Journal of the Neurological Sciences 339 (2014) 153–156
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Acute vertigo due to hemispheric stroke A case report and comprehensive review of the literature Michael von Brevern ⁎, Sina Süßmilch, Daniel Zeise Department of Neurology, Park-Klinik Weissensee, Schönstrasse 80, 13086 Berlin, Germany
a r t i c l e
i n f o
Article history: Received 6 September 2013 Received in revised form 7 January 2014 Accepted 5 February 2014 Available online 14 February 2014 Keywords: Vertigo Stroke Middle cerebral artery Vestibular cortex Acute vestibular syndrome Nystagmus
a b s t r a c t Acute cortical lesions rarely cause vertigo. We report a 51-year-old patient presenting with an acute vestibular syndrome including spontaneous vertigo and nystagmus, lateropulsion and nausea due to middle cerebral artery infarction. The central origin of the acute vestibular syndrome was revealed by a normal head impulse test. A comprehensive literature review on patients with hemispheric stroke manifesting with acute vertigo is provided. Typically, patients with an acute vestibular syndrome due to cortical stroke have involvement of the temporoparietal junction. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Pseudo-vestibular neuritis (PVN) is characterized by an acute vestibular syndrome that mimics acute peripheral vestibular loss. Usually, PVN is caused by brainstem or cerebellar stroke in the territory of the anterior inferior cerebellar artery or the posterior inferior cerebellar artery [1]. Clinical examination is of paramount importance for the detection of PVN as subtle neuro-otologic signs are more sensitive than magnetic resonance imaging (MRI) in the acute phase [2]. Pseudo-vestibular neuritis is not uncommon and it has been estimated that about 25% of patients with an acute vestibular syndrome (AVS) harbor a posterior circulation stroke [1]. In contrast, AVS due to cortical stroke in the distribution of the carotid artery is very rare.
2. Methods We report a patient presenting with PVN due to infarction in the territory of the middle cerebral artery (MCA). Furthermore, a review of similar cases reported in the medical literature was performed. We reviewed the medical literature using PubMed in June 2013 with the search terms “vertigo”, “dizziness”, “ischemia”, “hemorrhage”, “stroke”, “cortex”, and “middle cerebral artery” in various combinations. We also
⁎ Corresponding author. Tel.: +49 30 96283700; fax: +49 30 96283705. E-mail address: [email protected] (M. von Brevern).
http://dx.doi.org/10.1016/j.jns.2014.02.005 0022-510X/© 2014 Elsevier B.V. All rights reserved.
identified articles through searches of reference lists of the articles found with these search terms and our own files. Only cases published in English with detailed description of vestibular symptoms and imaging findings were included in the analysis. 3. Results 3.1. Patient report A 51-year-old woman with a history of migraine without aura awoke at night with constant rotational vertigo [3], oscillopsia, slight nausea and severe imbalance. During that night she also developed habitual migraine headache. The next morning, the vertigo had subsided, but she still felt dizzy [3]. The intense headache did not ameliorate with zolmitriptane but ceased after application of acetylsalicylic acid 500 mg iv. Her medical history was unremarkable except for migraine headaches since age 16 and a slowly progressing bilateral hearing loss with hearing aid devices since 6 months. Besides hormonal contraception she did not take any regular medication. Neurological examination on admission three days after onset of symptoms revealed an AVS with horizontal-rotational spontaneous nystagmus to the right that increased in intensity with Frenzel's glasses. There was no contraversive gaze-evoked nystagmus or skew deviation but the horizontal head impulse test was normal, pointing to a central vestibular syndrome [1,2]. Vertical smooth pursuit eye movements (SP) were not saccadic and horizontal SP was only slightly saccadic to the right as expected when the eyes are moving against the slow component
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of spontaneous nystagmus. Tandem Romberg's test revealed a tendency to fall to the left. Otherwise no neurologic deficit was noticed on admission. Although the patient has never had episodic vertigo before, a tentative diagnosis of vestibular migraine was made. During the following days, she still noticed a mild, dull, bilateral headache, dizziness, impaired concentration, slowed mental activity and fatigue. Video-oculography performed four days after onset of vertigo showed only minor horizontal nystagmus to the right (slow phase velocity b 3°/s). Bithermal caloric irrigation was normal. Audiometry documented a moderate, symmetrical, sensorineural hearing loss involving predominantly high frequencies. Subjective visual vertical with binocular viewing was pathologic with a deviation to the right by 3.2° (normal b 2.0°). Cerebral MRI performed six days after onset of vertigo yielded an infarction of the posterior fraction of the right MCA involving the posterior insula, superior temporal gyrus, middle temporal gyrus, supramarginal gyrus, angular gyrus and inferior parietal lobule (Fig. 1). The cardiovascular diagnostic workup (including Holter's ECG, transthoracic and transesophageal echocardiography, extra- and intracranial doppler/duplex ultrasound) revealed no source of embolus. Electroencephalography and examination of cerebrospinal fluid was normal. The hypercoagulable screen (activated protein C resistance, antiphospholipid antibodies) was negative. We conclude that the infarction was cryptogenic, probably due to embolism or thrombosis of the MCA. After all, only migraine without aura and hormonal contraception could be identified as vascular risk factors. Clinical re-examination after identification of the stroke yielded a minor defect in the left lower visual field and moderate difficulties imitating finger positions (interlocking finger test), indicating parietal lobe dysfunction. Neuropsychological testing revealed attentive deficits, decelerated information processing and the tendency to neglect visual stimuli. At this time, spontaneous nystagmus, gaze-evoked nystagmus
