Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy

Marian Galovic, Irene Baudracco, Evan Wright-Goff, Galo Pillajo, Parashkev Nachev, Britta Wandschneider, Friedrich Woermann, Pamela Thompson, Sallie Baxendale, Andrew W. McEvoy, Mark Nowell, Matteo Mancini, Sjoerd B. Vos, Gavin P. Winston, Rachel Sparks, Ferran Prados, Anna Miserocchi, Jane De Tisi, Louis André Van Graan, Roman RodionovChengyuan Wu, Mahdi Alizadeh, Lauren Kozlowski, Ashwini D. Sharan, Lohith G. Kini, Kathryn A. Davis, Brian Litt, Sebastien Ourselin, Solomon L. Moshé, Solomon L. Moshe, Wolfgang Löscher, John S. Duncan, Matthias J. Koepp

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2 Citations (Scopus)

Abstract

Importance: A functional area associated with the piriform cortex, termed area tempestas, has been implicated in animal studies as having a crucial role in modulating seizures, but similar evidence is limited in humans. Objective: To assess whether removal of the piriform cortex is associated with postoperative seizure freedom in patients with temporal lobe epilepsy (TLE) as a proof-of-concept for the relevance of this area in human TLE. Design, Setting, and Participants: This cohort study used voxel-based morphometry and volumetry to assess differences in structural magnetic resonance imaging (MRI) scans in consecutive patients with TLE who underwent epilepsy surgery in a single center from January 1, 2005, through December 31, 2013. Participants underwent presurgical and postsurgical structural MRI and had at least 2 years of postoperative follow-up (median, 5 years; range, 2-11 years). Patients with MRI of insufficient quality were excluded. Findings were validated in 2 independent cohorts from tertiary epilepsy surgery centers. Study follow-up was completed on September 23, 2016, and data were analyzed from September 24, 2016, through April 24, 2018. Exposures: Standard anterior temporal lobe resection. Main Outcomes and Measures: Long-term postoperative seizure freedom. Results: In total, 107 patients with unilateral TLE (left-sided in 68; 63.6% women; median age, 37 years [interquartile range {IQR}, 30-45 years]) were included in the derivation cohort. Reduced postsurgical gray matter volumes were found in the ipsilateral piriform cortex in the postoperative seizure-free group (n = 46) compared with the non-seizure-free group (n = 61). A larger proportion of the piriform cortex was resected in the seizure-free compared with the non-seizure-free groups (median, 83% [IQR, 64%-91%] vs 52% [IQR, 32%-70%]; P <.001). The results were seen in left- and right-sided TLE and after adjusting for clinical variables, presurgical gray matter alterations, presurgical hippocampal volumes, and the proportion of white matter tract disconnection. Findings were externally validated in 2 independent cohorts (31 patients; left-sided TLE in 14; 54.8% women; median age, 41 years [IQR, 31-46 years]). The resected proportion of the piriform cortex was individually associated with seizure outcome after surgery (derivation cohort area under the curve, 0.80 [P <.001]; external validation cohorts area under the curve, 0.89 [P <.001]). Removal of at least half of the piriform cortex increased the odds of becoming seizure free by a factor of 16 (95% CI, 5-47; P <.001). Other mesiotemporal structures (ie, hippocampus, amygdala, and entorhinal cortex) and the overall resection volume were not associated with outcomes. Conclusions and Relevance: These results support the importance of resecting the piriform cortex in neurosurgical treatment of TLE and suggest that this area has a key role in seizure generation.

Original languageEnglish (US)
JournalJAMA Neurology
DOIs
StatePublished - Jan 1 2019

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Temporal Lobe Epilepsy
Seizures
Magnetic Resonance Imaging
Area Under Curve
Epilepsy
Entorhinal Cortex
Piriform Cortex
Temporal Lobe
Amygdala
Hippocampus
Cohort Studies
Outcome Assessment (Health Care)

ASJC Scopus subject areas

  • Clinical Neurology

Cite this

Galovic, M., Baudracco, I., Wright-Goff, E., Pillajo, G., Nachev, P., Wandschneider, B., ... Koepp, M. J. (2019). Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy. JAMA Neurology. https://doi.org/10.1001/jamaneurol.2019.0204

Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy. / Galovic, Marian; Baudracco, Irene; Wright-Goff, Evan; Pillajo, Galo; Nachev, Parashkev; Wandschneider, Britta; Woermann, Friedrich; Thompson, Pamela; Baxendale, Sallie; McEvoy, Andrew W.; Nowell, Mark; Mancini, Matteo; Vos, Sjoerd B.; Winston, Gavin P.; Sparks, Rachel; Prados, Ferran; Miserocchi, Anna; De Tisi, Jane; Van Graan, Louis André; Rodionov, Roman; Wu, Chengyuan; Alizadeh, Mahdi; Kozlowski, Lauren; Sharan, Ashwini D.; Kini, Lohith G.; Davis, Kathryn A.; Litt, Brian; Ourselin, Sebastien; Moshé, Solomon L.; Moshe, Solomon L.; Löscher, Wolfgang; Duncan, John S.; Koepp, Matthias J.

In: JAMA Neurology, 01.01.2019.

Research output: Contribution to journalArticle

Galovic, M, Baudracco, I, Wright-Goff, E, Pillajo, G, Nachev, P, Wandschneider, B, Woermann, F, Thompson, P, Baxendale, S, McEvoy, AW, Nowell, M, Mancini, M, Vos, SB, Winston, GP, Sparks, R, Prados, F, Miserocchi, A, De Tisi, J, Van Graan, LA, Rodionov, R, Wu, C, Alizadeh, M, Kozlowski, L, Sharan, AD, Kini, LG, Davis, KA, Litt, B, Ourselin, S, Moshé, SL, Moshe, SL, Löscher, W, Duncan, JS & Koepp, MJ 2019, 'Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy', JAMA Neurology. https://doi.org/10.1001/jamaneurol.2019.0204
Galovic, Marian ; Baudracco, Irene ; Wright-Goff, Evan ; Pillajo, Galo ; Nachev, Parashkev ; Wandschneider, Britta ; Woermann, Friedrich ; Thompson, Pamela ; Baxendale, Sallie ; McEvoy, Andrew W. ; Nowell, Mark ; Mancini, Matteo ; Vos, Sjoerd B. ; Winston, Gavin P. ; Sparks, Rachel ; Prados, Ferran ; Miserocchi, Anna ; De Tisi, Jane ; Van Graan, Louis André ; Rodionov, Roman ; Wu, Chengyuan ; Alizadeh, Mahdi ; Kozlowski, Lauren ; Sharan, Ashwini D. ; Kini, Lohith G. ; Davis, Kathryn A. ; Litt, Brian ; Ourselin, Sebastien ; Moshé, Solomon L. ; Moshe, Solomon L. ; Löscher, Wolfgang ; Duncan, John S. ; Koepp, Matthias J. / Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy. In: JAMA Neurology. 2019.
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title = "Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy",
abstract = "Importance: A functional area associated with the piriform cortex, termed area tempestas, has been implicated in animal studies as having a crucial role in modulating seizures, but similar evidence is limited in humans. Objective: To assess whether removal of the piriform cortex is associated with postoperative seizure freedom in patients with temporal lobe epilepsy (TLE) as a proof-of-concept for the relevance of this area in human TLE. Design, Setting, and Participants: This cohort study used voxel-based morphometry and volumetry to assess differences in structural magnetic resonance imaging (MRI) scans in consecutive patients with TLE who underwent epilepsy surgery in a single center from January 1, 2005, through December 31, 2013. Participants underwent presurgical and postsurgical structural MRI and had at least 2 years of postoperative follow-up (median, 5 years; range, 2-11 