Automatic detection of interictal ripples on scalp EEG to evaluate the effect and prognosis of ACTH therapy in patients with infantile spasms
Wei Wang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorHua Li
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Search for more papers by this authorJiaqing Yan
College of Electrical and Control Engineering, North China University of Technology, Beijing, China
Search for more papers by this authorHerui Zhang
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorXiaonan Li
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorSu Zheng
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Search for more papers by this authorJiaoyang Wang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorYue Xing
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorLipeng Cheng
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorDonghong Li
The Third Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorHuanling Lai
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorJunda Qu
Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, School of Biomedical Engineering, Capital Medical University, Beijing, China
Search for more papers by this authorHorace H. Loh
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorCorresponding Author
Fang Fang
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Correspondence
Xiaofeng Yang, Beijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing, 100069, China and Bioland.
Email: [email protected]
Fang Fang, Department of Neurology, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, 100045, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Xiaofeng Yang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Correspondence
Xiaofeng Yang, Beijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing, 100069, China and Bioland.
Email: [email protected]
Fang Fang, Department of Neurology, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, 100045, China.
Email: [email protected]
Search for more papers by this authorWei Wang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorHua Li
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Search for more papers by this authorJiaqing Yan
College of Electrical and Control Engineering, North China University of Technology, Beijing, China
Search for more papers by this authorHerui Zhang
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorXiaonan Li
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorSu Zheng
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Search for more papers by this authorJiaoyang Wang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorYue Xing
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorLipeng Cheng
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorDonghong Li
The Third Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorHuanling Lai
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorJunda Qu
Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, School of Biomedical Engineering, Capital Medical University, Beijing, China
Search for more papers by this authorHorace H. Loh
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Search for more papers by this authorCorresponding Author
Fang Fang
Department of Neurology, National Center for Children's Health, Beijing Children's Hospital, Capital Medical University, Beijing, China
Correspondence
Xiaofeng Yang, Beijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing, 100069, China and Bioland.
Email: [email protected]
Fang Fang, Department of Neurology, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, 100045, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Xiaofeng Yang
Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China
Bioland Laboratory Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou, China
Correspondence
Xiaofeng Yang, Beijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing, 100069, China and Bioland.
Email: [email protected]
Fang Fang, Department of Neurology, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, 100045, China.
Email: [email protected]
Search for more papers by this authorAbstract
Objective
We aimed to explore the feasibility of using scalp-recorded high-frequency oscillations (HFOs) to evaluate the efficacy and prognosis of adrenocorticotropic hormone (ACTH) treatment in patients with infantile spasms.
Methods
Thirty-nine children with infantile spasms were enrolled and divided into seizure-free and non–seizure-free groups after ACTH treatment. Patients who were seizure-free were further divided into relapse and non-relapse subgroups based on the observations made during a 6-month follow-up period. Scalp ripples were detected and compared during the interictal periods before and after 2 weeks of treatment.
Results
After ACTH treatment, the number and channels of ripples were significantly lower, whereas the percentage decrease in the number, spectral power, and channels of ripples was significantly higher in the seizure-free group than in the non–seizure-free group. In addition, the relapse subgroup showed higher number and spectral power and wider distribution of ripples than did the non-relapse subgroup. Changes in HFOs in terms of number, spectral power, and channel of ripples were closely related to the severity of epilepsy and can indicate disease susceptibility.
Significance
Scalp HFOs can be used as an effective biomarker to monitor the effect and evaluate the prognosis of ACTH therapy in patients with infantile spasms.
CONFLICT OF INTEREST
None of the authors has financial interests or potential conflicts of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
Supporting Information
| Filename | Description |
|---|---|
| epi17018-sup-0001-FigureS1.tifTIFF image, 54.5 MB | Figure S1 |
| epi17018-sup-0002-FigureS2.tifTIFF image, 48.3 MB | Figure S2 |
| epi17018-sup-0003-TableS1.docxWord document, 13.5 KB | Table S1 |
| epi17018-sup-0004-TableS2.docxWord document, 14.2 KB |
Table S2 MATLAB_code |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Knupp KG, Leister E, Coryell J, Nickels KC, Ryan N, Juarez-Colunga E, et al. Response to second treatment after initial failed treatment in a multicenter prospective infantile spasms cohort. Epilepsia. 2016; 57: 1834–42.
- 2D'Alonzo R, Rigante D, Mencaroni E, Esposito S. West syndrome: a review and guide for Paediatricians. Clin Drug Investig. 2018; 38: 113–24.
- 3Frauscher B, Bartolomei F, Kobayashi K, Cimbalnik J, van't Klooster MA, Rampp S, et al. High-frequency oscillations: the state of clinical research. Epilepsia. 2017; 58(8): 1316–29.
- 4Jacobs J, Staba R, Asano E, Otsubo H, Wu JY, Zijlmans M, et al. High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol. 2012; 98(3): 302–15.
