Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection
Abstract Objective Epilepsy surgery is an effective treatment for drug‐resistant patients. However, how different surgical approaches affect long‐term brain structure remains poorly characterized. Here, we present a semiautomated method for quantifying structural changes after epilepsy surgery and c...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2023-06-01
|
| Series: | Epilepsia Open |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/epi4.12733 |
| _version_ | 1797813801886679040 |
|---|---|
| author | T. Campbell Arnold Lohith G. Kini John M. Bernabei Andrew Y. Revell Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Dario J. Englot Victoria L. Morgan Brian Litt Kathryn A. Davis |
| author_facet | T. Campbell Arnold Lohith G. Kini John M. Bernabei Andrew Y. Revell Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Dario J. Englot Victoria L. Morgan Brian Litt Kathryn A. Davis |
| author_sort | T. Campbell Arnold |
| collection | DOAJ |
| description | Abstract Objective Epilepsy surgery is an effective treatment for drug‐resistant patients. However, how different surgical approaches affect long‐term brain structure remains poorly characterized. Here, we present a semiautomated method for quantifying structural changes after epilepsy surgery and compare the remote structural effects of two approaches, anterior temporal lobectomy (ATL), and selective amygdalohippocampectomy (SAH). Methods We studied 36 temporal lobe epilepsy patients who underwent resective surgery (ATL = 22, SAH = 14). All patients received same‐scanner MR imaging preoperatively and postoperatively (mean 2 years). To analyze postoperative structural changes, we segmented the resection zone and modified the Advanced Normalization Tools (ANTs) longitudinal cortical pipeline to account for resections. We compared global and regional annualized cortical thinning between surgical treatments. Results Across procedures, there was significant cortical thinning in the ipsilateral insula, fusiform, pericalcarine, and several temporal lobe regions outside the resection zone as well as the contralateral hippocampus. Additionally, increased postoperative cortical thickness was seen in the supramarginal gyrus. Patients treated with ATL exhibited greater annualized cortical thinning compared with SAH cases (ATL: −0.08 ± 0.11 mm per year, SAH: −0.01 ± 0.02 mm per year, t = 2.99, P = 0.006). There were focal postoperative differences between the two treatment groups in the ipsilateral insula (P = 0.039, corrected). Annualized cortical thinning rates correlated with preoperative cortical thickness (r = 0.60, P < 0.001) and had weaker associations with age at surgery (r = −0.33, P = 0.051) and disease duration (r = −0.42, P = 0.058). Significance Our evidence suggests that selective procedures are associated with less cortical thinning and that earlier surgical intervention may reduce long‐term impacts on brain structure. |
| first_indexed | 2024-03-13T07:58:08Z |
| format | Article |
| id | doaj.art-6e8b20f7f78e4b2e959c76e9d88b37bf |
| institution | Directory Open Access Journal |
| issn | 2470-9239 |
| language | English |
| last_indexed | 2024-03-13T07:58:08Z |
| publishDate | 2023-06-01 |
| publisher | Wiley |
| record_format | Article |
| series | Epilepsia Open |
| spelling | doaj.art-6e8b20f7f78e4b2e959c76e9d88b37bf2023-06-02T03:50:17ZengWileyEpilepsia Open2470-92392023-06-018255957010.1002/epi4.12733Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resectionT. Campbell Arnold0Lohith G. Kini1John M. Bernabei2Andrew Y. Revell3Sandhitsu R. Das4Joel M. Stein5Timothy H. Lucas6Dario J. Englot7Victoria L. Morgan8Brian Litt9Kathryn A. Davis10Department of Bioengineering, School of Engineering & Applied Science University of Pennsylvania Philadelphia Pennsylvania USADepartment of Bioengineering, School of Engineering & Applied Science University of Pennsylvania Philadelphia Pennsylvania USADepartment of Bioengineering, School of Engineering & Applied Science University of Pennsylvania Philadelphia Pennsylvania USACenter for Neuroengineering and Therapeutics University of Pennsylvania Philadelphia Pennsylvania USADepartment of Neurology, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USADepartment of Radiology, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USACenter for Neuroengineering and Therapeutics University of Pennsylvania Philadelphia Pennsylvania USADepartment of Neurological Surgery Vanderbilt University Medical Center Nashville Tennessee USADepartment of Neurological Surgery Vanderbilt University Medical Center Nashville Tennessee USADepartment of Bioengineering, School of Engineering & Applied Science University of Pennsylvania Philadelphia Pennsylvania USACenter for Neuroengineering and Therapeutics University of Pennsylvania Philadelphia Pennsylvania USAAbstract Objective Epilepsy surgery is an effective treatment for drug‐resistant patients. However, how different surgical approaches affect long‐term brain structure remains poorly characterized. Here, we present a semiautomated method for quantifying structural changes after epilepsy surgery and compare the remote structural effects of two approaches, anterior temporal lobectomy (ATL), and selective amygdalohippocampectomy (SAH). Methods We studied 36 temporal lobe epilepsy patients who underwent resective surgery (ATL = 22, SAH = 14). All patients received same‐scanner MR imaging preoperatively and postoperatively (mean 2 years). To analyze postoperative structural changes, we segmented the resection zone and modified the Advanced Normalization Tools (ANTs) longitudinal cortical pipeline to account for resections. We compared global and regional annualized cortical thinning between surgical treatments. Results Across procedures, there was significant cortical thinning in the ipsilateral insula, fusiform, pericalcarine, and several temporal lobe regions outside the resection zone as well as the contralateral hippocampus. Additionally, increased postoperative cortical thickness was seen in the supramarginal gyrus. Patients treated with ATL exhibited greater annualized cortical thinning compared with SAH cases (ATL: −0.08 ± 0.11 mm per year, SAH: −0.01 ± 0.02 mm per year, t = 2.99, P = 0.006). There were focal postoperative differences between the two treatment groups in the ipsilateral insula (P = 0.039, corrected). Annualized cortical thinning rates correlated with preoperative cortical thickness (r = 0.60, P < 0.001) and had weaker associations with age at surgery (r = −0.33, P = 0.051) and disease duration (r = −0.42, P = 0.058). Significance Our evidence suggests that selective procedures are associated with less cortical thinning and that earlier surgical intervention may reduce long‐term impacts on brain structure.https://doi.org/10.1002/epi4.12733brain atrophycortical thicknesscortical thinningneurosurgeryseizurevirtual resection |
| spellingShingle | T. Campbell Arnold Lohith G. Kini John M. Bernabei Andrew Y. Revell Sandhitsu R. Das Joel M. Stein Timothy H. Lucas Dario J. Englot Victoria L. Morgan Brian Litt Kathryn A. Davis Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection Epilepsia Open brain atrophy cortical thickness cortical thinning neurosurgery seizure virtual resection |
| title | Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection |
| title_full | Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection |
| title_fullStr | Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection |
| title_full_unstemmed | Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection |
| title_short | Remote effects of temporal lobe epilepsy surgery: Long‐term morphological changes after surgical resection |
| title_sort | remote effects of temporal lobe epilepsy surgery long term morphological changes after surgical resection |
| topic | brain atrophy cortical thickness cortical thinning neurosurgery seizure virtual resection |
| url | https://doi.org/10.1002/epi4.12733 |
| work_keys_str_mv | AT tcampbellarnold remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT lohithgkini remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT johnmbernabei remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT andrewyrevell remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT sandhitsurdas remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT joelmstein remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT timothyhlucas remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT dariojenglot remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT victorialmorgan remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT brianlitt remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection AT kathrynadavis remoteeffectsoftemporallobeepilepsysurgerylongtermmorphologicalchangesaftersurgicalresection |