Minimum standards for inpatient long-term video-EEG monitoring (LTVEM): A clinical practice guideline of the international league against epilepsy and international federation of clinical neurophysiology.
Abstract
The objective of this clinical practice guideline is to provide recommendations on the indications and minimum standards for inpatient long-term video-electroencephalographic monitoring (LTVEM). The Working Group of the International League Against Epilepsy and the International Federation of Clinical Neurophysiology develop guidelines aligned with the Epilepsy Guidelines Task Force. We reviewed published evidence using The Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) statement. We found limited high-level evidence aimed at specific aspects of diagnosis for LTVEM performed to evaluate patients with seizures and nonepileptic events (see Table S1). For classification of evidence, we used the Clinical Practice Guideline Process Manual of the American Academy of Neurology. We formulated recommendations for the indications, technical requirements, and essential practice elements of LTVEM to derive minimum standards used in the evaluation of patients with suspected epilepsy using GRADE (Grading of Recommendations, Assessment, Development, and Evaluation). Further research is needed to obtain evidence about long-term outcome effects of LTVEM and establish its clinical utility. 2021 International Federation of Clinical Neurophysiology, Inc. and International League Against Epilepsy.
1. Introduction
Long-term video-EEG monitoring (LTVEM) provides an objective means to evaluate selected people with seizures (England et al., 2012) from a cohort of more than 65 million active cases of epilepsy in the world each year (Perucca et al., 2014; Thijs et al., 2019; Feigin et al., 2019). Seizures impair normal neurological function and impart safety risk (Fisher et al., 2014), affecting people of all ages, gender, ethnic backgrounds, and cultures (Perucca et al., 2014; Feigin et al., 2019). One-third of people with epilepsy are uncontrolled by antiseizure medication (ASM) (Kwan and Brodie, 2000; Merrell et al., 2010). Practice guidelines and quality measures are available to provide national and international standards for diagnosis and treatment of patients (Nunes et al., 2012; Scottish Intercollegiate Guidelines Network, 2003; Boon et al., 2021). Because the manifestations of epilepsy are brief and intermittent, a standard 20–30 minute electroencephalogram (EEG) often fails to show epileptiform activity. Inpatient LTVEM is the reference standard to provide a definitive diagnosis when standard EEG in conjunction with a clinical approach to diagnosis and management is unrevealing (Fisher et al., 2014; Tatum et al., 2018; Rugg-Gunn et al., 2001; Deacon et al., 2003; Velis et al., 2007; Eddy and Cavanna, 2014; Shih et al., 2018; Ghougassian et al., 2004; Kumar-Pelayo et al., 2013; McBride et al., 2002; Nordli, 2006). Position papers and standards (Shih et al., 2018), services (Fitzsimons et al., 2000) and guidelines (Tatum et al., 2018; Velis et al., 2007; American Clinical Neurophysiology Society, 2008; Pressler et al., 2017; Scheffer et al., 2017; Seeck et al., 2017) exist for specific indications and certain aspects of LTVEM, though an international guideline to identify minimum performance standards is needed. In this clinical practice guideline (CPG), we address the current minimum standards for performing LTVEM as they apply to recording seizures and events for the purposes of differential diagnosis, classification, quantification, and characterization for presurgical evaluation. This adds to the International League Against Epilepsy (ILAE) and the International Federation of Clinical Neurophysiology (IFCN) guidelines on neurophysiological methods in people with epilepsy. The target audience for this CPG are clinicians and allied healthcare personnel. LTVEM is increasingly being performed in the home or ambulatory setting, although for this CPG, we refer to traditional inpatient use. Our objective is to provide evidence-based recommendations for performing inpatient LTVEM.
2. Study methods
We extracted, reviewed, and evaluated published evidence on standards in LTVEM using The Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) statement (Moher et al., 2010). For the purposes of this study, we defined LTVEM as inpatient video-EEG monitoring lasting more than 24 hours (usually days to 1–2 weeks). Data sources included PubMed and EMBASE supplemented with articles from Ovid Medline, CINAHL (Cumulative Index of Nursing and Allied Health Literature), and Cochrane databases including conference proceedings. All articles involving human subjects were included in the search, without language restrictions. The search strategy included broad search terms (‘‘epilepsy AND seizures AND video-EEG”) and synonyms (‘‘epilepsy AND Seizures AND telemetry”) pertaining to LTVEM and subtopics evaluated (i.e., ‘‘epilepsy AND standards/guidelines”). Article search took place before Oct 16, 2019 and relevant articles were supplemented thereafter, with high-level evidence identified (Fig. 1). Studies on neonates and continuous EEG monitoring during critical illness were excluded. Two independent reviewers screened titles and abstracts and full text articles were examined for eligibility.
