Optimized multi-scale entropy to localize epileptogenic hemisphere of temporal lobe epilepsy based on resting-state functional magnetic resonance imaging_Journal of Biomedical Engineering

Authors：

XIE Chong ^1,2 , GE Manling ^1,2 , FU Xiaoxuan ^1,2 ,  CHEN Shenghua ^1,2 , ZHANG Fuyi ^1,2 , GUO Zhitong ^1,2 ,  ZHANG Zhiqiang ³

1. State Key Laboratory of Reliability and Intelligence of Electrical Equipment, Hebei University of Technology, Tianjin 300130, P.R.China;
2. Key Laboratory of Electromagnetic Field and Electrical Apparatus Reliability of Hebei Province, Hebei University of Technology, Tianjin 300130, P.R.China;
3. Department of Medical Imaging, Jinling Hospital, Nanjing University School of Medicine/General Hospital of Eastern Theater, Nanjing 210002, P.R.China;

Corresponding?author：

CHEN Shenghua, Email: chenshenghua@hebut.edu.cn; ZHANG Zhiqiang, Email: zhangzq2001@126.com

Keywords：

multi-scale entropy; resting-state functional magnetic resonance imaging; temporal lobe epilepsy; support vector machine; epileptogenic hemisphere

DOI：

10.7507/1001-5515.202011048

Video：

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Entropy model is widely used in epileptic electroencephalogram (EEG) analysis, but there are few reports on how to objectively select the parameters to compute the entropy model in the analysis of resting-state functional magnetic resonance imaging (rfMRI). Therefore, an optimization algorithm to confirm the parameters in multi-scale entropy (MSE) model was proposed, and the location of epileptogenic hemisphere was taken as an example to test the optimization effect by supervised machine learning. The rfMRI data of 20 temporal lobe epilepsy (TLE) patients with hippocampal sclerosis, positive on structural magnetic resonance imaging, were divided into left and right groups. Then, the parameters in MSE model were optimized by the receiver operating characteristic curves (ROC) and area under ROC curve (AUC) values in sensitivity analysis, and the entropy value of the brain regions with statistically significant difference between the groups were taken as sensitive features to epileptogenic hemisphere lateral. The optimized entropy values of these bio-marker brain areas were considered as feature vectors input into the support vector machine (SVM). Finally, combining optimized MSE model with SVM could accurately distinguish epileptogenic hemisphere in TLE at an average accuracy rate of 95%, which was higher than the current level. The results show that the MSE model parameter optimization algorithm can accurately extract the functional imaging markers sensitive to the epileptogenic hemisphere, and achieve the purpose of objectively selecting the parameters for MSE in rfMRI, which provides the basis for the application of entropy in advanced technology detection.

Citation： XIE Chong, GE Manling, FU Xiaoxuan, CHEN Shenghua, ZHANG Fuyi, GUO Zhitong, ZHANG Zhiqiang. Optimized multi-scale entropy to localize epileptogenic hemisphere of temporal lobe epilepsy based on resting-state functional magnetic resonance imaging. Journal of Biomedical Engineering, 2021, 38(6): 1163-1172. doi: 10.7507/1001-5515.202011048 Copy

