Seizure Semiology: Its Value and Limitations in Localizing the Epileptogenic Zone PDF

REVIEW Print ISSN 1738-6586 / On-line ISSN 2005-5013 J Clin Neurol 2012;8:243-250 http://dx.doi.org/10.3988/jcn.2012.8.4.243 Ope...

REVIEW Print ISSN 1738-6586 / On-line ISSN 2005-5013 J Clin Neurol 2012;8:243-250 http://dx.doi.org/10.3988/jcn.2012.8.4.243 Open Access Seizure Semiology: Its Value and Limitations in Localizing the Epileptogenic Zone Krikor Tufenkjian, Hans O. Lüders Epilepsy Center, Department of Neurology, University Hospitals Case Medical Center, Cleveland, OH, USA Epilepsy surgery has become an important treatment option in patients with medically refractory epilepsy. The ability to precisely localize the epileptogenic zone is crucial for surgical success. The tools available for localization of the epileptogenic zone are limited. Seizure semiology is a simple and cost effective tool that allows localization of the symptomatogenic zone which either overlaps or is in close proximity of the epileptogenic zone. This becomes particularly important in cases of MRI negative focal epilepsy. The ability to video record seizures made it possible to discover new localizing signs and quantify the sensitivity and specificity of others. Ideally the Received July 5, 2012 signs used for localization should fulfill these criteria; 1) Easy to identify and have a high inter- Revised September 10, 2012 rater reliability, 2) It has to be the first or one of the earlier components of the seizure in order to Accepted September 10, 2012 have localizing value. Later symptoms or signs are more likely to be due to ictal spread and may Correspondence have only a lateralizing value. 3) The symptomatogenic zone corresponding to the recorded ictal Krikor Tufenkjian, MD symptom has to be clearly defined and well documented. Reproducibility of the initial ictal symp- Epilepsy Cener, toms with cortical stimulation identifies the corresponding symptomatogenic zone. Unfortunate- Department of Neurology, ly, however, not all ictal symptoms can be reproduced by focal cortical stimulation. Therefore, the University Hospitals of Cleveland, problem the clinician faces is trying to deduce the epileptogenic zone from the seizure semiology. 11100 Euclid Ave. Lakeside 3200, The semiological classification system is particularly useful in this regard. We present the Cleveland, OH 44106, USA known localizing and lateralizing signs based on this system. J Clin Neurol 2012;8:243-250 Tel +1-216-844-3650 Fax +1-216-844-5066 Key Wordszzsemiology, localization, epilepsy surgery. E-mail [email protected] Introduction into organic (for example cardiogenic events such as syncope) and psychogenic events. For a diagnosis of non-epileptic psy- This review summarizes semiological findings that are valu- chogenic paroxysmal events the EEG should not show any able in localizing the epileptogenic zone. The information is epileptiform discharges during a typical paroxysmal event. based on literature review with results that are consistent with Preserved awareness, eye flutter and the ability of the bystand- our experience. The discussion will focus on the signs that are ers to modify or alleviate were found to be significant markers more prominent and consistent. While there are other signs for these events.1 The presence of a normal alpha activity described anecdotally; however their infrequency makes them while the patient is unresponsive and has amnesia for the ev- unreliable as an evaluation tool for epilepsy surgery. ent is essentially pathognomonic for psychogenic non-epilep- tic seizures. Classification of Paroxysmal Events Epileptic Paroxysmal Events Paroxysmal events can be classified into epileptic and non-ep- ileptic events. Non-epileptic paroxysmal events are classified Auras cc This is an Open Access article distributed under the terms of the Cre- Somatosensory auras ative Commons Attribution Non-Commercial License (http://creative- These are abnormal somatosensations (usually “tingling” or commons.org/licenses/by-nc/3.0) which