Due to the large heterogeneity in study design and the use of different LTVEM outcomes, quantitative synthesis (meta-analysis) was not possible. Therefore, we conducted a qualitative synthesis of high-level studies (Table 1). We posed questions to address patient populations, interventions, comparators, and measured outcome (Table 2) and aimed at answering the following questions: (1) What are the indications for LTVEM that influence management? (2) What are the technical requirements for LTVEM? and (3) What are the essential practice elements for performing LTVEM?
Individual studies were rated using predefined published criteria (Tatum et al., 2018) to evaluate the evidence assessing the risk of bias given the paucity of high-level evidence. (Gronseth et al., 2011; Sterne et al., 2001). The most relevant articles were identified, rated, and linked to recommendations predicated on category I and II rated studies. Pre-existing guidelines, consensus/position statements, and task force proposals were incorporated when applicable. Studies had to specify key outcome metrics (diagnosis and management) according to the STARD (Standards for Reporting Diagnostic Accuracy Studies) criteria (Bossuyt et al., 2003; Bossuyt et al., 2015). High-level evidence was classified, rated, and subjected to a second rating. We used the Grading of Recommendations Assessment, Development and Evaluation (GRADE) system to formulate recommendations.
We developed this CPG as an evidence-based and consensusdriven document modeled after the Epilepsy Guidelines Working Group. (Sauro et al., 2015) The ILAE Commission on Diagnostic Methods and the Executive Committee of the IFCN each appointed members of the Working Group. Two face-to-face meetings were held to review objectives and progress. Where relevant highlevel evidence was absent, we used the Delphi method to obtain blind consensus when a majority agreed. (Pressler et al., 2017).
3. Indications
Epilepsy and neurology communities have produced 11 references to LTVEM in the form of guidelines and position papers, although comprehensive assessment of practices outside individual topics involved in LTVEM is limited in adults and children. (Velis et al., 2007; Shih et al., 2018; American Clinical Neurophysiology Society, 2008; Seeck et al., 2017; Kobulashvili et al., 2016).
3.1. Differential diagnosis
LTVEM is most used for differential diagnosis of epileptic and non-epileptic attacks, with compelling evidence from 143 LTVEM papers (no category I, 6 category II) for clinical usefulness to distinguish between them. (Ghougassian et al., 2004; Baheti et al., 2011; Alving and Beniczky, 2009; Yogarajah et al., 2009; Alsaadi et al., 2004; Je˛drzegczak et al., 1999) One category II study involved 22 epileptologists performing a blinded review of a sample of video and EEG extracted from LTVEM. Classifying events as epileptic, nonepileptic psychogenic, and nonepileptic physiologic categories demonstrated good inter-rater reliability for epilepsy, but only moderate reliability for psychogenic nonepileptic attacks (PNEA), and only fair inter-rater reliability for physiologic nonepileptic events. (Benbadis et al., 2009; Benbadis et al., 2001) Overall, most evaluable studies involved adult patients. Some studies support a misdiagnosis rate of epilepsy in 20–30% of patients admitted for LTVEM (Alving and Beniczky, 2009; Alsaadi et al., 2004) whereas others note a wider prevalence between 5% and 50%. (McGonigal et al., 2004; Hubsch et al., 2011) Misinterpretation of an interictal EEG reporting epileptiform activity was one reason for misdiagnosis prior to LTVEM. (McGonigal et al., 2004; Hubsch et al., 2011; Benbadis and Tatum, 2003; Benbadis, 2007; Krauss et al., 2005; Benbadis and Lin, 2008) A meta-analysis of 135 LTVEM studies found 60% of referrals were for diagnostic reasons. (Sauro et al., 2016) Most epilepsy mimics demonstrate generalized motor activity (Asadi-Pooya et al., 2016), and to correctly interpret them based on clinical grounds alone is