or head-shaking nystagmus was not present and smooth pursuit was normal. 3.2. Review of the literature We identified detailed case reports on nine patients with AVS due to hemispheric stroke [4–10]. Results of cerebral imaging with MRI were available for all patients. In the following, we report on findings in ten patients including our patient described above (mean age 58 years, seven female and three male). Except for one patient with a small hemorrhage in the left medial temporal gyrus [6] all patients had ischemic stroke in the territory of the MCA. The etiology of ischemia was cardioembolic in one patient [4], dissection of the internal carotid artery in another patient [7], stenosis of the internal carotid artery in two patients [5] and remained unknown in five patients. Seven patients experienced vertigo and three patients had acute dizziness (Table 1). No patient had pure positional vertigo but vertigo was most pronounced in the upright position in two patients [4,6] and increased with head movements in another patient [8]. Five patients reported nausea and two vomited. The duration of vertigo and dizziness was one day to a few weeks in most patients except for one patient with vertigo lasting less than 30 min. This patient was drowsy due to cerebral infarction and minor vestibular symptoms may have been missed in the further course [7]. One patient subsequently experienced short attacks of spontaneous vertigo lasting 1 or 2 min after resolution of the initial episode of vertigo [9]. Unsteadiness was reported in seven patients, in most of them gait and stance was severely affected. All patients except for two [5,8] had additional neurologic symptoms or signs besides AVS. The most common concurrent symptoms were sensory loss (n = 4) and mild hemiparesis (n = 3). In two patients onset of vertigo was preceded by other neurologic symptoms [9,10].
Fig. 1. MRI showing an infarction in the distribution of the right middle cerebral artery involving the temporal and parietal lobe and the posterior insular cortex. (a–c) Axial DWI sequences. (d–f) Coronal FLAIR sequences.
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Table 1 Characteristics of AVS due to stroke in the territory of the middle cerebral artery in 10 patients. Reference
Sex, age (y)
Vestibular syndrome
Neuro-otological findings
Concurrent symptoms/ findings
Duration of vestibular symptoms
Lesion
Ahn et al. [9]
F, 51
Acute rotatory vertigo, no nausea
Word finding difficulty
Few weeks
Naganuma et al. [8]
F, 65
No
1 day a
Nakajiama et al. [10]
M, 57
Hemiparesis left
Not reported
Infarction of the left anterior and posterior insula and small parts of frontal operculum Left parietal infarction involving supramarginal lobe Infarction of the right putamen
Present case
F, 52
Acute rotatory vertigo, no nausea Acute vertigo and truncal ataxia, vomiting Acute rotatory vertigo, severe unsteadiness, nausea
Contraversive horizontal spontaneous nystagmus, HIT and calorics normal Contraversive horizontal spontaneous nystagmus Contraversive horizontal spontaneous nystagmus Ipsiversive horizontal spontaneous nystagmus, HIT and calorics normal, SVV tilted ipsiversive to lesion
Mild limb kinetic apraxia and mild hemianopia
Days
Debette et al. [7]
M, 51
Acute rotatory vertigo, nausea
Ipsiversive gaze evoked nystagmus
b30 min
Boiten et al. [6]
F, 53
Acute rotatory vertigo, severe unsteadiness, nausea
Brandt et al. [4]
F, 30
Cereda et al. [5]
F, 73
Cereda et al. [5]
M, 69
Cereda et al. [5]
F, 75
Acute rotatory vertigo, unsteadiness, nausea and vomiting Case 1: acute nonrotatory vertigo, severe unsteadiness, no nausea Case 2: acute dizziness, severe unsteadiness, no nausea Case 4: acute dizziness, unsteadiness
No nystagmus, SVV tilted contraversive to lesion, calorics normal No nystagmus, lateropulsion contraversive to lesion, SVV tilted contraversive to lesion No nystagmus
Left sensorimotor hemiparesis, right Horner syndrome, drowsiness Slurring of speech
No nystagmus
No nystagmus
Few weeks
Infarction of the posterior insula, superior and middle temporal gyrus, supramarginal gyrus, angular gyrus and inferior parietal lobule Infarction in the territories of the right MCA and AChA involving the insular cortex, superior temporal gyrus and retroinsular areas Hemorrhage of the left medial temporal gyrus
Minimal weakness and sensory loss left side
1 week
Infarction of the right posterior insula and right parietal cortex
No
Days
Right posterior insula infarction
Right hemisensory deficit, fluent aphasia, dysarthria Sensory deficit of left arm with somatoparaphrenia
Days
Left posterior insula infarction
2 weeks
Right posterior insula infarction
AChA anterior choroidal artery; MCA middle cerebral artery; SVV subjective visual vertical; HIT head impulse test. a Recurrence of vertigo after one week.