- 5Jacobs J, Zijlmans M, Zelmann R, Chatillon CE, Hall J, Olivier A, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol. 2010; 67: 209–20.
- 6Holler Y, Kutil R, Klaffenbock L, Thomschewski A, Holler PM, Bathke AC, et al. High-frequency oscillations in epilepsy and surgical outcome. A meta-analysis. Front Hum Neurosci. 2015; 9: 574.
- 7Haegelen C, Perucca P, Chatillon CE, Andrade-Valenca L, Zelmann R, Jacobs J, et al. High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia. 2013; 54: 848–57.
- 8Jiang C, Li X, Yan J, Yu T, Wang X, Ren Z, et al. Determining the quantitative threshold of high-frequency oscillation distribution to delineate the epileptogenic zone by automated detection. Front Neurol. 2018; 9: 889.
- 9Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80-500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia. 2008; 49(11): 1893–907.
- 10Jacobs J, Vogt C, LeVan P, Zelmann R, Gotman J, Kobayashi K. The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes. Clin Neurophysiol. 2016; 127: 129–42.
- 11Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia. 2004; 45: 1017–23.
- 12Zijlmans M, Jacobs J, Zelmann R, Dubeau F, Gotman J. High frequency oscillations and seizure frequency in patients with focal epilepsy. Epilepsy Res. 2009; 85: 287–92.
- 13Zijlmans M, Huiskamp GM, Cremer OL, Ferrier CH, van Huffelen AC, Leijten FS. Epileptic high-frequency oscillations in intraoperative electrocorticography: the effect of propofol. Epilepsia. 2012; 53: 1799–809.
- 14Lévesque M, Behr C, Avoli M. The anti-ictogenic effects of levetiracetam are mirrored by interictal spiking and high-frequency oscillation changes in a model of temporal lobe epilepsy. Seizure. 2015; 25: 18–25.
- 15Worrell GA, Parish L, Cranstoun SD, Jonas R, Baltuch G, Litt B. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain. 2004; 127: 1496–506.
- 16Cooper R, Winter AL, Crow HJ, Walter WG. Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroencephalogr Clin Neurophysiol. 1965; 18: 217–28.
- 17Tao JX, Ray A, Hawes-Ebersole S, Ebersole JS. Intracranial EEG substrates of scalp EEG interictal spikes. Epilepsia. 2005; 46: 669–76.
- 18Winden KD, Bragin A, Engel J, Geschwind DH. Molecular alterations in areas generating fast ripples in an animal model of temporal lobe epilepsy. Neurobiol Dis. 2015; 78: 35–44.
- 19Zijlmans M, Worrell GA, Dumpelmann M, Stieglitz T, Barborica A, Heers M, et al. How to record high-frequency oscillations in epilepsy: a practical guideline. Epilepsia. 2017; 58: 1305–15.
- 20Kobayashi K, Watanabe Y, Inoue T, Oka M, Yoshinaga H, Ohtsuka Y. Scalp-recorded high-frequency oscillations in childhood sleep-induced electrical status epilepticus. Epilepsia. 2010; 51: 2190–4.
- 21Thomschewski A, Hincapie AS, Frauscher B. Localization of the epileptogenic zone using high frequency oscillations. Front Neurol. 2019; 10: 94.
- 22Shibata T, Kobayashi K. Epileptic high-frequency oscillations in scalp electroencephalography. Acta Med Okayama. 2018; 72: 325–9.
- 23Qian P, Li H, Xue J, Yang Z. Scalp-recorded high-frequency oscillations in atypical benign partial epilepsy. Clin Neurophysiol. 2016; 127: 3306–13.
- 24Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology. 2011; 9(77): 524–31.
- 25Iwatani Y, Kagitani-Shimono K, Tominaga K, Okinaga T, Kishima H, Kato A, et al. Ictal high-frequency oscillations on scalp EEG recordings in symptomatic West syndrome. Epilepsy Res. 2012; 102: 60–70.
- 26Fahoum F, Melani F, Andrade-Valenca L, Dubeau F, Gotman J. Epileptic scalp ripples are associated with corticothalamic BOLD changes. Epilepsia. 2014; 55: 1611–9.
- 27Kuhnke N, Schwind J, Dumpelmann M, Mader M, Schulze-Bonhage A, Jacobs J. High frequency oscillations in the ripple band (80-250 Hz) in scalp EEG: higher density of electrodes allows for better localization of the seizure onset zone. Brain Topogr. 2018; 31: 1059–72.
- 28Cao D, Chen Y, Liao J, Nariai H, Li L, Zhu Y, et al. Scalp EEG high frequency oscillations as a biomarker of treatment response in epileptic encephalopathy with continuous spike-and-wave during sleep (CSWS). Seizure. 2019; 71: 151–7.
