Forniceal and hippocampal atrophy in temporal lobe epilepsy patients with a history of complex febrile convulsion

Year 2021, Volume: 15 Issue: 2, 137 - 144, 31.08.2021

Kaan Yücel Bahattin Hakyemez İbrahim Bora

Abstract

Objectives: Temporal lobe epilepsy (TLE) is the most common seizure type in adults. Recent studies showed that 28–58% of TLE patients had a previous history of complex febrile convulsions (CFC). We compared the hippocampal volumes and volumes of amygdaloid body and widths of fornix and mammillary bodies on magnetic resonance imaging (MRI) of TLE patients with and without history of CFC.
Methods: MRI scans of 42 subjects retrospectively examined. The amount of atrophy in hippocampus, amygdaloid body, fornix and mammillary bodies were determined by two formulas depending on the mean values of the controls.
Results: We found no difference between TLE patients with a history of CFC and TLE patients without such a history in terms of all the quantitative measurements results (p>0.05) except the absolute right-left hippocampus volume and fornix % difference rate (p<0.01, p<0.05 respectively).
Conclusion: Forniceal atrophy was more prominent in the TLE group of patients with previous CFC history when compared to those patients without a CFC history. The CFCs should not be underestimated in the childhood, as they are associated with more atrophy in the particular brain structures in patients with TLE.

Keywords

complex febrile convulsion, limbic system, magnetic resonance imaging, morphometry, temporal lobe epilepsy

