Clinical and Electrographic Findings in Epileptic Vertigo and Dizziness: a Systematic Review

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Year: 2015

Clinical and electrographic findings in epileptic vertigo and dizziness: A systematic review

Tarnutzer, A A ; Lee, S H ; Robinson, K A ; Kaplan, P W ; Newman-Toker, D E

Abstract: OBJECTIVE Seizures can cause vestibular symptoms, even without obvious epileptic features. We sought to characterize epileptic vertigo or dizziness (EVD) to improve differentiation from nonepileptic causes, particularly when vestibular symptoms are the sole manifestation. METHODS We conducted a systematic review with electronic (Medline) and manual search for English-language studies (1955- 2014). Two independent reviewers selected studies. Study/patient characteristics were abstracted. We defined 3 study population types: (1) seizures, some experiencing vertigo/dizziness (disease cohort); (2) vertigo/dizziness, some due to seizures (symptom cohort); (3) vertigo/dizziness due to seizures in all patients (EVD-only cohort). RESULTS We identified 84 studies describing 11,354 patients (disease cohort = 8,129; symptom cohort = 2,965; EVD-only cohort = 260). Among 1,055 EVD patients in whom a distinction could be made, non-isolated EVD was present in 8.5%, isolated EVD in 0.8%. Thorough diagnostic workups (ictal EEG, vestibular testing, and brain MRI to exclude other causes) were rare (<0.1%). Ictal EEG was reported in 487 (4.3%), formal neuro-otologic assessment in 1,107 (9.7%). Localized EEG abnormalities (n = 350) were most frequently temporal (79.8%) and uncommonly parietal (11.8%). Duration of episodic vestibular symptoms varied, but was very brief (<30 seconds) in 69.6% of isolated EVD and 6.9% of non-isolated EVD. CONCLUSIONS Non-isolated EVD is much more prevalent than isolated EVD, which appears to be rare. Diagnostic evaluations for EVD are often incomplete. EVD is primarily associated with temporal lobe seizures; whether this reflects greater epidemiologic prevalence of temporal lobe seizures or a tighter association with dizziness/vertigo presentations than with other brain regions remains unknown. Consistent with clinical wisdom, isolated EVD spells often last just seconds, although many patients experience longer spells.

DOI: https://doi.org/10.1212/WNL.0000000000001474

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-110942 Journal Article Published Version

Originally published at: Tarnutzer, A A; Lee, S H; Robinson, K A; Kaplan, P W; Newman-Toker, D E (2015). Clinical and electrographic findings in epileptic vertigo and dizziness: A systematic review. Neurology, 84(15):1595- 1604. DOI: https://doi.org/10.1212/WNL.0000000000001474 VIEWS & REVIEWS Clinical and electrographic findings in epileptic vertigo and dizziness A systematic review

Alexander A. Tarnutzer, ABSTRACT MD Objective: Seizures can cause vestibular symptoms, even without obvious epileptic features. We Seung-Han Lee, MD sought to characterize epileptic vertigo or dizziness (EVD) to improve differentiation from none- Karen A. Robinson, PhD pileptic causes, particularly when vestibular symptoms are the sole manifestation. Peter W. Kaplan, MD Methods: We conducted a systematic review with electronic (Medline) and manual search for David E. Newman-Toker, English-language studies (1955–2014). Two independent reviewers selected studies. Study/patient MD, PhD characteristics were abstracted. We defined 3 study population types: (1) seizures, some experiencing vertigo/dizziness (disease cohort); (2) vertigo/dizziness, some due to seizures (symptom cohort); (3) vertigo/dizziness due to seizures in all patients (EVD-only cohort). Correspondence to Dr. Tarnutzer: Results: We identified 84 studies describing 11,354 patients (disease cohort 5 8,129; symptom [email protected] cohort 5 2,965; EVD-only cohort 5 260). Among 1,055 EVD patients in whom a distinction could be made, non-isolated EVD was present in 8.5%, isolated EVD in 0.8%. Thorough diagnostic workups (ictal EEG, vestibular testing, and brain MRI to exclude other causes) were rare (,0.1%). Ictal EEG was reported in 487 (4.3%), formal neuro-otologic assessment in 1,107 (9.7%). Localized EEG abnormalities (n 5 350) were most frequently temporal (79.8%) and uncommonly parietal (11.8%). Duration of episodic vestibular symptoms varied, but was very brief (,30 seconds) in 69.6% of isolated EVD and 6.9% of non-isolated EVD. Conclusions: Non-isolated EVD is much more prevalent than isolated EVD, which appears to be rare. Diagnostic evaluations for EVD are often incomplete. EVD is primarily associated with temporal lobe seizures; whether this reflects greater epidemiologic prevalence of temporal lobe seizures or a tighter association with dizziness/vertigo presentations than with other brain regions remains unknown. Consistent with clinical wisdom, isolated EVD spells often last just seconds, although many patients experience longer spells. Neurology® 2015;84:1595–1604

GLOSSARY AED 5 antiepileptic drug; EVD 5 epileptic vertigo or dizziness; i-EVD 5 isolated epileptic vertigo or dizziness; ni-EVD 5 non- isolated epileptic vertigo or dizziness.

