American Clinical Neurophysiology Society's Standardized Critical Care EEG Terminology 2021 PDF

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2021

Lawrence J. Hirsch, Michael W.K. Fong, Markus Leitinger, Suzette M. LaRoche, Sandor Beniczky, Nicholas S. Abend, Jong Woo Lee, Courtney J. Wusthoff, Cecil D. Hahn, M. Brandon Westover, Elizabeth E. Ge

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critical care EEG neurophysiology medical terminology medical sciences

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This document provides a standardized terminology for periodic and rhythmic EEG patterns in critically ill patients, as defined by the American Clinical Neurophysiology Society (ACNS) in 2021. The authors are from various medical institutions and universities. It details changes in the 2021 terminology compared to previous versions.

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HHS Public Access Author manuscript J Clin Neurophysiol. Author manuscript; available in PMC 2021 October 01. Author Manuscript Published in final edited form as: J Clin Neurophysiol. 2021 Janua...

HHS Public Access Author manuscript J Clin Neurophysiol. Author manuscript; available in PMC 2021 October 01. Author Manuscript Published in final edited form as: J Clin Neurophysiol. 2021 January 01; 38(1): 1–29. doi:10.1097/WNP.0000000000000806. American Clinical Neurophysiology Society’s Standardized Critical Care EEG Terminology: 2021 Version Lawrence J. Hirsch*, Michael W.K. Fong†, Markus Leitinger‡, Suzette M. LaRoche§, Sandor Beniczkyǁ, Nicholas S. Abend¶, Jong Woo Lee#, Courtney J. Wusthoff**, Cecil D. Hahn††, M. Brandon Westover‡‡, Elizabeth E. Gerard§§, Susan T. Hermanǁǁ, Hiba Arif Haider§, Gamaleldin Osman¶¶, Andres Rodriguez-Ruiz§, Carolina B. Maciel##, Emily J. Gilmore*, Author Manuscript Andres Fernandez***, Eric S. Rosenthal†††, Jan Claassen‡‡‡, Aatif M. Husain§§§, Ji Yeoun Yooǁǁǁ, Elson L. So¶¶¶, Peter W. Kaplan###, Marc R. Nuwer****, Michel van Putten††††, Raoul Sutter‡‡‡‡, Frank W. Drislane§§§§, Eugen Trinka‡, Nicolas Gaspardǁǁǁǁ *Comprehensive Epilepsy Center, Department of Neurology, Yale University School of Medicine, New Haven, Connecticut, U.S.A. †Westmead Comprehensive Epilepsy Unit, Westmead Hospital, University of Sydney, Sydney, Australia ‡Department of Neurology, Christian Doppler Klinik, Paracelsus Medical University, Salzburg, Austria §Department of Neurology, Emory University School of Medicine, Atlanta, Georgia, U.S.A. ǁDepartment of Clinical Neurophysiology, Danish Epilepsy Center, Dianalund and Aarhus University Hospital, Aarhus, Denmark ¶Departments of Neurology and Pediatrics, The Children’s Hospital of Philadelphia and the Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A. #Brigham and Author Manuscript Women’s Hospital, Boston, Massachusetts, U.S.A. **Division of Child Neurology, Stanford University, Palo Alto, California, U.S.A. ††Division of Neurology, The Hospital for Sick Children, and Department of Pediatrics, University of Toronto, Toronto, Canada ‡‡Neurology Department, Massachusetts General Hospital, Massachusetts, U.S.A. §§Comprehensive Epilepsy Center, Department of Neurology, Northwestern University, Chicago, Illinois, U.S.A. ǁǁBarrow Neurological Institute, Phoenix, Arizona, U.S.A. ¶¶Department of Neurology, Henry Ford Hospital, Detroit, Michigan, U.S.A. ##Division of Neurocritical Care, Department of Neurology, University of Florida, Gainesville, Florida, U.S.A. ***Department of Neurology, Thomas Jefferson University Hospital, Philadelphia, Pennsylvania, U.S.A. †††Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A. ‡‡‡Neurocritical Care, Department of Neurology, Columbia University, New York, New York, U.S.A. §§§Department of Medicine (Neurology), Duke University Medical Center, and Veterans Affairs Medical Center, Durham, Author Manuscript North Carolina, U.S.A. ǁǁǁDepartment of Neurology, Icahn School of Medicine at Mount Sinai, New York, New York, U.S.A. ¶¶¶Division of Epilepsy, Mayo Clinic, Rochester, Minnesota, U.S.A. ###Department