Application of graph theory-based brain network in developmental and epileptic encephalopathy_Journal of Epilepsy

Authors：

SUN Xinbin , LIU Zhisheng ,  SUN dan

Department of Neurology, Wuhan Children’s Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430000, China;

Corresponding author：

SUN dan, Email: bloveriver@163.com

Keywords：

Developmental and epileptic encephalopathy; Brain network; Graph theory; Functional connectivity; Structural connectivity

DOI：

10.7507/2096-0247.202411006

Video：

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Abstract Full text Figures/Tables Video References Cited by

Developmental and epileptic encephalopathy (DEE) is a group of diseases that severely affects the neurological development of children, characterized by frequent seizures and significant neurodevelopmental impairments. These diseases not only impact the quality of life of affected children but also impose a heavy burden on families and society. In recent years, the development of brain network theory has provided a new perspective on understanding the pathological mechanisms of DEE, especially the role of structural and functional brain networks in the process of epilepsy. This review systematically summarized the research progress of structural and functional brain networks in DEE, highlighted their importance in seizure activity, disease progression, and prognosis evaluation.

1.	Zuberi SM, Wirrell E, Yozawitz E, et al. ILAE classification and definition of epilepsy syndromes with onset in neonates and infants: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia, 2022, 63(6): 1349-1397.
2.	郑小红, 周有峰, 胡春辉. 遗传性发育性癫痫性脑病神经生物学及临床诊治研究进展. 癫痫杂志, 2024, 10(3): 254-259.
3.	Happ HC, Carvill GL. A 2020 View on the genetics of developmental and epileptic encephalopathies. Epilepsy Curr, 2020, 20(2): 90-96.
4.	童培, 刘艳. 发育性及癫痫性脑病的遗传学研究进展. 癫痫杂志, 2022, 8(4): 338-341.
5.	Guerrini R, Conti V, Mantegazza M, et al. Developmental and epileptic encephalopathies: from genetic heterogeneity to phenotypic continuum. Physiol Rev, 2023, 103(1): 433-513.
6.	Royer J, Bernhardt BC, Larivière S, et al. Epilepsy and brain network hubs. Epilepsia, 2022, 63(3): 537-550.
7.	van Diessen E, Diederen SJ, Braun KP, et al. Functional and structural brain networks in epilepsy: what have we learned? Epilepsia, 2013, 54(11): 1855-65.
8.	Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci, 2009, 10(3): 186-98.
9.	Sporns O. Graph theory methods: applications in brain networks. Dialogues Clin Neurosci, 2018, 20(2): 111-121.
10.	Gleichgerrcht E, Kocher M, Bonilha L. Connectomics and graph theory analyses: Novel insights into network abnormalities in epilepsy. Epilepsia, 2015, 56(11): 1660-1668.
11.	Goodman AM, Szaflarski JP. Recent advances in neuroimaging of epilepsy. Neurotherapeutics, 2021, 18(2): 811-826.
12.	Winklewski PJ, Sabisz A, Naumczyk P, et al. Understanding the physiopathology behind axial and radial diffusivity changes-what do we know? Front Neurol, 2018, 9: 92.
13.	Wurina, Zang YF, Zhao SG. Resting-state fMRI studies in epilepsy. Neurosci Bull, 2012, 28(4): 449-455.
14.	Mégevand P, Seeck M. Electroencephalography, magnetoencephalography and source localization: their value in epilepsy. Curr Opin Neurol, 2018, 31(2): 176-183.
15.	Baillet S. Magnetoencephalography for brain electrophysiology and imaging. Nat Neurosci, 2017, 20(3): 327-339.
16.	Whelan CD, Altmann A, Botía JA, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain, 2018, 141(2): 391-408.
17.	Bröhl T, Rings T, Pukropski J, et al. The time-evolving epileptic brain network: concepts, definitions, accomplishments, perspectives. Front Netw Physiol, 2024, 16(3): 1338864.
18.	Zhang F, Daducci A, He Y, et al. Quantitative mapping of the brain's structural connectivity using diffusion MRI tractography: A review. Neuroimage, 2022, 249: 118870.
19.	Natsume J, Ogawa C, Fukasawa T, et al. White Matter Abnormality Correlates with Developmental and Seizure Outcomes in West Syndrome of Unknown Etiology. AJNR Am J Neuroradiol, 2016, 37(4): 698-705.
20.	Ogawa C, Kidokoro H, Fukasawa T, et al. Cytotoxic edema at onset in West syndrome of unknown etiology: A longitudinal diffusion tensor imaging study. Epilepsia, 2018, 59(2): 440-448.
21.	Lee YJ, Yum MS, Kim MJ, et al. Large-scale structural alteration of brain in epileptic children with SCN1A mutation. Neuroimage Clin, 2017, 15: 594-600.