permits unrestricted non-com- mercial use, distribution, and reproduction in any medium, provided the ori- “numbness”) that are limited to a clearly defined somatosen- ginal work is properly cited. sory region of the body. The contralateral primary sensory cor- Copyright © 2012 Korean Neurological Association 243 Localizing Value of Seizure Semiology tex is usually the symptomatogenic zone of somatosensory Autonomic auras auras of unilateral, distal distribution. Bilateral and more wi- These are subjective sensations suggesting possible autono- despread somatosensations can be produced from the supple- mic alterations such as palpitations, sweating, “goose bumps”, mentary sensorymotor area (SSMA) and also the second so- etc. The episodes should be diagnosed as “autonomic seizu- matosensory area (S2) located in the superior bank of the res” when there is objective documentation of autonomic al- Sylvian fissure and/or the posterior insula.2 In addition, stim- terations [for example when tachycardia is documented with ulation of S2 can also produce unpleasant sensations of heat or an electrocardiogram (ECG) recording]. The symptomatogenic pain.3 It is also important to remember that low intensity cor- zone of most autonomic auras is most likely the insular cortex. tical stimulation of motor areas may elicit muscle contractions that are not sufficient to result in actual movements. The pa- Abdominal auras tient may interpret such a mild motor activity as a somato- Abdominal auras are frequent and are usually secondary to sensory aura. Poorly localized or lateralized “all body sensa- temporal lobe epilepsies. However, occasionally abdominal tions” have no localizing or lateralizing value and should not auras may also be triggered by extratemporal epilepsies (ma- be classified as somatosensory auras. inly frontal lobe and insula). These auras are the result of ei- ther a sensation produced by increased peristalsis or 2) as a Visual auras sensory phenomena resulting from direct activation of the sen- These are visual hallucinations that usually consist of flashing sory cortical areas of the abdominal viscera. Van Buren8 as- lights of different colors that may blink and move in the visual sessed peristaltic motility with gastric balloons during sponta- field. Frequently the patient reports the visual hallucinations neous and induced abdominal auras. His studies showed no in front of both eyes without a clear lateralization. However, effect upon gastromotor function except of rare occasions of occasionally the visual aura may be lateralized to one visual gastric inhibition. field (contralateral to the symptomatogenic zone) and may The abdominal auras have been described by a plethora of even be localized to the upper or lower visual field. Not infre- symptoms such as nausea, tenseness, knot, external weight or quently the patient reports amaurosis either during or after the squeezing, rolling, turning or whirling movement in the abdo- epileptic seizure.4 In these cases the flashing lights may appear men, tickling, tingling or electric shock sensation, pain, vibrat- on top of the blind visual field. The symptomatogenic zone ing, fluttering or butterflies sensation, gas or pressure within the for the visual hallucinations is Broadmann’s area 17 and 18. abdomen, an empty, hungry feeling, sensation of warmth, sen- Complex visual hallucinations and visual illusions are more sation of sudden descent in an elevator, burning or heartburn. likely to involve the association cortex (parieto-temporal) or The sensation begins usually in the epigastrium or stomach in the adjacent lobes and frequently are part of psychic auras. the midline and can remain localized there but not infrequ- ently rises to the chest, throat, head or even face.7 Almost in- Auditory auras variably when the aura rises to the neck or face the patient los- These are simple auditory hallucinations, like hearing a “buzz” es consciousness. Epigastric sensations closely resembling epi- or a “noise”. The symptomatogenic zone is Heschell’s