References

• Cho YW, Kim KT. The latest classification of epilepsy and clinical significance of electroencephalography. Journal of Neurointensive Care 2019;2:1–3.
• Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J, Pringsheim T, Lorenzetti DL, Jetté N. Prevalence and incidence of epilepsy: a systematic review and meta-analysis of international studies. Neurology 2017;88:296–303.
• Blair RD. Temporal lobe epilepsy semiology. Epilepsy Res Treat 2012;2012:751510.
• Cendes F. Mesial temporal lobe epilepsy syndrome: an updated overview. Journal of Epilepsy and Clinical Neurophysiology 2005;11: 141–4.
• Farias-Serratos F, Kensuke K, Nobuhito S. Temporal lobe epilepsy. Archivos de Neurociencias (Mex) 2014;19:88–94.
• Granados Sánchez AM, Orejuela Zapata JF. Diagnosis of mesial temporal sclerosis: sensitivity, specificity and predictive values of the quantitative analysis of magnetic resonance imaging. Neuroradiol J 2018;31:50–9.
• Beheshti I, Sone D, Farokhian F, Maikusa N, Matsuda H. Gray matter and white matter abnormalities in temporal lobe epilepsy patients with and without hippocampal sclerosis. Front Neurol 2018;13;9: 107.
• Sone D, Ota M, Maikusa N, Kimura Y, Sumida K, Yokoyama K, Imabayashi E, Watanabe M, Watanabe Y, Okazaki M, Sato N, Matsuda H. White matter abnormalities in patients with temporal lobe epilepsy and amygdaloid body enlargement: comparison with hippocampal sclerosis and healthy subjects. Epilepsy Res 2016;127: 221–8.
• Cascino GD. Temporal lobe epilepsy: more than hippocampal pathology. Epilepsy Curr 2005;5:187–9.
• Baldwin GN, Tsuruda JS, Maravilla KR, Hamill GS, Hayes CE. The fornix in patients with seizures caused by unilateral hippocampal sclerosis: detection of unilateral volume loss on MR images. AJR Am J Roentgenol 1994;162:1185–9.
• Ng SE, Lau TN, Hui FK, Chua GE, Lee WL, Chee MW, Chee TS, Boey HK. MRI of the fornix and mamillary body in temporal lobe epilepsy. Neuroradiology 1997;39:551–5.
• O’Brien CE, Cook MJ, Boweden S, Vogrin SJ. Modelling human medial temporal lobe structures and mamillary bodies using volumetric MRI. Proceedings of Annual Meeting of the American Epilepsy Society, Orlando, Florida, United States of America. Epilepsia 1999; 40:188.
• Salmenpera T, Kalviainen R, Partanen K, Pitkanen A. Hippocampal and amygdaloid damage in partial epilepsy: a cross-sectional MRI study of 241 patients. Epilepsy Res 2001;46:69–82.
• Rocca WA, Sharbrough FW, Hauser WA, Annegers JF, Schoenberg BS. Risk factors for complex partial seizures: a population-based case-control study. Annals of Neurology 1987;21:22–31.
• Baram TZ, Jackson GD, Soltesz I, Sperber EE. Do febrile seizures cause temporal lobe epilepsy? an update. Proceedings of Annual Meeting of the American Epilepsy Society, Orlando, Florida, United States of America, Epilepsia 1999;40:S3.
• Berg AT, Shinnar S. Complex febrile seizures. Epilepsia 1996;37:126– 33.
• Tasch E, Cendes F, Li LM, Dubeau F, Andermann F, Arnold DL. Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol 1999;45:568–76.
• Spanaki MV, Kopylev L, Liow K, DeCarli C, Fazilat S, Gaillard WD, Theodore WH. Relationship of seizure frequency to hippocampus volume and metabolism in temporal lobe epilepsy. Epilepsia 2000;41: 1227–9.
• Cendes F, Andermann F, Dubeau F, Gloor P, Evans A, Jones-Gotman M, Olivier A, Andermann E, Robitaille Y, Lopes-Cendes I, Peters T, Melanson D. Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study. Neurology 1993;43:1083– 7.
• Maher J, McLachlan RS. Febrile convulsions. Is seizure duration the most important predictor of temporal lobe epilepsy? Brain 1995;118: 1521–8.
• Gulec G, Noyan B. Do recurrent febrile convulsions decrease the threshold for pilocarpine-induced seizures? Effects of nitric oxide. Brain Res Dev Brain Res 2001;126:223–8.
• Sagar HJ, Oxbury JM. Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann Neurol 1987;22:334–40.
• Meldrum BS. Anatomy, physiology, and pathology of epilepsy. Lancet 1990;336:231–4.
• Al Sufiani F, Ang LC. Neuropathology of temporal lobe epilepsy. Epilepsy Res Treat 2012;2012:624519.
• Patterson KP, Baram TZ, Shinnar S. Origins of temporal lobe epilepsy: febrile seizures and febrile status epilepticus. Neurotherapeutics 2014;11:242–50.
• Cendes F, Andermann F, Gloor P, Lopes-Cendes I, Andermann E, Melanson D, Jones-Gotman M, Robitaille Y, Evans A, Peters T. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures? Ann Neurol 1993;34:795– 801.