Clinical examination yielded horizontal spontaneous nystagmus in four patients. In three of them the direction of spontaneous nystagmus was contraversive to the cerebral lesion, while in our patient spontaneous nystagmus was ipsiversive. Another patient showed transient ipsilesional gaze-evoked nystagmus. Caloric stimulation was performed in three patients and was normal in all of them. Measurement of the subjective visual vertical was reported in three patients with a pathologic tilt contraversive to the lesion in two patients and towards the lesion in one patient. The lesion was located in the right hemisphere in six patients and in the left hemisphere in four. The posterior insula was involved in most patients (n = 7). In four patients, retroinsular areas including the supramarginal gyrus were affected. In those three patients without a lesion of the posterior insula, MRI identified involvement of the middle temporal gyrus, the supramarginal gyrus and the putamen. 4. Discussion The review of the literature including our patient identifies a small series of ten well-documented patients with acute vertigo and dizziness as the prevailing symptom due to ischemia or hemorrhage in the territory of the MCA. Interestingly, six of these patients were below the age of sixty. In most patients, vertigo and dizziness with severe unsteadiness lasted at least several days and was thus similar to the time course of vestibular neuritis. How could the central origin of the AVS in these patients be differentiated from a benign vestibular disorder? Most patients showed additional neurologic signs which were, however, absent in two patients and too mild to be initially noticed in another one. What leads to the suspicion of a central vestibular disorder in the three patients with minor or absent signs of central involvement? In our patient central vestibular dysfunction was suspected based on the combination of a horizontal spontaneous nystagmus and a normal head impulse test and in
another patient the absence of spontaneous nystagmus was not compatible with vestibular neuritis [5]. The reason to perform cerebral imaging in the third patient was not communicated [8]. Four patients showed spontaneous horizontal nystagmus at the time of presentation. The direction of spontaneous nystagmus was contraversive to the cerebral lesion in three of them and ipsiversive in another patient. Generally, spontaneous nystagmus in AVS is regarded as a sign of a vestibular tone imbalance at the level of the peripheral vestibular organ, the vestibular nerve or vestibular structures in the brainstem and cerebellum. It is almost a doctrine that acute hemispheric lesions do not cause spontaneous nystagmus. Rarely, lesions of the temporoparieto-occipital cortex have been described presenting with ipsiversive spontaneous nystagmus and impaired SP more to the lesion side. This “pursuit-paretic nystagmus” has been ascribed to an imbalance in horizontal SP tone due to lesions involving the human homologues of medial temporal (MT) and middle superior temporal (MST) areas [11,12]. In humans, the homologues of these visual motion-sensitive areas have been identified most commonly within the ascending limb of the inferior temporal sulcus [13]. This area was involved in our patient but not in the other patients identified in our literature search. Furthermore, SP was not impaired in any patient reported with AVS due to supratentorial stroke. Thus, it is not likely that an imbalance in horizontal SP tone is the cause of spontaneous nystagmus in these patients. Occasionally, spontaneous nystagmus has been documented in patients with epileptic seizures involving mainly the temporoparietal–occipital region [14,15], presenting either with or without vertigo. Vestibular symptoms of epileptic origin have been ascribed most often to epileptogenic foci in the temporal lobe, the temporoparietal junction, and the parietal lobe [16–18]. More rarely, epileptic vertigo originates from the frontal lobe [19]. As a rule, epileptic nystagmus almost always beats contraversive to the epileptogenic focus [14,15]. Theoretically, spontaneous nystagmus in patients with an acute cortical lesion could be due to focal epileptic
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activity but the long duration of nystagmus and vestibular symptoms, the time course with acute onset and gradual recovery, and the absence of electroencephalographic abnormalities renders this hypothesis unlikely. In almost all reported patients with acute vertigo due to cortical stroke, cerebral imaging has shown involvement of the temporoparietal junction. This observation fits well into our current knowledge of cortical vestibular areas. Animal experiments have shown that there is no primary vestibular cortex that obtains projections exclusively from vestibular afferents. Instead, several multimodal areas have been identified which integrate vestibular, visual, and somatosensory signals [20]. Similarly, in humans a widely distributed multisensory vestibular cortical network has been identified by cortical electrical stimulation, by clinical studies in patients with acute cortical lesions, and by functional imaging studies [21]. These areas include the posterior insula and