CASE REPORT

Severe Hemispatial Neglect as a Manifestation of Seizures and Nonconvulsive Status Epilepticus: Utility of Prolonged EEG Monitoring Andrew C. Schomer and Frank W. Drislane

Purpose: Seizures and status epilepticus causing hemispatial neglect syndromes are seldom diagnosed, in part because, without motor signs, EEGs are not performed. Also, nonconvulsive seizures are often intermittent and missed on a single EEG. Two patients had severe neglect syndromes thought due to strokes. Correct diagnosis of epileptic seizures required longer-term EEG monitoring. Methods: Review of clinical history, neurologic examination, imaging, and findings on prolonged EEG monitoring. Results: A patient with a new onset of a profound left neglect had normal strength and language use, with no obvious clinical seizures. A right hemisphere embolic stroke was diagnosed, but MRI with diffusionweighted imaging showed no evidence of ischemia. The initial EEG showed marked right parietal voltage suppression, with subsequent brief electrographic seizures and later, right parietal periodic discharges. The second patient had an earlier right subdural hematoma and focal motor seizures but was admitted with a new neglect syndrome and no clear clinical seizures. Head computed tomography showed no new lesion. EEG showed frequent right parieto–temporal epileptiform discharges and electrographic seizures. The neglect syndromes resolved with anticonvulsant treatment, but in both cases, electrographic seizures were intermittent, and there was no strict correlation between the clinical deficit and EEG manifestations of seizures. Conclusions: Infrequently, the sudden onset of new hemispatial neglect can be caused by nonconvulsive seizures and nonconvulsive status epilepticus, even when there is no weakness and no clear clinical seizure activity. Nonconvulsive status epilepticus can cause primarily perceptual and cognitive syndromes. The correlation between the clinical deficits and seizure activity on the EEG, however, is imprecise. A single EEG may miss seizure activity, and repeated or prolonged EEG recording may be necessary to make the diagnosis. Key Words: Neglect syndrome, Status epilepticus, Nonconvulsive status epilepticus, EEG monitoring. (J Clin Neurophysiol 2015;32: e4–e7)

S

evere hemispatial neglect of sudden onset is most often due to large parietal strokes, usually in the right hemisphere and often associated with a severe left hemiparesis (Caplan, 2009). Several other forms of cognitive or perceptual dysfunction, such as aphasia (Benatar, 2002), can be caused by nonconvulsive seizures and nonconvulsive status epilepticus (NCSE). These seizures and NCSE,

From the Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, U.S.A. Address correspondence and reprint requests to Frank W. Drislane, MD, Department of Neurology, Beth Israel Deaconess Medical Center, Kirstein 479, 330 Brookline Avenue, Boston, MA 02215, U.S.A.; e-mail: fdrislan@ bidmc.harvard.edu. Copyright Ó 2014 by the American Clinical Neurophysiology Society

ISSN: 0736-0258/14/3202-0004

e4

however, may remain undiagnosed because of the lack of motor signs of seizures, and even when suspected, it may be difficult to demonstrate the seizures on EEG because some seizures are not evident in surface leads (Devinsky et al., 1988), and other seizures may fluctuate, such that they are not always present despite the ongoing deficit (Ericson et al., 2011). We report two patients with sudden onset, profound left hemineglect syndromes (without significant motor dysfunction or other deficits) caused by epileptic seizures or NCSE. Both required long-term EEG monitoring to make the diagnosis.

METHODS The history, clinical and neurologic examinations, and radiologic and EEG findings of two patients with left hemispatial neglect syndromes were reviewed. This included examination of the patients by one of the authors (A.C.S.), review of the clinical course in the hospital charts, computed tomography (CT) and MRI scans of the head, and EEG monitoring over several days for each patient, detailing the evolution of EEG abnormalities.