of Neurology, Johns Hopkins University School of Medicine, Johns Hopkins Address correspondence and reprint requests to Lawrence J. Hirsch, MD, Department of Neurology, Comprehensive Epilepsy Center, Yale University School of Medicine, P.O. box 208018, New Haven, CT 06520, U.S.A.; [email protected]. SUPPLEMENTAL DIGITAL CONTENT The “ACNS Standardized Critical Care EEG Terminology 2021: Condensed Version” is available at Supplemental Digital Content, http://links.lww.com/JCNP/A149, and the “ACNS Standardized Critical Care EEG Terminology 2021: Reference Chart” is available at Supplemental Digital Content, http://links.lww.com/JCNP/A150. EEG LIST Supplemental figures are available as Supplemental Digital Content at http://links.lww.com/JCNP/A134. Hirsch et al. Page 2 Author Manuscript Bayview Medical Center, Baltimore, Maryland, U.S.A. ****Department of Neurology, David Geffen School of Medicine at University of California Los Angeles, Los Angeles, California, U.S.A. ††††Medisch Spectrum Twente and University of Twente, Enschede, The Netherlands ‡‡‡‡Medical Intensive Care Units and Department of Neurology, University Hospital Basel, Basel, Switzerland §§§§Department of Neurology, Harvard Medical School, and Comprehensive Epilepsy Center, Beth Israel Deaconess Medical Center, Boston, Massachusetts, U.S.A. ǁǁǁǁDepartment of Neurology, Université Libre de Bruxelles, Hôpital Erasme, Brussels, Belgium. INTRODUCTION In the early 2000s, a subcommittee of the American Clinical Neurophysiology Society (ACNS) set out to “standardize terminology of periodic and rhythmic EEG patterns in the Author Manuscript critically ill to aid in future research involving such patterns.” The initial proposed terminology was published in 2005.1 This was presented at many meetings on several continents, subjected to multiple rounds of testing of interrater reliability, underwent many revisions, and was then published as an ACNS guideline in 2013.2 Interrater agreement of the 2012 version (published in early 2013) was very good, with almost perfect agreement for seizures, main terms 1 and 2, the +S modifier, sharpness, absolute amplitude, frequency, and number of phases.3 Agreement was substantial for the +F and +R modifiers (66% and 67%) but was only moderate for triphasic morphology (58%) and fair for evolution (21%, likely at least partly because of the short EEG samples provided).3 The authors concluded that interrater agreement for most terms in the ACNS critical care EEG terminology was high and that these terms were suitable for multicenter research on the clinical significance of these critical care EEG patterns. Author Manuscript With the help of infrastructure funding from the American Epilepsy Society and administrative and website support from the ACNS, a database that incorporated the ACNS terminology was developed for clinical and research purposes, tested during routine clinical care in multiple centers,4 and made available at no cost on the ACNS website (https:// www.acns.org/research/critical-care-eeg-monitoring-research-consortium-ccemrc/ccemrc- public-database). This greatly enhanced the ability to complete multicenter investigations. After the establishment of the standardized terminology and free access to a database incorporating these terms, there have been many investigations into the clinical significance of rhythmic and periodic patterns (RPPs) in critically ill patients. Patterns such as lateralized rhythmic delta activity (LRDA) were found to be highly associated with acute seizures,5,6 equivalent to the association found with lateralized periodic discharges (LPDs) in one study. Author Manuscript 5 The association of all the main patterns in the nomenclature with seizures was defined in a multicenter cohort of almost 5,000 patients, with seizure rates highest for LPDs, intermediate for LRDA and generalized periodic discharges (GPDs), and lowest for generalized rhythmic delta activity (GRDA).6 This and other studies have shown that several of the modifiers within the nomenclature do indeed have