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2.	Warren B. Surgical considerations of intractable mesial temporal lobe epilepsy. Brain Sci, 2018, 8(2): 35.
3.	Kumar A, Valentín A, Humayon D, et al. Preoperative estimation of seizure control after resective surgery for the treatment of epilepsy. Seizure-Eur J Epilep, 2013, 22(10): 818-826.
4.	李欣, 王正閣, 張冰, 等. fMRI在顳葉癲癇術前定位和預后評估中的研究進展. 磁共振成像, 2020, 11(8): 691-694.
5.	Wang Cong, Sun Wanbing, Zhang Jun, et al. An electric-field-responsive paramagnetic contrast agent enhances the visualization of epileptic foci in mouse models of drug-resistant epilepsy. Nat Biomed Eng, 2020, 5(3): 278-289.
6.	楊宏宇, 陳楠, 李坤成. 伴認知功能障礙的顳葉癲癇MRI研究進展. 中國醫學影像技術, 2017, 33(9): 1421-1424.
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8.	韓靜, 劉亞洲. 磁共振成像對顳葉癲癇患者病灶定側定位的診斷評估. 實用醫學影像雜志, 2018, 19(6): 531-533.
9.	Kerr W T, Nguyen S T, Cho A Y, et al. Computer-aided diagnosis and localization of lateralized temporal lobe epilepsy using interictal FDG-PET. Front Neurol, 2013, 4: 31-45.
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11.	Barron D S, Fox P T, Pardoe H, et al. Thalamic functional connectivity predicts seizure laterality in individual TLE patients: Application of a biomarker development strategy. Neuroimage-Clin, 2015, 7: 273-280.
12.	Yang Zhengyi, Jeiran C P, David R, et al. Lateralization of temporal lobe epilepsy based on resting-state functional magnetic resonance imaging and machine learning. Front Neurol, 2015, 6: 184.
13.	Tong Xin, An D M, Xiao Fenglai, et al. Real-time effects of interictal spikes on hippocampus and amygdala functional connectivity in unilateral temporal lobe epilepsy: An EEG-fMRI study. Epilepsia, 2019, 60(2): 246-254.
14.	Reyes A, Thesen T, Wang X Y, et al. Resting-state functional MRI distinguishes temporal lobe epilepsy subtypes. Epilepsia, 2016, 57(9): 1475-1484.
15.	Jones A L, Cascino G D. Evidence on use of neuroimaging for surgical treatment of temporal lobe epilepsy. JAMA Neurol, 2016, 73(4): 464-470.
16.	Costa M, Goldberger A L, Peng C K. Multiscale entropy analysis of complex physiologic time series. Phys Rev Lett, 2002, 89(6): 068102.
17.	Hadoush H, Alafeef M, Abdulhay E. Brain complexity in children with mild and severe autism spectrum disorders: Analysis of multiscale entropy in EEG. Brain Topogr, 2019, 32(5): 914-921.
18.	Ives-Deliperi V, Butler J T, Jokeit H. Left or right? Lateralizing temporal lobe epilepsy by dynamic amygdala fMRI. Epilepsy Behav, 2017, 70(Pt A): 118-124.
19.	張夫一, 葛曼玲, 郭志彤, 等. 靜息態功能磁共振成像評估健康老年人認知行為的多尺度熵模型研究. 物理學報, 2020, 69(10): 108703.
20.	Li Xuanyu, Zhu Zhaojun, Zhao Weina, et al. Decreased resting-state brain signal complexity in patients with mild cognitive impairment and Alzheimer's disease: A multi-scale entropy analysis. Biomed Opt Express, 2018, 9(4): 1916-1929.
21.	Wang D, Jann K, Fan Chang, et al. Neurophysiological basis of multi-scale entropy of brain complexity and its relationship with functional connectivity. Front Neurosci, 2018, 12: 352.
22.	覃國萍, 李雙燕. 多尺度熵算法研究進展及其在神經信號分析中的應用. 生物醫學工程學雜志, 2020, 37(3): 541-548.
23.	Roldan E, Calero S, Hidalgo V M, et al. Multi-scale entropy evaluates the proarrhythmic condition of persistent atrial fibrillation patients predicting early failure of electrical cardioversion. Entropy, 2020, 22(7): 748.