RESULTS Case 1 An 80-year-old left-handed woman was brought to the emergency department by her son after she “sounded confused” on the phone. She was not using her left hand for tasks (despite being left hand dominant), although she could move it. She was not looking to the left. Examination in the emergency department noted a visual neglect of the left side. She had a history of transient ischemic attacks, a patent foramen ovale, and an atrial septal aneurysm. She was admitted to the Medicine service because of a slight troponin elevation. Later, history showed that she had had several episodes of feeling “at a distance” in the previous month. Neurology consultation was sought because of a profound left neglect. She was inattentive to the left visual field and would only bisect lines on the right half of a page. She did not recognize her own left hand held in front of her face; she was unaware of her own deficits. There was very minimal weakness and an upward (“parietal”) drift of the outstretched left arm. Language use and gait were normal. A CT scan of the head showed no ischemic stroke or hemorrhage. Given the presentation and vascular risk factors, the Vascular Neurology/Stroke service consultants made an initial diagnosis of a right middle cerebral artery (MCA) ischemic stroke, with a suspected cardiac source of embolism. Heparin was started. On hospital day 2,

Journal of Clinical Neurophysiology  Volume 32, Number 2, April 2015

Journal of Clinical Neurophysiology  Volume 32, Number 2, April 2015

an MRI scan of the head, however, showed no evidence of ischemia, including on diffusion-weighted imaging. Continuous EEG and video monitoring was started late on hospital day 2 and showed marked suppression of background electrical activity over the right parietal region, and later, 3 brief (10– 25 seconds) electrographic seizures centered in the left temporal and centroparietal regions, with rhythmic right hand twitching seen on video. The left body inattention continued when seizures were no longer evident on the EEG. When treated with 500 mg of levetiracetam (LEV) that morning, there was a quick (reported as “dramatic”) resolution of the neglect. She began attending to stimuli on the left. Later EEGs showed bilateral epileptiform discharges (but not seizures), including in the right parieto–occipital region. The right-sided EEG background suppression persisted (though improving) for the three days of monitoring. All neglect and sensory deficits had resolved and did not recur.

Case 2 A 62-year-old right-handed woman had a serious fall and injury 1 year before admission, resulting in a right subdural hematoma requiring surgical evacuation, and partial right temporal lobectomy. Subsequently, she had right frontal seizures consisting of rhythmic twitching of the left arm and face. Treatment with valproic acid and LEV led to good seizure control, but LEV was stopped when she had mood swings and struck a nurse. Neurology consultation was sought for persistent confusion on transfer from her nursing home.

Neglect, Nonconvulsive Status, and EEG Monitoring

On examination, she was completely inattentive to the entire left visual field (she had had a left superior visual field cut attributed to the temporal lobectomy). When finishing a meal, she had not touched any food on the left side of the plate. She did not respond to auditory cues from the left. She had full and symmetric strength, with no jerking or other abnormal movements. Language was fluent; she could read and write, but she had occasional pauses in her speech. A CT scan of the head showed no change from earlier, showing the old right frontal craniotomy and a right frontal, 6 mm hypodense subdural fluid collection, and right temporal encephalomalacia from the earlier surgery. EEG monitoring later that day showed nearly constant sharp and slow wave discharges at EEG leads P4, T4, and T6, and rightsided periodic lateralized epileptiform discharges (PLEDs), interrupted overnight by runs of a few minutes of rhythmic 2- to 4-Hz sharp waves, consistent with right parieto–temporal electrographic seizures (Fig. 1), all without motor manifestations. Levetiracetam was restarted; phenytoin was initiated. As the patient was lethargic, anticonvulsant doses were increased slowly. Levetiracetam was increased to a total dose of 3 g per day. On the third day, right parietal focal slowing continued, but electrographic seizures had resolved; right-sided PLEDs were slower, approximately 0.5 Hz. Slower periodic discharges, especially in the parietal area, continued for a week. During that time, she was lethargic, often confused, and difficult to examine. Once she could be examined more carefully, she was no longer neglecting the left side. The CT scan remained unchanged, without evidence of a new stroke or other lesion.

