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Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia

BACKGROUND: Trigeminal Neuralgia (TN) is a chronic neurological disease that is strongly associated with neurovascular compression (NVC) of the trigeminal nerve near its root entry zone. The trigeminal nerve at the site of NVC has been extensively studied but limbic structures that are potentially i...

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Autores principales: Alper, Judy, Seifert, Alan C., Verma, Gaurav, Huang, Kuang-Han, Jacob, Yael, Al Qadi, Ameen, Rutland, John W., Patel, Sheetal, Bederson, Joshua, Shrivastava, Raj K., Delman, Bradley N., Balchandani, Priti
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Milan 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8461944/
https://www.ncbi.nlm.nih.gov/pubmed/34556025
http://dx.doi.org/10.1186/s10194-021-01325-4
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author Alper, Judy
Seifert, Alan C.
Verma, Gaurav
Huang, Kuang-Han
Jacob, Yael
Al Qadi, Ameen
Rutland, John W.
Patel, Sheetal
Bederson, Joshua
Shrivastava, Raj K.
Delman, Bradley N.
Balchandani, Priti
author_facet Alper, Judy
Seifert, Alan C.
Verma, Gaurav
Huang, Kuang-Han
Jacob, Yael
Al Qadi, Ameen
Rutland, John W.
Patel, Sheetal
Bederson, Joshua
Shrivastava, Raj K.
Delman, Bradley N.
Balchandani, Priti
author_sort Alper, Judy
collection PubMed
description BACKGROUND: Trigeminal Neuralgia (TN) is a chronic neurological disease that is strongly associated with neurovascular compression (NVC) of the trigeminal nerve near its root entry zone. The trigeminal nerve at the site of NVC has been extensively studied but limbic structures that are potentially involved in TN have not been adequately characterized. Specifically, the hippocampus is a stress-sensitive region which may be structurally impacted by chronic TN pain. As the center of the emotion-related network, the amygdala is closely related to stress regulation and may be associated with TN pain as well. The thalamus, which is involved in the trigeminal sensory pathway and nociception, may play a role in pain processing of TN. The objective of this study was to assess structural alterations in the trigeminal nerve and subregions of the hippocampus, amygdala, and thalamus in TN patients using ultra-high field MRI and examine quantitative differences in these structures compared with healthy controls. METHODS: Thirteen TN patients and 13 matched controls were scanned at 7-Tesla MRI with high resolution, T1-weighted imaging. Nerve cross sectional area (CSA) was measured and an automated algorithm was used to segment hippocampal, amygdaloid, and thalamic subregions. Nerve CSA and limbic structure subnuclei volumes were compared between TN patients and controls. RESULTS: CSA of the posterior cisternal nerve on the symptomatic side was smaller in patients (3.75 mm(2)) compared with side-matched controls (5.77 mm(2), p = 0.006). In TN patients, basal subnucleus amygdala volume (0.347 mm(3)) was reduced on the symptomatic side compared with controls (0.401 mm(3), p = 0.025) and the paralaminar subnucleus volume (0.04 mm(3)) was also reduced on the symptomatic side compared with controls (0.05 mm(3), p = 0.009). The central lateral thalamic subnucleus was larger in TN patients on both the symptomatic side (0.033 mm(3)) and asymptomatic side (0.035 mm(3)), compared with the corresponding sides in controls (0.025 mm(3) on both sides, p = 0.048 and p = 0.003 respectively). The inferior and lateral pulvinar thalamic subnuclei were both reduced in TN patients on the symptomatic side (0.2 mm(3) and 0.17 mm(3) respectively) compared to controls (0.23 mm(3), p = 0.04 and 0.18 mm(3), p = 0.04 respectively). No significant findings were found in the hippocampal subfields analyzed. CONCLUSIONS: These findings, generated through a highly sensitive 7 T MRI protocol, provide compelling support for the theory that TN neurobiology is a complex amalgamation of local structural changes within the trigeminal nerve and structural alterations in subnuclei of limbic structures directly and indirectly involved in nociception and pain processing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s10194-021-01325-4.
