The incidence and significance of periictal apnea in epileptic seizures

Nuria Lacuey; Bilal Zonjy; Johnson P. Hampson; M. R.Sandhya Rani; Anita Zaremba; Rup K. Sainju; Brian K. Gehlbach; Stephan Schuele; Daniel Friedman; Orrin Devinsky; Maromi Nei; Ronald M. Harper; Luke Allen; Beate Diehl; John J. Millichap; Lisa Bateman; Mark A. Granner; Deidre N. Dragon; George B. Richerson; Samden D. Lhatoo

doi:10.1111/epi.14006

The incidence and significance of periictal apnea in epileptic seizures

Nuria Lacuey^*, Bilal Zonjy, Johnson P. Hampson, M. R.Sandhya Rani, Anita Zaremba, Rup K. Sainju, Brian K. Gehlbach, Stephan Schuele, Daniel Friedman, Orrin Devinsky, Maromi Nei, Ronald M. Harper, Luke Allen, Beate Diehl, John J. Millichap, Lisa Bateman, Mark A. Granner, Deidre N. Dragon, George B. Richerson, Samden D. Lhatoo

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

108 Scopus citations

Abstract

Objective: The aim of this study was to investigate periictal central apnea as a seizure semiological feature, its localizing value, and possible relationship with sudden unexpected death in epilepsy (SUDEP) pathomechanisms. Methods: We prospectively studied polygraphic physiological responses, including inductance plethysmography, peripheral capillary oxygen saturation (SpO₂), electrocardiography, and video electroencephalography (VEEG) in 473 patients in a multicenter study of SUDEP. Seizures were classified according to the International League Against Epilepsy (ILAE) 2017 seizure classification based on the most prominent clinical signs during VEEG. The putative epileptogenic zone was defined based on clinical history, seizure semiology, neuroimaging, and EEG. Results: Complete datasets were available in 126 patients in 312 seizures. Ictal central apnea (ICA) occurred exclusively in focal epilepsy (51/109 patients [47%] and 103/312 seizures [36.5%]) (P <.001). ICA was the only clinical manifestation in 16/103 (16.5%) seizures, and preceded EEG seizure onset by 8 ± 4.9 s, in 56/103 (54.3%) seizures. ICA ≥60 s was associated with severe hypoxemia (SpO₂ <75%). Focal onset impaired awareness (FOIA) motor onset with automatisms and FOA nonmotor onset semiologies were associated with ICA presence (P <.001), ICA duration (P =.002), and moderate/severe hypoxemia (P =.04). Temporal lobe epilepsy was highly associated with ICA in comparison to extratemporal epilepsy (P =.001) and frontal lobe epilepsy (P =.001). Isolated postictal central apnea was not seen; in 3/103 seizures (3%), ICA persisted into the postictal period. Significance: ICA is a frequent, self-limiting semiological feature of focal epilepsy, often starting before surface EEG onset, and may be the only clinical manifestation of focal seizures. However, prolonged ICA (≥60 s) is associated with severe hypoxemia and may be a potential SUDEP biomarker. ICA is more frequently seen in temporal than extratemporal seizures, and in typical temporal seizure semiologies. ICA rarely persists after seizure end. ICA agnosia is typical, and thus it may remain unrecognized without polygraphic measurements that include breathing parameters.

Original language	English (US)
Pages (from-to)	573-582
Number of pages	10
Journal	Epilepsia
Volume	59
Issue number	3
DOIs	https://doi.org/10.1111/epi.14006
State	Published - Mar 2018

Funding

Samden Lhatoo is funded by the Center for SUDEP Research: NIH/NINDS U01-NS090405 and NIH/NINDS U01-NS090407. Bilal Zonjy, Sandhya Rani, Anita Zaremba, Rup Sainju, Brian K. Gehlbach, Stephan Schuele, Daniel Friedman, Maromi Nei, Ronald Harper, Luke Allen, Beate Diehl, John Millichap, Lisa Bateman, and George B. Richerson are funded by NIH/NINDS U01-NS090407. Orrin Devinsky is funded by Center for SUDEP Research NIH/NINDS UO1-NS090415 and NIH/NINDS U01-NS090407. Stephan Schuele is on the speaker’s bureau for Sunovion and Eisai. Nuria Lacuey, Johnson D. Hampson, Mark A. Granner, and Deidre N. Dragon report no disclosures. 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. We would like to thank the Universitat Autonoma de Barcelona for supporting NL's Doctoral thesis in Medicine and Shailen Nandy (Cardiff University, UK) for his assistance with the statistical analysis.

