Pediatric Neurology 57 (2016) 88e90

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Pediatric Neurology journal homepage: www.elsevier.com/locate/pnu

Clinical Observations

Ictal Coprolalia: A Case Report and Review of Ictal Speech as a Localizing Feature in Epilepsy Cerin Daniel a, M. Scott Perry MD b, * a b

University of North Texas Health Science Center College of Osteopathic Medicine, Fort Worth, Texas Jane and John Justin Neuroscience Center, Cook Children’s Medical Center, Fort Worth, Texas

abstract BACKGROUND: Recognizing ictal semiology is an essential component to localization of seizure onset, especially in intractable epilepsy where surgical therapies may be beneficial. Ictal speech can be a common component of seizure semiology, but the various forms of ictal speech may have different lateralizing and localizing value. Coprolalia is a very rare form of ictal speech. METHODS: We present a 15 year old with medically intractable seizures characterized by agitation and coprolalia. RESULTS: The patient underwent surgical evaluation including video EEG, MRI, and functional neuroimaging. These studies indicated onset within the dominant frontal lobe which was further localized using stereo-electroencephalography prior to focal cortical resection. CONCLUSIONS: Ictal coprolalia is a rare presentation of ictal speech. We review the various forms of ictal speech and their value in localizing seizure onset. Keywords: ictal speech, coprolalia, ictal semiology, frontal lobe, temporal lobe

Pediatr Neurol 2016; 57: 88-90 Ó 2016 Elsevier Inc. All rights reserved.

Introduction

Patient description

Ictal speech is commonly encountered as a semiological feature of seizures and can vary from simple vocalizations to intelligible speech. The cortical origins of ictal speech differ, although certain forms of ictal speech can be both localizing and lateralizing. Thus ictal speech can be an important semiological feature to appreciate, especially in patients with intractable epilepsy undergoing surgical evaluation. Coprolalia is a form of involuntary swearing that is used out of social and emotional context. Although it occurs most commonly in individuals with Tourette syndrome, it may be present in other neurological disorders such as traumatic brain injuries, stroke, encephalitis, and, very rarely, epilepsy.1 We describe an individual with dominant frontal lobe epilepsy manifesting ictal coprolalia as a prominent feature. We review the localizing and lateralizing value of coprolalia and explore the localizing value of other forms of ictal speech.

This 15-year-old boy presented with intractable focalonset seizures since age five years. Seizure semiology was of arousal from sleep with hypermotor activity or aggressive behavior lasting 10 to 30 seconds and occurring nightly. Initial electroencephalography (EEG) suggested onset from the left frontal lobe, and treatment with oxcarbazepine resulted in seizure remission for seven years, after which the medication was weaned. He returned to our clinic at age 12 years for evaluation of possible Tourette syndrome after being treated by mental health providers for coprolalia in the setting of oppositional defiant disorder. Careful history revealed no motor or vocal tics; however, his events were characterized by a sudden onset of downturned pursed lips (chapeau de gendarme), followed by prominent agitation with coprolalia and bilateral manual automatisms (Fig 1 and Video). After his coprolalia was recognized to be related to frontal lobe epilepsy, he was treated with maximum doses of oxcarbazepine, zonisamide, lacosomide, and clobazam without remission, prompting an epilepsy surgery evaluation. Presurgical testing revealed a nonlesional magnetic resonance imaging with video EEG

* Communications should be addressed to: Dr. Perry; 4th Floor; 1500 Cooper Street; Fort Worth, TX 76104. E-mail address: [email protected] 0887-8994/$ e see front matter Ó 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.pediatrneurol.2015.11.013

C. Daniel, M.S. Perry / Pediatric Neurology 57 (2016) 88e90

FIGURE 1. Patient’s typical frontal lobe seizure beginning with stereotyped facial appearance followed by agitation, coprolalia, and bimanual automatisms. The video related to this figure can be found at http://dx.doi.org/10.1016/j. pediatrneurol.2015.11.013. (The color version of this figure is available in the online edition.)

demonstrating bifrontal interictal spikes with typical ictal events characterized by bifrontal attenuation with maximum evolution of repetitive spike discharges within the left frontal lobe. Positron emission tomography (PET) demonstrated a focal region of hypometabolism within the left mesial frontal lobe extending to the anterior cingulate gyrus, which was also a region of interictal dipole localization by magnetoencephalography (Fig 2). Language was localized to the left hemisphere. Given the likelihood of deep mesial frontal localization based on presurgical evaluation and the need to investigate the presence or absence of primary speech (i.e., Broca area) involvement in the epileptogenic zone, we pursued stereoelectroencephalography (SEEG) with depth electrodes over a subdural grid placement. The SEEG approach allows monitoring of deep, difficult-to-access cortical regions and can aid in delineating the epileptogenic network when more diffuse cortical regions may be involved. Depth electrodes were placed within the left anterior insula, left anterior cingulate, body of the left cingulate gyrus, Broca region, left frontal pole, and orbitofrontal surface. SEEG data of typical seizures localized the seizure onset within the mesial left frontal lobe at the appearance of typical chapeau facies, followed by involvement of the left anterior cingulate gyrus when coprolalia begins corresponding to the hypometabolic cortex demonstrated by PET. The Broca area was not involved in the ictal EEG pattern. Surgical resection of the region of PET hypometabolism including the left frontal pole and anterior cingulate gyrus was completed without complication and he has remained seizure free since surgery. Discussion

