Neuroimaging features of the nervous system in young children with epileptic encephalopathies according to MR-tractography

Authors

DOI:

https://doi.org/10.15574/SP.2024.138.41

Keywords:

children, epileptic encephalopathies, neurodevelopmental disorders, cognitive and behavioral disorders, epileptic seizures, structural changes in the brain, magnetic resonance imaging, tractography

Abstract

The aim is to analyze neuroimaging changes in the nervous system of children of an early and preschool age with epileptic encephalopathies (EE) according to MR-tractography to improve the diagnosis of these conditions.

Materials and methods. 157 children aged 0 to 6 years with EE, epileptiform and developmental encephalopathies (DEE) were examined. The study included MR-tractography using a 3 Tesla MR scanner.

Fractional anisotropy (FA) and average diffusion coefficient (ADC) were determined in Broca's and Wernicke's areas, left arcuate tract, both uncinate tracts, corpus callosum and thalamus. The examined children were divided into 3 groups: I - 75 children with EE, with the onset of seizures before 1 year of age; II - 44 children with EE, with the onset of seizures at the age of 1-3 years; III - 38 children with DEE. Differences between groups were assessed using the Kruskal-Wallis test and Pearson's Chi-square (χ²) test.

Results. In children with EE from groups I and II, there was a significant decrease in FA and an increase in ADC in the areas of both language centers and the right uncinate tract in comparison with children of group III (p<0.05). In the group I with EE, there was a significant decrease in FA in the left uncinate tract, knee and trunk of the MT in comparison with the groups II and III of children (p<0.05).

It was found that more than 60% of children from group I had destruction of the fibers of the arcuate tract and in the area of one of the speech centers, and 70% had hypoplasia and destruction of the left uncinate tract. In the children of group II with EE, hypoplasia of the anterior (63.6%) and posterior (65.9%) parts of the arcuate tract and the right uncinate tract (81.8%) was detected. Among children from group III, more than 60% had an abnormal location of Broca's speech center, and more than 70 % had an abnormal location of Wernicke's center, almost 80 % had an abnormal location of the left uncinate tract.

Conclusions. It was found that in children with EE and DEE, according to MR tractography, there is a decrease in FA indicators and an increase in ADC in all studied structures (arcuate and uncinate tract, corpus callosum, thalamus) in comparison with the reference values given in the scientific literature. The detected changes indicate a violation of the structural integrity of the white matter in Broca's and Wernicke's centers and associative pathways, which will lead to the optimization of early diagnosis and prognosis of consequences in children with EE and DEE.

The study was carried out in accordance with the principles of the Declaration of Helsinki. The study protocol was approved by the Local Ethics Committees of the institutions indicated in the work. The informed consent of the children's parents was obtained for conducting the research.

No conflict of interest was declared by the authors.

References

Alyoubi RA, Daghistani RK, Albogmi AM, Alshahrany TA, Al Ahmed AB et al. (2023). The Spectrum of MRI and Electrographic Findings in Pediatric Patients With Seizures: A Retrospective Tertiary Care Center Study. Cureus. 15(3): e35851. https://doi.org/10.7759/cureus.35851

Bonekamp D, Nagae LM, Degaonkar M, Matson M, Abdalla WM, Barker PB et al. (2007, Jan 15). Diffusion tensor imaging in children and adolescents: reproducibility, hemispheric, and age-related differences. Neuroimage. 34(2): 733-742. Epub 2006 Nov 7. https://doi.org/10.1016/j.neuroimage.2006.09.020; PMid:17092743 PMCid:PMC1815474

Chen B, Linke A, Olson L, Kohli J, Kinnear M, Sereno M et al. (2022). Cortical myelination in toddlers and preschoolers with autism spectrum disorder. Developmental neurobiology. 82(3): 261-274. https://doi.org/10.1002/dneu.22874; PMid:35348301 PMCid:PMC9325547

Depienne C, Gourfinkel-An I, Baulac S et al. (2012). Genes in infantile epileptic encephalopathies. In: Noebels JL, Avoli M, Rogawski MA, et al., editors. Jasper's Basic Mechanisms of the Epilepsies. 4th edition. Bethesda (MD): National Center for Biotechnology Information (US); Table 1, Main etiologies of epileptic encephalopathies. URL: https://www.ncbi.nlm.nih.gov/books/NBK98182/table/depienne.t1/. https://doi.org/10.1093/med/9780199746545.003.0062