24.	Yang A C, Huang C C, Yeh H L, et al. Complexity of spontaneous BOLD activity in default mode network is correlated with cognitive function in normal male elderly: A multiscale entropy analysis. Neurobiol Aging, 2013, 34(2): 428-438.
25.	Morgan V L, Gore J C, Abou-Khalil B. Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI. Epilepsy Res, 2010, 88(2-3): 168-178.
26.	Wu Rina, Zang Yufeng, Zhao Shigang. Resting-state fMRI studies in epilepsy. Neurosci Bull, 2012, 28(4): 449-455.
27.	吳寒, 張志強, 許強, 等. 間期癇樣發放對內側顳葉癲癇腦網絡的影響. 磁共振成像, 2015, 6(11): 801-806.
28.	Woolrich M W, Jbabdi S, Patenaude B, et al. Bayesian analysis of neuroimaging data in FSL. Neuroimage, 2009, 45(1): S173-S186.
29.	Jenkinson M, Bannister P, Brady M, et al. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 2002, 2(17): 825-841.
30.	Wang Danhong, Li Meiling, Wang Meiyun, et al. Individual-specific functional connectivity markers track dimensional and categorical features of psychotic illness. Mol Psychiatr, 2020, 25(9): 2119-2129.
31.	Yeo B T, Krienen F M, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol, 2011, 3(106): 1125-1165.
32.	Smith S M. Fast robust automated brain extraction. Hum Brain Mapp, 2002, 17(3): 143-155.
33.	Richman J S, Moorman J R. Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol, 2000, 278(6): H2039-H2049.
34.	Xia Mingrui, Wang Jinhui, He Yong, et al. BrainNet Viewer: A network visualization tool for human brain connectomics. PLoS One, 2013, 8(7): e68910.
35.	Cortes C, Vapnik V. Support vector networks. Mach Learn, 1995, 20(3): 273-297.
36.	Peter A, Lino R, Nelson D, et al. A support vectors classifier approach to predicting the risk of progression of adolescent idiopathic scoliosis. IEEE Trans Inf Technol Biomed, 2005, 9(2): 276-282.
37.	Jafari-Khouzani K, Elisevich K, Karvelis K C, et al. Quantitative multi-compartmental SPECT image analysis for lateralization of temporal lobe epilepsy. Epilepsy Res, 2011, 95(1): 35-30.
38.	Jin S H, Chung C K. Electrophysiological resting-state biomarker for diagnosing mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsy Res, 2017, 129: 138-145.
39.	Beheshti I, Sone D, Maikusa N, et al. FLAIR-Wise machine-learning classification and lateralization of MRI-negative 18F-FDG PET-positive temporal lobe epilepsy. Front Neurol, 2020, 11: 580713.
40.	Morgan V L, Englot D J, Rogers B P, et al. Magnetic resonance imaging connectivity for the prediction of seizure outcome in temporal lobe epilepsy. Epilepsia, 2017, 58(7): 1251-1260.
41.	Laufs H. Functional imaging of seizures and epilepsy: Evolution from zones to networks. Curr Opin Neurol, 2012, 25(2): 194-200.
42.	Fahoum F, Lopes R, Pittau F, et al. Widespread epileptic networks in focal epilepsies: EEG-fMRI study. Epilepsia, 2012, 53(9): 1618-1627.
43.	Farid N, Girard H M, Kemmotsu N, et al. Temporal lobe epilepsy: Quantitative MR volumetry in detection of hippocampal atrophy. Radiology, 2012, 264(2): 542-550.
44.	Moran N F, Lemieux L, Kitchen N D, et al. Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain, 2001, 124(Pt1): 167-175.
45.	Bonilha L, Rorden C, Castellano G, et al. Voxel-based morphometry of the thalamus in patients with refractory medial temporal lobe epilepsy. Neuroimage, 2005, 25(3): 1016-1021.