Vertigo (defined as a sensation of self-motion when no self-motion is occurring or as the sensation of distorted self-motion during an otherwise normal head movement)1 ordizziness(definedasa sensation of disturbed or impaired spatial orientation without a false/distorted sense of motion)1 are common symptoms, often reported by patients known to have epileptic seizures. These vestibular symptoms may be related to the seizure itself (i.e., representing an aura symptom), to side effects of antiepileptic drug (AED) therapy, or may be linked to a second, comorbid nonepileptic disorder (e.g., vestibular migraine). Episodic vestibular symptoms deemed to result directly from focal, intermittent epileptic discharges have been variously known as epileptic vertigo,2 vestibular epilepsy,3 vestibular seizures,4 vertiginous seizures,4–6 or epilepsia tornado.7 In this article, we use the more inclusive term epileptic vertigo or dizziness (EVD). Seminal work by Penfield and Jasper8 established the scientific basis for understanding the pathophysiology of EVD. By means of surface electrical stimulation, they elicited illusionary Supplemental data at Neurology.org From the Department of Neurology (A.A.T.), University Hospital Zurich and the University of Zurich, Switzerland; the Department of Neurology (S.-H.L.), Chonnam National University Medical School, Gwangju, South Korea; the Departments of Medicine (K.A.R.), Neurology (D.E.N.-T.), and Otolaryngology Head & Neck Surgery (D.E.N.-T.), The Johns Hopkins University School of Medicine; and the Department of Neurology (P.W.K.), Johns Hopkins Bayview Medical Center, Baltimore, MD. Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

© 2015 American Academy of Neurology 1595 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. transient sensations of rotation, translation, or parietal14 areas, suggesting either processing of undirected motion in their patients, mapping vestibular-related input across large cortical re- the extent of the vestibular cortex and demon- gions15 or spread of excitation to or from nearby strating that seizures cause vertigo/dizziness regions. Lesion studies in humans provide addi- because they lead to hyperactivity in vestibular tional insights into the extent of cortical network cortical areas. They described EVD during processing of vestibular/graviceptive inputs. Insu- both temporal and parietal lobe stimulation. lar and parietal lesions dominate the literature on These cortical areas were confirmed by Kahane vertigo/dizziness from stroke,16 including the et al.,9 reporting vestibular sensations after seminal study of Brandt et al.,17 reporting shifts electrical stimulation centered around a lateral in perceived verticality in lesions affecting the cortical temporo-parietal area, known as the posterior insula. temporo-peri-Sylvian vestibular cortex. Less The differential diagnosis for isolated epi- frequently, Kahane et al. found vestibular sen- sodic vertigo/dizziness is broad and cuts across sations by stimulating within the occipital, medical specialties, including neurology (vestibu- frontal, and insular cortex. Congruent but lar migraine, TIA, seizures), otolaryngology (Me- somewhat more expansive than these experi- niere disease, vestibular paroxysmia), internal mentally derived results, epileptic discharges medicine (hypoglycemia), cardiology (arrhyth- on ictal EEG in symptomatic EVD were indi- mia), and psychiatry (panic attacks), so knowing vidually localized to frontal,2 frontotemporal,10 when (or when not) to consider EVD would be temporal,11,12 temporo-parieto-occipital,13 and helpful. When obvious seizure-related symptoms or signs (e.g., a generalized convulsion) accom- pany vestibular symptoms, EVD is readily rec- Table 1 Rating of EEG and vestibular assessment and strength of association between seizures and vertigo/dizziness ognized. EVD causing isolated vestibular symptoms was reported,2,18,19 but there is lim- Quality of EEG assessment ited information about prevalence and clinical High characteristics (e.g., accompanying symptoms, a Ictal (symptomatic ) EEG recordings duration) that might help distinguish it from Medium nonepileptic causes. Interictal EEG recordings We performed a systematic review of studies Low reporting on (1) vestibular symptoms in seizure No EEG recordings notedb patients (disease cohort), (2) seizures in vestibu- Quality of vestibular evaluation lar patients (symptom cohort), and (3) clinical Complete details in reports of patients with EVD (EVD- Vestibular evaluation by a subspecialist neuro-otologist or specific description of vestibular only cohort). The aim of this work was to better testing that includes a measure of vestibulo-ocular reflex function (e.g., caloric tests or head impulse tests) and a search for nystagmus with suppression of visual fixation (e.g., Frenzel characterize the prevalence of non-isolated EVD goggles) and positional tests (ni-EVD) and isolated EVD (i-EVD) in adults Partial and children, seizure localization, and episode Any mention of neuro-otologic testing short of complete duration. None

No mention of any testing for vestibular disorders METHODS A MEDLINE search was performed (April Strength of association between seizures and dizziness/vertigo 2014) to identify articles reporting on EVD using terms related to seizures/epilepsy and vertigo/dizziness. Both retro- High spective and prospective case series and single case reports Ictal EEG demonstrating epileptiform discharges at the time of vertigo/dizziness were eligible. Studies sought for reported on the differential Medium diagnosis of dizzy patients or on aura symptoms in patients with a given type of epilepsy. Specific search terms and inclu- Episodic vertigo/dizziness with an ictal (nonvestibular symptoms) or interictal EEG demonstrating epileptiform discharges sion/exclusion criteria can be found in appendix e-1 on the Neurology® Web site at Neurology.org. We identified 1,137 Low electronic citations for screening and included 84 studies Episodic vertigo/dizziness with a clinical diagnosis of seizures/epilepsy (no confirmation by (appendix e-1; flow chart). When extracting the data from the EEG or no EEG obtainedc) selected studies, we assessed the type of the study, whether the a Ictal EEG recordings may have been taken during nonvestibular seizures. vestibular symptoms were isolated or accompanied by other b If the report was unclear, the quality of EEG assessment was recorded as low. seizure symptoms, the duration of EVD episodes, and EEG c If the report was unclear, the strength of association was coded as low. findings. In all EVD patients, we rated the quality of EEG and

1596 Neurology 84 April 14, 2015 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. retrieved where EEG recordings were available and were coded as Table 2 Characterization of study sample temporal, parietal, occipital, or frontal in origin. If the reported seizure location was linked to more than one of these areas Adults Children Age NR Total (e.g., frontotemporal), a count was given to each lobe for cal- Study cohorts culating the relative frequency of discharges in different lobes.