challenging. (Chadwick and Smith, 2002) In an evaluation of 181 consecutive patient LTVEM records, useful information was obtained in 72% and the clinical diagnostic question answered in 67%. (Binnie et al., 1981) In older adults (mean age 51 years), LTVEM was most useful in 93.5% of 31 patients with pure PNEA. (Baheti et al., 2011) Standards for diagnosis of PNEA including use of LTVEM have been developed by an international consensus group of clinician-researchers. (LaFrance et al., 2013) A diagnostic LTVEM outcome study in 230 people resulted in a change in diagnosis in 133 (58%) and refinement of a diagnosis in 29 (13%) to provide overall diagnostic value in 71% of patients and was particularly useful to differentiate frontal lobe seizures from generalized seizures and non-epileptic attacks. (Yogarajah et al., 2009) Similarly, another diagnostic LTVEM outcome study found 58% of 131 patients had their diagnosis altered by LTVEM, with the greatest change being an increase from 7 to 31% of patients with nonepileptic attacks. (Ghougassian et al., 2004) Following LTVEM the diagnosis was reversed in 29 (24%) out of 121 patients and 4 diagnoses changed from nonepileptic to epileptic seizures. (Alsaadi et al., 2004) Overall, patients with pure PNEA are more common than those with a dual diagnosis (Je˛drzegczak et al., 1999; Raymond et al., 1999) and those with physiological non-epileptic events identified by LTVEM. (McBride et al., 2002) In one category II controlled study of 1083 patients diagnosed with epilepsy, 85 (7.8%) were clinically diagnosed with PNEA, 48 were believed to manifest only PNEA, and 37 patients were suspected of both PNEA and epileptic seizures. (Je˛drzegczak et al., 1999) When LTVEM was subsequently performed, 55 of 70 (79%) cases had PNEA only and only 9 of 230 (3.9%) with PNEA also had epileptic seizures, demonstrating the pitfalls for dual diagnoses based on clinical grounds alone. One retrospective study in 49 patients with PNEA identified 18.2% with pseudo-status compared with 5.2% of 154 patients with epileptic status epilepticus. (Dworetzky et al., 2006).
In a systematic review of diagnostic procedures, 33 papers comprising a range of procedures including seizure induction, Minnesota Multiphasic Personality Inventory, prolactin levels, single photon emission computed tomography (SPECT), and clinical metrics (i.e., pre-ictal pseudosleep, ictal, and post-ictal characteristics) found no procedure attained reliability equivalent to video-EEG monitoring (VEM), (Cuthill and Espie, 2005) with none of the tests investigated demonstrating both high sensitivity and high specificity. In one pediatric retrospective diagnostic accuracy study (category IV), chart review found superior sensitivity of 54% and comparable specificity of 88% with LTVEM compared to standard EEG even in the absence ictal recording. (Knox et al., 2018).
In a group of 221 patients undergoing LTVEM, sessions were significantly shorter in the diagnostic group (mean: 2.4 days) than in a group admitted for presurgical evaluation (3.5 days). (Alsaadi et al., 2004). With respect to management following LTVEM, one study of 148 consecutive patients over approximately 3 years noted a significant reduction in ASM usage in people with epilepsy and PNEA. (Baheti et al., 2011). When PNEA are misdiagnosed as epilepsy, potential adverse consequences of unnecessary ASM and invasive procedures may be averted by LTVEM (Arain et al., 2011).
The highest-level studies in this area included 6 level II studies which are downgraded due to unexplainable inconsistencies between these studies but upgraded due to the magnitude of effects. The overall confidence in evidence for these studies is therefore moderate for LTVEM to provide differential diagnostic utility in differentiating epileptic from non-epileptic events.
Recommendation: LTVEM monitoring should be used to differentiate between epileptic and non-epileptic events, in patients where the diagnosis is in question (strong recommendation).