years). Patients with MRI of insufficient quality were excluded. Findings were validated in 2 independent cohorts from tertiary epilepsy surgery centers. Study follow-up was completed on September 23, 2016, and data were analyzed from September 24, 2016, through April 24, 2018. Exposures: Standard anterior temporal lobe resection. Main Outcomes and Measures: Long-term postoperative seizure freedom. Results: In total, 107 patients with unilateral TLE (left-sided in 68; 63.6{\%} women; median age, 37 years [interquartile range {IQR}, 30-45 years]) were included in the derivation cohort. Reduced postsurgical gray matter volumes were found in the ipsilateral piriform cortex in the postoperative seizure-free group (n = 46) compared with the non-seizure-free group (n = 61). A larger proportion of the piriform cortex was resected in the seizure-free compared with the non-seizure-free groups (median, 83{\%} [IQR, 64{\%}-91{\%}] vs 52{\%} [IQR, 32{\%}-70{\%}]; P <.001). The results were seen in left- and right-sided TLE and after adjusting for clinical variables, presurgical gray matter alterations, presurgical hippocampal volumes, and the proportion of white matter tract disconnection. Findings were externally validated in 2 independent cohorts (31 patients; left-sided TLE in 14; 54.8{\%} women; median age, 41 years [IQR, 31-46 years]). The resected proportion of the piriform cortex was individually associated with seizure outcome after surgery (derivation cohort area under the curve, 0.80 [P <.001]; external validation cohorts area under the curve, 0.89 [P <.001]). Removal of at least half of the piriform cortex increased the odds of becoming seizure free by a factor of 16 (95{\%} CI, 5-47; P <.001). Other mesiotemporal structures (ie, hippocampus, amygdala, and entorhinal cortex) and the overall resection volume were not associated with outcomes. Conclusions and Relevance: These results support the importance of resecting the piriform cortex in neurosurgical treatment of TLE and suggest that this area has a key role in seizure generation.",
author = "Marian Galovic and Irene Baudracco and Evan Wright-Goff and Galo Pillajo and Parashkev Nachev and Britta Wandschneider and Friedrich Woermann and Pamela Thompson and Sallie Baxendale and McEvoy, {Andrew W.} and Mark Nowell and Matteo Mancini and Vos, {Sjoerd B.} and Winston, {Gavin P.} and Rachel Sparks and Ferran Prados and Anna Miserocchi and {De Tisi}, Jane and {Van Graan}, {Louis Andr{\'e}} and Roman Rodionov and Chengyuan Wu and Mahdi Alizadeh and Lauren Kozlowski and Sharan, {Ashwini D.} and Kini, {Lohith G.} and Davis, {Kathryn A.} and Brian Litt and Sebastien Ourselin and Mosh{\'e}, {Solomon L.} and Moshe, {Solomon L.} and Wolfgang L{\"o}scher and Duncan, {John S.} and Koepp, {Matthias J.}",
year = "2019",
month = "1",
day = "1",
doi = "10.1001/jamaneurol.2019.0204",
language = "English (US)",
journal = "JAMA Neurology",
issn = "2168-6149",
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TY - JOUR