Disease cohort (seizures) 2,162 70 5,897 8,129 RESULTS Demographic information. Eighty-four studies Symptom cohort (dizziness/vertigo) 920 596 1,449 2,965 reporting on 11,354 patients matched the inclusion cri- EVD-only cohort 50 21 189 260 teria (appendix e-2, table e-1, and table e-2). The major- All cohorts pooled 3,132 687 7,535 11,354 ity of these 84 studies were retrospective case series (n 5 Imaging 52, 61.9%) or single cases (n 5 26, 31.0%) (table e-1). Brain MRI 486 26 372 884 The remaining 6 studies were prospective (n 5 5, 6.0%) 5 Brain CT 78 40 296 414 or ambispective (n 1, 1.2%) case series. Retrospective case series were the most frequent study type both in the SPECT 32 1 0 33 disease (81.1%, study size 5 1–1,563 patients) and the Modality unclear 0 55 174 229 symptom (83.3%, study size 5 8–907 patients) cohort, All brain imaging pooled 596 122 842 1,560 while prospective case series were rare in either cohort Reported diagnosis in dizzy patientsa,b,c (disease cohort: 8.1%, study size 5 3–1,897; symptom Other disorders 10 25 857 892 cohort: 11.1%, study size 5 70–142). Overall,

Benign paroxysmal positional vertigo 1 10 391 402 71.6% of patients were in the disease cohort, while

Meniere disease 2 3 193 198 26.1% were in the symptom cohort. The remaining 2.3% fulfilled criteria for the EVD-only cohort Psychogenic 13 24 130 167 (table 1). The distribution of adult and pediatric d Migraine 7 85 56 148 patients among the cohorts was distinct: 69% of all Secondary to head trauma 22 104 12 138 adults belonged to the disease cohort; 87% of all Benign paroxysmal vertigo of childhood 095 4 99 children were part of the symptom cohort. Various

Vestibular neuritis 12 20 65 97 other diagnoses were reported in 2,499 patients

Unresolved 15 23 55 93 (table 2).

Various cerebrovascular disorders 3 0 72 75 Diagnostic testing. EEG findings were reported in

Labyrinthitis 153 8 62 50.9% of patients. Surface recordings were available

Cerebellopontine angle tumors 427 4 35 in 50.1%, intracranial recordings in 2.7%. We judged the quality of EEG assessment based on the presence/ Otitis media 10 5 15 30 absence of EEG-documented seizures and clinical Secondary to ototoxic substances 120 8 29 findings during these seizures. A high-quality (ictal) Multiple sclerosis 1 0 20 21 EEG assessment was found in 4.3%, a medium- Meningitis 13 1 5 quality (interictal) EEG assessment in 46.6%. In

Perilymph fistula 14 0 5 49.1%, the electrographic assessment was considered

Delayed endolymphatic hydrops 02 1 3 low quality, and the diagnosis of seizures was made on the clinical history alone (table 3). All diagnoses pooled 104 503 1,892 2,499 Neuroimaging was available in 13.7%, vestibular Abbreviations: EVD 5 epileptic vertigo or dizziness; NR 5 not reported. testing in 26.3% (table 3). In many of these patients, a Seizures are reported separately in tables 4 and 5. results from vestibular testing were not reported and b Complete or partial vestibular evaluation was available from 29 studies. From those, specific diagnoses related to dizziness/vertigo were available in 12 studies (all belonging to only in 4 patients (0.04%) was complete vestibular the symptom cohort). Two other studies provided diagnoses in the dizzy patient only on the testing accompanied by ictal EEG and MRI. level of categories (peripheral-vestibular disorders, central disorders).57,58 The results from these studies are not shown in this table. In addition, 2 patients from the disease cohort and Fraction of patients with ni-EVD and i-EVD. From from the combined cohort each were diagnosed with migraine. 11,354 patients included (disease cohort 5 8,129; c All except 3 of those patients belonged to the symptom cohort. symptom cohort 5 2,965; EVD-only cohort 5 d A diagnosis of migraine (no further distinction among migraine headaches, vestibular migraine, basilar-type migraine, or other) was made in 148 patients; however, the criteria 260), 1,055 patients (9.3%) had EVD, and were applied to obtain a diagnosis of migraine were not specified. From these 148 patients, 147 coded as ni-EVD (n 5 967, 8.5% of total) or had both migraine headaches and episodic dizziness, fulfilling the current international i-EVD (n 5 88, 0.8% of total) (table 4). Of all diagnostic criteria for possible vestibular migraine.59 EVD patients, 64.7% were in the disease cohort, 10.7% were in the symptom cohort. The frequency vestibular assessment and the quality of the association between for diagnosing i-EVD or ni-EVD was about seizures and vertigo/dizziness (table 1). A single expert epileptologist (P.W.K.) assessed all published 2-fold greater for patients in the disease cohort EEG recordings from the included studies for quality to establish (683/8,129, 8.4%) relative to the symptom cohort a definitive diagnosis of EVD. Seizure location and laterality was (113/2,965, 3.8%).

Neurology 84 April 14, 2015 1597 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. by contrast, in the disease cohort, EVD was diag- Table 3 Summary of vestibular and EEG assessment nosed just 1.3-fold more often in children (11/70,

Patients, n 15.7%) than adults (253/2,162, 11.7%).