clinically relevant meaning. For example, studies have shown that higher frequency (especially >1.5 Hz), higher prevalence, longer duration, and having a “plus” modifier are all associated with a higher chance of J Clin Neurophysiol. Author manuscript; available in PMC 2021 October 01. Hirsch et al. Page 3 acute seizures.6,7 On the other hand, whether a pattern was spontaneous or “stimulus- induced” did not seem to have a significant effect on its association with seizures.6 In other Author Manuscript investigations, the “triphasic morphology” modifier was investigated blindly with multiple expert reviewers, calling into question its relationship with metabolic encephalopathy and its lack of a relationship with seizures.8,9 For patients with refractory status epilepticus treated with anesthetic-induced coma, the presence of “highly epileptiform” bursts suggested that an attempted wean off of anesthetics at that time was much more likely to lead to seizure recurrence than if the bursts were not highly epileptiform.10 Even long-term outcome seemed to be associated with some modifiers, with a higher risk of later epilepsy found if LPDs were more prevalent, had longer duration, or had a “plus” modifier.7 CHANGES IN THE 2021 VERSION OF THE TERMINOLOGY Although the previous version of the terminology was easy to use, reliable, and valuable for Author Manuscript both research and clinical care, new terms and concepts have emerged. In this version, we incorporate recent research findings, add definitions of several new terms, and clarify a few definitions of old terms. Most of the old terms remain unchanged, but there have been some important clarifications and corrections (such as the calculation of the number of phases) and multiple additions. All changes have been summarized in Table 1. One new main term 1 was added (Unilateral Independent), and main term 2 “Lateralized” was updated to include “bilateral asynchronous” patterns. Electrographic seizures (ESz), electrographic status epilepticus (ESE), electroclinical seizures (ECSz), and electroclinical status epilepticus (ECSE) have now been defined, largely based on the “Salzburg criteria.”11,12 Brief potentially ictal rhythmic discharges (BIRDs) have been added based on recent publications13,14, and a consensus definition of the ictal-interictal continuum (IIC) has been proposed. We also added definitions of identical bursts,15 state changes, cyclic alternating Author Manuscript pattern of encephalopathy (CAPE), and extreme delta brush (EDB).16 To facilitate daily use, we are also providing the “ACNS Standardized Critical Care EEG Terminology 2021: Condensed Version” (see Supplemental Digital Content, http://links.lww.com/JCNP/A149) and the “ACNS Standardized Critical Care EEG Terminology 2021: Reference Chart” (see Supplemental Digital Content, http://links.lww.com/JCNP/A150). Finally, for educational purposes and conceptual clarity, we provided extensive schematic diagrams (Figures 1-42) of most patterns to quickly demonstrate the core features and principles. Supplemental figures include EEG examples from 30 cases and are available as Supplemental Digital Content at http://links.lww.com/JCNP/A134. METHODS Author Manuscript All the definitions are based on extensive discussions not only among the authors of this document but also among many others, both live and via email and questionnaires. There was not always complete consensus on some issues; electronic voting (with each voter blinded to the opinion of others for the first round) was used for most of these issues. We considered additional changes from previous versions or from the literature such as eliminating the 10-second cutoff for defining electrographic seizures but because no clear consensus was reached (it was close to a split decision), this was not changed. J Clin Neurophysiol. Author manuscript; available in PMC 2021 October 01. Hirsch et al. Page 4 2021 ACNS CRITICAL CARE EEG TERMINOLOGY Author Manuscript General Notes NOTE: This terminology is intended to be used at all ages, excluding