T1 - Association of Piriform Cortex Resection with Surgical Outcomes in Patients with Temporal Lobe Epilepsy

AU - Galovic, Marian

AU - Baudracco, Irene

AU - Wright-Goff, Evan

AU - Pillajo, Galo

AU - Nachev, Parashkev

AU - Wandschneider, Britta

AU - Woermann, Friedrich

AU - Thompson, Pamela

AU - Baxendale, Sallie

AU - McEvoy, Andrew W.

AU - Nowell, Mark

AU - Mancini, Matteo

AU - Vos, Sjoerd B.

AU - Winston, Gavin P.

AU - Sparks, Rachel

AU - Prados, Ferran

AU - Miserocchi, Anna

AU - De Tisi, Jane

AU - Van Graan, Louis André

AU - Rodionov, Roman

AU - Wu, Chengyuan

AU - Alizadeh, Mahdi

AU - Kozlowski, Lauren

AU - Sharan, Ashwini D.

AU - Kini, Lohith G.

AU - Davis, Kathryn A.

AU - Litt, Brian

AU - Ourselin, Sebastien

AU - Moshé, Solomon L.

AU - Moshe, Solomon L.

AU - Löscher, Wolfgang

AU - Duncan, John S.

AU - Koepp, Matthias J.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Importance: A functional area associated with the piriform cortex, termed area tempestas, has been implicated in animal studies as having a crucial role in modulating seizures, but similar evidence is limited in humans. Objective: To assess whether removal of the piriform cortex is associated with postoperative seizure freedom in patients with temporal lobe epilepsy (TLE) as a proof-of-concept for the relevance of this area in human TLE. Design, Setting, and Participants: This cohort study used voxel-based morphometry and volumetry to assess differences in structural magnetic resonance imaging (MRI) scans in consecutive patients with TLE who underwent epilepsy surgery in a single center from January 1, 2005, through December 31, 2013. Participants underwent presurgical and postsurgical structural MRI and had at least 2 years of postoperative follow-up (median, 5 years; range, 2-11 years). Patients with MRI of insufficient quality were excluded. Findings were validated in 2 independent cohorts from tertiary epilepsy surgery centers. Study follow-up was completed on September 23, 2016, and data were analyzed from September 24, 2016, through April 24, 2018. Exposures: Standard anterior temporal lobe resection. Main Outcomes and Measures: Long-term postoperative seizure freedom. Results: In total, 107 patients with unilateral TLE (left-sided in 68; 63.6% women; median age, 37 years [interquartile range {IQR}, 30-45 years]) were included in the derivation cohort. Reduced postsurgical gray matter volumes were found in the ipsilateral piriform cortex in the postoperative seizure-free group (n = 46) compared with the non-seizure-free group (n = 61). A larger proportion of the piriform cortex was resected in the seizure-free compared with the non-seizure-free groups (median, 83% [IQR, 64%-91%] vs 52% [IQR, 32%-70%]; P <.001). The results were seen in left- and right-sided TLE and after adjusting for clinical variables, presurgical gray matter alterations, presurgical hippocampal volumes, and the proportion of white matter tract disconnection. Findings were externally validated in 2 independent cohorts (31 patients; left-sided TLE in 14; 54.8% women; median age, 41 years [IQR, 31-46 years]). The resected proportion of the piriform cortex was individually associated with seizure outcome after surgery (derivation cohort area under the curve, 0.80 [P <.001]; external validation cohorts area under the curve, 0.89 [P <.001]). Removal of at least half of the piriform cortex increased the odds of becoming seizure free by a factor of 16 (95% CI, 5-47; P <.001). Other mesiotemporal structures (ie, hippocampus, amygdala, and entorhinal cortex) and the overall resection volume were not associated with outcomes. Conclusions and Relevance: These results support the importance of resecting the piriform cortex in neurosurgical treatment of TLE and suggest that this area has a key role in seizure generation.

AB - Importance: A functional area associated with the piriform cortex, termed area tempestas, has been implicated in animal studies as having a crucial role in modulating seizures, but similar evidence is limited in humans. Objective: To assess whether removal of the piriform cortex is associated with postoperative seizure freedom in patients with temporal lobe epilepsy (TLE) as a proof-of-concept for the relevance of this area in human TLE. Design, Setting, and Participants: This cohort study used voxel-based morphometry and volumetry to assess differences in structural magnetic resonance imaging (MRI) scans in consecutive patients with TLE who underwent epilepsy surgery in a single center from January 1, 2005, through December 31, 2013. Participants underwent presurgical and postsurgical structural MRI and had at least 2 years of postoperative follow-up (median, 5 years; range, 2-11 years). Patients with MRI of insufficient quality were excluded. Findings were validated in 2 independent cohorts from tertiary epilepsy surgery centers. Study follow-up was completed on September 23, 2016, and data were analyzed from September 24, 2016, through April 24, 2018. Exposures: Standard anterior temporal lobe resection. Main Outcomes and Measures: Long-term postoperative seizure freedom. Results: In total, 107 patients with unilateral TLE (left-sided in 68; 63.6% women; median age, 37 years [interquartile range {IQR}, 30-45 years]) were included in the derivation cohort. Reduced postsurgical gray matter volumes were found in the ipsilateral piriform cortex in the postoperative seizure-free group (n = 46) compared with the non-seizure-free group (n = 61). A larger proportion of the piriform cortex was resected in the seizure-free compared with the non-seizure-free groups (median, 83% [IQR, 64%-91%] vs 52% [IQR, 32%-70%]; P <.001). The results were seen in left- and right-sided TLE and after adjusting for clinical variables, presurgical gray matter alterations, presurgical hippocampal volumes, and the proportion of white matter tract disconnection. Findings were externally validated in 2 independent cohorts (31 patients; left-sided TLE in 14; 54.8% women; median age, 41 years [IQR, 31-46 years]). The resected proportion of the piriform cortex was individually associated with seizure outcome after surgery (derivation cohort area under the curve, 0.80 [P <.001]; external validation cohorts area under the curve, 0.89 [P <.001]). Removal of at least half of the piriform cortex increased the odds of becoming seizure free by a factor of 16 (95% CI, 5-47; P <.001). Other mesiotemporal structures (ie, hippocampus, amygdala, and entorhinal cortex) and the overall resection volume were not associated with outcomes. Conclusions and Relevance: These results support the importance of resecting the piriform cortex in neurosurgical treatment of TLE and suggest that this area has a key role in seizure generation.

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