Adults Children Age NR Total Quality of the association between epilepsy and vertigo/

Quality of EEG assessment dizziness. From all EVD patients, a high-quality association was found in 4.1% (43/1,055), while High (ictal EEG) medium (512/1,055, 48.5%) or low (500/1,055, Disease cohort (IC seizures)a 150 9 314 473 47.4%) quality was noted in the remaining 95.9%. b Symptom cohort (IC vertigo/dizziness) 00 0 0 Published EEG traces from EVD cases (n 5 33) were EVD-only cohortc 77 0 14 reviewed. From the 14 EEG recordings originally rated as 19,20 All cohorts pooled 157 16 314 487 ictal, this was confirmed in 11, while in 2 cases the

Medium (interictal EEG) EEG data presented was only probably consistent with an 21 Disease cohort (IC seizures)a 335 42 4,385 4,762 ongoing seizure and in one case no seizure was depicted. Diagnosis in the remaining 19 cases (interictal EEG Symptom cohort (IC vertigo/dizziness)b 307 124 0 431 changes) was confirmed. EVD-only cohortc 42 14 43 99

All cohorts pooled 684 180 4,428 5,292 Seizure location. Results from ictal/interictal EEG recordings were available in 580 EVD patients (table 5). EEG Low (no EEG) seizure locations (n 5 350) were assigned as described in Disease cohort (IC seizures)a 1,717 19 1,158 2,894 the Methods. Since more than one location was reported b Symptom cohort (IC vertigo/dizziness) 755 472 1,307 2,534 in 73 patients, the total count (n 5 391) exceeded the EVD-only cohortc 1 0 146 147 number of EVD patients with localized EEG changes. All cohorts pooled 2,473 491 2,611 5,575 The most frequent location was temporal (79.8%); pari-

Extent of vestibular assessment etal (11.8%), occipital (5.4%), and frontal (3.1%) seiz-

Complete ures were found in small fractions.

Disease cohort (IC seizures)a 1 0 29 30 Lateralization of focal EEG changes. From the 350

Symptom cohort (IC vertigo/dizziness)b 106 506 400 1,012 EVD cases with localized EEG changes, the side of the EEG focus was reported in 126 (36.0%). Right- EVD-only cohortc 20 15 30 65 hemisphere (n 5 51) and left-hemisphere (n 5 57) All cohorts pooled 127 521 459 1,107 seizure foci occurred with similar frequency (40.5% vs Partial 45.2%, Fisher exact p 5 0.50). In 18 cases, a Disease cohort (IC seizures)a 48 0 0 48 bihemispheric focus was observed. In ni-EVD Symptom cohort (IC vertigo/dizziness)b 160 69 1,596 1,825 (n 5 86; 10 bilateral foci), right- and left-hemisphere 5 EVD-only cohortc 10 0 1 foci had identical frequency (n 38, 44.2% each). For 5 All cohorts pooled 209 69 1,596 1,874 i-EVD (n 40; 8 bilateral foci), left-hemispheric foci were slightly more frequent than right-hemispheric foci None (19 vs 13; 47.5% vs 32.5%, p 5 0.21). a Disease cohort (IC seizures) 4,013 70 3,841 7,924 For cases with information on sidedness of focal Symptom cohort (IC vertigo/dizziness)b 127 1 127 255 EEG changes (n 5 126), we assessed laterality by EVD-only cohortc 29 6 159 194 seizure location (total of 163 locations recorded).

All cohorts pooled 4,169 77 4,127 8,373 There were clinically meaningful but not statistically significant differences in sidedness based on the seizure Abbreviations: EVD 5 epileptic vertigo or dizziness; IC 5 inclusion criteria; NR 5 not reported. location (right % [n] vs left % [n]): (1) temporal (37.8% a This cohort contains patients from studies that had a diagnosis of seizures as IC and the [37] vs 44.9% [44], p 5 0.35); (2) parietal (59.0% [23] study reported on vertigo or dizziness. vs 35.9% [14], p 5 0.06); (3) occipital (62.5% [10] vs b This cohort contains patients from studies that had dizziness or vertigo as IC and the 25% [4], p 5 0.06); and (4) frontal (30.0% [3] vs study reported on seizures. 5 c This cohort includes patients from studies that required both the presence of vertigo or 70.0% [7], p 0.18). dizziness and seizures as inclusion criteria. Duration of EVD and effect of treatment. Specific numbers on EVD duration were available in 108 patients In the study sample, the overall fraction of EVD in (table 5). Comparing i-EVD and ni-EVD cases, brief children (73/687, 10.6%) and adults (300/3,132, spell duration (#30 seconds) was noted in a much 9.6%) was similar, but the distribution was heteroge- larger fraction in i-EVD cases than ni-EVD cases neous across study cohorts. In the symptom cohort, (69.6% vs 6.9%, p , 0.001). EVD was diagnosed nearly 9-fold more often in chil- Effect of treatment with various AEDs was reported dren (52/596, 8.7%) than in adults (9/920, 1.0%); in 110 patients (10.4%), with 90.0% considered

1598 Neurology 84 April 14, 2015 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. Table 4 Distribution of patients with EVD with regards to strength of association between EVD and EEG

Diagnosis of non-isolated EVD, Diagnosis of isolated EVD, All diagnoses of EVD, strength of strength of association,a n strength of association, n association, n

High Medium Low All High Medium Low All High Medium Low All

Symptom cohort (n 5 2,965)

Adults 04 5900 0004 59

Children 0 38 11 49 0 3 0 3 0 41 11 52

Age NR 0 3 48 51 0 1 0 1 0 4 48 52

% of cohort 0.0 1.5 2.2 3.7 0.0 0.1 0.0 0.1 0.0 1.7 2.2 3.8

Disease cohort (n 5 8,129)