Although speech can be a common semiological feature of seizures, ictal coprolalia is rare. To decipher the localizing value of ictal coprolalia, it is crucial to differentiate

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FIGURE 2. Sagittal view from patient’s nonlesional magnetic resonance imaging of the left hemisphere demonstrating localization of presurgical positron emission tomography hypometabolism (red). Subsequent stereoelectroencephalogram with placement of depth electrodes (blue) confirmed onset within the same region including the mesial left frontal lobe and anterior cingulate gyrus, which was resected (yellow) resulting in seizure freedom. (The color version of this figure is available in the online edition.)

forms of ictal speech such as coprolalia from other speech manifestations, such as ictal vocalizations and speech impediments, considering the cortical origins of each. Ictal vocalizations have been defined as an audible sound that carries no speech quality.1 They occur in 40% to 60% of patients with frontal lobe epilepsy and often present as repetitive nonspeech sounds, such as the grunting noted at the onset of our patient’s seizures.2 Recently, Bonini et al.3 demonstrated a rostrocaudal hierarchy of the frontal lobe with more extensive ictal behaviors arising from the rostral prefrontal cortex, and progressively less extensive behaviors arising in the posterior prefrontal region. Patients with ictal vocalizations such as singing and humming as well as proximal stereotypies were shown to have coinvolvement of the left anterior prefrontal region and the anterior cingulate gyrus either concurrently during seizure onset or by propagation, as was present in our patient. Although ictal vocalizations are commonly localized to the frontal lobe, they are not clearly lateralizing. Conversely, vocalizations may be an ictal manifestation of temporal lobe epilepsy and present as grunting, moaning, and crying.4 Gabr et al.4 demonstrated that ictal vocalizations occurred more often in patients with dominant foci in temporal lobe epilepsy, suggesting nonspeech vocalizations have lateralizing value when seizure onset is localized to the temporal lobe. Speech impediments are more commonly encountered in temporal lobe epilepsy and have a wide spectrum of presentations.5 Dysphasia is the most common presentation of speech disturbance in temporal lobe epilepsy associated with the dominant hemisphere.4 Gabr et al.4 investigated the lateralizing value of dysphasia associated

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C. Daniel, M.S. Perry / Pediatric Neurology 57 (2016) 88e90

with temporal lobe epilepsy, as well as other speech impediments such as speech arrest and dysarthria. Seizures originated from the dominant hemisphere in 92% of patients with postictal dysphasia present as either expressive or receptive dysphasia. When dysphasia resulted fromnondominant temporal lobe seizures, the patient had isolated events of paraphasic errors with no evidence of impairments in fluency or comprehension. In addition, patients with seizures originating in the nondominant hemisphere did not exhibit concurrent ictal and postictal expressive or receptive dysphasia. In contrast, speech arrest and dysarthria occurred as isolated events in patients with temporal lobe epilepsy, and did not hold significant lateralizing value. In the case of frontal lobe epilepsy involving the dominant hemisphere, speech arrest and dysphasia occur more commonly in the ictal period and are associated with rapid postictal recovery, which may help differentiate frontal from temporal localization.5 An absence of verbal response in frontal lobe epilepsies can be attributed as a localizing sign of impairment of Broca’s area.5 Ictal speech includes intelligible, propositional, and nonpropositional speech that is coherent while consciousness is sufficiently impaired.1 Nonpropositional ictal speech has often been regarded as a lateralizing sign in temporal lobe epilepsies with nondominant hemisphere dysfunction, but is rarely seen in frontal lobe epilepsies.6 Using subdural EEG, identifiable nonpropositional ictal speech has been lateralized to the nondominant lobe in temporal lobe epilepsy.4 When ictal speech is encountered in frontal lobe epilepsy, it is often associated with bizarre behavior.1 Frontal lobe epilepsy is associated with florid emotional outbursts and bizarre behavior, which includes aggression, kicking, compulsive behaviors, and genital manipulation.7 The constellation of clinical features in these seizures can be bizarre and are often misdiagnosed as nonepileptic deviant behavior as with our patient. Coprolalia, a unique form of nonpropositional ictal speech, may be a unique localizing and lateralizing feature of frontal lobe epilepsy. Nonpropositional swearing presents as overlearned and automatic expressions, whereas propositional forms of cursing present in a controlled manner, and involve both intact Broca and Wernicke areas.8 Although the definitive pathophysiologic mechanism remains unknown, dysfunction in the cortical-striatal-limbic pathways has been implicated to play a role in coprolalia.1 Ictal swearing has previously been lateralized within the nondominant hemisphere.9 This same study proposed that ictal swearing could not be localized, because temporal, frontal, parietal, and parieto-occipital lobes were affected in different patients when investigated using PET, magnetoencephalography, intracranial EEGs, and surgical outcomes. However, cortical stimulation of electrodes in the temporal and parietal regions failed to provoke disturbances in language, and epilepsy surgery in the right parieto-occipital region did not produce any language difficulties, suggesting coprolalia in these patients was more likely part of a propagation pattern than direct influence of these cortical regions. Recent SEEG investigations have demonstrated rage including swearing or screaming involves the medialprefrontal network with propagation to the amygdala.3 Speech production typically arises from the Broca area of the dominant hemisphere, whereas nonpropositional