Gajdoš M, Říha P, Kojan M, Doležalová I, Mutsaerts HJMM et al. (2021). Epileptogenic zone detection in MRI negative epilepsy using adaptive thresholding of arterial spin labeling data. Scientific reports. 11(1): 10904. https://doi.org/10.1038/s41598-021-89774-4; PMid:34035336 PMCid:PMC8149682

Hakulinen U, Brander A, Ryymin P et al. (2012). Repeatability and variation of region-of-interest methods using quantitative diffusion tensor MR imaging of the brain. BMC MedImaging. 12: 30. https://doi.org/10.1186/1471-2342-12-30; PMid:23057584 PMCid:PMC3533516

Hrdlicka M, Sanda J, Urbanek T, Kudr M, Dudova I, Kickova S et al. (2019). Diffusion Tensor Imaging And Tractography In Autistic, Dysphasic, And Healthy Control Children. Neuropsychiatric disease and treatment. 15: 2843-2852. https://doi.org/10.2147/NDT.S219545; PMid:31632032 PMCid:PMC6781738

Japaridze N, Muthuraman M, Dierck C, von Spiczak S, Boor R, Mideksa KG et al. (2016). Neuronal networks in epileptic encephalopathies with CSWS. Epilepsia. 57(8): 1245-1255. https://doi.org/10.1111/epi.13428; PMid:27302532

Kabat J, Król P. (2012). Focal cortical dysplasia - review. Polish journal of radiology. 77(2): 35-43. https://doi.org/10.12659/PJR.882968; PMid:22844307 PMCid:PMC3403799

Khan S, Al Baradie R. (2012). Epileptic encephalopathies: an overview. Epilepsy research and treatment. 2012: 403592. https://doi.org/10.1155/2012/403592; PMid:23213494 PMCid:PMC3508533

Kimiwada T, Juhász C, Makki M, Muzik O, Chugani DC et al. (2006, Jan). Hippocampal and thalamic diffusion abnormalities in children with temporal lobe epilepsy. Epilepsia. 47(1): 167-175. https://doi.org/10.1111/j.1528-1167.2006.00383.x; PMid:16417545

Korostenskaja M, Griskova-Bulanova I, Lee KH, Chen P-C, Kleineschay T, Cook, J et al. (2014). Contributions of neuroimaging to understand childhood epileptic encephalopathies. Journal of Pediatric Epilepsy. 3. 131-156. https://doi.org/10.3233/PEP-14087

Kyrylova LH, Miroshnykov OO. (2020). Dyferentsialna diahnostyka syndromu rannoi dytiachoi nervovosti u praktytsi pediatra. Zdorov'ia dytyny. 15(5): 24-32.

Kyrylova LH, Miroshnykov OO. (2022). Klinichna otsinka efektyvnosti neiroprotektornoi terapii v ditei z porushenniamy movlennievoho y kohnityvnoho rozvytku. Mizhnarodnyi nevrolohichnyi zhurnal. 18(4): 17-23. https://doi.org/10.22141/2224-0713.18.4.2022.954

Lee MJ, Kim HD, Lee JS, Kim DS, Lee SK. (2013). Usefulness of diffusion tensor tractography in pediatric epilepsy surgery. Yonsei medical journal. 54(1): 21-27. https://doi.org/10.3349/ymj.2013.54.1.21; PMid:23225794 PMCid:PMC3521255

Li YH, Li JJ, Lu QC, Gong HQ, Liang PJ, Zhang PM. (2014). Involvement of thalamus in initiation of epileptic seizures induced by pilocarpine in mice. Neuralplasticity. 2014: 675128. https://doi.org/10.1155/2014/675128; PMid:24778885 PMCid:PMC3981117

Millichap JJ, Stack CV, Millichap JG. (2011). Frequency of Epileptiform Discharges in the Sleep-Deprived Electroencephalogram in Children Evaluated for Attention-Deficit Disorders. Journal of Child Neurology. 26(1): 6-11. https://doi.org/10.1177/0883073810371228; PMid:20716706

