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Original Investigation
March 11, 2019

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

Author Affiliations
  • 1UK National Institute for Health Research, University College London (UCL) Hospitals Biomedical Research Centre, Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, United Kingdom
  • 2Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, United Kingdom
  • 3Department of Neurology, Kantonsspital St Gallen, St Gallen, Switzerland
  • 4Department of Imaging, Hospital de Especialidades Eugenio Espejo, Quito, Ecuador
  • 5Division of Neuroanatomy, Facultad de Medicina, Universidad Internacional del Ecuador, Quito
  • 6Magnetic Resonance Imaging Unit, Klinik Mara, Bethel Epilepsy Centre, Bielefeld, Germany
  • 7Institute of Cognitive Neuroscience, UCL, London, United Kingdom
  • 8Translational Imaging Group, Centre for Medical Image Computing, Department of Medical Physics and Bioengineering, UCL, London, United Kingdom
  • 9Wellcome EPSRC Centre for Interventional and Surgical Sciences, UCL, London, United Kingdom
  • 10School of Biomedical Engineering and Image Sciences, Kings College London, London, United Kingdom
  • 11Queen Square Multiple Sclerosis Centre, Department of Neuroinflammation, UCL Institute of Neurology, London, United Kingdom
  • 12Department of Neurosurgery, Vickie and Jack Farber Institute for Neuroscience, Thomas Jefferson University, Philadelphia, Pennsylvania
  • 13Jefferson Integrated Magnetic Resonance Imaging Center, Department of Radiology, Thomas Jefferson University, Philadelphia, Pennsylvania
  • 14medical student at Sidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania
  • 15Center for Neuroengineering and Therapeutics, Department of Bioengineering, University of Pennsylvania, Philadelphia
  • 16Department of Neurology, Hospital of the University of Pennsylvania, Philadelphia
  • 17Department of Neurosurgery, Hospital of the University of Pennsylvania, Philadelphia
  • 18Dementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, London, United Kingdom
  • 19Laboratory of Developmental Epilepsy, Saul R. Korey Department of Neurology, Montefiore/Einstein Epilepsy Management Center, Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, New York
  • 20Dominick P. Purpura Department of Neuroscience, Montefiore/Einstein Epilepsy Management Center, Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, New York
  • 21Department of Pediatrics, Montefiore/Einstein Epilepsy Management Center, Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, New York
  • 22Department of Pharmacology, Toxicology and Pharmacy, University of Veterinary Medicine, Hannover, Germany
  • 23Center for Systems Neuroscience, University of Veterinary Medicine, Hannover, Germany
JAMA Neurol. 2019;76(6):690-700. doi:10.1001/jamaneurol.2019.0204
Key Points

Question  Does resecting the piriform cortex improve surgical outcome in temporal lobe epilepsy?

Findings  In this multicenter study that included 107 adults with temporal lobe epilepsy in the derivation cohort and 31 in the validation cohort, resecting a larger proportion of the piriform cortex (78% in seizure-free vs 46% in non–seizure-free cases in pooled data) was significantly associated with a favorable outcome. Removal of at least half the piriform cortex significantly increased the odds of becoming seizure free by a factor of 16.

Meaning  These findings support including the piriform cortex in standard anterior temporal lobe resections to achieve seizure freedom.

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.

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