FIG. 1. EEG from patient 2 shows right hemisphere periodic lateralized epileptiform discharges progressing to more rapid spike and rhythmic slow wave activity, centering at P4 in the right parietal region. Copyright Ó 2014 by the American Clinical Neurophysiology Society

e5

A. C. Schomer and F. W. Drislane

Journal of Clinical Neurophysiology  Volume 32, Number 2, April 2015

These two patients had presentations and neurologic examinations showing almost exclusively hemispatial neglect syndromes, one with absolutely no motor manifestations at the time and the other with very minimal weakness and even an upward drift. Neither had language deficits. Presentation of patient 1 was thought by the stroke specialists typical (or even “classic”) for a right parietal ischemic stroke, with a strong neglect of the left side of the world as the primary manifestation. She was even started on anticoagulation for a presumed cardiac source of embolism (for which she had several risk factors). On the initial EEG, the profound voltage suppression on the right correlated with the left neglect. The first electrographic seizures seen were on the left side (the “wrong side”), but epileptiform discharges were bilateral. On the third day, when continuous EEG showed evidence of seizures, she improved markedly and quickly on receiving an antiepileptic drug (AED), with a dramatic response in the neglect. At no time, there was evidence of a stroke or other nonepileptic cause of the neglect, indicating that epileptic seizures, prolonged enough to constitute NCSE, were the cause of the neglect syndrome. There was no significant neurologic deficit other than the neglect. No clear etiology of the seizures was found. There was no sign of infection at any time. It was speculated that an episode of poor perfusion (on presentation) combined with old “small vessel disease” to cause the seizures. Patient 2 also had a dramatic neglect syndrome, very similar to that of a right parietal stroke. She had a history of earlier focal motor seizures but absolutely no motor manifestations of seizures during the current illness or admission. She had PLEDs in the right parieto–temporal region at the time of the neglect, and brief electrographic seizures were seen intermittently. Treatment with AEDs decreased the frequency of epileptiform discharges. The neglect cleared only after several days, but there was no new lesion on scans or other disease process found to explain the neglect or the improvement. Complete resolution of the neglect syndrome could be attributed to treatment with AEDs alone, making it most likely to be “ictal” or epileptic in origin. EEG in both cases showed right hemisphere epileptiform discharges, or PLEDs, or electrographic seizures (most nonconvulsive), but while the neglect persisted, seizures were intermittent and not always present, at least as evident on surface electrodes.

DISCUSSION Nonconvulsive status epilepticus has protean manifestations. Without clonic limb movements or other motor phenomena that provide a clue to epileptic seizures, nonconvulsive seizures and NCSE are often very difficult to diagnose or even suspect (Kaplan, 1996; Manford and Shorvon, 1992). Focal NCSE is even harder to diagnose because non-motor focal neurologic deficits are usually attributed to focal lesions and processes such as strokes, tumors, and migraine. Generalized NCSE is often manifested by poor responsiveness or abnormal behavior (Kaplan, 2002; Thomas and Snead, 2008). Focal NCSE may cause a focal or regional neurologic deficit, such as an ictal aphasia (Benatar, 2002; Ericson et al., 2011; Kirshner et al., 1995; Knight and Cooper, 1986), hemianopia (Barry et al., 1985; Shaw et al., 2012), or sensory deficits (Manford and Shorvon, 1992) as the primary manifestation. Often, these episodes present with clinical manifestations suggestive of a stroke, even after thorough history, neurologic examination, a single EEG, and radiologic studies such as CT or MRI. e6

