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The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response

BACKGROUND: Medically-refractory trigeminal neuralgia (TN) can be treated successfully with operative intervention, but a significant proportion of patients are non-responders despite undergoing technically successful surgery. The thalamus is a key component of the trigeminal sensory pathway involve...

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Autores principales: Danyluk, Hayden, Andrews, Jennifer, Kesarwani, Rohit, Seres, Peter, Broad, Robert, Wheatley, B. Matt, Sankar, Tejas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8305513/
https://www.ncbi.nlm.nih.gov/pubmed/34303364
http://dx.doi.org/10.1186/s12883-021-02323-4
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author Danyluk, Hayden
Andrews, Jennifer
Kesarwani, Rohit
Seres, Peter
Broad, Robert
Wheatley, B. Matt
Sankar, Tejas
author_facet Danyluk, Hayden
Andrews, Jennifer
Kesarwani, Rohit
Seres, Peter
Broad, Robert
Wheatley, B. Matt
Sankar, Tejas
author_sort Danyluk, Hayden
collection PubMed
description BACKGROUND: Medically-refractory trigeminal neuralgia (TN) can be treated successfully with operative intervention, but a significant proportion of patients are non-responders despite undergoing technically successful surgery. The thalamus is a key component of the trigeminal sensory pathway involved in transmitting facial pain, but the role of the thalamus in TN, and its influence on durability of pain relief after TN surgery, are relatively understudied. We aimed to test the hypothesis that variations in thalamic structure and metabolism are related to surgical non-response in TN. METHODS: We performed a longitudinal, peri-operative neuroimaging study of the thalamus in medically-refractory TN patients undergoing microvascular decompression or percutaneous balloon compression rhizotomy. Patients underwent structural MRI and MR spectroscopy scans pre-operatively and at 1-week following surgery, and were classified as responders or non-responders based on 1-year post-operative pain outcome. Thalamus volume, shape, and metabolite concentration (choline/creatine [Cho/Cr] and N-acetylaspartate/creatine [NAA/Cr]) were evaluated at baseline and 1-week, and compared between responders, non-responders, and healthy controls. RESULTS: Twenty healthy controls and 23 patients with medically-refractory TN treated surgically (17 responders, 6 non-responders) were included. Pre-operatively, TN patients as a group showed significantly larger thalamus volume contralateral to the side of facial pain. However, vertex-wise shape analysis showed significant contralateral thalamus volume reduction in non-responders compared to responders in an axially-oriented band spanning the outer thalamic circumference (peak p = 0.019). Further, while pre-operative thalamic metabolite concentrations did not differ between responders and non-responders, as early as 1-week after surgery, long-term non-responders showed a distinct decrease in contralateral thalamic Cho/Cr and NAA/Cr, irrespective of surgery type, which was not observed in responders. CONCLUSIONS: Atrophy of the contralateral thalamus is a consistent feature across patients with medically-refractory TN. Regional alterations in preoperative thalamic structure, and very early post-operative metabolic changes in the thalamus, both appear to influence the durability of pain relief after TN surgery. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12883-021-02323-4.
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spelling pubmed-83055132021-07-28 The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response Danyluk, Hayden Andrews, Jennifer Kesarwani, Rohit Seres, Peter Broad, Robert Wheatley, B. Matt Sankar, Tejas BMC Neurol Research Article BACKGROUND: Medically-refractory trigeminal neuralgia (TN) can be treated successfully with operative intervention, but a significant proportion of patients are non-responders despite undergoing technically successful surgery. The thalamus is a key component of the trigeminal sensory pathway involved in transmitting facial pain, but the role of the thalamus in TN, and its influence on durability of pain relief after TN surgery, are relatively understudied. We aimed to test the hypothesis that variations in thalamic structure and metabolism are related to surgical non-response in TN. METHODS: We performed a longitudinal, peri-operative neuroimaging study of the thalamus in medically-refractory TN patients undergoing microvascular decompression or percutaneous balloon compression rhizotomy. Patients underwent structural MRI and MR spectroscopy scans pre-operatively and at 1-week following surgery, and were classified as responders or non-responders based on 1-year post-operative pain outcome. Thalamus volume, shape, and metabolite concentration (choline/creatine [Cho/Cr] and N-acetylaspartate/creatine [NAA/Cr]) were evaluated at baseline and 1-week, and compared between responders, non-responders, and healthy controls. RESULTS: Twenty healthy controls and 23 patients with medically-refractory TN treated surgically (17 responders, 6 non-responders) were included. Pre-operatively, TN patients as a group showed significantly larger thalamus volume contralateral to the side of facial pain. However, vertex-wise shape analysis showed significant contralateral thalamus volume reduction in non-responders compared to responders in an axially-oriented band spanning the outer thalamic circumference (peak p = 0.019). Further, while pre-operative thalamic metabolite concentrations did not differ between responders and non-responders, as early as 1-week after surgery, long-term non-responders showed a distinct decrease in contralateral thalamic Cho/Cr and NAA/Cr, irrespective of surgery type, which was not observed in responders. CONCLUSIONS: Atrophy of the contralateral thalamus is a consistent feature across patients with medically-refractory TN. Regional alterations in preoperative thalamic structure, and very early post-operative metabolic changes in the thalamus, both appear to influence the durability of pain relief after TN surgery. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12883-021-02323-4. BioMed Central 2021-07-24 /pmc/articles/PMC8305513/ /pubmed/34303364 http://dx.doi.org/10.1186/s12883-021-02323-4 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
Danyluk, Hayden
Andrews, Jennifer
Kesarwani, Rohit
Seres, Peter
Broad, Robert
Wheatley, B. Matt
Sankar, Tejas
The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title_full The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title_fullStr The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title_full_unstemmed The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title_short The thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
title_sort thalamus in trigeminal neuralgia: structural and metabolic abnormalities, and influence on surgical response
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8305513/
https://www.ncbi.nlm.nih.gov/pubmed/34303364
http://dx.doi.org/10.1186/s12883-021-02323-4
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