speech such as coprolalia may arise in the nondominant hemisphere. It has been shown that patients who have global aphasia and have suffered left hemispheric strokes or undergone left hemispherectomy have preserved swearing capabilities.1 It is suggested that aggression occurs with left hemispheric damage as the capability to curse nonpropositionally remains intact in the right hemisphere, and the left hemisphere cannot suppress these emotions.8 Recently Bonini et al.3 delineated different anatomic localizations of clinical patterns produced by frontal lobe epilepsy through SEEG. The characteristic downward movement of the mouth, known as the chapeau de gendarme was exclusively localized to the premotor and lateral prefrontal regions. Our patient’s aggressive behavior and typical chapeau facies suggested frontal lobe onset, but his florid coprolalia was a unique ictal feature. Our patient had dominant frontal lobe onset, which suggests coprolalia may also arise from the dominant frontal lobe, although we cannot exclude the possibility that coprolalia arose from the nondominant lobe as a result of ictal dominant frontal lobe dysfunction. Thus, although ictal coprolalia may have variable lateralizing value, it does appear to have better localizing value to the mesial frontal lobe most often and less frequently the temporal lobe. Our report highlights a rare individual with dominant frontal lobe epilepsy who presented with prominent nonpropositional coprolalia. We emphasize the localizing value ictal speech, especially when combined with coexisting semiological features. Ictal speech can present in multiple forms, and differentiating these features is essential in gaining localizing and lateralizing value. The frontal and temporal lobes are most often involved either directly or through propagation, and delineating the form of ictal speech may aid in further localizing and lateralizing seizure onset. There remain discrepancies in localizing all forms of ictal speech, underscoring the complex connectivity of speech networks; thus further research into ictal speech patterns will provide more precise data.

References 1. Dolatshahi M, Yankovsky A. Ictal forced repetitive swearing in frontal lobe epilepsy: Case report and review of the literature. J Epileptology. 2014;22:113-119. 2. Janszkya J, Fogarasia A, Jokeita H, Ebnera A. Are ictal vocalisations related to the lateralisation of frontal lobe epilepsy? J Neurol Neurosurg Psychiatry. 2000;69:244-247. 3. Bonini F, McGonigal A, Trébuchon A, et al. Frontal lobe seizures: From clinical semiology to localization. Epilepsia. 2014;55:264-277. 4. Gabr M, Lüders H, Dinner D, Morris H, Wyllie E. Speech manifestations in lateralization of temporal lobe seizures. Ann Neurol. 1989;25: 82-87. 5. Bertti P, Tejada J, Martins A, et al. Looking for complexity in quantitative semiology of frontal and temporal lobe seizures using neuroethology and graph theory. Epilepsy Behav. 2014;38:81-93. 6. Horvath R, Fogaras A, Schulz R, et al. Ictal vocalizations occur more often in temporal lobe epilepsy with dominant (left-sided) epileptogenic zone. Epilepsia. 2009;50:1542-1546. 7. Shih J, Mazwi L, Falcao G, Gerpen J. Directed aggressive behavior in frontal lobe epilepsy: A video-EEG and ictal SPECT case study. Neurology. 2009;73:1804-1806. 8. Battistella E. Why we curse: A neuro-psycho-social theory of speech. Language. 2001;77:633-634. 9. Birca V, Tayah T, Saint-Hilaire J, Nguyen D. Ictal swearing: A case series and review. Epileptic Disord. 2013;15:377-381.

Ictal Coprolalia: A Case Report and Review of Ictal Speech as a Localizing Feature in Epilepsy.

Recognizing ictal semiology is an essential component to localization of seizure onset, especially in intractable epilepsy where surgical therapies ma...
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