gyrus gastric auras can be elicited by electrical stimulation of the in the superior temporal gyrus. Usually the patient has diffi- insula. There are also reports of abdominal auras elicited by culty lateralizing the sound. Besides, even when the sound is electrical stimulation of other structures such as the mesial tem- perceived as lateralized to one side it is not a reliable sign to la- poral structures, the basal ganglia, the supplementary motor teralize the epilepsy.5 area, the pallidum and the centrum medianum of the thalamus.8 However, in these studies the possibility that the stimulation Olfactory auras produced after discharges spreading to other structures was Most of the time these are hallucinations of unpleasant smells. not excluded. They have no lateralizing value but are most frequently seen in patients with mesial temporal lobe epilepsy. Interestingly Psychic auras a relatively high percentage of these patients have neoplasms These are complex hallucinations and/or illusions that usually that involve the amygdala.6 affect different senses. Psychic auras include phenomena such as autoscopy, fear, elation, déjà vu and jamais vu. Autoscopic Gustatory auras phenomena have several variations. The more common ones These auras consist of unpleasant taste. Cortical stimulation are seeing a double of the whole or part of the body, feeling of studies have found the insula to be a symptomatogenic zone presence without optical image, out of body experience with for this aura.3 These auras have no lateralizing value. observing the self from an elevated position, as well as nega- 244 J Clin Neurol 2012;8:243-250  Tufenkjian K and Lüders HO tive phenomena with failure to perceive one’s own body. The complexity of the ictal movement itself. Simple motor sei- temporal lobe is usually involved with these phenomena but zures refer to unnatural but simple movements, usually involv- they have no lateralizing value.9 Some of these sensations can ing only one articulation in one plane. These movements can be elicited by electrical stimulation of the temporal lobe con- be reproduced by electrical cortical stimulation of the motor vexity or the junction of the posterior temporal lobe with the areas. Complex motor seizures refer to movements that imi- occipital or parietal lobe. Mesial temporal structures were con- tate natural movements. The latter are usually complex involv- currently involved in most cases.10 ing several articulations in different planes, and tend to be re- petitive. These movements cannot be elicited by electrical cor- Autonomic seizures tical stimulation unless a seizure discharge is triggered. Autonomic seizures are epileptic seizures in which the main symptomatology is an autonomic alteration that can be docu- Simple motor seizures mented objectively (for example; an ictal tachycardia that is documented with an ECG recording and can be with or with- Myoclonic seizures out an associated sensation of tachycardia). Pilomotor sei- These are short muscle contractions lasting 10 sec), forced, unnatural positioning of ciated only with slower falls and only infrequently result in an upper extremity on one side of the body with a clear rota- significant injuries.32 tional component. In patients with temporal lobe epilepsy this www.thejcn.com 247 Localizing Value of Seizure Semiology is a reliable lateralizing sign to the contralateral hemisphere.37 The mechanism of ipsilateral eye blinking has not been elu- Although more common in temporal lobe epilepsy this sign cidated. can occur in extra temporal lobe epilepsy as well. It is thought to be related to activation of the basal ganglia through spread Ictal nystagmus of the epileptifom discharges. Basal ganglia were shown to Most cases described a predominantly horizontal binocular be involved during dystonic posturing on ictal SPECT.38 nystagmus. In these cases the fast phase of the nystagmus was opposite the seizure focus. The seizures originate from either Ictal speech the occipital or the temporo-occipital junction and are often