3.2. Classification
Classification of seizures and epilepsy syndromes is essential for appropriate selection of ASM. (Benbadis and Tatum, 2003; Penry et al., 1975; Engel, 2006) LTVEM studies reporting seizure and epilepsy classification are category III and IV for specific purposes of classifying some patients with epilepsy. A minority will remain unclassified despite LTVEM until more information becomes available. One retrospective diagnostic study of 230 patients changed diagnosis in 133 patients, and in this group of patients LTVEM proved useful in differentiating focal from generalized epilepsy in 47 of 133 (35%) (Yogarajah et al., 2009) in compliance with the International Classification of Epileptic Seizures that divides seizure types into focal, generalized, and unknown (Berg et al., 2010). LTVEM provides a definitive diagnosis and supports a continuum of disease (Tatum et al., 2018; Engel, 2006; Commission on Classification and Terminology of the International League Against Epilepsy, 1989; Holmes et al., 2004; Koutroumanidis et al., 2008) by identifying a spectrum of clinical seizure types and neurophysiologic patterns on EEG. (Deacon et al., 2003; McBride et al., 2002; Scheffer et al., 2017; Berg et al., 2010; Friedman and Hirsch, 2009; Louis and Cascino, 2016) A prospective study of inpatient LTVEM (minimum 3 hours) clarified the epilepsy syndrome in 93% of 143 epilepsy patients (7% remained unclassified) with one-third eligible for epilepsy surgery. (Chemmanam et al., 2009).
Alternative classification systems based purely on semiology have been proposed. (Lüders et al., 1998) A prospective comparison (category II) between ILAE and semiological seizure classification systems in 78 consecutive patients found seizure classification changed significantly between pre- and post-LTVEM, using ILAE more than semiological classification. (Benbadis et al., 2001). Another adult semiology study (category IV) of 90 patients found some seizure types (e.g., myoclonic and hypermotor seizures) had excellent consistency between historical description and an LTVEM confirmed diagnosis, although focal seizures were less reliable (Hirfanoglu et al., 2007). In a large study (category IV) of 323 children (mean age of 7 years) with episodes of staring, myoclonic jerking, and abnormal eye movements and posturing, 53% of epileptic patients were correctly classified for seizure type or epilepsy syndrome by new information derived from LTVEM.
(Bennett-Back et al., 2016). Other retrospective (category IV) studies involving patients with juvenile myoclonic epilepsy reported focal clinical and EEG features in about one-half of patients, complicating clinical diagnosis. (Usui et al., 2005; Aliberti et al., 1994).
A large retrospective LTVEM-based surgical series classified patients by EEG, with a focal EEG found in two-thirds, generalized abnormalities in 22%, lateralized features in 4%, and 6% that were mislocalized or mislateralized. (Foldvary et al., 2001). Sleep-related events can be diagnosed and correctly classified (focal vs generalized) with overnight LTVEM. (Derry et al., 2009; Sadleir et al., 2009). Despite a small number of patients, one retrospective (category IV) study found the percentage of patients with a diagnosis of generalized epilepsy more than doubled after LTVEM (Ghougassian et al., 2004). In genetic generalized epilepsies (GGE), gene defects do not lend themselves to reliable classification. (Mullen et al., 2013). EEGs with interictal epileptiform discharges (IEDs) noted during LTVEM are not specific for seizure type(s) or for epilepsy syndromes (Seneviratne et al., 2012; Foong and Seneviratne, 2016). However, LTVEM may classify and subclassify GGE (Oehl et al., 2010), and reclassify seizures to guide ASM selection (Benbadis and Tatum, 2003).
The practical usefulness of LTVEM for classifying epilepsy is axiomatic, as ILAE classification is based on data extracted from LTVEM to serve as the standard, with a consistent effect across subjects. Therefore, the group issues a strong recommendation despite the presence of weak evidence.
Recommendation: LTVEM helps classify patients with epilepsy in whom the seizure type or epilepsy syndrome is undetermined (strong recommendation).