retroinsular regions, the superior temporal gyrus, the inferior parietal lobule, an area deep within the intraparietal sulcus, the postcentral and precentral gyrus, the anterior insula and the adjacent inferior frontal gyrus. The temporoparietal junction is considered the core region within this network [20–22]. Vestibular cortical areas are very frequently affected by ischemia and the insular cortex is involved in almost half of patients with nonlacunar ischemic MCA territory strokes [23]. Why vertigo is rare in hemispheric stroke is unclear. Whereas the vestibular neurophysiology of brainstem and cerebellar structures is well known, the principles of vestibular information processing at the cortical level are poorly understood. Neurophysiological studies in humans indicate that trisynaptic vestibular–cortical pathways project to the temporoparietal area ipsilaterally but also to the contralateral hemisphere [24]. On the level of single cells, experiments with primates have shown that the response properties of vestibular cortex neurons in response to motion are similar to those in the vestibular nuclei [25]. However, we lack knowledge how vestibular information is further processed in the cortex to understand why vertigo is comparatively rare in acute hemispheric lesions. Probably, protection and resilience against vertigo in hemispheric stroke is partly provided by parallel processing in the vestibular cortical network. Nonetheless, the prevalence of vertigo as defined as the sensation of self-motion when no self-motion is occurring [3] might be more common in hemispheric stroke than traditionally thought. In a prospective study including 112 patients with supratentorial stroke 13% of patients reported an illusionary movement sensation. These patients did not describe a spinning illusion but typically a rolling or rocking of the visual scene. Almost all patients had right hemispheric stroke but no preponderance of a specific lesion location could be elaborated [26]. Our case series does not suggest a strong hemispheric dominance for AVS in acute supratentorial stroke but the sample is too small to draw a definite conclusion. Functional imaging studies have indicated that vestibular information is predominantly processed in the non-dominant hemisphere [27]. Pathologic tilt of the subjective visual vertical seems to be more common in the right than in left hemispheric lesions [28,29]. Similarly, case series of patients with vestibular epilepsy observed that the majority of patients have right-sided epileptic discharges [18] and vestibular sensation can be induced from more anatomical sites in the right hemisphere than in the left hemisphere [22]. In contrast, preponderance for one hemisphere has not been described in epileptic nystagmus [15]. There is another vestibular symptom much more common than vertigo in MCA infarction, namely deviation of the subjective visual vertical (SVV). Abnormal tilt of the SVV – reflecting central imbalance of otolith input – occurs in one third to half of patients with infarction of the MCA in the acute stage [28,29]. Tilts of SVV are more commonly contraversive than ipsiversive to the lesion and occur both with right-sided and leftsided lesions [29]. The overlapping area of infarction centers on the insular cortex, but also involves other areas such as the inferior frontal gyrus and in right sided lesions the superior temporal gyrus [29]. Not surprisingly, all three patients identified in our review in whom measurement of the SVV has been performed showed a pathologic deviation of the SVV.
In conclusion, stroke in the territory of the MCA may occasionally cause an AVS including vertigo, nausea and unsteadiness. In most patients with an AVS due to supratentorial stroke the parietotemporal junction is involved. The presence of spontaneous nystagmus does not prove an infratentorial or peripheral vestibular lesion but can also occur in hemispheric stroke. Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest. References [1] Tarnutzer AA, Berkowitz AL, Robinson KA, Hsieh YH, Newman-Toker DE. Does my dizzy patient have a stroke? A systematic review of bedside diagnosis in acute vestibular syndrome. CMAJ 2011;183:E971–92. [2] Kattah JC, Talkad AV, Wang DZ, Hsiang YH, Newman-Toker DE. HINTS to diagnose stroke in the acute vestibular syndrome. Three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging. Stroke 2009;40:3504–10. [3] Bisdorff A, von Brevern M, Lempert T, Newman-Toker DE. Classification of vestibular symptoms: towards an international classification of vestibular disorders. J Vestib Res 2009;19:1–13. [4] Brandt T, Bötzel K, Yousry T, Dieterich M, Schulze S. Rotational vertigo in embolic stroke of the vestibular and auditory cortices. Neurology 1995;45:42–4. [5] Cereda C, Ghika J, Maeder P, Bogousslavsky J. Strokes restricted to the insular cortex. Neurology 2002;59:1950–5. [6] Boiten J, Wilmink J, Kingma H. Acute rotatory vertigo caused by a small haemorrhage of the vestibular cortex. J Neurol Neurosurg Psychiatry 2003;74:388–94. [7] Debette S, Michelin E, Hénon H, Leys D. Transient rotatory vertigo as the initial symptom of a middle cerebral artery territory infarct involving the insula. Cerebrovasc Dis 2003;16:97–8. [8] Naganuma