22.	Guerrini R, Striano P, Catarino C, et al. Neuroimaging and neuropathology of Dravet syndrome. Epilepsia, 2011, 52(Suppl 2): 30-34.
23.	Lenge M, Balestrini S, Mei D, et al. Morphometry and network-based atrophy patterns in SCN1A-related Dravet syndrome. Cereb Cortex, 2023, 33(16): 9532-9541.
24.	Lenge M, Balestrini S, Napolitano A, et al. Morphometric network-based abnormalities correlate with psychiatric comorbidities and gene expression in PCDH19-related developmental and epileptic encephalopathy. Transl Psychiatry, 2024, 14(1): 35.
25.	Wang J, Li Y, Wang Y, et al. Multimodal data and machine learning for detecting specific biomarkers in pediatric epilepsy patients with generalized tonic-clonic seizures. Front Neurol, 2018, 9: 1038.
26.	Zhang CT, Sun YL, Shi WB, et al. Brain complexity predicts response to adrenocorticotropic hormone in infantile epileptic spasms syndrome: a retrospective study. Neurol Ther, 2023, 12(1): 129-144.
27.	Shrey DW, Kim McManus O, Rajaraman R, et al. Strength and stability of EEG functional connectivity predict treatment response in infants with epileptic spasms. Clin Neurophysiol, 2018, 129(10): 2137-2148.
28.	Dong Y, Jin L, Li M, et al. Crucial involvement of fast waves and Delta band in the brain network attributes of infantile epileptic spasms syndrome. Front Pediatr, 2023, 11: 1249789.
29.	Dong Y, Xu R, Zhang Y, et al. Different frequency bands in various regions of the brain play different roles in the onset and wake-sleep stages of infantile spasms. Front Pediatr, 2022, 10: 878099.
30.	Zheng R, Feng Y, Wang T, et al. Scalp EEG functional connection and brain network in infants with West syndrome. Neural Netw, 2022, 153: 76-86.
31.	Park KM, Park S, Hur YJ. Brain network reconstruction of abnormal functional connectivity in Lennox-Gastaut syndrome according to drug responsiveness: a retrospective study. Epilepsy Res, 2024, 200: 107312.
32.	Wang Z, Larivière S, Xu Q, et al. Community-informed connectomics of the thalamocortical system in generalized epilepsy. Neurology, 2019, 93(11): e1112-e1122.
33.	Moeller F, Maneshi M, Pittau F, et al. Functional connectivity in patients with idiopathic generalized epilepsy. Epilepsia, 2011, 52(3): 515-22.
34.	Silva Alves A, Rigoni I, Mégevand P, et al. High-density electroencephalographic functional networks in genetic generalized epilepsy: Preserved whole-brain topology hides local reorganization. Epilepsia, 2024, 65(4): 961-973.
35.	Wang Y, Li Y, Yang L, et al. Altered topological organization of resting-state functional networks in children with infantile spasms. Front Neurosci, 2022, 16: 952940.
36.	Tan Z, Li Y, Zang D, et al. Altered regional homogeneity in epileptic patients with infantile spasm: a resting-state fMRI study. J Xray Sci Technol, 2016, 24(2): 285-295.
37.	Gonen OM, Kwan P, O'Brien TJ, et al. Resting-state functional MRI of the default mode network in epilepsy. Epilepsy Behav, 2020, 111: 107308.
38.	Siniatchkin M, van Baalen A, Jacobs J, et al. Different neuronal networks are associated with spikes and slow activity in hypsarrhythmia. Epilepsia, 2007, 48(12): 2312-2321.
39.	Japaridze N, Muthuraman M, Moeller F, et al. Neuronal networks in west syndrome as revealed by source analysis and renormalized partial directed coherence. Brain Topogr, 2013, 26(1): 157-170.
40.	Archer JS, Warren AE, Jackson GD, et al. Conceptualizing Lennox-Gastaut syndrome as a secondary network epilepsy. Front Neurol, 2014, 5: 225.
41.	Warren AEL, Harvey AS, Vogrin SJ, et al. The epileptic network of Lennox-Gastaut syndrome: Cortically driven and reproducible across age. Neurology, 2019, 93(3): e215-e226.
42.	Moehring J, von Spiczak S, Moeller F, et al. Variability of EEG-fMRI findings in patients with SCN1A-positive Dravet syndrome. Epilepsia, 2013, 54(5): 918-926.
43.	Burianová H, Faizo NL, Gray M, et al. Altered functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res, 2017, 137: 45-52.
44.	Vaessen MJ, Jansen JF, Braakman HM, et al. Functional and structural network impairment in childhood frontal lobe epilepsy. PLoS One, 2014, 9(3): e90068.
45.	Stacey W, Kramer M, Gunnarsdottir K, et al. Emerging roles of network analysis for epilepsy. Epilepsy Res, 2020, 159: 106255.
46.	Kim J, Kim MJ, Kim HJ, et al. Electrophysiological network predicts clinical response to vigabatrin in epileptic spasms. Front Neurol, 2023, 14: 1209796.
47.	Piper RJ, Richardson RM, Worrell G, et al. Towards network-guided neuromodulation for epilepsy. Brain, 2022, 145(10): 3347-3362.