Determining that a focal deficit is due to epileptic seizures can be very difficult. The absence of any other evident lesion or disease process that explains the syndrome is suggestive, but not specific or conclusive. The presence of epileptiform EEG abnormalities, including electrographic seizures at some point in the same illness, is also suggestive. Nonconvulsive status epilepticus may also be diagnosed by a clear and rapid response to AEDs, especially when the EEG does not provide a clear diagnosis (Dong et al., 2009). It should be acknowledged that the clinical improvement of our first patient after AED administration could have been coincidental, but seizures were demonstrated, and there were no other plausible causes of the neglect syndrome in this case. Our two patients had prominent and relatively isolated, or pure hemispatial neglect syndromes, without significant motor impairment, indicating a more focal or regional syndrome rather than a hemispheric deficit. Most earlier cases of hemispatial neglect syndromes caused by seizures have occurred along with significant motor or other clinical deficits, for example, cases of parietal lobe NCSE with a concomitant contralateral hemiparesis (Thomas et al., 1998) or other neurologic deficits (Feinberg et al., 1998; Turtzo et al., 2008), indicating more widespread hemispheric dysfunction. Parietal lobe seizures and NCSE appear to be rare, but it is possible that they are simply hard to recognize and under diagnosed. Most begin with somatosensory auras though they may spread to become tonic seizures or complex partial seizures (Williamson et al., 1992). Some include by symptoms of abnormal lateralized somatosensory perception (van Paesschen et al., 2007; Williamson et al., 1992), body image, or even ictal pain syndromes (Salanova et al., 1995; Siegel et al., 1999). Some have vertiginous sensations, complex visual or auditory hallucinations, aphasia, or tonic posturing (Salanova et al., 1995). Recovery can be quite prolonged, with cognitive deficits lasting up to months after the seizures cease, possibly related to long-lasting hypometabolism (van Paesschen et al., 2007). The slow recovery could be the cognitive or sensory equivalent of a “Todd paralysis.” EEG recordings in our patients did not localize the seizures unequivocally, but the clinical manifestations suggest that the right parietal lobe was involved, possibly by spread from the “epileptogenic” to the “symptomatogenic” region (Tufenkjian and Lüders, 2012). Even with deficits that are localized clearly by clinical evaluation, the causative lesions, as shown by MRI scans, can be at a distance (van Paesschen et al., 2007; Toledo et al., 2008), and radiologic, and EEG findings may be modest in proportion to the severity of the clinical syndrome at the time. These cases have some similarity to those of patients with aphasic SE (Ericson et al., 2011) in that EEG evidence of seizures was not always present on surface EEGs during the most severe manifestation of symptoms, whether neglect or aphasia. In our first patient, the initial EEG showed a very suppressed background (possibly representing postictal inhibition or hypometabolism), and only later were electrographic seizures recorded. In the aphasia patients (Ericson et al., 2011), electrographic seizures were eventually demonstrable in most cases but were evident on EEG in only five of nine patients (with PLEDs in two) when the clinical deficit was maximaldalthough the aphasia was clearly caused by seizures. In both series, improvement on the EEG correlated with eventual clinical improvement, but not immediately. Not all epileptic seizures are evident on surface EEGs (Devinsky et al., 1988; Dong et al., 2009; Waziri et al., 2009) although some of these are evident on invasive EEG monitoring (Hirsch et al., 2001). Also, clinical deficits may persist when earlier seizures are no longer evident on EEG. Some prolonged deficits Copyright Ó 2014 by the American Clinical Neurophysiology Society

Journal of Clinical Neurophysiology  Volume 32, Number 2, April 2015

might result from discontinuous seizures (Ericson et al., 2011) or be caused by interictal or postictal inhibition (van Paesschen et al., 2007). There is not always a good correlation between the clinical manifestations and EEG seizure activity, even when a patient may reasonably be considered in NCSE. That the evidence of seizures on EEG appears and disappears over the course of the illness suggests that long-term continuous EEG monitoring may be necessary to diagnose some such cases, rather than relying on a 20 to 30-minute EEG recording (Claassen et al., 2004). When suspicion for seizures is high, but a single EEG does not provide a clear diagnosis, more prolonged EEG monitoring can be diagnostic. Both of these series show the value of continuous (or at least much more prolonged) EEG monitoring in detecting nonconvulsive seizures or NCSE as the cause of focal cortical or cognitive neurologic deficits. In conclusion, severe hemispatial neglect syndromes can be caused by nonconvulsive seizures or NCSE and can occur in an isolated form, without significant motor, regional or wholehemisphere deficits. Also, focal nonconvulsive epileptic syndromes (whether neglect or aphasia) do not necessarily show ongoing seizures in the clinically involved area on a single surface EEG, interictal or postictal inhibition may contribute. Long-term, continuous EEG can help to demonstrate the presence of epileptic seizures that are not evident at presentation, even when the EEG is done at the time of maximal deficit. REFERENCES Barry E, Sussman NM, Bosley TM, Harner RN. Ictal blindness and status epilepticus amauroticus. Epilepsia 1985;26:577–584. Benatar M. Ictal aphasia. Epilepsy Behav 2002;3:413–419. Caplan LR. Large vessel occlusive disease of the anterior circulation. Chapter 6. In: Caplan’s stroke: a clinical approach. 4th ed. Philadelphia: Elsevier, 2009:221–257. Claassen J, Mayer SA, Kowalski RG, et al. Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology 2004;62:1743–1748. Devinsky O, Kelley K, Porter RJ, Theodore WH. Clinical and electroencephalographic features of simple partial seizures. Neurology 1988;38:1347–1352.

