The role of the amygdala in ictal central apnea: insights from brain MRI morphometry

Abstract Objective Ictal central apnea (ICA) is a frequent correlate of focal seizures, particularly in temporal lobe epilepsy (TLE), and regarded as a potential electroclinical biomarker of sudden unexpected death in epilepsy (SUDEP). Aims of this study are to investigate morphometric changes of su...

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Main Authors: Elisa Micalizzi, Alice Ballerini, Giada Giovannini, Maria Cristina Cioclu, Simona Scolastico, Matteo Pugnaghi, Niccolò Orlandi, Marcella Malagoli, Maurilio Genovese, Alessandra Todeschini, Leandra Giunta, Flavio Villani, Stefano Meletti, Anna Elisabetta Vaudano
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Annals of Clinical and Translational Neurology
Online Access:https://doi.org/10.1002/acn3.51938
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author Elisa Micalizzi
Alice Ballerini
Giada Giovannini
Maria Cristina Cioclu
Simona Scolastico
Matteo Pugnaghi
Niccolò Orlandi
Marcella Malagoli
Maurilio Genovese
Alessandra Todeschini
Leandra Giunta
Flavio Villani
Stefano Meletti
Anna Elisabetta Vaudano
author_facet Elisa Micalizzi
Alice Ballerini
Giada Giovannini
Maria Cristina Cioclu
Simona Scolastico
Matteo Pugnaghi
Niccolò Orlandi
Marcella Malagoli
Maurilio Genovese
Alessandra Todeschini
Leandra Giunta
Flavio Villani
Stefano Meletti
Anna Elisabetta Vaudano
author_sort Elisa Micalizzi
collection DOAJ
description Abstract Objective Ictal central apnea (ICA) is a frequent correlate of focal seizures, particularly in temporal lobe epilepsy (TLE), and regarded as a potential electroclinical biomarker of sudden unexpected death in epilepsy (SUDEP). Aims of this study are to investigate morphometric changes of subcortical structures in ICA patients and to find neuroimaging biomarkers of ICA in patients with focal epilepsy. Methods We prospectively recruited focal epilepsy patients with recorded seizures during a video‐EEG long‐term monitoring with cardiorespiratory polygraphic recordings from April 2020 to September 2022. Participants were accordingly subdivided into two groups: patients with focal seizures with ICA (ICA) and without (noICA). A pool of 30 controls matched by age and sex was collected. All the participants underwent MRI scans with volumetric high‐resolution T1‐weighted images. Post‐processing analyses included a whole‐brain VBM analysis and segmentation algorithms performed with FreeSurfer. Results Forty‐six patients were recruited (aged 15–60 years): 16 ICA and 30 noICA. The whole‐brain VBM analysis showed an increased gray matter volume of the amygdala ipsilateral to the epileptogenic zone (EZ) in the ICA group compared to the noICA patients. Amygdala sub‐segmentation analysis revealed an increased volume of the whole amygdala, ipsilateral to the EZ compared to controls [F(1, 76) = 5.383, pFDR = 0.042] and to noICA patients ([F(1, 76) = 5.383, pFDR = 0.038], specifically of the basolateral complex (respectively F(1, 76) = 6.160, pFDR = 0.037; F(1, 76) = 5.121, pFDR = 0.034). Interpretation Our findings, while confirming the key role of the amygdala in participating in ictal respiratory modifications, suggest that structural modifications of the amygdala and its subnuclei may be valuable morphological biomarkers of ICA.
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spelling doaj.art-85186136f4cd4f65b9b8cd1f0f5f67e62024-01-16T18:36:37ZengWileyAnnals of Clinical and Translational Neurology2328-95032024-01-0111112113210.1002/acn3.51938The role of the amygdala in ictal central apnea: insights from brain MRI morphometryElisa Micalizzi0Alice Ballerini1Giada Giovannini2Maria Cristina Cioclu3Simona Scolastico4Matteo Pugnaghi5Niccolò Orlandi6Marcella Malagoli7Maurilio Genovese8Alessandra Todeschini9Leandra Giunta10Flavio Villani11Stefano Meletti12Anna Elisabetta Vaudano13Department of Neuroscience IRCCS San Martino Hospital Genoa ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Radiology AOU Modena Modena ItalyDepartment of Radiology AOU Modena Modena ItalyDepartment of Radiology AOU Modena Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Neuroscience IRCCS San Martino Hospital Genoa ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyDepartment of Biomedical, Metabolic and Neural Sciences University of Modena and Reggio Emilia Modena ItalyAbstract Objective Ictal central apnea (ICA) is a frequent correlate of focal seizures, particularly in temporal lobe epilepsy (TLE), and regarded as a potential electroclinical biomarker of sudden unexpected death in epilepsy (SUDEP). Aims of this study are to investigate morphometric changes of subcortical structures in ICA patients and to find neuroimaging biomarkers of ICA in patients with focal epilepsy. Methods We prospectively recruited focal epilepsy patients with recorded seizures during a video‐EEG long‐term monitoring with cardiorespiratory polygraphic recordings from April 2020 to September 2022. Participants were accordingly subdivided into two groups: patients with focal seizures with ICA (ICA) and without (noICA). A pool of 30 controls matched by age and sex was collected. All the participants underwent MRI scans with volumetric high‐resolution T1‐weighted images. Post‐processing analyses included a whole‐brain VBM analysis and segmentation algorithms performed with FreeSurfer. Results Forty‐six patients were recruited (aged 15–60 years): 16 ICA and 30 noICA. The whole‐brain VBM analysis showed an increased gray matter volume of the amygdala ipsilateral to the epileptogenic zone (EZ) in the ICA group compared to the noICA patients. Amygdala sub‐segmentation analysis revealed an increased volume of the whole amygdala, ipsilateral to the EZ compared to controls [F(1, 76) = 5.383, pFDR = 0.042] and to noICA patients ([F(1, 76) = 5.383, pFDR = 0.038], specifically of the basolateral complex (respectively F(1, 76) = 6.160, pFDR = 0.037; F(1, 76) = 5.121, pFDR = 0.034). Interpretation Our findings, while confirming the key role of the amygdala in participating in ictal respiratory modifications, suggest that structural modifications of the amygdala and its subnuclei may be valuable morphological biomarkers of ICA.https://doi.org/10.1002/acn3.51938
spellingShingle Elisa Micalizzi
Alice Ballerini
Giada Giovannini
Maria Cristina Cioclu
Simona Scolastico
Matteo Pugnaghi
Niccolò Orlandi
Marcella Malagoli
Maurilio Genovese
Alessandra Todeschini
Leandra Giunta
Flavio Villani
Stefano Meletti
Anna Elisabetta Vaudano
The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
Annals of Clinical and Translational Neurology
title The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
title_full The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
title_fullStr The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
title_full_unstemmed The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
title_short The role of the amygdala in ictal central apnea: insights from brain MRI morphometry
title_sort role of the amygdala in ictal central apnea insights from brain mri morphometry
url https://doi.org/10.1002/acn3.51938
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