• Santana MT, Jackowski AP, da Silva HH, Caboclo LO, Centeno RS, Bressan RA, Carrete H Jr, Yacubian EM. Auras and clinical features in temporal lobe epilepsy: a new approach on the basis of voxel-based morphometry. Epilepsy Res 2010;89:327–38.
• Finegersh A, Avedissian C, Shamim S, Dustin I, Thompson PM, Theodore WH. Bilateral hippocampal atrophy in temporal lobe epilepsy: effect of depressive symptoms and febrile seizures. Epilepsia 2011;52:689–97.
• Gong G, Alexander RP, Shi F, Beaulieu C, Gross DW. Isolated febrile seizures are not associated with structural abnormalities of the limbic system. Epilepsy Res 2012;102:216–20.
• Adam C, Baulac M, Saint-Hilaire JM, Landau J, Granat O, Laplane D. Value of magnetic resonance imaging-based measurements of hippocampal formations in patients with partial epilepsy. Arch Neurol 1994;51:130–8.
• Güven A, Deda G, Şalvarlı Ş, Uysal S, Erden I, Karagöl U. Measurement of hippocampal volume in children with early febrile seizures. Proceedings of 23rd International Epilepsy Congress, Prag, Czech Republic. Epilepsia 1999;40:S45.
• Cendes F, Andermann F, Gloor P, Evans A, Jones-Gotman M, Watson C, Melanson D, Olivier A, Peters T, Lopes-Cendes I, Leroux G. MRI volumetric measurement of amygdaloid body and hippocampus in temporal lobe epilepsy. Neurology 1993;43:719–25.
• Yücel K, Hakyemez B, Parlak M, Oygucu IH. Morphometry of some elements of limbic system in normal population: a quantitative MRI study. Neuroanatomy 2002;1:15–21.
• Free SL, Bergin PS, Fish DR, Cook MJ, Shorvon SD, Stevens JM. Methods for normalization of hippocampal volumes measured with MR. JNR Am J Neuroradiol 1995;16:637–43.
• Cook M, Stevens JM. Imaging in epilepsy. In: Hopkins A, Shorvon S, Cascino G, editors. Epilepsy, 2nd ed. London: Chapman and Hall Medial; 1995. p. 143–54.
• Cook MJ, Fish DR, Shorvon SD, Straughan K, Stevens JM. Hippocampal volumetric and morphometric studies in frontal and temporal lobe epilepsy. Brain 1992;115:1001–15.
• Jack CR Jr, Sharbrough FW, Twomey CK, Cascino GD, Hirschorn KA, Marsh WR, Zinsmeister AR, Scheithauer B. Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. Radiology 1990;175:423–9.
• Farid N, Girard HM, Kemmotsu N, Smith ME, Magda SW, Lim WY, Lee RR, McDonald CR. Temporal lobe epilepsy: quantitative MR volumetry in detection of hippocampal atrophy. Radiology 2012; 264:542–50.
• Bower SP, Kilpatrick CJ, Vogrin SJ, Morris K, Cook MJ. Degree of hippocampal atrophy is not related to a history of febrile seizures in patients with proved hippocampal sclerosis. J Neurol Neurosurg Psychiatry 2000;69:733–88.
• Notenboom RGE, Ramakers GMJ, Kamal A, Spruijt BM, de Graan PNE. Long-lasting modulation of synaptic plasticity in rat hippocampus after early-life complex febrile seizures. Eur J Neurosci 2010;32: 749–58.
• Li Y, Wang C, Wang P, Li X, Zhou L. Effects of febrile seizures in mesial temporal lobe epilepsy with hippocampal sclerosis on gene expression using bioinformatical analysis. Acta Epileptologica 2020;2: 20.
• Ramantani G, Holthausen H. Epilepsy after cerebral infection: review of the literature and the potential for surgery. Epileptic Disord 2017;19:117–36.
• Baulac M. MTLE with hippocampal sclerosis in adult as a syndrome. Rev Neurol (Paris) 2015;171:259–66.
• Mayanagi Y, Watanabe E, Kaneko Y. Mesial temporal lobe epilepsy: clinical features and seizure mechanism. Epilepsia 1996;37:S57–S60.
• Kim JS, Koo DL, Joo EY, Kim ST, Seo DW, Hong SB. Asymmetric gray matter volume changes associated with epilepsy duration and seizure frequency in temporal-lobe-epilepsy patients with favorable surgical outcome. J Clin Neurol 2016;12:323–31.
• Fuerst D, Shah J, Kupsky WJ, Johnson R, Shah A, Hayman-Abello B, Ergh T, Poore Q, Canady A, Watson C. Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis. Neurology 2001;57:184–8.
• Mamourian AC, Cho CH, Saykin AJ, Poppito NL. Association between size of the lateral ventricle and asymmetry of the fornix in patients with temporal lobe epilepsy. AJNR Am J Neuroradiol 1998;19:9–13.
• Kim JH, Tien RD, Felsberg GJ, Osumi AK, Lee N. Clinical significance of asymmetry of the fornix and mamillary body on MR in hippocampal sclerosis. AJNR Am J Neuroradiol 1995;16:509–15.
• Pujar SS, Seunarine KK, Martinos MM, Neville BGR, Scott RC, Chin RFM, Clark CA. Long-term white matter tract reorganization following prolonged febrile seizures. Epilepsia 2017;58:772–80.
• Fitsiori A, Hiremath SB, Boto J, Garibotto V, Vargas MI. Morphological and advanced imaging of epilepsy: beyond the basics. Children (Basel) 2019;6:43.