Clinical characteristics of epileptic seizures in insular gliomas

Buklina S.B.; Bykanov A.E.; Pitskhelauri D.I.

doi:https://doi.org/10.17116/jnevro201611612113-19

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Abstract:

Objective. To study the characteristics of epileptic seizures in insular gliomas. Material and methods. Forty-five patients with insular gliomas were examined. The spread of a tumor was established by MRI results and intraoperational findings. A tumor within the insular only was found in 9 out of 45 patients (7 left-sided and 2 right-sided). In 36 patients, a tumor slightly spread into temporal lobe pole and medial-basal regions of the frontal lobe (27 left-sided and 18 right-sided). The control group consisted of 50 patients with tumors of temporal and frontal lobes. Results. Paroxysmal symptoms were similar in patients with tumors of the insular and patients with tumors of temporal lobes. Seizures in patients with frontal lobe tumors differed significantly from insular and temporal tumors, with the exception of a tumor localized in the opercula area. The following quantitative differences were identified: different forms of unconsciousness were significantly less frequent in symptomatic epilepsy in patients with insular tumor than in epilepsy caused by temporal lobe tumors (36% of patients vs 84% in temporal tumors (p<0.0001)). In patients with insular tumors, olfactory and taste hallucinations occur more often compared to temporal lobe tumors (51% vs 16% (p<0.003). The frequency of paroxysmal seizures of fear and anxiety in patients with those tumors was similar (20% with insular tumors and 14 with temporal tumors). An autonomic component of episeizures did not differ between tumors of both localizations. Olfactory and taste hallucinations were qualitatively similar in insular and temporal lobe tumors: smell and taste were unpleasant or associated with a danger: smell of burning, gas, something spoiled, sour, tart chemistry, taste of somethong metallic, chemical, sour. No pleasant smell or taste were reported. Conclusion. Epileptic seizures in insular tumors had similarities and certain differences compared with temporal seizures that well reflect function of the insula and its links, in the first turn, with limbic system structures.

Keywords:

insula

symptomatic epilepsy

olfactory and taste hallucinations

gliomas

Authors:

Buklina S.B.

FGBU "NII neĭrokhirurgii im. akad. N.N. Burdenko" RAMN, Moskva

Bykanov A.E.

FGBU "NII neĭrokhirurgii im. akad. N.N. Burdenko" RAMN, Moskva

Pitskhelauri D.I.

Burdenko Neurosurgical Center

SPIN RSCI: 3261-2144
Scopus AuthorID: 6507820245
ORCID: 0000-0003-0374-7970

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References:

KerkHof M, Vecht CJ. Seizure characteristics and prognostic factors of fliomas. Epilepsia. 2013;54(suppl 9):12-17. doi: 10. 1111/epi. 12437
Kurzwelly D, Herrlinger U, Simon M. Seizures in patients with low-grade gliomas- incidence, pathogenesis, surgical management, and pharmacotherapy. Adv Tech Stand Neurosurg. 2010;35:81-111.
Brogna C, Gil Robles S, Duffau H. Brain tumors and epilepsy. Expert Rev Neurother. 2008;8:6:941-955. doi: 10. 1586/14737175.8.6.941
Blecic S, Rynkowsky M, De Witte O, Lefranc F. Glutamate and malignant gliomas, from epilepsia to biological aggressiveness: therapeutic implications. Bull Cancer. 2013;100:9:829-835. doi: 10. 1684/bds. 2013. 1781
Campbell SL, Buckingham SC, Sontheimer H. Human glioma cells induce hyperexitability in cortical networks. Epilepsia. 2012;53:8:1360-1370. doi: 10. 1111/j. 1528-1167.2012.03557.x
Pallud J, Capelle L, Huberfeld G. Tumoral epileptogenicity: how does it happen? Epilepsia. 2013;54(Suppl 9):30-34. doi: 10. 1111/epi. 12440
Ruda R, Bello L, Duffau H, Soffetti R. Seizures in low-grade gliomas: natural history, pathogenesis, and outcome after treatments. Neuro Oncol. 2012;(suppl 4):55-64. doi: 10. 10.93/neuonc/nos 199
You G, Sha Z, Jiang T. The pathogenesis of tumor-related epilepsy and its implications for clinical treatment. Seizure. 2012;21:3:153-159. doi: 10. 1016/j. seizure. 2011. 12.016
Lee JW, Wen PY, Hurwitz S, Black P, Kessari S, Drappatz J, Golby AJ, Wells WM 3rd, Warfield SK, Kikinis R, Bromfield EB. Morphological characteristics of brain tumors causing seizures. Arch Neurol. 2010;67:3:336-342. doi: 10.1001/archneurol.2010.2
Pallud J, Audurau E, Blonski M, Sanai N, Bauchet L, Fontaine D, Mandonnet E, Dezamis E, Psimaras D, Guyotat J, Peruzzi P, Page P, Gal B, Parraga E, Baron MH, Vlaicu M, Guillevin R, Devaux B, Duffau H, Taillander L, Capelle L, Huberfeld G. Epileptic seizures in diffuse low-grade gliomas in adults. Brain. 2014;137(Pt 2):449-462. doi: 10.1093/brain/awt345
Taillandier L, Duffau H. Epilepsy and insular Grade II gliomas: an interdisciplinary point of view from retrospective monocentric series of 46 cases. Neurosurg Focus. 2009;27:2:8. doi: 10.3171/2009.6. FOCUS09102
Zaatreh MM, Firlik KS, Spencer DD, Spencer SS. Temporal lobe tumoral epilepsy: characteristics and predictors of surgical outcome. Neurol. 2003;61:5:636-641. PMID: 12963754.
Zaatreh MM, Spencer DD, Thompson JL, Blumenfeld H, Novotny EJ, Mattson RH, Spencer SS. Frontal lobe tumoral epilepsy: clinical, neurophysiologic features and predictors of surgical outcome. Epilepsia. 2002;43:7:727-733. PMID: 12102675
Isnard J, Guénot M, Sindou M, Mauguière F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia. 2004;45(9):1079-1090. PMID: 15329073
Guenot M, Isnard J. Epilepsy and insula. Neurochirurgie. 2008;54:3:374-381. doi: 10.1016/j.neuchi.2008.02.010
Isnard J. Insular epilepsy: a model of cryptic epilepsy. The Lyon experience. Rev Neurol. 2009;165:10:746-749. doi: 10.1016/J.neurol.2009.07.013
Isnard J, Mauguière F. The insula in partial epilepsy. Rev Neurol. 2005;161:1:17-26. PMID: 15677998
Nguyen DKh, Nguyen DB, Malak R, Leroux J-M, Carmant L, Saint-Hilaire J-M, Giard N, Cossette P, Bouthillier A. Revisting the role of the insula in refractory partial epilepsy. Epilepsia. 2009;50:3:510-520. doi: 10.1111/J.1528-1167.2008.01758.x
Karlov VA. Epilepsiya. M. 1990. (In Russ.).
Mukhin KYu, Petrukhin AS. Epilepsiya: osnovnye printsipy diagnostiki i lecheniya. www.Nevromed.ru/cosultations/epi/p_epi_basi. (In Russ.).
Mukhin KYu, Petrukhin AS, Mironov MB. Epilepticheskie sindromy. Diagnostika i terapiya. Spravochnoe rukovodstvo dlya vrachei. M. 2008;224. (In Russ.).
Wang Y, Qian T, You G, Peng X, Chen C, You Y, Yao K, Wu C, Ma J, Sha Z, Wang S, Jiang T. Localizing seizure-susceptible brain regions associated with low-grade gliomas using voxel-based lesion-symptom mapping. Neuro Oncol. 2014. pii:nou130
Putsillo MV, Vinokurov AG, Belov AI. Neirokhirurgicheskaya anatomiya. Atlas. Ch. II. M. 2007;306. (In Russ.).
Maffei A, Haley M, Fontanini A. Neural processing of gustatory information in insular circuits. Curr Opin Neurobiol. 2012;22:4:709-716. doi: 10/1016/j.conb.2012.04.001
Shelley BP, Trimble MR. The insular lobe of reil-its anatomico-functional, behavioural and neuropsychiatric attributes in humans — a rewiew. Wold J Biol Psychiatry. 2004;5:176-200. PMID: 15543513
Shi C-G, Cassell MD. Cortical, Thalamic and amygdaloid connections of the anterior and posterior insular cortices. J of Comparative Neurol. 1998;399:440-468. PMID: 9741477