Ictal verbalization is defined as the presence of clearly intel- associated with ictal vertigo.47 ligible speech when the patient already shows unresponsive- ness and/or has clear distal automatisms. It tends to lateralize Limitations of using semiology as a localizing tool the epilepsy to the non-dominant hemisphere in patients with temporal lobe epilepsy. However, exceptions to this rule are not Seizure semiology is subjective so infrequent making this a poorly reliable lateralizing sign. Be- There is significant inter-rater variability particularly when sides, pure vocalization has no lateralizing significance.39,40 observers come from different epilepsy centers which may de- fine symptoms and signs differently. This occurs despite using Post ictal aphasia systematic approach to analyze the seizure semiology with Postictal aphasia lateralizes the epilepsy to the language do- video recording and highly trained individuals. An example minant hemisphere in patients with temporal lobe epilepsy.39 would be misinterpretation between versive seizures and non- Recovery of language function after the ictal EEG pattern has versive head rotations among different observers. stopped was found to be significantly more delayed in patients with left temporal lobe epilepsy.41 It has been reported that Seizure semiology is the manifestation of the activation post-ictal language delay is less significantly affected in fron- of the symptomatogenic zone tal lobe epilepsy unless there is extension to the ipsilateral That implies that it can be the result of ictal spread from a more temporal lobe.42 To diagnose post-ictal aphasia it is essential distant epileptogenic zone. In other words seizures arising from to have a patient who is cooperative postictally (i.e., clearly different epileptogenic zones could activate the same sympto- tries to understand language and tries to talk) who, however, matogenic zone or, vice-versa, seizure originating from the is aphasic. Besides, the patient should be tested continuously same epileptogenic zone could activate different symptom- and language should recover slowly (10-20 minutes) but pro- atogenic zones producing different seizure semiologies. gressively. Seizure semiology does not always permit differentiation Todd’s paralysis of focal or generalized epilepsies This is a non-localizing but highly lateralizing sign. It is always Focal epilepsy may trigger seizures of “generalized” semiolo- preceded by prominent ipsilateral motor activity of the affect- gy, and vice versa generalized epilepsies may have seizures of ed limb. focal symptomatology. So for example, focal signs were found in 46% of patients in a group with juvenile myoclonic epilep- Post-ictal nose wipe sy. Focal semiologic findings in this group included unilateral This lateralizes the epilepsy to the ipsilateral hemisphere in clonic, unilateral myoclonic, version and asymmetric tonic patients with temporal lobe epilepsy.43 It is assumed that the seizures.48 hemisphere contralateral to the nose-wipe (which is the hemi- sphere of seizure onset) suffers from post-ictal neglect. Conclusions Peri-ictal water drinking Seizure semiology is a very useful tool; however, it requires This has been reported as a lateralizing sign to the non-domi- standardization among evaluators. It is necessary to include nant temporal lobe epilepsy.44 The validity of this has been only signs that are unambiguous and achieve a consensus of contested.45 several qualified observers. It is not infrequent to see con- flicting lateralizing or localizing signs occurring in a single Unilateral eye blinking seizure. In this situation the importance of each sign is deter- This is infrequent but has been reported as a good lateralizing mined based on its sequence during the seizure as well as the sign to the ipsilateral hemisphere. It has no localizing value.46 specificity of the sign. 248 J Clin Neurol 2012;8:243-250  Tufenkjian K and Lüders HO Conflicts of Interest infantile spasms: medical or surgical? Epilepsia 1992;33 Suppl 4: The authors have no financial conflicts of interest. S26-S31. 