Adults 13 69 155 237 3 13 0 16 16 82 155 253

Children 34 31010 0144 311

Age NR 13 262 131 406 0 13 0 13 13 275 131 419

% of cohort 0.4 4.1 3.6 8.0 0.0 0.3 0.0 0.4 0.4 4.4 3.6 8.4

EVD-only cohort (n 5 260)

Adults 228 13125 07433 138

Children 34 0730 0364 010

Age NR 0 21 146 167 0 44 0 44 0 65 146 211

% of cohort 1.9 20.4 56.6 78.8 1.9 18.8 0.0 20.8 3.8 39.2 56.5 99.6

All cohorts pooled

No. identified cases (all ages pooled) 34 433 500 967 9 79 0 88 43 512 500 1,055

% of all cohorts 0.3 3.8 4.4 8.5 0.1 0.7 0.0 0.8 0.4 4.5 4.4 9.3

Abbreviations: EVD 5 epileptic vertigo or dizziness; NR 5 not reported. a Strength of association between EVD and EEG: high (dizziness or vertigo during EEG-documented seizure), medium (episodic dizziness or vertigo in a patient with EEG-confirmed seizures), low (episodic dizziness or vertigo in a patient with clinical diagnosis of seizures—may have had also normal EEG), all (high, medium, and low combined).

responders. Among responders with details on drug the clinical intuition that EVD is uncommon, and iso- treatment (n 5 54), phenytoin (n 5 16), carbamazepine lated EVD is rare (although it is probably more preva- (n 5 12), and valproate (n 5 5) were applied most often lent in children presenting vestibular symptoms than (table e-2). in adults). It further confirms that, when EVD is isolated, episodes are most often very brief (lasting sec- Type of vestibular and accompanying seizure symptoms. onds), although our results also suggest that longer A majority of studies did not provide definitions of the episodes (lasting minutes) are not uncommon. This terms used to describe the vestibular spells (9,506 pa- study suggests 2 other findings that are somewhat unex- tients, 83.7%), including vertigo or vertiginous pected: (1) epileptic foci causing EVD are much more (6,302, 55.5%), dizziness (93, 0.8%), and vertigo or likely to be temporal than parietal, and (2) they are dizziness (3,114, 27.4%). Definitions for vertigo and equally likely to originate in the right and left hemi- dizziness were provided in 9 studies (vertigo 5 304 spheres. These results may assist clinicians in determin- patients [2.7%], dizziness 5 2 patients [0.2%]) ing whether their patients presenting vertigo or dizziness (appendix e-1). In 3 studies (1,539, 13.6%), the 4 should be evaluated for seizures and whether those with categories brought forward by Drachman and Hart22 epilepsy require further vestibular assessment. (dizziness vs vertigo vs lightheadedness vs faintness) were used. From the 1,055 EVD patients, defini- EVD prevalence in adults and children. We cannot draw tions for vertigo (n 5 135, 12.8%) and dizziness strong inferences about the incidence or prevalence of (n 5 2, 0.2%) were provided in 137. Information EVD in the general population, but our data offer some about other seizure symptoms/signs occurring in the insights into the epidemiology of EVD. First, ni-EVD same epileptic attack could be retrieved from 171 appears to be uncommon in both symptom (3.7%) and EVD patients (table 6). disease (8.0%) cohorts; since some of these might have actually been missed comorbid vestibular disorders (see DISCUSSION Our systematic review of EVD in the below), and studies not reporting vertigo/dizziness in medical literature offers quantitative confirmation for epilepsy or epilepsy in dizziness (i.e., with lower

Neurology 84 April 14, 2015 1599 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. Table 5 EEG findings in patients with ni-EVD or i-EVD and duration of dizzy spells

ni-EVD, n (%) i-EVD, n (%) All EVD, n (%)

EEG findings in EVD

No. of EEGs in EVD (% all EVD cases)a

All EEGs 459 (47.5) 75 (85.2) 580 (55.0)

EEGs with localized pathologiesb 291 (30.1) 43 (48.9) 350 (33.2)

EEG seizure location (% all EEGs)

Localized EEG changes 291 (63.4) 43 (57.3) 350 (60.3)

Generalized seizures 14 (3.1) 2 (2.7) 28 (4.8)

No seizure location 134 (29.2) 29 (38.7) 163 (28.1)

Seizure location looked for but not found 20 (4.4) 1 (1.3) 39 (6.7)

Breakdown EEGs with localized changes (% all localized EEGs)

All counts with localized changesc 322 (100) 53 (100) 391 (100)

Temporal 256 (79.5) 40 (75.5) 312 (79.8)

Parietal 41 (12.7) 5 (9.4) 46 (11.8)

Occipital 16 (5.0) 5 (9.4) 21 (5.4)

Frontal 9 (2.8) 3 (5.7) 12 (3.1)

Duration of dizzy spells in EVDd

<1min 4 (12.5) 38 (82.6) 52 (46.8)

£30 s 2 (6.3) 32 (69.6) 34 (30.6)

30–60 s 2 (6.3) 4 (8.7) 6 (5.4)

No further separation possible 0 (0.0) 2 (4.3) 12 (10.8)

>1min 13 (40.6) 8 (17.4) 44 (39.6)

Variable duratione 15 (46.9) 0 (0.0) 15 (13.5)

All 32 (100) 46 (100) 111 (100)