Duffau H, Moritz-Gasser S, Gatignol P. Functional outcome after mapping for insular World Health Organization Grade II gliomas in the dominant hemisphere: experience with 24 patients. Neurosurg Focus. 2009;27:2:1-10.
Duffau H, Taillander L, Gatinol P, Capelle L. The insular lobe and brain plasticity: lessons from tumor surgery. Clin Neurol Neurosurg. 2006;108:6:543-548. PMID: 162113653
Shipley MT, Grinisman YA. Anatomical evidence for convergence of olfactory, gustatory and visceral afferent pathways in mouse cerebral cortex. Brain Res Bull. 1984;12:3:221-226. PMID: 6722597
Smith AR, Steinberg L, Chein J. The role of the anterior insula in adolescent decision making. Dev Neurosci. 2014.
Wager TD. From affect to control: functional specialization of the insula in motivation and regulation. www.affective-science.org/pubs/2004/Wager_submitted_copy.pdf
Wang X, Gu X, Fan J, Wang S, Zhao F, Hof PR, Liu P, Gao Z. Recovery of empathetic function following resection of insular gliomas. J Neurooncol. 2014;117;2:269-277. doi: 10. 1007/s11060-014-1380-y
Wu AS, Witgert ME, Lang FF, Xiao L, Bekele BN, Meyers CA, Ferson D, Wefel JS. Neurocognitive function before and after surgery for insular gliomas. J neurosurg. 2011;115:6:1115-1125. doi: 10/3171/2011.8.JNS11488
Craig AD. An interoceptive neuroanatomical perspective on feelings, energy and effort. Behav Brain Sci. 2013;36:6:685-726. doi: 10. 1017/S0140525X130011489
Chikama M, Mchfarland NR, Amaral DG, Haber SN. Insular cortical projections to functional regions of the striatum correlate with cortical cytoarchitectonic organization in the primate. J of Neurosci. 1997;17:9686-9705. PMID: 9391023
Wiech K, Jbabdi S, Lin CS, Andersson J, Tracey I. Differential structural and resting state connectivity between insular subdivisions and other pain-related brain regions. Pain. 2014;155:10:2047-2055. doi: 10.1016/j.pain.2014.07.009
Afif Afif, Minotti L, Kahane Ph, Hoffmann D. Anatomofunctional organization of the insular cortex: a study using intracerebral electrical stimulation in epileptic patients. Epilepsia. 2010;51:11:2305-2315. doi: 10.1111/j.1528-1167.2010.02755x
Mazzola L, Lopez C, Faillenot I, Chouchou F, Mauquiere F, Isnard J. Vestibular responses to direct stimulation of the human insular cortez. Ann Neueol. 2014;76:4:609-619. doi: 10.1002/ana.24252
Ostrowsky K, Isnard J, Ryvlin P, Guenot M, Fischer C, Mauguiere F. Functional mapping of the insular cortex: clinical implication in temporal lobe epilepsy. Epilepsia. 2000;41:6:681-686. PMID: 10840399
Bayer ShA. Neurogenesis in the rat primary olfactory cortex. Int J Devl Neuroscience. 1986;4:3:251-271. PMID: 3455589
Francis S, Rolls ET, Bowtell R, McGlone F, O’Doherty J, Browning A, Clare S, Smith E. The representation of pleasant touch in the brain and relationship with taste and olfactory areas. Cogninive Neurosci. 1999;10:453-459. PMID: 10208571
Rolls ET. The rules of formation of the olfactory representations found in the orbitofrontal cortex olfactory areas in primates. Chem Senses. 2001;26:595-604. PMID: 11418505
Rolls ET, Critchley HD, Verhagen JV, Kadohisa M. The representation of information about taste and odor in orbitofrontal cortex. Chem Percept. 2010;3:16-33. doi: 10.1007/s12078-009-9054-4
Frank S, Kullmann S, Veit R. Food related processes in the insular cortex. Front Hum Neurosci. 2013;7:499:1-6. doi: 3389/fnhum.2013.00499. eCollection 2013
Frank GK, Shott ME, Hagman JO, Mittal VA. Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. Am J Psychiatry. 2013;170:10:1152-1160. doi: 10.1176/appi.ajp.2013.12101294
Oberndorfer TA, Frank GK, Simmons AN, Wagner A, McCurdy D, Fudge JL, Yang TT, Paulus MP, Kaye WH. Altered insula response to sweet taste processing after recovery from anorexia and bulimia nervosa. Am J Psychiatry. 2013;170:10:1143-1151. doi: 10.1176/appi.ajp.2013.11111745
El Bouzidi K, Duncan S, Whittle IR, Butler CR. Lesional reflex epilepsy associated with the thought of food. Neurology. 2010;74:7:610-612. doi: 10.1212/WNL.0b013e3181cff6c3
Ferlazzo E, Zifkin BG, Andermann E, Andermann F. Cortical triggers in generalized reflex seizures and epilepsies. Brain. 2005;128:700-710. PMID: 15728654
Robertson WCJr, Fariello RG. Eating epilepsy associated with a deep forebrain glioma. Ann Neurol. 1979;6:3:271-273. Eating epilepsy associated with a deep forebrain glioma. Ann Neurol. 1979;6:3:271-273. PMID: 118704