22. Juhász C, Chugani HT, Muzik O, Chugani DC. Neuroradiological as- sessment of brain structure and function and its implication in the REFERENCES pathogenesis of West syndrome. Brain Dev 2001;23:488-495. 1. Syed TU, LaFrance WC Jr, Kahriman ES, Hasan SN, Rajasekaran V, 23. Janszky J, Fogarasi A, Jokeit H, Ebner A. Lateralizing value of unilat- Gulati D, et al. Can semiology predict psychogenic nonepileptic sei- eral motor and somatosensory manifestations in frontal lobe seizures. zures? A prospective study. Ann Neurol 2011;69:997-1004. Epilepsy Res 2001;43:125-133. 2. Pugnaghi M, Meletti S, Castana L, Francione S, Nobili L, Mai R, et 24. Bonelli SB, Lurger S, Zimprich F, Stogmann E, Assem-Hilger E, Bau- al. Features of somatosensory manifestations induced by intracranial mgartner C. Clinical seizure lateralization in frontal lobe epilepsy. Epi- electrical stimulations of the human insula. Clin Neurophysiol 2011; lepsia 2007;48:517-523. 122:2049-2058. 25. Walser G, Unterberger I, Dobesberger J, Embacher N, Falkenstetter T, 3. Stephani C, Fernandez-Baca Vaca G, Maciunas R, Koubeissi M, Lud- Larch J, et al. Asymmetric seizure termination in primary and second- ers HO. Functional neuroanatomy of the insular lobe. Brain Struct ary generalized tonic-clonic seizures. Epilepsia 2009;50:2035-2039. Funct 2011;216:137-149. 26. Marks WJ Jr, Laxer KD. Semiology of temporal lobe seizures: value in 4. Kuzniecky R. Symptomatic occipital lobe epilepsy. Epilepsia 1998; lateralizing the seizure focus. Epilepsia 1998;39:721-726. 39 Suppl 4:S24-S31. 27. Chee MW, Kotagal P, Van Ness PC, Gragg L, Murphy D, Lüders HO. 5. Florindo I, Bisulli F, Pittau F, Naldi I, Striano P, Striano S, et al. Later- Lateralizing signs in intractable partial epilepsy: blinded multiple-ob- alizing value of the auditory aura in partial seizures. Epilepsia 2006; server analysis. Neurology 1993;43:2519-2525. 47 Suppl 5:68-72. 28. Proserpio P, Cossu M, Francione S, Tassi L, Mai R, Didato G, et al. In- 6. Acharya V, Acharya J, Lüders H. Olfactory epileptic auras. Neurology sular-opercular seizures manifesting with sleep-related paroxysmal 1998;51:56-61. motor behaviors: a stereo-EEG study. Epilepsia 2011;52:1781-1791. 7. Baumgartner C, Lurger S, Leutmezer F. Autonomic symptoms during 29. Staack AM, Bilic S, Wendling AS, Scholly J, Kraus U, Strobl K, et al. epileptic seizures. Epileptic Disord 2001;3:103-116. Hyperkinetic seizures in patients with temporal lobe epilepsy: clinical 8. Van Buren JM. The abdominal aura. A study of abdominal sensations features and outcome after temporal lobe resection. Epilepsia 2011; occurring in epilepsy and produced by depth stimulation. Electroen- 52:1439-1446. cephalogr Clin Neurophysiol 1963;15:1-19. 30. Téllez-Zenteno JF, Serrano-Almeida C, Moien-Afshari F. Gelastic sei- 9. Devinsky O, Feldmann E, Burrowes K, Bromfield E. Autoscopic phe- zures associated with hypothalamic hamartomas. An update in the cli- nomena with seizures. Arch Neurol 1989;46:1080-1088. nical presentation, diagnosis and treatment. Neuropsychiatr Dis Treat 10. Bancaud J, Brunet-Bourgin F, Chauvel P, Halgren E. Anatomical ori- 2008;4:1021-1031. gin of deja vu and vivid ‘memories’ in human temporal lobe epilepsy. 31. So NK. Atonic phenomena and partial seizures. A reappraisal. Adv Brain 1994;117:71-90. Neurol 1995;67:29-39. 11. Caboclo LO, Miyashira FS, Hamad AP, Lin K, Carrete H Jr, Sakamoto 32. Satow T, Ikeda A, Yamamoto J, Takayama M, Matsuhashi M, Ohara S, AC, et al. Ictal spitting in left temporal lobe epilepsy: report of three et al. Partial epilepsy manifesting atonic seizure: report of two cases. cases. Seizure 2006;15:462-467. Epilepsia 2002;43:1425-1431. 12. Shah J, Zhai H, Fuerst D, Watson C. Hypersalivation in temporal lobe 33. Källén K, Wyllie E, Lüders HO, Lachhwani D, Kotagal P. Hypomotor epilepsy. Epilepsia 2006;47:644-651. seizures in infants and children. Epilepsia 2002;43:882-888. 