Abbreviations: EVD 5 epileptic vertigo or dizziness; i-EVD 5 isolated epileptic vertigo or dizziness; ni-EVD 5 non-isolated epileptic vertigo or dizziness. a In one study reporting on both ni-EVD and i-EVD, no information could be retrieved on which EEG changes applied to the ni-EVD and which applied to the i-EVD cases.60 These 46 cases (33 ni-EVD; 13 i-EVD) are therefore excluded from this part of the data analysis. b In the study by Erkwoh,60 16 cases with EVD of mostly (13/16) temporal lobe origin could not be separated into ni-EVD and i-EVD; therefore these cases are not included in the subgroup (ni-EVD and i-EVD) analysis. c In 32 cases, epileptic discharges were localized to more than one of the 4 principal lobes; in these cases, one count was given to each area (this included temporo-parietal, temporo-occipital, frontotemporal, parieto-occipital, and temporo- parieto-occipital locations). Accordingly, the total number of counts exceeded the number of patients with EVD by 41. d Duration of episodes in individual subjects ranging from seconds to minutes. We noted reports of EVD lasting “several hours” in 8 patients from a single study.47 e A distinction between ni-EVD and i-EVD was possible only in part of the patients. Only these patients are reported in the ni-EVD and i-EVD columns, while all patients are considered in the “all” column.

prevalence) would not have been captured by our both symptom and disease cohorts. Again, because search, these numbers are probably plausible upper our search strategy was skewed toward studies seeking limits for the frequency of EVD in dizziness and in EVD in dizziness, these estimates probably represent epilepsy. The higher prevalence of ni-EVD in the plausible upper bounds, although we cannot be sure disease cohort makes intuitive sense (i.e., known that more rigorous diagnostic ascertainment would seizure patients are more likely to have epileptic not have identified some missed cases. dizziness than patients evaluated for dizziness). Third, as suggested previously, EVD may be more Second, i-EVD is probably rare in both dizziness common in children than in adults.24 This claim is (0.1%) and in epilepsy (0.4%). It is not surprising supported by our finding of a higher frequency of that i-EVD would be much less common than ni- EVD in children relative to adults in our symptom EVD. Although this difference could be attributed cohort (ratio children:adults, 8.7:1), which suggests to diagnostic ascertainment bias,23 it seems plausible that EVD probably accounts for a greater fraction of that i-EVD is, indeed, substantially less common in vertigo/dizziness presentations in children than adults

1600 Neurology 84 April 14, 2015 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. about equally likely to produce vertigo/dizziness in chil- Table 6 Accompanying seizure symptoms in EVD patientsa,b dren and adults (although this finding must be viewed Sensory phenomena 133 cautiously given the small number of children relative to

Cephalic sensations (pressure, heat, pain) 61 adults in this cohort: 70 vs 2,162). These findings sug-

Visual hallucinations 32 gest that it is not a biological interaction with age (e.g., seizures in a young brain are more likely to produce Auditory hallucinations 23 dizziness), but an epidemiologic one. In other words, Simple (tinnitus, sounds, dysacusis) 19 the proportion of dizziness cases due to EVD is prob- Complex (music, voices) 4 ably higher in children than adults based on different Somatosensory, excluding cephalic sensations 16 population distributions of etiologies for dizziness in

Olfactory hallucinations 1 children vs adults. This could be because seizures are

Motor symptoms 120 more common in children, other causes (e.g., benign paroxysmal positional vertigo, stroke) are more com- Focal motor seizures 28 mon in adults, or a combination of both. Generalized tonic-clonic seizures 25

Arrest (speech, activity) 22 Seizure location and lateralization. Acriticalroleof Falls 14 temporal areas in self-motion perception has been Automatisms 12 previously proposed based on functional MRI 25 Head deviation 8 studies during caloric irrigation, case reports with focal lesions within the temporal gyrus,26,27 Nystagmus 8 and transcranial magnetic stimulation over the superior Verbal (screaming, vocalization) 3 temporal gyrus.28 Illusionary sensations of self-motion Disturbances of consciousness 104 can be elicited by cortical electrical stimulation within Transient loss of consciousness 45 a fairly large area including temporal and parietal lobes, Emotional (fear, anxiety, agitation) 16 but also, less frequently, occipital and frontal lobes,8 and

Emergence of an idea 15 may include sensations of rotation in different planes, 9 Loss of contact 11 translations, and indefinable body motion. The high frequency of temporal over parietal lobe seizure Dysmnestic (e.g., déjà vu) 6 location in our review does not reflect the distribution Conscious confusion 5 noted in these electrical stimulation studies and current Aphasia 4 expert opinion. Potentially, this discrepancy is a result of Disturbance of body image 2 the overall higher prevalence of temporal lobe seizures 29 Autonomic/visceral phenomena 57 compared to parietal lobe seizures in epileptic patients

Vomiting 18 and as a result, EVD is more often associated with a temporal than a parietal location on epidemiologic Nausea 12 rather than biological grounds. Malaise/weakness 8 Regardless, based on the distribution of seizure lo- Epigastric (rising sensation) 6 cations observed here, symptoms and signs of tempo- Pallor 5 ral lobe origin (e.g., rising epigastric sensations, Thermoregulatory 5 auditory hallucinations, emotional/dysmnestic phe-

