Regional brain morphology predicts pain relief in trigeminal neuralgia

Background: Trigeminal neuralgia, a severe chronic neuropathic pain disorder, is widely believed to be amenable to surgical treatments. Nearly 20% of patients, however, do not have adequate pain relief after surgery. Objective tools for personalized pre-treatment prognostication of pain relief follo...

Full description

Bibliographic Details
Main Authors: Peter Shih-Ping Hung, Alborz Noorani, Jia Y. Zhang, Sarasa Tohyama, Normand Laperriere, Karen D. Davis, David J. Mikulis, Frank Rudzicz, Mojgan Hodaie
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221001509
_version_ 1818882665651109888
author Peter Shih-Ping Hung
Alborz Noorani
Jia Y. Zhang
Sarasa Tohyama
Normand Laperriere
Karen D. Davis
David J. Mikulis
Frank Rudzicz
Mojgan Hodaie
author_facet Peter Shih-Ping Hung
Alborz Noorani
Jia Y. Zhang
Sarasa Tohyama
Normand Laperriere
Karen D. Davis
David J. Mikulis
Frank Rudzicz
Mojgan Hodaie
author_sort Peter Shih-Ping Hung
collection DOAJ
description Background: Trigeminal neuralgia, a severe chronic neuropathic pain disorder, is widely believed to be amenable to surgical treatments. Nearly 20% of patients, however, do not have adequate pain relief after surgery. Objective tools for personalized pre-treatment prognostication of pain relief following surgical interventions can minimize unnecessary surgeries and thus are of substantial benefit for patients and clinicians. Purpose: To determine if pre-treatment regional brain morphology-based machine learning models can prognosticate 1 year response to Gamma Knife radiosurgery for trigeminal neuralgia. Methods: We used a data-driven approach that combined retrospective structural neuroimaging data and support vector machine-based machine learning to produce robust multivariate prediction models of pain relief following Gamma Knife radiosurgery for trigeminal neuralgia. Surgical response was defined as ≥ 75% pain relief 1 year post-treatment. We created two prediction models using pre-treatment regional brain gray matter morphology (cortical thickness or surface area) to distinguish responders from non-responders to radiosurgery. Feature selection was performed through sequential backwards selection algorithm. Model out-of-sample generalizability was estimated via stratified 10-fold cross-validation procedure and permutation testing. Results: In 51 trigeminal neuralgia patients (35 responders, 16 non-responders), machine learning models based on pre-treatment regional brain gray matter morphology (14 regional surface areas or 13 regional cortical thicknesses) provided robust a priori prediction of surgical response. Cross-validation revealed the regional surface area model was 96.7% accurate, 100.0% sensitive, and 89.1% specific while the regional cortical thickness model was 90.5% accurate, 93.5% sensitive, and 83.7% specific. Permutation testing revealed that both models performed beyond pure chance (p < 0.001). The best predictor for regional surface area model and regional cortical thickness model was contralateral superior frontal gyrus and contralateral isthmus cingulate gyrus, respectively. Conclusions: Our findings support the use of machine learning techniques in subsequent investigations of chronic neuropathic pain. Furthermore, our multivariate framework provides foundation for future development of generalizable, artificial intelligence-driven tools for chronic neuropathic pain treatments.
first_indexed 2024-12-19T15:21:22Z
format Article
id doaj.art-75cf11bf122a476784544a3ac8eac2ad
institution Directory Open Access Journal
issn 2213-1582
language English
last_indexed 2024-12-19T15:21:22Z
publishDate 2021-01-01
publisher Elsevier
record_format Article
series NeuroImage: Clinical
spelling doaj.art-75cf11bf122a476784544a3ac8eac2ad2022-12-21T20:15:59ZengElsevierNeuroImage: Clinical2213-15822021-01-0131102706Regional brain morphology predicts pain relief in trigeminal neuralgiaPeter Shih-Ping Hung0Alborz Noorani1Jia Y. Zhang2Sarasa Tohyama3Normand Laperriere4Karen D. Davis5David J. Mikulis6Frank Rudzicz7Mojgan Hodaie8Division of Brain, Imaging &amp; Behaviour, Krembil Brain Institute, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, CanadaDivision of Brain, Imaging &amp; Behaviour, Krembil Brain Institute, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, CanadaSchulich School of Medicine &amp; Dentistry, Western University, London, Ontario, CanadaDivision of Brain, Imaging &amp; Behaviour, Krembil Brain Institute, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, CanadaDepartment of Radiation Oncology, University of Toronto, Toronto, Ontario, CanadaDivision of Brain, Imaging &amp; Behaviour, Krembil Brain Institute, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; Department of Surgery, Faculty of Medicine, University of Toronto, Toronto, Ontario, CanadaInstitute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; Division of Neuroradiology, Joint Department of Medical Imaging, University Health