M, Inatomi Y, Yonehara T, Fujioka S, Hashimoto Y, Hirano T, et al. Rotational vertigo associated with parietal cortical infarction. J Neurol Sci 2006;246:159–61. [9] Ahn BY, Bae JW, Kim DH, Choi KD, Kim HJ, Kim EJ. Pseudovestibular neuritis associated with isolated insular stroke. J Neurol 2010;257:1570–2. [10] Nakajiama M, Inatomi Y, Yonehara T, Hirano T, Uchino M. Rotational vertigo associated with putaminal infarction. J Stroke Cerebrovasc Dis 2012;21:e9-10. [11] Sharpe JA, Lo AW, Rabinovitch HE. Control of saccadic and smooth pursuit systems after cerebral hemidecortication. Brain 1979;102:387–403. [12] Choi SY, Kim Y, Oh SW, Jeong SH, Kim JS. Pursuit-paretic and epileptic nystagmus in MELAS. J Neuro-Ophthalmol 2012;32:135–8. [13] Dumoulin SO, Bittar RG, Kabani NJ, Baker CL, Le Goualher G, Bruce Pike G, et al. A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 2000;10:454–63. [14] Kaplan PW, Tusa RJ. Neurophysiologic and clinical correlations of epileptic nystagmus. Neurology 1993;43:2508–14. [15] Weber YG, Roesche J, Lerche H. Epileptic nystagmus. Two case reports, clinical and pathophysiological review of the literature. J Neurol 2006;253:767–71. [16] Salanova V, Andermann F, Rasmussen T, Olivier A, Quesney LF. Parietal lobe epilepsy: clinical manifestation and outcome in 82 patients treated surgically between 1929 and 1988. Brain 1995;118:607–27. [17] Fried I, Spencer DD, Spencer SS. The anatomy of epileptic aura: focal pathology and surgical outcome. J Neurosurg 1995;83:60–6. [18] Hewett R, Guye M, Gavaret M, Bartolomie F. Benign temporo-parietal–occipital junction epilepsy with vestibular disturbance: an underrecognized form of epilepsy? Epilepsy Res 2011;21:412–6. [19] Kluge M, Beyenburg S, Fernández G, Elger CE. Epileptic vertigo: evidence for vestibular representation in human frontal cortex. Neurology 2000;55:1906–8. [20] Guldin WO, Grüsser OJ. Is there a vestibular cortex? Trends Neurosci 1998;21:254–9. [21] Dieterich M, Brandt T. Functional brain imaging of peripheral and central vestibular disorders. Brain 2008;131:2538–52. [22] Kahane P, Hoffmann D, Minotti L, Berthoz A. Reappraisal of the human vestibular cortex by cortical electrical stimulation study. Ann Neurol 2003;54:615–24. [23] Fink JN, Selim MH, Kumar S, Voetsch B, Fong WC, Caplan LR. Insular cortex infarction in acute middle cerebral artery territory stroke: predictor of stroke severity and vascular lesion. Arch Neurol 2005;62:1081–5. [24] de Waele C, Baudonnière PM, Lepecq JC, Tran Ba Huy P, Vidal PP. Vestibular projections in the human cortex. Exp Brain Res 2001;141:541–51. [25] Liu SL, Dickman D, Angelaki DE. Response dynamics and tilt versus translation discrimination in parietoinsular vestibular cortex. Cereb Cortex 2011;21:563–73. [26] Anagnostou E, Spengos K, Vassilopoulou S, Paraskevas GP, Vassilopoulos D. Incidence of rotational vertigo in supratentorial stroke: a prospective analysis of 112 consecutive patients. J Neurol Sci 2010;290:33–6. [27] Dieterich M, Bense S, Lutz S, Stephan T, Bartenstein P, Brandt T. Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 2003;13:994–1007. [28] Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403–12. [29] Baier B, Suchan J, Karnath HO, Dieterich M. Neural correlates of disturbed perception of verticality. Neurology 2012;78:728–35.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Acute vertigo due to hemispheric stroke A case report and comprehensive review of the literature Michael von Brevern ⁎, Sina Süßmilch, Daniel Zeise Department of Neurology, Park-Klinik Weissensee, Schönstrasse 80, 13086 Berlin, Germany
a r t i c l e
i n f o
Article history: Received 6 September 2013 Received in revised form 7 January 2014 Accepted 5 February 2014 Available online 14 February 2014 Keywords: Vertigo Stroke Middle cerebral artery Vestibular cortex Acute vestibular syndrome Nystagmus
a b s t r a c t Acute cortical lesions rarely cause vertigo. We report a 51-year-old patient presenting with an acute vestibular syndrome including spontaneous vertigo and nystagmus, lateropulsion and nausea due to middle cerebral artery infarction. The central origin of the acute vestibular syndrome was revealed by a normal head impulse test. A comprehensive literature review on patients with hemispheric stroke manifesting with acute vertigo is provided. Typically, patients with an acute vestibular syndrome due to cortical stroke have involvement of the temporoparietal junction. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Pseudo-vestibular neuritis (PVN) is characterized by an acute vestibular syndrome that mimics acute peripheral vestibular loss. Usually, PVN is caused by brainstem or cerebellar stroke in the territory of the anterior inferior cerebellar artery or the posterior inferior cerebellar artery [1]. Clinical examination is of paramount importance for the detection of PVN as subtle neuro-otologic signs are more sensitive than magnetic resonance imaging (MRI) in the acute phase [2]. Pseudo-vestibular neuritis is not uncommon and it has been estimated that about 25% of patients with an acute vestibular syndrome (AVS) harbor a posterior circulation stroke [1]. In contrast, AVS due to cortical stroke in the distribution of the carotid artery is very rare.