neonates, although some terms may not be ideal for infants. For the neonatal version of the terminology, please see https://www.acns.org/UserFiles/file/ The_American_Clinical_Neurophysiology_Society_s.12.pdf.18 NOTE: This terminology is intended for use in the critically ill, although it can be applied in other settings as well. It is mostly compatible with the 2017 multinational revised glossary of terms most commonly used by clinical electroencephalographers.19 NOTE: Although any finding on EEG can be focal, regional, or hemispheric, such as an asymmetry or slowing, and this is a very important distinction in some circumstances such Author Manuscript as epilepsy surgery, all of these are combined within the terms “lateralized” or “asymmetric” in this nomenclature. However, additional localizing information (e.g., where the pattern is maximal and which lobes are involved) can be provided and can also be applied to several modifiers and sporadic epileptiform discharges. This additional localizing information was built into the freely available Critical Care EEG Monitoring Research Consortium (CCEMRC) database that incorporated the previous version of this nomenclature (https:// www.acns.org/research/critical-care-eeg-monitoring-research-consortium-ccemrc/ccemrc- public-database).4 A new database is being created with this 2021 nomenclature fully incorporated. NOTE: In this section and throughout the document, the term “ictal” is used to refer to an EEG pattern seen during an epileptic seizure, whether clinical or electrographic-only, as the Author Manuscript term is commonly used in EEG literature. NOTE: “Hz” is used as an abbreviation for “per second” for all types of periodic or rhythmic patterns, even when referring to noncontinuous waveforms. NOTE: All voltage measurements in this document are based on peak to trough (not peak to baseline) measurements in a standard 10–20 longitudinal bipolar recording. However, for assessing voltage symmetry, an appropriate referential recording is preferred. NOTE: The term “consistent” or “consistently” refers to >80% of instances (e.g., >80% of discharges in a periodic pattern, >80% of cycles of a rhythmic pattern, or present >80% of the record for a background pattern). Author Manuscript A. EEG BACKGROUND 1. Symmetry a. Symmetric. b. Mild asymmetry (consistent asymmetry in voltage [Fig. 1A] on an appropriate referential recording of 1 Hz frequency asymmetry [Fig. 1C]). Author Manuscript NOTE: When any of the following features (Section A2-A10) are asymmetric, they should be described separately for each hemisphere. 2. Predominant Background Frequency When Most Awake or After Stimulation a. Beta (>13 Hz) b. Alpha. c. Theta. d. Delta. NOTE: If two or three frequency bands are equally prominent, report each one. Author Manuscript 3. Posterior Dominant (“Alpha”) Rhythm (must be demonstrated to attenuate with eye opening; wait >1 second after eye closure to determine frequency to avoid “alpha squeak”) a. Present: Specify frequency to the nearest 0.5 Hz. b. Absent. c. Unclear. 4. Continuity (Fig. 2) a. Continuous Author Manuscript b. Nearly Continuous: continuous, but with occasional (1–9% of the record) periods of attenuation or suppression lasting ≥1 second. Describe typical duration of attenuation/suppression. i. Attenuation: periods of lower voltage are ≥10 μV but 50%) bursts; record maximum frequency and location if this occurs (Fig. Author Manuscript 6B). v. The presence or absence of “Identical Bursts”: Present if the first 0.5 seconds or longer of each burst (Fig. 7A) or of each stereotyped cluster of 2 or more bursts (Fig. 7B) appears visually similar in all channels in most (>90%) bursts (see Supp EEG 4, Supplemental Digital Content 1, http://links.lww.com/JCNP/A134). J Clin Neurophysiol. Author manuscript; available in PMC 2021 October 01. Hirsch et al. Page 7 e. Suppression/attenuation: entirety or near-entirety (>99%) of the record consists Author Manuscript of either suppression (all

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