3.3. Seizure quantification
Thirty articles (categories III and IV) addressed seizure quantification and LTVEM. On average, fewer than 50% of seizures (47– 63%) are correctly documented by patients prior to diagnosis established by LTVEM with reporting accuracy that varies over time (Elger and Hoppe, 2018). One (category IV) questionnaire study that focused on patient awareness noted 44.2% of LTVEMproven seizures went unnoticed (Kerling et al., 2006). Selfreporting seizures is essential for appropriate management (US FDA, 2019). Ambulatory EEG and LTVEM studies reveal 20–25% of patients are always unaware of seizures (Blum et al., 1996; Langston and Tatum, 2015; Tatum et al., 2001; Heo et al., 2006; DuBois et al., 2010). Patients with temporal lobe epilepsy (TLE) (Kerling et al., 2006; Langston and Tatum, 2015; Heo et al., 2006), cognitive decline (Helmstaedter et al., 2003; Jokeit and Ebner, 1999; Oyegbile et al., 2004; Semah et al., 1998) and transient epileptic amnesia are at risk for under-reporting seizures that may be clarified during LTVEM (Zeman and Butler, 2010; Butler et al., 2007). In a (category III) LTVEM study evaluating 327 consecutive TLE patients, subclinical seizures were detected in 8.3%, and 1% had only subclinical seizures recorded (all of which were detected within first 24 hours) (Wang et al., 2017). One LTVEM study used post-ictal surveys and found awareness present in patients with convulsions associated with GGE, but those with focal to bilateral tonic-clonic seizures had incomplete awareness (Blum et al., 1996).
Patients with generalized epilepsies, severe epilepsies, and those with frequent seizures are candidates for seizure quantification by LTVEM, and more pediatric studies are represented in this section. Convulsions are readily identifiable (Aghaei-Lasboo and Fisher, 2016), however, subtle nonconvulsive seizures and frequent IEDs (i.e., electrical status epilepticus in sleep), subclinical seizures, and nocturnal seizures may evade clinical detection. Failure to recognize nocturnal seizures may occur in up to 86% of patients (Hoppe et al., 2007). Irrespective of semiology, LTVEM can quantify seizure burden and identify clinical phenomenology to yield more favorable response to treatment (Stefan et al., 2011) and improved patient outcome (Heo et al., 2006).
Most available literature consists of lower-class studies that were inconsistent, and the overall confidence in evidence for utility of LTVEM to quantify seizures is low, depending upon duration.
Recommendation: The usefulness of LTVEM to quantify seizures in patients with epilepsy is unknown (confidence in effect estimates is so low that a recommendation would be speculative).
3.4. Seizure characterization for surgical management
Three prospective longitudinal cohort studies evaluating patients with epilepsy managed with ASMs over 30 years failed to show a meaningful decline in the number of people with drug-resistant epilepsy (Chen et al., 2018), and despite new advances (Moshé et al., 2015), risks exist for patients when seizures are uncontrolled (Wiebe et al., 2001; Engel et al., 2012; Dwivedi et al., 2017; Engel et al., 2003). Three category 1 randomized controlled clinical trials including one in children, and multiple category III and IV studies support the effectiveness of epilepsy surgery compared with best medical practice following LTVEM (Wiebe et al., 2001; Engel et al., 2012; Dwivedi et al., 2017). Adult studies focus on TLE (Wiebe et al., 2001; Engel et al., 2012; Dwivedi et al., 2017) whereas proportionally more extratemporal resections have been performed in children reflecting site and pathology specificity (Wiebe et al., 2001; Engel et al., 2012; Dwivedi et al., 2017). Position statements recommend a presurgical evaluation be considered incorporating LTVEM when patients are resistant to ASMs to confirm an epilepsy diagnosis and seek concordance with other evaluations (i.e., history, magnetic resonance imaging, positron emission tomography) (Engel et al., 2003). Surgery remains greatly under-utilized (Asadi-Pooya et al., 2017; Tian et al., 2018; Fisher et al., 2017; Vaughan et al., 2018), with multiple reports of efficacy (Sauro et al., 2016; Tanaka et al., 2018).