2. Methods We report a patient presenting with PVN due to infarction in the territory of the middle cerebral artery (MCA). Furthermore, a review of similar cases reported in the medical literature was performed. We reviewed the medical literature using PubMed in June 2013 with the search terms “vertigo”, “dizziness”, “ischemia”, “hemorrhage”, “stroke”, “cortex”, and “middle cerebral artery” in various combinations. We also
⁎ Corresponding author. Tel.: +49 30 96283700; fax: +49 30 96283705. E-mail address: [email protected] (M. von Brevern).
http://dx.doi.org/10.1016/j.jns.2014.02.005 0022-510X/© 2014 Elsevier B.V. All rights reserved.
identified articles through searches of reference lists of the articles found with these search terms and our own files. Only cases published in English with detailed description of vestibular symptoms and imaging findings were included in the analysis. 3. Results 3.1. Patient report A 51-year-old woman with a history of migraine without aura awoke at night with constant rotational vertigo [3], oscillopsia, slight nausea and severe imbalance. During that night she also developed habitual migraine headache. The next morning, the vertigo had subsided, but she still felt dizzy [3]. The intense headache did not ameliorate with zolmitriptane but ceased after application of acetylsalicylic acid 500 mg iv. Her medical history was unremarkable except for migraine headaches since age 16 and a slowly progressing bilateral hearing loss with hearing aid devices since 6 months. Besides hormonal contraception she did not take any regular medication. Neurological examination on admission three days after onset of symptoms revealed an AVS with horizontal-rotational spontaneous nystagmus to the right that increased in intensity with Frenzel's glasses. There was no contraversive gaze-evoked nystagmus or skew deviation but the horizontal head impulse test was normal, pointing to a central vestibular syndrome [1,2]. Vertical smooth pursuit eye movements (SP) were not saccadic and horizontal SP was only slightly saccadic to the right as expected when the eyes are moving against the slow component
154
M. von Brevern et al. / Journal of the Neurological Sciences 339 (2014) 153–156
of spontaneous nystagmus. Tandem Romberg's test revealed a tendency to fall to the left. Otherwise no neurologic deficit was noticed on admission. Although the patient has never had episodic vertigo before, a tentative diagnosis of vestibular migraine was made. During the following days, she still noticed a mild, dull, bilateral headache, dizziness, impaired concentration, slowed mental activity and fatigue. Video-oculography performed four days after onset of vertigo showed only minor horizontal nystagmus to the right (slow phase velocity b 3°/s). Bithermal caloric irrigation was normal. Audiometry documented a moderate, symmetrical, sensorineural hearing loss involving predominantly high frequencies. Subjective visual vertical with binocular viewing was pathologic with a deviation to the right by 3.2° (normal b 2.0°). Cerebral MRI performed six days after onset of vertigo yielded an infarction of the posterior fraction of the right MCA involving the posterior insula, superior temporal gyrus, middle temporal gyrus, supramarginal gyrus, angular gyrus and inferior parietal lobule (Fig. 1). The cardiovascular diagnostic workup (including Holter's ECG, transthoracic and transesophageal echocardiography, extra- and intracranial doppler/duplex ultrasound) revealed no source of embolus. Electroencephalography and examination of cerebrospinal fluid was normal. The hypercoagulable screen (activated protein C resistance, antiphospholipid antibodies) was negative. We conclude that the infarction was cryptogenic, probably due to embolism or thrombosis of the MCA. After all, only migraine without aura and hormonal contraception could be identified as vascular risk factors. Clinical re-examination after identification of the stroke yielded a minor defect in the left lower visual field and moderate difficulties imitating finger positions (interlocking finger test), indicating parietal lobe dysfunction. Neuropsychological testing revealed attentive deficits, decelerated information processing and the tendency to neglect visual stimuli. At this time, spontaneous nystagmus, gaze-evoked nystagmus
or head-shaking nystagmus was not present and smooth pursuit was normal. 3.2. Review of the literature We identified detailed case reports on nine patients with AVS due to hemispheric stroke [4–10]. Results of cerebral imaging with MRI were available for all patients. In the following, we report on findings in ten patients including our patient described above (mean age 58 years, seven female and three male). Except for one patient with a small hemorrhage in the left medial temporal gyrus [6] all patients had ischemic stroke in the territory of the MCA. The etiology of ischemia was cardioembolic in one patient [4], dissection of the internal carotid artery in another patient [7], stenosis of the internal carotid artery in two patients [5] and remained unknown in five patients. Seven patients experienced vertigo and three patients had acute dizziness (Table 1). No patient had pure positional vertigo but vertigo was most pronounced in the upright position in two patients [4,6] and increased with head movements in another patient [8]. Five patients reported nausea and two vomited. The duration of vertigo and dizziness was one day to a few weeks in most patients except for one patient with vertigo lasting less than 30 min. This patient was drowsy due to cerebral infarction and minor vestibular symptoms may have been missed in the further course [7]. One patient subsequently experienced short attacks of spontaneous vertigo lasting 1 or 2 min after resolution of the initial episode of vertigo [9]. Unsteadiness was reported in seven patients, in most of them gait and stance was severely affected. All patients except for two [5,8] had additional neurologic symptoms or signs besides AVS. The most common concurrent symptoms were sensory loss (n = 4) and mild hemiparesis (n = 3). In two patients onset of vertigo was preceded by other neurologic symptoms [9,10].
Fig. 1. MRI showing an infarction in the distribution of the right middle cerebral artery involving the temporal and parietal lobe and the posterior insular cortex. (a–c) Axial DWI sequences. (d–f) Coronal FLAIR sequences.