Copyright Ó 2014 by the American Clinical Neurophysiology Society

Neglect, Nonconvulsive Status, and EEG Monitoring

Dong C, Sriram S, Delbeke D, et al. Aphasic or amnesic status epilepticus detected on PET but not EEG. Epilepsia 2009;50:251–255. Ericson EJ, Gerard EE, Macken MP, Schuele SU. Aphasic status epilepticus: electroclinical correlation. Epilepsia 2011;52:1452–1458. Feinberg TE, Roane DM, Cohen J. Partial status epilepticus associated with asomatognosia and private alien hand-like behaviors. Arch Neurol 1998;55:1574–1576. Hirsch LJ, Emerson RG, Pedley TA. Prolonged “postictal” aphasia: demonstration of persistent ictal activity with intracranial electrodes. Neurology 2001;56:134–136. Kaplan PW. Nonconvulsive status epilepticus in the emergency room. Epilepsia 1996;37:643–650. Kaplan PW. Behavioral manifestations of nonconvulsive status epilepticus. Epilepsy Behav 2002;3:122–139. Kirshner HS, Hughes T, Fakhoury T, Abou-Khalil B. Aphasia secondary to partial status epilepticus of the basal temporal language area. Neurology 1995;45:1616–1618. Knight RT, Cooper J. Status epilepticus manifesting as reversible Wernicke’s aphasia. Epilepsia 1986;27:301–304. Manford M, Shorvon SD. Prolonged sensory or visceral symptoms: an underdiagnosed form of non-convulsive focal (simple partial) status epilepticus. J Neurol Neurosurg Psychiatry 1992;55:714–716. Salanova V, Andermann F, Rasmussen T, et al. Parietal lobe epilepsy. Clinical manifestations and outcome in 82 patients treated surgically between 1929 and 1988. Brain 1995;118:607–627. Shaw S, Kim P, Millett D. Status epilepticus amauroticus revisited. Ictal and periictal homonymous hemianopsia. Arch Neurol 2012;69:1504–1507. Siegel AM, Williamson PD, Roberts DW, et al. Localized pain associated with seizures originating in the parietal lobe. Epilepsia 1999;40:845–855. Thomas P, Snead OC. Absence status epilepticus. Chapter 60. In: Engel J, Pedley TA, eds. Epilepsy: a comprehensive textbook. 2nd ed. Philadelphia: Lippincott-Raven Publishers, 2008:693–703. Thomas P, Giraud K, Alchaar H, Chatel M. Ictal asomatognosia with hemiparesis. Neurology 1998;51:280–282. Toledo M, Munuera J, Sueiras M, et al. MRI findings in aphasic status epilepticus. Epilepsia 2008;49:1465–1469. Tufenkjian K, Lüders HO. Seizure semiology: its value and limitations in localizing the epileptogenic zone. J Clin Neurol 2012;8:243–250. Turtzo C, Kleinman JT, Llinas RH. Capgras syndrome and unilateral spatial neglect in nonconvulsive status epilepticus. Behav Neurol 2008;20:61–64. van Paesschen W, Porke K, Fannes K, et al. Cognitive deficits during status epilepticus and time course of recovery: a case report. Epilepsia 2007:48: 1979–1983. Waziri A, Claassen J, Stuart RM, et al. Intracortical electroencephalography in acute brain injury. Ann Neurol 2009;66:366–377. Williamson PD, Boon PA, Thadani VM, et al. Parietal lobe epilepsy: diagnostic considerations and results of surgery. Ann Neurol 1992;31:193–201.

e7

Severe hemispatial neglect as a manifestation of seizures and nonconvulsive status epilepticus: utility of prolonged EEG monitoring.

Seizures and status epilepticus causing hemispatial neglect syndromes are seldom diagnosed, in part because, without motor signs, EEGs are not perform...
462KB Sizes 2 Downloads 5 Views