1. Duncan J S, Winston G P, Koepp M J, et al. Brain imaging in the assessment for epilepsy surgery. Lancet Neurol, 2016, 15(4): 420-433.
2. Warren B. Surgical considerations of intractable mesial temporal lobe epilepsy. Brain Sci, 2018, 8(2): 35.
3. Kumar A, Valentín A, Humayon D, et al. Preoperative estimation of seizure control after resective surgery for the treatment of epilepsy. Seizure-Eur J Epilep, 2013, 22(10): 818-826.
4. 李欣, 王正閣, 張冰, 等. fMRI在顳葉癲癇術前定位和預后評估中的研究進展. 磁共振成像, 2020, 11(8): 691-694.
5. Wang Cong, Sun Wanbing, Zhang Jun, et al. An electric-field-responsive paramagnetic contrast agent enhances the visualization of epileptic foci in mouse models of drug-resistant epilepsy. Nat Biomed Eng, 2020, 5(3): 278-289.
6. 楊宏宇, 陳楠, 李坤成. 伴認知功能障礙的顳葉癲癇MRI研究進展. 中國醫學影像技術, 2017, 33(9): 1421-1424.
7. Lee R W, Hoogs M M, Burkholder D B, et al. Outcome of intracranial electroencephalography monitoring and surgery in magnetic resonance imaging-negative temporal lobe epilepsy. Epilepsy Res, 2014, 108(5): 937-944.
8. 韓靜, 劉亞洲. 磁共振成像對顳葉癲癇患者病灶定側定位的診斷評估. 實用醫學影像雜志, 2018, 19(6): 531-533.
9. Kerr W T, Nguyen S T, Cho A Y, et al. Computer-aided diagnosis and localization of lateralized temporal lobe epilepsy using interictal FDG-PET. Front Neurol, 2013, 4: 31-45.
10. Pereira F R S, Alessio A, Sercheli M S, et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: Evidence from resting state fMRI. BMC Neurosci, 2010, 11(1): 66.
11. Barron D S, Fox P T, Pardoe H, et al. Thalamic functional connectivity predicts seizure laterality in individual TLE patients: Application of a biomarker development strategy. Neuroimage-Clin, 2015, 7: 273-280.
12. Yang Zhengyi, Jeiran C P, David R, et al. Lateralization of temporal lobe epilepsy based on resting-state functional magnetic resonance imaging and machine learning. Front Neurol, 2015, 6: 184.
13. Tong Xin, An D M, Xiao Fenglai, et al. Real-time effects of interictal spikes on hippocampus and amygdala functional connectivity in unilateral temporal lobe epilepsy: An EEG-fMRI study. Epilepsia, 2019, 60(2): 246-254.
14. Reyes A, Thesen T, Wang X Y, et al. Resting-state functional MRI distinguishes temporal lobe epilepsy subtypes. Epilepsia, 2016, 57(9): 1475-1484.
15. Jones A L, Cascino G D. Evidence on use of neuroimaging for surgical treatment of temporal lobe epilepsy. JAMA Neurol, 2016, 73(4): 464-470.
16. Costa M, Goldberger A L, Peng C K. Multiscale entropy analysis of complex physiologic time series. Phys Rev Lett, 2002, 89(6): 068102.
17. Hadoush H, Alafeef M, Abdulhay E. Brain complexity in children with mild and severe autism spectrum disorders: Analysis of multiscale entropy in EEG. Brain Topogr, 2019, 32(5): 914-921.
18. Ives-Deliperi V, Butler J T, Jokeit H. Left or right? Lateralizing temporal lobe epilepsy by dynamic amygdala fMRI. Epilepsy Behav, 2017, 70(Pt A): 118-124.
19. 張夫一, 葛曼玲, 郭志彤, 等. 靜息態功能磁共振成像評估健康老年人認知行為的多尺度熵模型研究. 物理學報, 2020, 69(10): 108703.
20. Li Xuanyu, Zhu Zhaojun, Zhao Weina, et al. Decreased resting-state brain signal complexity in patients with mild cognitive impairment and Alzheimer's disease: A multi-scale entropy analysis. Biomed Opt Express, 2018, 9(4): 1916-1929.
21. Wang D, Jann K, Fan Chang, et al. Neurophysiological basis of multi-scale entropy of brain complexity and its relationship with functional connectivity. Front Neurosci, 2018, 12: 352.
22. 覃國萍, 李雙燕. 多尺度熵算法研究進展及其在神經信號分析中的應用. 生物醫學工程學雜志, 2020, 37(3): 541-548.
23. Roldan E, Calero S, Hidalgo V M, et al. Multi-scale entropy evaluates the proarrhythmic condition of persistent atrial fibrillation patients predicting early failure of electrical cardioversion. Entropy, 2020, 22(7): 748.