Keywords

apnea
breathing
seizures
sudden unexpected death in epilepsy
temporal epilepsy

ASJC Scopus subject areas

Neurology
Clinical Neurology

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Lacuey, N., Zonjy, B., Hampson, J. P., Rani, M. R. S., Zaremba, A., Sainju, R. K., Gehlbach, B. K., Schuele, S., Friedman, D., Devinsky, O., Nei, M., Harper, R. M., Allen, L., Diehl, B., Millichap, J. J., Bateman, L., Granner, M. A., Dragon, D. N., Richerson, G. B., & Lhatoo, S. D. (2018). The incidence and significance of periictal apnea in epileptic seizures. Epilepsia, 59(3), 573-582. https://doi.org/10.1111/epi.14006

@article{51f8562bc77a41729bcb6b9d6541de9a,

title = "The incidence and significance of periictal apnea in epileptic seizures",

abstract = "Objective: The aim of this study was to investigate periictal central apnea as a seizure semiological feature, its localizing value, and possible relationship with sudden unexpected death in epilepsy (SUDEP) pathomechanisms. Methods: We prospectively studied polygraphic physiological responses, including inductance plethysmography, peripheral capillary oxygen saturation (SpO2), electrocardiography, and video electroencephalography (VEEG) in 473 patients in a multicenter study of SUDEP. Seizures were classified according to the International League Against Epilepsy (ILAE) 2017 seizure classification based on the most prominent clinical signs during VEEG. The putative epileptogenic zone was defined based on clinical history, seizure semiology, neuroimaging, and EEG. Results: Complete datasets were available in 126 patients in 312 seizures. Ictal central apnea (ICA) occurred exclusively in focal epilepsy (51/109 patients [47%] and 103/312 seizures [36.5%]) (P <.001). ICA was the only clinical manifestation in 16/103 (16.5%) seizures, and preceded EEG seizure onset by 8 ± 4.9 s, in 56/103 (54.3%) seizures. ICA ≥60 s was associated with severe hypoxemia (SpO2 <75%). Focal onset impaired awareness (FOIA) motor onset with automatisms and FOA nonmotor onset semiologies were associated with ICA presence (P <.001), ICA duration (P =.002), and moderate/severe hypoxemia (P =.04). Temporal lobe epilepsy was highly associated with ICA in comparison to extratemporal epilepsy (P =.001) and frontal lobe epilepsy (P =.001). Isolated postictal central apnea was not seen; in 3/103 seizures (3%), ICA persisted into the postictal period. Significance: ICA is a frequent, self-limiting semiological feature of focal epilepsy, often starting before surface EEG onset, and may be the only clinical manifestation of focal seizures. However, prolonged ICA (≥60 s) is associated with severe hypoxemia and may be a potential SUDEP biomarker. ICA is more frequently seen in temporal than extratemporal seizures, and in typical temporal seizure semiologies. ICA rarely persists after seizure end. ICA agnosia is typical, and thus it may remain unrecognized without polygraphic measurements that include breathing parameters.",

keywords = "apnea, breathing, seizures, sudden unexpected death in epilepsy, temporal epilepsy",

author = "Nuria Lacuey and Bilal Zonjy and Hampson, {Johnson P.} and Rani, {M. R.Sandhya} and Anita Zaremba and Sainju, {Rup K.} and Gehlbach, {Brian K.} and Stephan Schuele and Daniel Friedman and Orrin Devinsky and Maromi Nei and Harper, {Ronald M.} and Luke Allen and Beate Diehl and Millichap, {John J.} and Lisa Bateman and Granner, {Mark A.} and Dragon, {Deidre N.} and Richerson, {George B.} and Lhatoo, {Samden D.}",

note = "Publisher Copyright: Wiley Periodicals, Inc. {\textcopyright} 2018 International League Against Epilepsy",

year = "2018",

month = mar,

doi = "10.1111/epi.14006",

language = "English (US)",

volume = "59",

pages = "573--582",

journal = "Epilepsia",

issn = "0013-9580",

publisher = "Wiley-Blackwell",

number = "3",

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Lacuey, N, Zonjy, B, Hampson, JP, Rani, MRS, Zaremba, A, Sainju, RK, Gehlbach, BK, Schuele, S, Friedman, D, Devinsky, O, Nei, M, Harper, RM, Allen, L, Diehl, B, Millichap, JJ, Bateman, L, Granner, MA, Dragon, DN, Richerson, GB & Lhatoo, SD 2018, 'The incidence and significance of periictal apnea in epileptic seizures', Epilepsia, vol. 59, no. 3, pp. 573-582. https://doi.org/10.1111/epi.14006

TY - JOUR

T1 - The incidence and significance of periictal apnea in epileptic seizures

AU - Lacuey, Nuria

AU - Zonjy, Bilal

AU - Hampson, Johnson P.

AU - Rani, M. R.Sandhya

AU - Zaremba, Anita

AU - Sainju, Rup K.

AU - Gehlbach, Brian K.

AU - Schuele, Stephan

AU - Friedman, Daniel

AU - Devinsky, Orrin

AU - Nei, Maromi

AU - Harper, Ronald M.