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spelling pubmed-84619442021-09-24 Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia Alper, Judy Seifert, Alan C. Verma, Gaurav Huang, Kuang-Han Jacob, Yael Al Qadi, Ameen Rutland, John W. Patel, Sheetal Bederson, Joshua Shrivastava, Raj K. Delman, Bradley N. Balchandani, Priti J Headache Pain Research Article BACKGROUND: Trigeminal Neuralgia (TN) is a chronic neurological disease that is strongly associated with neurovascular compression (NVC) of the trigeminal nerve near its root entry zone. The trigeminal nerve at the site of NVC has been extensively studied but limbic structures that are potentially involved in TN have not been adequately characterized. Specifically, the hippocampus is a stress-sensitive region which may be structurally impacted by chronic TN pain. As the center of the emotion-related network, the amygdala is closely related to stress regulation and may be associated with TN pain as well. The thalamus, which is involved in the trigeminal sensory pathway and nociception, may play a role in pain processing of TN. The objective of this study was to assess structural alterations in the trigeminal nerve and subregions of the hippocampus, amygdala, and thalamus in TN patients using ultra-high field MRI and examine quantitative differences in these structures compared with healthy controls. METHODS: Thirteen TN patients and 13 matched controls were scanned at 7-Tesla MRI with high resolution, T1-weighted imaging. Nerve cross sectional area (CSA) was measured and an automated algorithm was used to segment hippocampal, amygdaloid, and thalamic subregions. Nerve CSA and limbic structure subnuclei volumes were compared between TN patients and controls. RESULTS: CSA of the posterior cisternal nerve on the symptomatic side was smaller in patients (3.75 mm(2)) compared with side-matched controls (5.77 mm(2), p = 0.006). In TN patients, basal subnucleus amygdala volume (0.347 mm(3)) was reduced on the symptomatic side compared with controls (0.401 mm(3), p = 0.025) and the paralaminar subnucleus volume (0.04 mm(3)) was also reduced on the symptomatic side compared with controls (0.05 mm(3), p = 0.009). The central lateral thalamic subnucleus was larger in TN patients on both the symptomatic side (0.033 mm(3)) and asymptomatic side (0.035 mm(3)), compared with the corresponding sides in controls (0.025 mm(3) on both sides, p = 0.048 and p = 0.003 respectively). The inferior and lateral pulvinar thalamic subnuclei were both reduced in TN patients on the symptomatic side (0.2 mm(3) and 0.17 mm(3) respectively) compared to controls (0.23 mm(3), p = 0.04 and 0.18 mm(3), p = 0.04 respectively). No significant findings were found in the hippocampal subfields analyzed. CONCLUSIONS: These findings, generated through a highly sensitive 7 T MRI protocol, provide compelling support for the theory that TN neurobiology is a complex amalgamation of local structural changes within the trigeminal nerve and structural alterations in subnuclei of limbic structures directly and indirectly involved in nociception and pain processing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s10194-021-01325-4. Springer Milan 2021-09-23 /pmc/articles/PMC8461944/ /pubmed/34556025 http://dx.doi.org/10.1186/s10194-021-01325-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Alper, Judy
Seifert, Alan C.
Verma, Gaurav
Huang, Kuang-Han
Jacob, Yael
Al Qadi, Ameen
Rutland, John W.
Patel, Sheetal
Bederson, Joshua
Shrivastava, Raj K.
Delman, Bradley N.
Balchandani, Priti
Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title_full Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title_fullStr Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title_full_unstemmed Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title_short Leveraging high-resolution 7-tesla MRI to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
title_sort leveraging high-resolution 7-tesla mri to derive quantitative metrics for the trigeminal nerve and subnuclei of limbic structures in trigeminal neuralgia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8461944/
https://www.ncbi.nlm.nih.gov/pubmed/34556025
http://dx.doi.org/10.1186/s10194-021-01325-4
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