Cardiovascular 2 nomena) should be sought in patients with suspected EVD. However, temporal lobe seizures may be diffi- Pulmonary 1 cult to diagnose clinically and by standard surface Abbreviation: EVD 5 epileptic vertigo or dizziness; i-EVD 5 isolated epileptic vertigo or EEG,30,31 with invasive recordings offering improved 5 dizziness; ni-EVD non-isolated epileptic vertigo or dizziness. 32,33 a A total of 411 seizure symptoms were retrieved from 171 EVD patients (166 with ni-EVD spatial resolution and increased sensitivity. From and 5 with i-EVD, where nystagmus was the only sign besides the symptom of vertigo/ our 580 EVD patients with EEG available, only a dizziness); therefore some patients had more than one seizure symptom in one or several small fraction underwent intracranial EEG record- groups, leading to several counts. ings. This probably suggests that, clinically, some pa- b Note that only symptoms accompanying vertigo/dizziness, i.e., occurring during the same episode, were considered and that in some studies information about symptoms was tients with temporal lobe EVD remain undiagnosed abstracted and therefore not available on the level of individual patients. because of a false-negative surface EEG. Previously, a right-hemisphere dominance for (or at least that EVD is a more frequent focus of EVD had been proposed,34 which is a sensible diagnostic inquiry and publication in pediatric pop- hypothesis, given the right hemisphere’s predominant ulations). For the disease cohort, EVD was diagnosed role in spatial perception. In our dataset, however, no with roughly equal frequency (ratio children:adults, statistically significant differences were found. Left- 1.1:1), indicating that seizures, when present, are hemisphere foci were slightly more common overall

Neurology 84 April 14, 2015 1601 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. in this sample. There was, however, some heteroge- an ictal etiology in responders.18,34 However, treatment neity based on the focus of seizure activity: a slight response information was available in only 10% and, left-sided predominance was noted for temporal lobe for example, successful treatment strategies for vestib- seizures, but a relatively large (and borderline statisti- ular paroxysmia and vestibular migraine include AEDs cally significant) right-sided predominance was noted such as carbamazepine, valproate, and topiramate.40,42 in the subgroups with parietal and occipital lobe Thus, response to AED treatment in patients with epi- seizures. sodic vertigo/dizziness does not prove an epileptic origin of the spells. Duration of EVD: From few seconds to several minutes. Knowledge about the duration of vertigo/dizziness is Quality of EEG and vestibular and imaging assessment. A important to narrow the differential diagnosis.35 Tradi- thorough diagnostic workup (brain MRI plus complete tionally, EVD has been considered to last a few seconds vestibular testing plus ictal EEG) was rarely performed. only,18 and consequently, the clinician may have dis- In the disease cohort, only 9/34 case series placed empha- missed a diagnosis of EVD if spells exceeded this dura- sis on vestibular symptoms in study design,3,6,34,43–48 tion. In this review, we found brief spells (#1minute) which may explain why vestibular testing was infrequent in 46.3% of cases. The remaining patients presented in this cohort. Likewise, in the symptom cohort, seizures with spells lasting several minutes (a duration typically were just one of many differential diagnostic considera- associated with vestibular migraine,36 Meniere disease,37 tions, explaining a low rate of obtaining EEG. or episodic ataxia38) or had spells of variable duration. Incomplete workups in the disease cohort might Based on our data, dizzy spells exceeding a few seconds have led to overdiagnosis of EVD (misattribution of duration and lasting up to several minutes should still dizziness from another cause to known epilepsy caus- be considered as potentially epileptic. For the i-EVD ing other symptoms); likewise, incomplete workups cases, the dictum that epileptogenic vertigo/dizziness in the symptom cohort might have led to underdiag- lasts a few seconds held true with a duration of #30 nosis of EVD. Of note, the lifetime prevalence of seconds in 69.6%, suggesting that the clinical presen- migraine headaches is about 2.4 times greater in pa- tation of seizures (isolated vertigo/dizziness vs with tients with diagnosed epilepsy than in their relatives other seizure-like symptoms) may be linked to the without epilepsy,49 and the lifetime prevalence of duration of the dizzy spells. It is biologically plausible migraine in the epileptic population is 8%– that short bursts of epileptic activity would be more 24%.49–51 Likewise, in migraine headache patients, likely to produce short-lived, isolated symptoms, the lifetime prevalence of epilepsy is 1%–17%,50 while longer runs of epileptic activity would be more which is clearly higher than that of epilepsy in the likely to be sustained and spread, causing longer, general population (0.6%–1.5%).52 This nonchance nonisolated episodes of EVD. association may have led to diagnostic misclassifica- Interestingly, almost all cases with EVD localized to tion of vestibular migraine as EVD or vice versa. the temporal lobe (in which spell duration was pro- Epileptic nystagmus. From all EVD patients identified, vided) were in the range of few seconds to less than only 1% presented with both EVD and epileptic nystag- 1 minute, while the few EVD cases with nontemporal mus. This rate may be falsely low as, in most EVD pa- location lasted longer. This could indicate that EVD in tients, seizures were not observed by a physician and temporal lobe seizures is associated with especially brief eyewitness reports of nystagmus are usually not available. dizzy spells. Spontaneous spells lasting seconds are also The cortical areas associated with seizure activity leading typical in vestibular paroxysmia,39 a condition known to epileptic nystagmus spread across temporal, parietal, to be exquisitely carbamazepine-responsive,40 so some and occipital lobes and are presumably related to the con- such patients might readily be confused for i-EVD or trol of smooth-pursuit or saccadic eye movements.53 vice versa, including in our series, where the quality of These seizure locations partially overlap with the vestibular assessments was generally low. Whether a mostly temporal locations for EVD in our systematic high frequency of attacks per day (as seen in some review. However, reviews in the literature collecting patients with vestibular paroxysmia)40 excludes i-EVD cases of epileptic nystagmus report rates of associated is unknown; the reports we reviewed described patients episodic vertigo/dizziness of only 5%–7%.54–56 This with daily or more frequent spells in only 2 cases.10,41 dissociation suggests that the cortical areas eliciting Patients with suspected vestibular paroxysmia should epileptic nystagmus and EVD are activated at the same probably be assessed by EEG to exclude the possibility time by an epileptic attack in only a minority of cases. If of i-EVD as an alternative cause for brief paroxysms the clinician therefore witnesses a seizure presenting with before treatment with carbamazepine. EVD, it is unlikely that he or she will detect nystagmus High rate of AED treatment response. We found response and vice versa. rates to AED treatment in EVD of 90%. Some have EVD is primarily associated with temporal lobe suggested this be used as a diagnostic test to point to seizures and we found ni-EVD is more common than