1. Zuberi SM, Wirrell E, Yozawitz E, et al. ILAE classification and definition of epilepsy syndromes with onset in neonates and infants: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia, 2022, 63(6): 1349-1397.
2. 郑小红, 周有峰, 胡春辉. 遗传性发育性癫痫性脑病神经生物学及临床诊治研究进展. 癫痫杂志, 2024, 10(3): 254-259.
3. Happ HC, Carvill GL. A 2020 View on the genetics of developmental and epileptic encephalopathies. Epilepsy Curr, 2020, 20(2): 90-96.
4. 童培, 刘艳. 发育性及癫痫性脑病的遗传学研究进展. 癫痫杂志, 2022, 8(4): 338-341.
5. Guerrini R, Conti V, Mantegazza M, et al. Developmental and epileptic encephalopathies: from genetic heterogeneity to phenotypic continuum. Physiol Rev, 2023, 103(1): 433-513.
6. Royer J, Bernhardt BC, Larivière S, et al. Epilepsy and brain network hubs. Epilepsia, 2022, 63(3): 537-550.
7. van Diessen E, Diederen SJ, Braun KP, et al. Functional and structural brain networks in epilepsy: what have we learned? Epilepsia, 2013, 54(11): 1855-65.
8. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci, 2009, 10(3): 186-98.
9. Sporns O. Graph theory methods: applications in brain networks. Dialogues Clin Neurosci, 2018, 20(2): 111-121.
10. Gleichgerrcht E, Kocher M, Bonilha L. Connectomics and graph theory analyses: Novel insights into network abnormalities in epilepsy. Epilepsia, 2015, 56(11): 1660-1668.
11. Goodman AM, Szaflarski JP. Recent advances in neuroimaging of epilepsy. Neurotherapeutics, 2021, 18(2): 811-826.
12. Winklewski PJ, Sabisz A, Naumczyk P, et al. Understanding the physiopathology behind axial and radial diffusivity changes-what do we know? Front Neurol, 2018, 9: 92.
13. Wurina, Zang YF, Zhao SG. Resting-state fMRI studies in epilepsy. Neurosci Bull, 2012, 28(4): 449-455.
14. Mégevand P, Seeck M. Electroencephalography, magnetoencephalography and source localization: their value in epilepsy. Curr Opin Neurol, 2018, 31(2): 176-183.
15. Baillet S. Magnetoencephalography for brain electrophysiology and imaging. Nat Neurosci, 2017, 20(3): 327-339.
16. Whelan CD, Altmann A, Botía JA, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain, 2018, 141(2): 391-408.
17. Bröhl T, Rings T, Pukropski J, et al. The time-evolving epileptic brain network: concepts, definitions, accomplishments, perspectives. Front Netw Physiol, 2024, 16(3): 1338864.
18. Zhang F, Daducci A, He Y, et al. Quantitative mapping of the brain's structural connectivity using diffusion MRI tractography: A review. Neuroimage, 2022, 249: 118870.
19. Natsume J, Ogawa C, Fukasawa T, et al. White Matter Abnormality Correlates with Developmental and Seizure Outcomes in West Syndrome of Unknown Etiology. AJNR Am J Neuroradiol, 2016, 37(4): 698-705.
20. Ogawa C, Kidokoro H, Fukasawa T, et al. Cytotoxic edema at onset in West syndrome of unknown etiology: A longitudinal diffusion tensor imaging study. Epilepsia, 2018, 59(2): 440-448.
21. Lee YJ, Yum MS, Kim MJ, et al. Large-scale structural alteration of brain in epileptic children with SCN1A mutation. Neuroimage Clin, 2017, 15: 594-600.
22. Guerrini R, Striano P, Catarino C, et al. Neuroimaging and neuropathology of Dravet syndrome. Epilepsia, 2011, 52(Suppl 2): 30-34.
23. Lenge M, Balestrini S, Mei D, et al. Morphometry and network-based atrophy patterns in SCN1A-related Dravet syndrome. Cereb Cortex, 2023, 33(16): 9532-9541.
24. Lenge M, Balestrini S, Napolitano A, et al. Morphometric network-based abnormalities correlate with psychiatric comorbidities and gene expression in PCDH19-related developmental and epileptic encephalopathy. Transl Psychiatry, 2024, 14(1): 35.
25. Wang J, Li Y, Wang Y, et al. Multimodal data and machine learning for detecting specific biomarkers in pediatric epilepsy patients with generalized tonic-clonic seizures. Front Neurol, 2018, 9: 1038.