Scalp-based VEM and invasive EEG (iEEG) during LTVEM are standard neurophysiological techniques to characterize the seizure onset zone for surgery (Tatum et al., 2018; Sauro et al., 2016). Modern high-resolution video is an essential adjunct to EEG during LTVEM to corroborate semiology and localization of the seizureonset zone (see Section 5.2). Few studies characterize seizureonset patterns denoted by EEG relative to outcome and whereas some patterns are localizing, others are not (Yun et al., 2006; Wetjen et al., 2009; Worrell et al., 2002). In a retrospective category III study involving 3057 seizures in 75 consecutive patients with drug resistant focal epilepsies, individualized scalp and iEEG LTVEM sessions were compared following successful epilepsy surgery (Tanaka et al., 2018). A localized scalp EEG during LTVEM at seizure onset (independent of location) predicted a favorable outcome after surgery, whereas multi-lobar and widespread seizure onset predicted unfavorable surgical outcomes (Tanaka et al., 2018; Tanaka et al., 2019). Other retrospective category III studies involving combined scalp and iEEG during LTVEM demonstrate moderate to favorable sensitivity and specificity for scalp ictal EEG patterns predicting localization in patients with TLE (Ebersole and Pacia, 1996; Risinger et al., 1989). In a prior report, analyzing 61 patients with lesional drug-resistant focal epilepsies, 71 paired seizure-onset patterns matched between scalp EEG and iEEG found some scalp seizure-onset patterns were highly associated with a specific intracerebral pattern, specific pathologies, and depth localized seizure-onset (Vaughan et al., 2018). Singlecenter retrospective (category IV) studies demonstrate focal temporal (Goldenholz et al., 2016) and extratemporal scalp patterns predicted a seizure-free outcome (Worrell et al., 2002). Other reports, in contrast, note that dissimilar cerebral generators may produce similar ictal patterns on scalp recording (Ebersole, 1999; Tao et al., 2007), and that presurgical tools including LTVEM did not provide unambiguous long-term outcome predictions for TLE surgery (Goldenholz et al., 2016). A consortium funded by the European Union performed a systematic review and metaanalysis and found LTVEM had substantial heterogeneity across studies associated with moderate sensitivity and low specificity for identification of the epileptogenic zone, with higher sensitivity in lesional TLE compared to lesional extratemporal lobe epilepsy (ETLE) (Kobulashvili et al., 2018). As a result, LTVEM guidelines were implemented across Europe based upon the diagnostic accuracy of LTVEM in identifying the epileptogenic zone in epilepsy surgery candidates (Kobulashvili et al., 2018). Due to lack of evidence for the utility of LTVEM in children, a modified Delphi process was used among pediatric epilepsy experts to develop consensus-based guidelines for LTVEM in the pre-surgical evaluation of children with epilepsy in the United Kingdom (UK) (Pressler et al., 2017).
There is high confidence in evidence that LTVEM should be used as part of the presurgical evaluation for TLE patients. For ETLE there is heterogeneity and low confidence in evidence for or against LTVEM for seizure characterization in the presurgical evaluation. The evidence basis for LTVEM monitoring and ETLE is weak due to smaller number of cases (vs TLE), heterogeneous semiology, and poorly localized scalp ictal EEG. Unfortunately, there is not a better way to evaluate patients, and therefore the group issues a strong recommendation for ETLE too.
Recommendation: LTVEM must be used in the presurgical evaluation in of patients with drug resistant epilepsies (strong recommendation).
4. Yield of inpatient LTVEM
The overall diagnostic yield of LTVEM from category III and IV studies varies widely (19% to 75%) due to differences in endpoints, definitions, methodology, and patient cohort evaluated (Tatum et al., 2018; Deacon et al., 2003; Ghougassian et al., 2004; Alving and Beniczky, 2009; Alsaadi et al., 2004; Binnie et al., 1981) independent of the hospital course (Spritzer et al., 2014). A systematic review found most of the literature on LTVEM focused on noninvasive and invasive pre-surgical evaluation prior to epilepsy surgery (Sauro et al., 2016). A large, prospective study demonstrated LTVEM was useful to clarify the clinical diagnosis in 56.3% of patients (Sauro et al., 2014), and meta-analysis found the preadmission diagnosis changed in 35.6% of patients following LTVEM, implicating change in management (Sauro et al., 2016). Successful LTVEM sessions are significantly longer in a presurgical group of patients than in a diagnostic group (Alving and Beniczky, 2009). No difference in diagnostic yield has been identified with respect to age (McBride et al., 2002; Alix et al., 2014; Kipervasser and Neufeld, 2007; Uldall et al., 2006), patients with neurological impairment (Keränen et al., 2002), or reason LTVEM was performed (Alving and Beniczky, 2009). One retrospective study did not find a correlation between the preadmission frequency of seizures and the yield for recording events during LTVEM (Al Kasab et al., 2016). Despite undergoing thorough evaluation including repeat EEGs obtaining sleep recording and short-term video EEG in patients with daily spells, and in other patients evaluated with ambulatory EEG, (Alix et al., 2014) LTVEM was found to be useful in nearly one-half of cases (Alving and Beniczky, 2009). In a prospective comparative study (category II) of 129 patients with 10 month follow-up, after LTVEM, the diagnostic categories were changed from pre-admission in 41.1% of the patients, and 40.3% had revisions in management (Lee et al., 2009).