M. von Brevern et al. / Journal of the Neurological Sciences 339 (2014) 153–156
155
Table 1 Characteristics of AVS due to stroke in the territory of the middle cerebral artery in 10 patients. Reference
Sex, age (y)
Vestibular syndrome
Neuro-otological findings
Concurrent symptoms/ findings
Duration of vestibular symptoms
Lesion
Ahn et al. [9]
F, 51
Acute rotatory vertigo, no nausea
Word finding difficulty
Few weeks
Naganuma et al. [8]
F, 65
No
1 day a
Nakajiama et al. [10]
M, 57
Hemiparesis left
Not reported
Infarction of the left anterior and posterior insula and small parts of frontal operculum Left parietal infarction involving supramarginal lobe Infarction of the right putamen
Present case
F, 52
Acute rotatory vertigo, no nausea Acute vertigo and truncal ataxia, vomiting Acute rotatory vertigo, severe unsteadiness, nausea
Contraversive horizontal spontaneous nystagmus, HIT and calorics normal Contraversive horizontal spontaneous nystagmus Contraversive horizontal spontaneous nystagmus Ipsiversive horizontal spontaneous nystagmus, HIT and calorics normal, SVV tilted ipsiversive to lesion
Mild limb kinetic apraxia and mild hemianopia
Days
Debette et al. [7]
M, 51
Acute rotatory vertigo, nausea
Ipsiversive gaze evoked nystagmus
b30 min
Boiten et al. [6]
F, 53
Acute rotatory vertigo, severe unsteadiness, nausea
Brandt et al. [4]
F, 30
Cereda et al. [5]
F, 73
Cereda et al. [5]
M, 69
Cereda et al. [5]
F, 75
Acute rotatory vertigo, unsteadiness, nausea and vomiting Case 1: acute nonrotatory vertigo, severe unsteadiness, no nausea Case 2: acute dizziness, severe unsteadiness, no nausea Case 4: acute dizziness, unsteadiness
No nystagmus, SVV tilted contraversive to lesion, calorics normal No nystagmus, lateropulsion contraversive to lesion, SVV tilted contraversive to lesion No nystagmus
Left sensorimotor hemiparesis, right Horner syndrome, drowsiness Slurring of speech
No nystagmus
No nystagmus
Few weeks
Infarction of the posterior insula, superior and middle temporal gyrus, supramarginal gyrus, angular gyrus and inferior parietal lobule Infarction in the territories of the right MCA and AChA involving the insular cortex, superior temporal gyrus and retroinsular areas Hemorrhage of the left medial temporal gyrus
Minimal weakness and sensory loss left side
1 week
Infarction of the right posterior insula and right parietal cortex
No
Days
Right posterior insula infarction
Right hemisensory deficit, fluent aphasia, dysarthria Sensory deficit of left arm with somatoparaphrenia
Days
Left posterior insula infarction
2 weeks
Right posterior insula infarction
AChA anterior choroidal artery; MCA middle cerebral artery; SVV subjective visual vertical; HIT head impulse test. a Recurrence of vertigo after one week.
Clinical examination yielded horizontal spontaneous nystagmus in four patients. In three of them the direction of spontaneous nystagmus was contraversive to the cerebral lesion, while in our patient spontaneous nystagmus was ipsiversive. Another patient showed transient ipsilesional gaze-evoked nystagmus. Caloric stimulation was performed in three patients and was normal in all of them. Measurement of the subjective visual vertical was reported in three patients with a pathologic tilt contraversive to the lesion in two patients and towards the lesion in one patient. The lesion was located in the right hemisphere in six patients and in the left hemisphere in four. The posterior insula was involved in most patients (n = 7). In four patients, retroinsular areas including the supramarginal gyrus were affected. In those three patients without a lesion of the posterior insula, MRI identified involvement of the middle temporal gyrus, the supramarginal gyrus and the putamen. 4. Discussion The review of the literature including our patient identifies a small series of ten well-documented patients with acute vertigo and dizziness as the prevailing symptom due to ischemia or hemorrhage in the territory of the MCA. Interestingly, six of these patients were below the age of sixty. In most patients, vertigo and dizziness with severe unsteadiness lasted at least several days and was thus similar to the time course of vestibular neuritis. How could the central origin of the AVS in these patients be differentiated from a benign vestibular disorder? Most patients showed additional neurologic signs which were, however, absent in two patients and too mild to be initially noticed in another one. What leads to the suspicion of a central vestibular disorder in the three patients with minor or absent signs of central involvement? In our patient central vestibular dysfunction was suspected based on the combination of a horizontal spontaneous nystagmus and a normal head impulse test and in
another patient the absence of spontaneous nystagmus was not compatible with vestibular neuritis [5]. The reason to perform cerebral imaging in the third patient was not communicated [8]. Four patients showed spontaneous horizontal nystagmus at the time of presentation. The direction of spontaneous nystagmus was contraversive to the cerebral lesion in three of them and ipsiversive in another patient. Generally, spontaneous nystagmus in AVS is regarded as a sign of a vestibular tone imbalance at the level of the peripheral vestibular organ, the vestibular nerve or vestibular structures in the brainstem and cerebellum. It is almost a doctrine that acute hemispheric lesions do not cause spontaneous nystagmus. Rarely, lesions of the temporoparieto-occipital cortex have been described presenting with ipsiversive spontaneous nystagmus and impaired SP more to the lesion side. This “pursuit-paretic nystagmus” has been ascribed to an imbalance in horizontal SP tone due to lesions involving the human homologues of medial temporal (MT) and middle superior temporal (MST) areas [11,12]. In humans, the homologues of these visual motion-sensitive areas have been identified most commonly within the ascending limb of the inferior temporal sulcus [13]. This area was involved in our patient but not in the other patients identified in our literature search. Furthermore, SP was not impaired in any patient reported with AVS due to supratentorial stroke. Thus, it is not likely that an imbalance in horizontal SP tone is the cause of spontaneous nystagmus in these patients. Occasionally, spontaneous nystagmus has been documented in patients with epileptic seizures involving mainly the temporoparietal–occipital region [14,15], presenting either with or without vertigo. Vestibular symptoms of epileptic origin have been ascribed most often to epileptogenic foci in the temporal lobe, the temporoparietal junction, and the parietal lobe [16–18]. More rarely, epileptic vertigo originates from the frontal lobe [19]. As a rule, epileptic nystagmus almost always beats contraversive to the epileptogenic focus [14,15]. Theoretically, spontaneous nystagmus in patients with an acute cortical lesion could be due to focal epileptic
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activity but the long duration of nystagmus and vestibular symptoms, the time course with acute onset and gradual recovery, and the absence of electroencephalographic abnormalities renders this hypothesis unlikely. In almost all reported patients with acute vertigo due to cortical stroke, cerebral imaging has shown involvement of the temporoparietal junction. This observation fits well into our current knowledge of cortical vestibular areas. Animal experiments have shown that there is no primary vestibular cortex that obtains projections exclusively from vestibular afferents. Instead, several multimodal areas have been identified which integrate vestibular, visual, and somatosensory signals [20]. Similarly, in humans a widely distributed multisensory vestibular cortical network has been identified by cortical electrical stimulation, by clinical studies in patients with acute cortical lesions, and by functional imaging studies [21]. These areas include the posterior insula and retroinsular regions, the superior temporal gyrus, the inferior parietal lobule, an area deep within the intraparietal sulcus, the postcentral and precentral gyrus, the anterior insula and the adjacent inferior frontal gyrus. The temporoparietal junction is considered the core region within this network [20–22]. Vestibular cortical areas are very frequently affected by ischemia and the insular cortex is involved in almost half of patients with nonlacunar ischemic MCA territory strokes [23]. Why vertigo is rare in hemispheric stroke is unclear. Whereas the vestibular neurophysiology of brainstem and cerebellar structures is well known, the principles of vestibular information processing at the cortical level are poorly understood. Neurophysiological studies in humans indicate that trisynaptic vestibular–cortical pathways project to the temporoparietal area ipsilaterally but also to the contralateral hemisphere [24]. On the level of single cells, experiments with primates have shown that the response properties of vestibular cortex neurons in response to motion are similar to those in the vestibular nuclei [25]. However, we lack knowledge how vestibular information is further processed in the cortex to understand why vertigo is comparatively rare in acute hemispheric lesions. Probably, protection and resilience against vertigo in hemispheric stroke is partly provided by parallel processing in the vestibular cortical network. Nonetheless, the prevalence of vertigo as defined as the sensation of self-motion when no self-motion is occurring [3] might be more common in hemispheric stroke than traditionally thought. In a prospective study including 112 patients with supratentorial stroke 13% of patients reported an illusionary movement sensation. These patients did not describe a spinning illusion but typically a rolling or rocking of the visual scene. Almost all patients had right hemispheric stroke but no preponderance of a specific lesion location could be elaborated [26]. Our case series does not suggest a strong hemispheric dominance for AVS in acute supratentorial stroke but the sample is too small to draw a definite conclusion. Functional imaging studies have indicated that vestibular information is predominantly processed in the non-dominant hemisphere [27]. Pathologic tilt of the subjective visual vertical seems to be more common in the right than in left hemispheric lesions [28,29]. Similarly, case series of patients with vestibular epilepsy observed that the majority of patients have right-sided epileptic discharges [18] and vestibular sensation can be induced from more anatomical sites in the right hemisphere than in the left hemisphere [22]. In contrast, preponderance for one hemisphere has not been described in epileptic nystagmus [15]. There is another vestibular symptom much more common than vertigo in MCA infarction, namely deviation of the subjective visual vertical (SVV). Abnormal tilt of the SVV – reflecting central imbalance of otolith input – occurs in one third to half of patients with infarction of the MCA in the acute stage [28,29]. Tilts of SVV are more commonly contraversive than ipsiversive to the lesion and occur both with right-sided and leftsided lesions [29]. The overlapping area of infarction centers on the insular cortex, but also involves other areas such as the inferior frontal gyrus and in right sided lesions the superior temporal gyrus [29]. Not surprisingly, all three patients identified in our review in whom measurement of the SVV has been performed showed a pathologic deviation of the SVV.
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