26. Zhang CT, Sun YL, Shi WB, et al. Brain complexity predicts response to adrenocorticotropic hormone in infantile epileptic spasms syndrome: a retrospective study. Neurol Ther, 2023, 12(1): 129-144.
27. Shrey DW, Kim McManus O, Rajaraman R, et al. Strength and stability of EEG functional connectivity predict treatment response in infants with epileptic spasms. Clin Neurophysiol, 2018, 129(10): 2137-2148.
28. Dong Y, Jin L, Li M, et al. Crucial involvement of fast waves and Delta band in the brain network attributes of infantile epileptic spasms syndrome. Front Pediatr, 2023, 11: 1249789.
29. Dong Y, Xu R, Zhang Y, et al. Different frequency bands in various regions of the brain play different roles in the onset and wake-sleep stages of infantile spasms. Front Pediatr, 2022, 10: 878099.
30. Zheng R, Feng Y, Wang T, et al. Scalp EEG functional connection and brain network in infants with West syndrome. Neural Netw, 2022, 153: 76-86.
31. Park KM, Park S, Hur YJ. Brain network reconstruction of abnormal functional connectivity in Lennox-Gastaut syndrome according to drug responsiveness: a retrospective study. Epilepsy Res, 2024, 200: 107312.
32. Wang Z, Larivière S, Xu Q, et al. Community-informed connectomics of the thalamocortical system in generalized epilepsy. Neurology, 2019, 93(11): e1112-e1122.
33. Moeller F, Maneshi M, Pittau F, et al. Functional connectivity in patients with idiopathic generalized epilepsy. Epilepsia, 2011, 52(3): 515-22.
34. Silva Alves A, Rigoni I, Mégevand P, et al. High-density electroencephalographic functional networks in genetic generalized epilepsy: Preserved whole-brain topology hides local reorganization. Epilepsia, 2024, 65(4): 961-973.
35. Wang Y, Li Y, Yang L, et al. Altered topological organization of resting-state functional networks in children with infantile spasms. Front Neurosci, 2022, 16: 952940.
36. Tan Z, Li Y, Zang D, et al. Altered regional homogeneity in epileptic patients with infantile spasm: a resting-state fMRI study. J Xray Sci Technol, 2016, 24(2): 285-295.
37. Gonen OM, Kwan P, O'Brien TJ, et al. Resting-state functional MRI of the default mode network in epilepsy. Epilepsy Behav, 2020, 111: 107308.
38. Siniatchkin M, van Baalen A, Jacobs J, et al. Different neuronal networks are associated with spikes and slow activity in hypsarrhythmia. Epilepsia, 2007, 48(12): 2312-2321.
39. Japaridze N, Muthuraman M, Moeller F, et al. Neuronal networks in west syndrome as revealed by source analysis and renormalized partial directed coherence. Brain Topogr, 2013, 26(1): 157-170.
40. Archer JS, Warren AE, Jackson GD, et al. Conceptualizing Lennox-Gastaut syndrome as a secondary network epilepsy. Front Neurol, 2014, 5: 225.
41. Warren AEL, Harvey AS, Vogrin SJ, et al. The epileptic network of Lennox-Gastaut syndrome: Cortically driven and reproducible across age. Neurology, 2019, 93(3): e215-e226.
42. Moehring J, von Spiczak S, Moeller F, et al. Variability of EEG-fMRI findings in patients with SCN1A-positive Dravet syndrome. Epilepsia, 2013, 54(5): 918-926.
43. Burianová H, Faizo NL, Gray M, et al. Altered functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res, 2017, 137: 45-52.
44. Vaessen MJ, Jansen JF, Braakman HM, et al. Functional and structural network impairment in childhood frontal lobe epilepsy. PLoS One, 2014, 9(3): e90068.
45. Stacey W, Kramer M, Gunnarsdottir K, et al. Emerging roles of network analysis for epilepsy. Epilepsy Res, 2020, 159: 106255.
46. Kim J, Kim MJ, Kim HJ, et al. Electrophysiological network predicts clinical response to vigabatrin in epileptic spasms. Front Neurol, 2023, 14: 1209796.
47. Piper RJ, Richardson RM, Worrell G, et al. Towards network-guided neuromodulation for epilepsy. Brain, 2022, 145(10): 3347-3362.

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