The double inversion recovery study on the gray matter abnormalities of MRI negative temporal lobe epilepsy patients_Journal of Epilepsy

Authors：

CAI Yang ¹ , SUN Wei ² , MAO Lingyan ¹ , PENG Weifeng ¹ ,  DING Jing ¹ , CHEN Caizhong ² ,  WANG Xin ¹

1. Department of Neurology, Zhongshan hospital, Fudan University, Shanghai 200032, China;
2. Department of Radiology, Zhongshan hospital, Fudan University, Shanghai 200032, China;

Corresponding author：

DING Jing, Email: ding.jing@zs-hospital.sh.cn; WANG Xin, Email: wang.xin@zs-hospital.sh.cn

Keywords：

Temporal lobe epilepsy; Grey matter intensity; Double inversion recovery

DOI：

10.7507/2096-0247.20190014

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

ObjectivesTo study the gray matter (GM) volume of MRI-negative temporal lobe epilepsy (TLE) patients with double inversion recovery (DIR) combining with SPM analysis.MethodsTwenty-four MRI-negative TLE patients and twenty-four healthy controls (HC) with matched sex and age were collected from Zhongshan hospital from 2016 Januany to 2018 December. All the participants underwent DIR scanning and the MRI data were further postprocessed with Statistical Parametric Mapping (SPM).ResultsMRI-negative TLE patients showed reduced GM density in the left superior frontal gyrus (medial orbital), right temporal pole, right para-hippocampal gyrus, right lingual gyrus, and increased GM value in the right superior frontal gyrus (medial) than HC group with statistical significance (P<0 001="" cluster="">50). According to the EEG manifestation, the MRI-negative TLE group was classified into the multiple and single focal discharges group.The multiple focal discharges MRI-negative TLE group demonstrated decreased GM density in the right temporal pole, right superior occipital gyrus, right para-hippocampal gyrus and bilateral superiorfrontal gyrus (medial orbital), but increased GM value in the right superior frontal gyrus (medial) than HC group with statistical significance (P<0 001="" cluster="">50). No statistical differences were found in the single focal discharges MRI-negative TLE group comparing with either the HC or multiple focal discharges group. According to the seizure type with or without secondarily generalizedtonic-clonic seizures, the MRI-negative TLE patients were classified into sGTCS and non-sGTCS group. There existed greater statistical GM density for sGTCS group in the right lingual gyrus, right thalamus, left middle occipital gyrus, left basal ganglia and left cuneus than the non-sGTCS group (P<0 001="" cluster="">50).ConclusionsThere existed wider areas of GM volume changes in the brain regions of MRI negative TLE patients, including both the temporal and extra-temporal areas, with most significant GM alteration in multiple focal discharges and sGTCS TLE group.

Citation： CAI Yang, SUN Wei, MAO Lingyan, PENG Weifeng, DING Jing, CHEN Caizhong, WANG Xin. The double inversion recovery study on the gray matter abnormalities of MRI negative temporal lobe epilepsy patients. Journal of Epilepsy, 2019, 5(2): 81-87. doi: 10.7507/2096-0247.20190014 Copy