Network, Toronto Western Hospital, Toronto, Ontario, CanadaDepartment of Computer Science, University of Toronto, Toronto, Ontario, Canada; Vector Institute for Artificial Intelligence, Toronto, Ontario, Canada; Li Ka Shing Knowledge Institute, St Michael’s Hospital, Toronto, Ontario, CanadaDivision of Brain, Imaging &amp; Behaviour, Krembil Brain Institute, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; Department of Surgery, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; Division of Neurosurgery, Krembil Neuroscience Centre, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada; Corresponding author at: Toronto Western Hospital, Division of Neurosurgery, 399 Bathurst Street, 4W W-443, Toronto, Ontario M5T 2S8, Canada.Background: Trigeminal neuralgia, a severe chronic neuropathic pain disorder, is widely believed to be amenable to surgical treatments. Nearly 20% of patients, however, do not have adequate pain relief after surgery. Objective tools for personalized pre-treatment prognostication of pain relief following surgical interventions can minimize unnecessary surgeries and thus are of substantial benefit for patients and clinicians. Purpose: To determine if pre-treatment regional brain morphology-based machine learning models can prognosticate 1 year response to Gamma Knife radiosurgery for trigeminal neuralgia. Methods: We used a data-driven approach that combined retrospective structural neuroimaging data and support vector machine-based machine learning to produce robust multivariate prediction models of pain relief following Gamma Knife radiosurgery for trigeminal neuralgia. Surgical response was defined as ≥ 75% pain relief 1 year post-treatment. We created two prediction models using pre-treatment regional brain gray matter morphology (cortical thickness or surface area) to distinguish responders from non-responders to radiosurgery. Feature selection was performed through sequential backwards selection algorithm. Model out-of-sample generalizability was estimated via stratified 10-fold cross-validation procedure and permutation testing. Results: In 51 trigeminal neuralgia patients (35 responders, 16 non-responders), machine learning models based on pre-treatment regional brain gray matter morphology (14 regional surface areas or 13 regional cortical thicknesses) provided robust a priori prediction of surgical response. Cross-validation revealed the regional surface area model was 96.7% accurate, 100.0% sensitive, and 89.1% specific while the regional cortical thickness model was 90.5% accurate, 93.5% sensitive, and 83.7% specific. Permutation testing revealed that both models performed beyond pure chance (p < 0.001). The best predictor for regional surface area model and regional cortical thickness model was contralateral superior frontal gyrus and contralateral isthmus cingulate gyrus, respectively. Conclusions: Our findings support the use of machine learning techniques in subsequent investigations of chronic neuropathic pain. Furthermore, our multivariate framework provides foundation for future development of generalizable, artificial intelligence-driven tools for chronic neuropathic pain treatments.http://www.sciencedirect.com/science/article/pii/S2213158221001509Trigeminal neuralgiaChronic neuropathic painMachine learningPain reliefBrain morphology
spellingShingle Peter Shih-Ping Hung
Alborz Noorani
Jia Y. Zhang
Sarasa Tohyama
Normand Laperriere
Karen D. Davis
David J. Mikulis
Frank Rudzicz
Mojgan Hodaie
Regional brain morphology predicts pain relief in trigeminal neuralgia
NeuroImage: Clinical
Trigeminal neuralgia
Chronic neuropathic pain
Machine learning
Pain relief
Brain morphology
title Regional brain morphology predicts pain relief in trigeminal neuralgia
title_full Regional brain morphology predicts pain relief in trigeminal neuralgia
title_fullStr Regional brain morphology predicts pain relief in trigeminal neuralgia
title_full_unstemmed Regional brain morphology predicts pain relief in trigeminal neuralgia
title_short Regional brain morphology predicts pain relief in trigeminal neuralgia
title_sort regional brain morphology predicts pain relief in trigeminal neuralgia
topic Trigeminal neuralgia
Chronic neuropathic pain
Machine learning
Pain relief
Brain morphology
url http://www.sciencedirect.com/science/article/pii/S2213158221001509
work_keys_str_mv AT petershihpinghung regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT alborznoorani regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT jiayzhang regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT sarasatohyama regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT normandlaperriere regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT karenddavis regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT davidjmikulis regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT frankrudzicz regionalbrainmorphologypredictspainreliefintrigeminalneuralgia
AT mojganhodaie regionalbrainmorphologypredictspainreliefintrigeminalneuralgia