AU - Allen, Luke

AU - Diehl, Beate

AU - Millichap, John J.

AU - Bateman, Lisa

AU - Granner, Mark A.

AU - Dragon, Deidre N.

AU - Richerson, George B.

AU - Lhatoo, Samden D.

PY - 2018/3

Y1 - 2018/3

N2 - Objective: The aim of this study was to investigate periictal central apnea as a seizure semiological feature, its localizing value, and possible relationship with sudden unexpected death in epilepsy (SUDEP) pathomechanisms. Methods: We prospectively studied polygraphic physiological responses, including inductance plethysmography, peripheral capillary oxygen saturation (SpO2), electrocardiography, and video electroencephalography (VEEG) in 473 patients in a multicenter study of SUDEP. Seizures were classified according to the International League Against Epilepsy (ILAE) 2017 seizure classification based on the most prominent clinical signs during VEEG. The putative epileptogenic zone was defined based on clinical history, seizure semiology, neuroimaging, and EEG. Results: Complete datasets were available in 126 patients in 312 seizures. Ictal central apnea (ICA) occurred exclusively in focal epilepsy (51/109 patients [47%] and 103/312 seizures [36.5%]) (P <.001). ICA was the only clinical manifestation in 16/103 (16.5%) seizures, and preceded EEG seizure onset by 8 ± 4.9 s, in 56/103 (54.3%) seizures. ICA ≥60 s was associated with severe hypoxemia (SpO2 <75%). Focal onset impaired awareness (FOIA) motor onset with automatisms and FOA nonmotor onset semiologies were associated with ICA presence (P <.001), ICA duration (P =.002), and moderate/severe hypoxemia (P =.04). Temporal lobe epilepsy was highly associated with ICA in comparison to extratemporal epilepsy (P =.001) and frontal lobe epilepsy (P =.001). Isolated postictal central apnea was not seen; in 3/103 seizures (3%), ICA persisted into the postictal period. Significance: ICA is a frequent, self-limiting semiological feature of focal epilepsy, often starting before surface EEG onset, and may be the only clinical manifestation of focal seizures. However, prolonged ICA (≥60 s) is associated with severe hypoxemia and may be a potential SUDEP biomarker. ICA is more frequently seen in temporal than extratemporal seizures, and in typical temporal seizure semiologies. ICA rarely persists after seizure end. ICA agnosia is typical, and thus it may remain unrecognized without polygraphic measurements that include breathing parameters.

AB - Objective: The aim of this study was to investigate periictal central apnea as a seizure semiological feature, its localizing value, and possible relationship with sudden unexpected death in epilepsy (SUDEP) pathomechanisms. Methods: We prospectively studied polygraphic physiological responses, including inductance plethysmography, peripheral capillary oxygen saturation (SpO2), electrocardiography, and video electroencephalography (VEEG) in 473 patients in a multicenter study of SUDEP. Seizures were classified according to the International League Against Epilepsy (ILAE) 2017 seizure classification based on the most prominent clinical signs during VEEG. The putative epileptogenic zone was defined based on clinical history, seizure semiology, neuroimaging, and EEG. Results: Complete datasets were available in 126 patients in 312 seizures. Ictal central apnea (ICA) occurred exclusively in focal epilepsy (51/109 patients [47%] and 103/312 seizures [36.5%]) (P <.001). ICA was the only clinical manifestation in 16/103 (16.5%) seizures, and preceded EEG seizure onset by 8 ± 4.9 s, in 56/103 (54.3%) seizures. ICA ≥60 s was associated with severe hypoxemia (SpO2 <75%). Focal onset impaired awareness (FOIA) motor onset with automatisms and FOA nonmotor onset semiologies were associated with ICA presence (P <.001), ICA duration (P =.002), and moderate/severe hypoxemia (P =.04). Temporal lobe epilepsy was highly associated with ICA in comparison to extratemporal epilepsy (P =.001) and frontal lobe epilepsy (P =.001). Isolated postictal central apnea was not seen; in 3/103 seizures (3%), ICA persisted into the postictal period. Significance: ICA is a frequent, self-limiting semiological feature of focal epilepsy, often starting before surface EEG onset, and may be the only clinical manifestation of focal seizures. However, prolonged ICA (≥60 s) is associated with severe hypoxemia and may be a potential SUDEP biomarker. ICA is more frequently seen in temporal than extratemporal seizures, and in typical temporal seizure semiologies. ICA rarely persists after seizure end. ICA agnosia is typical, and thus it may remain unrecognized without polygraphic measurements that include breathing parameters.

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KW - breathing

KW - seizures

KW - sudden unexpected death in epilepsy

KW - temporal epilepsy

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The incidence and significance of periictal apnea in epileptic seizures

Abstract

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