13. Wyllie E, Lüders H, Morris HH, Lesser RP, Dinner DS. The lateraliz- 34. Lüders HO, Dinner DS, Morris HH, Wyllie E, Comair YG. Cortical ing significance of versive head and eye movements during epileptic electrical stimulation in humans. The negative motor areas. Adv Neurol seizures. Neurology 1986;36:606-611. 1995;67:115-129. 14. Vendrame M, Zarowski M, Alexopoulos AV, Wyllie E, Kothare SV, 35. Song IU, Lee DG, Kim JS, An JY, Lee SB, Kim YI, et al. Unilateral Loddenkemper T. Localization of pediatric seizure semiology. Clin epileptic negative myoclonus following focal lesion of the postcentral Neurophysiol 2011;122:1924-1928. cerebral cortex due to acute middle cerebral infarction. J Clin Neurol 15. Bagla R, Skidmore CT. Frontal lobe seizures. Neurologist 2011;17: 2006;2:272-275. 125-135. 36. Dong C, Sriram S, Delbeke D, Al-Kaylani M, Arain AM, Singh P, et 16. Werhahn KJ, Noachtar S, Arnold S, Pfänder M, Henkel A, Winkler al. Aphasic or amnesic status epilepticus detected on PET but not EEG. PA, et al. Tonic seizures: their significance for lateralization and fre- Epilepsia 2009;50:251-255. quency in different focal epileptic syndromes. Epilepsia 2000;41: 37. Bleasel A, Kotagal P, Kankirawatana P, Rybicki L. Lateralizing value 1153-1161. and semiology of ictal limb posturing and version in temporal lobe and 17. Ohara S, Ikeda A, Kunieda T, Yazawa S, Taki J, Nagamine T, et al. extratemporal epilepsy. Epilepsia 1997;38:168-174. Propagation of tonic posturing in supplementary motor area (SMA) 38. Mizobuchi M, Matsuda K, Inoue Y, Sako K, Sumi Y, Chitoku S, et al. seizures. Epilepsy Res 2004;62:179-187. Dystonic posturing associated with putaminal hyperperfusion depict- 18. Ajmone Marsan C, Ralston BL. The Epileptic Seizure, Its Functional ed on subtraction SPECT. Epilepsia 2004;45:948-953. Morphology and Diagnostic Significance: A Clinical-Electrographic 39. Gabr M, Lüders H, Dinner D, Morris H, Wyllie E. Speech manifesta- Analysis of Metrazol-Induced Attacks. Springfield, IL: Charles C tions in lateralization of temporal lobe seizures. Ann Neurol 1989;25: Thomas, 1957;85-88. 82-87. 19. Kotagal P, Bleasel A, Geller E, Kankirawatana P, Moorjani BI, Rybicki 40. Yen DJ, Su MS, Yiu CH, Shih, Kwan SY, Tsai CP, et al. Ictal speech L. Lateralizing value of asymmetric tonic limb posturing observed in manifestations in temporal lobe epilepsy: a video-EEG study. Epilepsia secondarily generalized tonic-clonic seizures. Epilepsia 2000;41:457- 1996;37:45-49. 462. 41. Privitera MD, Morris GL, Gilliam F. Postictal language assessment 20. O’Brien TJ, Mosewich RK, Britton JW, Cascino GD, So EL. History and lateralization of complex partial seizures. Ann Neurol 1991;30: and seizure semiology in distinguishing frontal lobe seizures and tem- 391-396. poral lobe seizures. Epilepsy Res 2008;82:177-182. 42. Goldberg-Stern H, Gadoth N, Cahill W, Privitera M. Language dys- 21. Shields WD, Shewmon DA, Chugani HT, Peacock WJ. Treatment of function after frontal lobe partial seizures. Neurology 2004;62:1637- www.thejcn.com 249 Localizing Value of Seizure Semiology 1638. 46. Benbadis SR, Kotagal P, Klem GH. Unilateral blinking: a lateralizing 43. Hirsch LJ, Lain AH, Walczak TS. Postictal nosewiping lateralizes and sign in partial seizures. Neurology 1996;46:45-48. localizes to the ipsilateral temporal lobe. Epilepsia 1998;39:991-997. 47. Weber YG, Roesche J, Lerche H. Epileptic nystagmus: two case re- 44. Trinka E, Walser G, Unterberger I, Luef G, Benke T, Bartha L, et al. ports, clinical and pathophysiological review of the literature. J Neurol Peri-ictal water drinking lateralizes seizure onset to the nondominant 2006;253:767-771. temporal lobe. Neurology 2003;60:873-876. 48. Usui N, Kotagal P, Matsumoto R, Kellinghaus C, Lüders HO. Focal 45. Szucs A, Fogarasi A, Rásonyi G, Kelemen A, Narula L, Tóth V, et al. semiologic and electroencephalographic features in patients with juve- Peri-ictal water drinking in temporal lobe epilepsy: Is it a reliable later- nile myoclonic epilepsy. Epilepsia 2005;46:1668-1676. alizing sign? Epilepsy Behav 2007;11:578-581. 250 J Clin Neurol 2012;8:243-250