1602 Neurology 84 April 14, 2015 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. i-EVD; i-EVD appears to be rare. Consistent with clin- 7. Ahmed I. Epilepsia tornado. J Kans Med Soc 1980;81: ical wisdom, i-EVD spells often last just seconds, 466–467. although many patients experience longer spells. Epilep- 8. Penfield W, Jasper H. Epilepsy and the Functional Anat- omy of the Human Brain. Boston: Little, Brown; 1954. tic nystagmus is an infrequent accompaniment, despite 9. Kahane P, Hoffmann D, Minotti L, Berthoz A. Reap- its apparent similarity. Prospective diagnostic studies in praisal of the human vestibular cortex by cortical electrical unselected symptom or disease cohorts would be stimulation study. Ann Neurol 2003;54:615–624. required to confirm and refine these estimates further, 10. Nicita F, Papetti L, Spalice A, et al. Epileptic nystagmus: which are based largely on retrospective case series data. description of a pediatric case with EEG correlation and In the meantime, clinicians should consider EVD when SPECT findings. J Neurol Sci 2010;298:127–131. assessing patients with dizziness/vertigo, particularly 11. Garcia-Herrero D, Fernandez-Torre JL, Barrasa J, Calleja J, Pascual J. Abdominal epilepsy in an adolescent with bilateral children with very brief episodes or when other suspi- perisylvian polymicrogyria. Epilepsia 1998;39:1370–1374. cious symptoms are present. 12. Bartolomei F, Regis J, Donnet A, Gastaut JL. Development of focal chronic epilepsy following focal status epilepticus in AUTHOR CONTRIBUTIONS adult patients. Neurophysiol Clin 1999;29:271–276. Dr. Tarnutzer conceived of the study, performed the literature search, reviewed 13. Erbayat Altay E, Serdaroglu A, Gucuyener K, Bilir E, identified manuscripts and selected matching inclusion criteria, performed the Karabacak NI, Thio LL. Rotational vestibular epilepsy from statistical analysis, drafted and critically reviewed the manuscript, and approved the temporo-parieto-occipital junction. Neurology 2005;65: the final version of the manuscript. Dr. Lee reviewed identified manuscripts and – selected matching inclusion criteria, critically reviewed and edited the manu- 1675 1676. script, and approved the final version of the manuscript. Dr. Robinson per- 14. Beun AM, Beintema DJ, Binnie CD, Debets RM, formed the literature search, critically reviewed and edited the manuscript, Overweg J, Van Heycop ten Ham MW. Epileptic nystag- and approved the final version of the manuscript. Dr. Kaplan reviewed identi- mus. Epilepsia 1984;25:609–614. fied EEG traces, critically reviewed and edited the manuscript, and approved 15. Hewett R, Bartolomei F. Epilepsy and the cortical vestib- the final version of the manuscript. Dr. Newman-Toker conceived of the study, ular system: tales of dizziness and recent concepts. Front critically reviewed and edited the manuscript, and approved the final version of Integr Neurosci 2013;7:73. the manuscript. 16. Zhou Y, Lee SH, Mantokoudis G, et al. Vertigo and dizziness in anterior circulation cerebrovascular disease: a sys- ACKNOWLEDGMENT tematic review. Neurology 2014;82(suppl):P3.092. The authors thank Ali Saber Tehrani for support in obtaining the original 17. Brandt T, Dieterich M, Danek A. Vestibular cortex lesions publications of the studies included here. affect the perception of verticality. Ann Neurol 1994;35: 403–412. STUDY FUNDING 18. Kogeorgos J, Scott DF, Swash M. Epileptic dizziness. Br Dr. Tarnutzer was supported by the Swiss National Science Foundation, – the Betty and David Koetser Foundation for Brain Research, and the Med J 1981;282:687 689. Zurich Center for Integrative Human Physiology, Switzerland. 19. Wiest G, Zimprich F, Prayer D, Czech T, Serles W, Baumgartner C. Vestibular processing in human parame- DISCLOSURE dian precuneus as shown by electrical cortical stimulation. – A. Tarnutzer, S. Lee, and K. Robinson report no disclosures relevant to the Neurology 2004;62:473 475. manuscript. P. Kaplan reports grants from Qatar National Research Founda- 20. Schneider RC, Calhoun HD, Crosby EC. Vertigo and tion (EEG in the ICU for nonconvulsive status epilepticus); personal fees from rotational movement in cortical and subcortical lesions. royalties from Wiley, Demos for books on epilepsy, EEG; honoraria for inter- J Neurol Sci 1968;6:493–516. national congresses and grand rounds from Europe and North America; travel 21. Kim KS, Kim YH, Hwang Y, Kang B, Kim DH, to give lectures from Europe and North America; consulting fee for EEG read- Kwon YS. Epileptic nystagmus and vertigo associated with ing from Eisai Pharma; expert testimony on qEEG in the courtroom; and bilateral temporal and frontal lobe epilepsy. 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1604 Neurology 84 April 14, 2015 ª 2015 American Academy of Neurology. Unauthorized reproduction of this article is prohibited. Clinical and electrographic findings in epileptic vertigo and dizziness: A systematic review Alexander A. Tarnutzer, Seung-Han Lee, Karen A. Robinson, et al. Neurology 2015;84;1595-1604 Published Online before print March 20, 2015 DOI 10.1212/WNL.0000000000001474

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