1.	Semah F, Picot MC, Adam C, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology, 1998, 51(5): 1256-1262.
2.	Cascino GD, Jack CR Jr, Parisi JE, et al. Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neurol, 1991, 30(1): 31-36.
3.	Mueller SG, Laxer KD, Barakos J, et al. Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis. Neuroimage, 2009, 46(2): 353-359.
4.	Muhlhofer W, Tan YL, Mueller SG, et al. MRI-negative temporal lobe epilepsy-What do we know?. Epilepsia, 2017, 58(5): 727-742.
5.	Kogias E, Altenmuller DM, Klingler JH, et al. Histopathology of 3Tesla MRI-negative temporal lobe epilepsies. J ClinNeurosci, 2018, 47: 273-277.
6.	Bernhardt BC, Bernasconi A, Liu M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol, 2016, 80(1): 142-153.
7.	Kim SE, Andermann F, Olivier A. The clinical and electrophysiological characteristics of temporal lobe epilepsy with normal MRI. J Clin Neurol, 2006, 2(1): 42-50.
8.	Carne RP, O'Brien TJ, Kilpatrick CJ, et al. MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain, 2004, 127(Pt 10): 2276-2285.
9.	Liu W, An D, Xiao J, et al. Malformations of cortical development and epilepsy: a cohort of 150 patients in western China. Seizure, 2015, 32: 92-99.
10.	Bonilha L, Edwards JC, Kinsman SL, et al. Extra hippocampal gray matter loss and hippocampal deafferentation in patients with temporal lobe epilepsy. Epilepsia, 2010, 51(4): 519-528.
11.	Toller G, Adhimoolam B, Rankin KP, et al. Right fronto-limbic atrophy is associated with reduced empathy in refractory unilateral mesial temporal lobe epilepsy. Neuropsychologia, 2015, 78: 80-87.
12.	Ryan ME. Utility of double inversion recovery sequences in MRI. Pediatr Neurol Briefs, 2016, 30(4): 26.
13.	Shen JF, Saunders JK. Double inversion recovery improves water suppression in vivo. Magn Reson Med, 1993, 29(4): 540-542.
14.	Faizy TD, Thaler C, Ceyrowski T, et al. Reliability of cortical lesion detection on double inversion recovery MRI applying the MAGNIMS-Criteria in multiple sclerosis patients within a 16-months period. PLoS One, 2017, 12(2): e0172923.
15.	Granata F, Morabito R, Mormina E, et al. 3T double inversion recovery magnetic resonance imaging: diagnostic advantages in the evaluation of cortical development anomalies. Eur J Radiol, 2016, 85(5): 906-914.
16.	SoaresBP, Porter SG, Saindane AM, et al. Utility of double inversion recovery MRI in paediatric epilepsy. Br J Radiol, 2016, 89(1057): 20150325.
17.	Rugg-Gunn FJ, Boulby PA, Symms MR, et al. Imaging the neocortex in epilepsy with double inversion recovery imaging. Neuroimage, 2006, 31(1): 39-50.
18.	Fisher RS, Cross JH, French JA, et al. Operational classification of seizure types by the International League Against Epilepsy: position paper of the ILAE Commission for classification and terminology. Epilepsia, 2017, 58(4): 522-530.
19.	Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia, 2017, 58(4): 512-521.
20.	Riederer F, Lanzenberger R, Kaya M, et al. Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology, 2008, 71(6): 419-425.
21.	Scanlon C, Mueller SG, Cheong I, et al. Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis. J Neurol, 2013, 260(9): 2320-2329.
22.	Elliott B, Joyce E, Shorvon S. Delusions, illusions and hallucinations in epilepsy: 1. Elementary phenomena. Epilepsy Res, 2009, 85(2-3): 162-171.
23.	Bien C, Benninger F, Urback H, et al. Localizing value of epileptic visual auras. Am J Ophthalmol, 2000, 129(5): 704.
24.	Stretton J, Pope r A, Winston GP, et al. Temporal lobe epilepsy and affective disorders: the role of the subgenual anterior cingulate cortex. J Neurol Neurosurg Psychiatry, 2015, 86(2): 144-151.
25.	Bao Y, He R, Zeng Q, et al. Investigation of microstructural abnormalities in white and gray matter around hippocampus with diffusion tensor imaging (DTI) in temporal lobe epilepsy (TLE). Epilepsy Behav, 2018, 83: 44-49.
26.	王韦, 林一聪, 周东, 等. MRI 图像后处理技术在局灶性皮质发育不良癫痫患者中的应用. 中风与神经疾病杂志, 2018, 11(11): 1028-1031.
27.	Fong JS, Jehi L, Najm I, et al. Seizure outcome and its predictors after temporal lobe epilepsy surgery in patients with normal MRI. Epilepsia, 2011, 52(8): 1393-1401.
28.	周东. 回顾癫痫 2016——脑科学计划与癫痫. 癫痫杂志, 2017, 1(1): 1-2.
29.	Chen C, Li H, Ding F, et al. Alterations in the hippocampal-thalamic pathway underlying secondarily generalized tonic-clonic seizures in mesial temporal lobe epilepsy: A diffusion tensor imaging study. Epilepsia, 2019, 60(1): 121-130.
30.	Holmes MD, Born DE, Kutsy RL, et al. Outcome after surgery in patients with refractory temporal lobe epilepsy and normal MRI. Seizure, 2000, 9(6): 407-411.
31.	Burkholder DB, Sulc V, Hoffman EM, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging-negative temporal lobe epilepsy surgery. JAMA Neurol, 2014, 71(6): 702-709.
32.	Rosati A, Aghakhani Y, Bernasconi A, et al. Intractable temporal lobe epilepsy with rare spikes is less severe than with frequent spikes. Neurology, 2003, 60(8): 1290-1295.
33.	Jeong SW, Lee SK, Hong KS, et al. Prognostic factors for the surgery for mesial temporal lobe epilepsy: longitudinal analysis. Epilepsia, 2005, 46(8): 1273-1279.
34.	周东, 鄢波. 早期识别和手术治疗促进颞叶内侧癫痫预后. 西部医学, 2015, 6(6): 801-806.