- 29Cuello-Oderiz C, von Ellenrieder N, Dubeau F, Gotman J. Influence of the location and type of epileptogenic lesion on scalp interictal epileptiform discharges and high-frequency oscillations. Epilepsia. 2017; 58: 2153–63.
- 30Nariai H, Hussain SA, Bernardo D, Motoi H, Sonoda M, Kuroda N, et al. Scalp EEG interictal high frequency oscillations as an objective biomarker of infantile spasms. Clin Neurophysiol. 2020; 131: 2527–36.
- 31Klotz KA, Sag Y, Schonberger J, Jacobs J. Scalp ripples can predict development of epilepsy after first unprovoked seizure in childhood. Ann Neurol. 2021; 89: 134–42.
- 32Zelmann R, Lina JM, Schulze-Bonhage A, Gotman J, Jacobs J. Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr. 2014; 27: 683–704.
- 33Kobayashi K, Akiyama T, Oka M, Endoh F, Yoshinaga H. A storm of fast (40-150Hz) oscillations during hypsarrhythmia in West syndrome. Ann Neurol. 2015; 77(1): 58–67.
- 34Holler P, Trinka E, Holler Y. High-frequency oscillations in the scalp electroencephalogram: mission impossible without computational intelligence. Comput Intell Neurosci. 2018; 2018: 1638097.
- 35Chaitanya G, Sinha S, Narayanan M, Satishchandra P. Scalp high frequency oscillations (HFOs) in absence epilepsy: an independent component analysis (ICA) based approach. Epilepsy Res. 2015; 115: 133–40.
- 36Bernardo D, Nariai H, Hussain SA, Sankar R, Salamon N, Krueger DA, et al. Visual and semi-automatic non-invasive detection of interictal fast ripples: A potential biomarker of epilepsy in children with tuberous sclerosis complex. Clin Neurophysiol. 2018; 129: 1458–66.
- 37von Ellenrieder N, Andrade-Valenca LP, Dubeau F, Gotman J. Automatic detection of fast oscillations (40–200 Hz) in scalp EEG recordings. Clin Neurophysiol. 2012; 123: 670–80.
- 38Charupanit K, Nunez MD, Bernardo D, Bebin M, Krueger DA, Northrup H, et al. Automated detection of high frequency oscillations in human scalp electroencephalogram. Annu Int Conf IEEE Eng Med Biol Soc. 2018; 2018: 3116–9.
- 39Ren GP, Yan JQ, Yu ZX, Wang D, Li XN, Mei SS, et al. Automated detector of high frequency oscillations in epilepsy based on maximum distributed peak points. Int J Neural Syst. 2018; 28: 1750029.
- 40Youden WJ. Index for rating diagnostic tests. Cancer. 1950; 3: 32–5.
10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3 CAS PubMed Web of Science® Google Scholar
- 41Zelmann R, Zijlmans M, Jacobs J, Chatillon CE, Gotman J. Improving the identification of high frequency oscillations. Clin Neurophysiol. 2009; 120: 1457–64.
- 42Urrestarazu E, Chander R, Dubeau F, Gotman J. Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain. 2007; 130: 2354–66.
- 43Mooij AH, Raijmann R, Jansen FE, Braun KPJ, Zijlmans M. Physiological ripples (± 100 Hz) in spike-free scalp EEGs of children with and without epilepsy. Brain Topogr. 2017; 30: 739–46.
- 44Mytinger JR, Vidaurre J, Moore-Clingenpeel M, Stanek JR, Albert DVF. A reliable interictal EEG grading scale for children with infantile spasms - The 2021 BASED score. Epilepsy Res. 2021; 2(173):e106631.
- 45Kramer MA, Ostrowski LM, Song DY, Thorn EL, Stoyell SM, Parnes M, et al. Scalp recorded spike ripples predict seizure risk in childhood epilepsy better than spikes. Brain. 2019; 1(142): 1296–309.
- 46Kobayashi K, Yoshinaga H, Toda Y, Inoue T, Oka M, Ohtsuka Y. High-frequency oscillations in idiopathic partial epilepsy of childhood. Epilepsia. 2011; 52: 1812–9.
- 47Hayashi Y, Yoshinaga H, Akiyama T, Endoh F, Ohtsuka Y, Kobayashi K. Predictive factors for relapse of epileptic spasms after adrenocorticotropic hormone therapy in West syndrome. Brain Dev. 2016; 38: 32–9.
- 48van Klink NE, van't Klooster MA, Leijten FSS, Jacobs J, Braun KPJ, Zijlmans M. Ripples on rolandic spikes: a marker of epilepsy severity. Epilepsia. 2016; 57(7): 1179–89.
- 49Frost JD Jr, Hrachovy RA. Pathogenesis of infantile spasms: a model based on developmental desynchronization. J Clin Neurophysiol. 2005; 22: 25–36.
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