsilateral facial palsy. In our patients, facial palsy occurred ipsilaterally, which is consistent with the findings of previous reports.6,20 In conclusion, the present study showed the atypical patterns of segmental sensory disturbance and patients of LMI involving severe truncal ataxia without vestibular symptoms, which suggests that the clinical symptoms of LMI vary markedly. An analysis of the bulbar symptoms of LMI indicated that the extent to which soft palate paralysis contributes to dysphagia depends on how badly the nucleus ambiguus is impaired. The variability in the clinical features of LMI can be explained by the differences in the severity and locations of such lesions.
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