1. Semah F, Picot MC, Adam C, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology, 1998, 51(5): 1256-1262.
2. Cascino GD, Jack CR Jr, Parisi JE, et al. Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neurol, 1991, 30(1): 31-36.
3. Mueller SG, Laxer KD, Barakos J, et al. Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis. Neuroimage, 2009, 46(2): 353-359.
4. Muhlhofer W, Tan YL, Mueller SG, et al. MRI-negative temporal lobe epilepsy-What do we know?. Epilepsia, 2017, 58(5): 727-742.
5. Kogias E, Altenmuller DM, Klingler JH, et al. Histopathology of 3Tesla MRI-negative temporal lobe epilepsies. J ClinNeurosci, 2018, 47: 273-277.
6. Bernhardt BC, Bernasconi A, Liu M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol, 2016, 80(1): 142-153.
7. Kim SE, Andermann F, Olivier A. The clinical and electrophysiological characteristics of temporal lobe epilepsy with normal MRI. J Clin Neurol, 2006, 2(1): 42-50.
8. Carne RP, O'Brien TJ, Kilpatrick CJ, et al. MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain, 2004, 127(Pt 10): 2276-2285.
9. Liu W, An D, Xiao J, et al. Malformations of cortical development and epilepsy: a cohort of 150 patients in western China. Seizure, 2015, 32: 92-99.
10. Bonilha L, Edwards JC, Kinsman SL, et al. Extra hippocampal gray matter loss and hippocampal deafferentation in patients with temporal lobe epilepsy. Epilepsia, 2010, 51(4): 519-528.
11. Toller G, Adhimoolam B, Rankin KP, et al. Right fronto-limbic atrophy is associated with reduced empathy in refractory unilateral mesial temporal lobe epilepsy. Neuropsychologia, 2015, 78: 80-87.
12. Ryan ME. Utility of double inversion recovery sequences in MRI. Pediatr Neurol Briefs, 2016, 30(4): 26.
13. Shen JF, Saunders JK. Double inversion recovery improves water suppression in vivo. Magn Reson Med, 1993, 29(4): 540-542.
14. Faizy TD, Thaler C, Ceyrowski T, et al. Reliability of cortical lesion detection on double inversion recovery MRI applying the MAGNIMS-Criteria in multiple sclerosis patients within a 16-months period. PLoS One, 2017, 12(2): e0172923.
15. Granata F, Morabito R, Mormina E, et al. 3T double inversion recovery magnetic resonance imaging: diagnostic advantages in the evaluation of cortical development anomalies. Eur J Radiol, 2016, 85(5): 906-914.
16. SoaresBP, Porter SG, Saindane AM, et al. Utility of double inversion recovery MRI in paediatric epilepsy. Br J Radiol, 2016, 89(1057): 20150325.
17. Rugg-Gunn FJ, Boulby PA, Symms MR, et al. Imaging the neocortex in epilepsy with double inversion recovery imaging. Neuroimage, 2006, 31(1): 39-50.
18. Fisher RS, Cross JH, French JA, et al. Operational classification of seizure types by the International League Against Epilepsy: position paper of the ILAE Commission for classification and terminology. Epilepsia, 2017, 58(4): 522-530.
19. Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia, 2017, 58(4): 512-521.
20. Riederer F, Lanzenberger R, Kaya M, et al. Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology, 2008, 71(6): 419-425.
21. Scanlon C, Mueller SG, Cheong I, et al. Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis. J Neurol, 2013, 260(9): 2320-2329.
22. Elliott B, Joyce E, Shorvon S. Delusions, illusions and hallucinations in epilepsy: 1. Elementary phenomena. Epilepsy Res, 2009, 85(2-3): 162-171.
23. Bien C, Benninger F, Urback H, et al. Localizing value of epileptic visual auras. Am J Ophthalmol, 2000, 129(5): 704.
24. Stretton J, Pope r A, Winston GP, et al. Temporal lobe epilepsy and affective disorders: the role of the subgenual anterior cingulate cortex. J Neurol Neurosurg Psychiatry, 2015, 86(2): 144-151.
25. Bao Y, He R, Zeng Q, et al. Investigation of microstructural abnormalities in white and gray matter around hippocampus with diffusion tensor imaging (DTI) in temporal lobe epilepsy (TLE). Epilepsy Behav, 2018, 83: 44-49.
26. 王韦, 林一聪, 周东, 等. MRI 图像后处理技术在局灶性皮质发育不良癫痫患者中的应用. 中风与神经疾病杂志, 2018, 11(11): 1028-1031.
27. Fong JS, Jehi L, Najm I, et al. Seizure outcome and its predictors after temporal lobe epilepsy surgery in patients with normal MRI. Epilepsia, 2011, 52(8): 1393-1401.
28. 周东. 回顾癫痫 2016——脑科学计划与癫痫. 癫痫杂志, 2017, 1(1): 1-2.
29. Chen C, Li H, Ding F, et al. Alterations in the hippocampal-thalamic pathway underlying secondarily generalized tonic-clonic seizures in mesial temporal lobe epilepsy: A diffusion tensor imaging study. Epilepsia, 2019, 60(1): 121-130.
30. Holmes MD, Born DE, Kutsy RL, et al. Outcome after surgery in patients with refractory temporal lobe epilepsy and normal MRI. Seizure, 2000, 9(6): 407-411.
31. Burkholder DB, Sulc V, Hoffman EM, et al. Interictal scalp electroencephalography and intraoperative electrocorticography in magnetic resonance imaging-negative temporal lobe epilepsy surgery. JAMA Neurol, 2014, 71(6): 702-709.
32. Rosati A, Aghakhani Y, Bernasconi A, et al. Intractable temporal lobe epilepsy with rare spikes is less severe than with frequent spikes. Neurology, 2003, 60(8): 1290-1295.
33. Jeong SW, Lee SK, Hong KS, et al. Prognostic factors for the surgery for mesial temporal lobe epilepsy: longitudinal analysis. Epilepsia, 2005, 46(8): 1273-1279.
34. 周东, 鄢波. 早期识别和手术治疗促进颞叶内侧癫痫预后. 西部医学, 2015, 6(6): 801-806.

Previous Article
福建省抗癫痫协会
Next Article
A case of Aicardi-Goutières syndrome

Journal of Epilepsy

The double inversion recovery study on the gray matter abnormalities of MRI negative temporal lobe epilepsy patients

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content