24. Yang A C, Huang C C, Yeh H L, et al. Complexity of spontaneous BOLD activity in default mode network is correlated with cognitive function in normal male elderly: A multiscale entropy analysis. Neurobiol Aging, 2013, 34(2): 428-438.
25. Morgan V L, Gore J C, Abou-Khalil B. Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI. Epilepsy Res, 2010, 88(2-3): 168-178.
26. Wu Rina, Zang Yufeng, Zhao Shigang. Resting-state fMRI studies in epilepsy. Neurosci Bull, 2012, 28(4): 449-455.
27. 吳寒, 張志強, 許強, 等. 間期癇樣發放對內側顳葉癲癇腦網絡的影響. 磁共振成像, 2015, 6(11): 801-806.
28. Woolrich M W, Jbabdi S, Patenaude B, et al. Bayesian analysis of neuroimaging data in FSL. Neuroimage, 2009, 45(1): S173-S186.
29. Jenkinson M, Bannister P, Brady M, et al. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 2002, 2(17): 825-841.
30. Wang Danhong, Li Meiling, Wang Meiyun, et al. Individual-specific functional connectivity markers track dimensional and categorical features of psychotic illness. Mol Psychiatr, 2020, 25(9): 2119-2129.
31. Yeo B T, Krienen F M, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol, 2011, 3(106): 1125-1165.
32. Smith S M. Fast robust automated brain extraction. Hum Brain Mapp, 2002, 17(3): 143-155.
33. Richman J S, Moorman J R. Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol, 2000, 278(6): H2039-H2049.
34. Xia Mingrui, Wang Jinhui, He Yong, et al. BrainNet Viewer: A network visualization tool for human brain connectomics. PLoS One, 2013, 8(7): e68910.
35. Cortes C, Vapnik V. Support vector networks. Mach Learn, 1995, 20(3): 273-297.
36. Peter A, Lino R, Nelson D, et al. A support vectors classifier approach to predicting the risk of progression of adolescent idiopathic scoliosis. IEEE Trans Inf Technol Biomed, 2005, 9(2): 276-282.
37. Jafari-Khouzani K, Elisevich K, Karvelis K C, et al. Quantitative multi-compartmental SPECT image analysis for lateralization of temporal lobe epilepsy. Epilepsy Res, 2011, 95(1): 35-30.
38. Jin S H, Chung C K. Electrophysiological resting-state biomarker for diagnosing mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsy Res, 2017, 129: 138-145.
39. Beheshti I, Sone D, Maikusa N, et al. FLAIR-Wise machine-learning classification and lateralization of MRI-negative 18F-FDG PET-positive temporal lobe epilepsy. Front Neurol, 2020, 11: 580713.
40. Morgan V L, Englot D J, Rogers B P, et al. Magnetic resonance imaging connectivity for the prediction of seizure outcome in temporal lobe epilepsy. Epilepsia, 2017, 58(7): 1251-1260.
41. Laufs H. Functional imaging of seizures and epilepsy: Evolution from zones to networks. Curr Opin Neurol, 2012, 25(2): 194-200.
42. Fahoum F, Lopes R, Pittau F, et al. Widespread epileptic networks in focal epilepsies: EEG-fMRI study. Epilepsia, 2012, 53(9): 1618-1627.
43. Farid N, Girard H M, Kemmotsu N, et al. Temporal lobe epilepsy: Quantitative MR volumetry in detection of hippocampal atrophy. Radiology, 2012, 264(2): 542-550.
44. Moran N F, Lemieux L, Kitchen N D, et al. Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. Brain, 2001, 124(Pt1): 167-175.
45. Bonilha L, Rorden C, Castellano G, et al. Voxel-based morphometry of the thalamus in patients with refractory medial temporal lobe epilepsy. Neuroimage, 2005, 25(3): 1016-1021.

Journal of Biomedical Engineering

Optimized multi-scale entropy to localize epileptogenic hemisphere of temporal lobe epilepsy based on resting-state functional magnetic resonance imaging

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