Moreno-Lopez Y, Bichara C, Delbecq G, Isope P, Cordero-Erausquin M. (2021). The corticospinal tract primarily modulates sensory inputs in the mouse lumbar cord. eLife. 10: e65304. https://doi.org/10.7554/eLife.65304; PMid:34497004 PMCid:PMC8439650

Ohtahara S, Yamatogi Y. (2003). Epileptic encephalopathies in early infancy with suppression-burst. Journal of Clinical Neurophysiology. 20(6): 398-407. https://doi.org/10.1097/00004691-200311000-00003; PMid:14734930

Rastin C, Schenkel LC, Sadikovic B. (2023). Complexity in Genetic Epilepsies: A Comprehensive Review. International journal of molecular sciences. 24(19): 14606. https://doi.org/10.3390/ijms241914606; PMid:37834053 PMCid:PMC10572646

Sartori S, Polli R, Bettella E et al. (2011). Pathogenic role of the X-linked cyclin-dependent kinase-like 5 and aristaless-related homeobox genes in epileptic encephalopathy of unknown etiology with onset in the first year of life. Journal of Child Neurology. 26(6): 683-691. https://doi.org/10.1177/0883073810387827; PMid:21482751

Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L et al. (2017). ILAE classification of the epilepsies: position paper of the ILAE commission for classification and terminology. Epilepsia. 58: 512-521. https://doi.org/10.1111/epi.13709; PMid:28276062 PMCid:PMC5386840

Shaikh Z, Torres A, Takeoka M. (2019). Neuroimaging in Pediatric Epilepsy. Brain sciences. 9(8): 190. https://doi.org/10.3390/brainsci9080190; PMid:31394851 PMCid:PMC6721420

Silver E, Korja R, Mainela-Arnold E, Pulli EP, Saukko E, Nolvi S et al. (2021). A systematic review of MRI studies of language development from birth to 2 years of age. Developmental neurobiology. 81(1): 63-75. https://doi.org/10.1002/dneu.22792; PMid:33220156

Takaya S, Liu H, Greve DN, Tanaka N, Leveroni C et al. (2016). Altered anterior-posterior connectivity through the arcuate fasciculus in temporal lobe epilepsy. Human brain mapping. 37(12): 4425-4438. https://doi.org/10.1002/hbm.23319; PMid:27452151 PMCid:PMC5319387

Urbach H, Scheiwe C, Shah MJ, Nakagawa JM, Heers M, San Antonio-Arce MV et al. (2023). Diagnostic Accuracy of Epilepsy-dedicated MRI with Post-processing. Clinical neuroradiology. 33(3): 709-719. https://doi.org/10.1007/s00062-023-01265-3; PMid:36856785 PMCid:PMC10449992

Wang I, Bernasconi A, Bernhardt B, Blumenfeld H, Cendes F, Chinvarun Y et al. (2020). MRI essentials in epileptology: a review from the ILAE Imaging Taskforce. Epileptic disorders : international epilepsy journal with videotape. 22(4): 421-437. https://doi.org/10.1684/epd.2020.1174; PMid:32763869

Von Der Heide RJ, Skipper LM, Klobusicky E, Olson IR. (2013). Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain : a journal of neurology. 136; Pt 6: 1692-1707. https://doi.org/10.1093/brain/awt094; PMid:23649697 PMCid:PMC3673595

Yamatogi Y, Ohtahara S. (2002). Early-infantile epileptic encephalopathy with suppression-bursts, Ohtahara syndrome; its overview referring to our 16 cases. Brainand Development. 24(1): 13-23. https://doi.org/10.1016/S0387-7604(01)00392-8; PMid:11751020

Yates L, Hobson H. (2020). Continuing to look in the mirror: A review of neuroscientific evidence for the broken mirror hypothesis, EP-M model and STORM model of autism spectrum conditions. Autism. 24(8): 1945-1959. https://doi.org/10.1177/1362361320936945; PMid:32668956 PMCid:PMC7539595

Published

2024-03-28

Issue

Section

Original articles