Pitfalls in diagnosis without LTVEM compromise yield if semiology alone is used and result in misdiagnosis as PNEA (Tatum et al., 2018; Kanner et al., 1996; Tatum et al., 2020). There is a small risk that provocation by suggestion may lead to false positive results in patients with PNEA (Smith, 2005). Results from category IV LTVEM studies and expert opinion support that over-interpretation of EEG may be a reason for epilepsy misdiagnosis in patients with PNEA (Benbadis and Tatum, 2003; Fowle and Binnie, 2000). During LTVEM, approximately 20– 30% of patients never have a seizure or event (McGonigal et al., 2004; Hall-Patch et al., 2010; Benbadis et al., 2004). In patients with epilepsy, LTVEM may not reveal IEDs in EEG or be devoid of a detectable scalp ictal rhythm during some focal seizures (Bautista et al., 1998; Noe et al., 2013) falsely leading to a nonepileptic diagnosis (Caplan et al., 2011). Furthermore, patients with PNEA can generate rhythmic movement artifacts that falsely mimic an electrographic seizure (Benbadis, 2006) or obscure the ictal EEG during hyperkinetic epileptic seizures to limit identification of the seizure onset zone (Tatum et al., 2011). Scalp ictal EEG may falsely localize and lateralize focal seizures (Catarino et al., 2012), especially those arising from mesial and posterior quadrant neocortices (Smith, 2005; Sammaritano et al., 1987) but may be potentially localized when iEEG is recorded (Antony et al., 2019; Ramantani et al., 2014).
Overall, one class II study provides low confidence in evidence that more than one-third of patients will experience a change in management after undergoing VEM.
Recommendation: LTVEM may result in a change in management in some patients (weak recommendation).
5. Technical standards
Minimal technical standards are required to ensure highquality recording, adequate storage, optimal review, and webbased remote exchange of information (Tatum et al., 2020; Sinha et al., 2016). With the advent of digital technology and increasing computer sophistication, instrumentation has transformed the practice of LTVEM (Burgess, 2001; Acharya et al., 2016). Signal processing, adjunctive software and analytics, high-speed electronic transfer, and larger storage capacity facilitate widespread use (Velis et al., 2007; Nuwer et al., 1998; Flink et al., 2002). Highlevel evidence-based standards evaluating equipment and instrumentation are lacking, with heterogeneity for clinical practices in epilepsy monitoring units (EMUs) (Rubboli et al., 2015). We assessed technical parameters for LTVEM using the modified Delphi method (Linstone and Turoff, 1975) to supplement prior published information (Tatum et al., 2018; Sinha et al., 2016; Burgess, 2001; Acharya et al., 2016; Nuwer et al., 1998; Flink et al., 2002).
5.1. Electrode array and EEG recording
LTVEM allows acquisition and analysis of signals from the brain that can be configured based on clinical need. Standard configurations apply the 10–20 system in common bipolar and referential montages for clinical EEG (Bragin et al., 2002) but in some cases, alternative arrays such as high density EEG may be used to improve detection (Pillai and Sperling, 2006; Tao et al., 2005). A minimum of 16 channels for diagnostic LTVEM, and 32 for presurgical evaluation is recommended by the American Clinical Neurophysiology Society (ACNS) (Velis et al., 2007; American Clinical Neurophysiology Society, 2008). Majority consensus was achieved for technical features and personnel-based issues (Tables 3A-B). Consensus was reached to endorse using more than the 21 electrodes of the International 10–20 system of electrode placement (Table 3A). Specifically, our results support IFCN recommendations to use 25 electrodes in children and adults during scalp based LTVEM (Seeck et al., 2017). Dense EEG arrays during LTVEM and higher sampling rates can improve electrical source localization (Seeck et al., 2017; Oostenveld and Praamstra, 2001; Michel et al., 2004; Gavaret et al., 2015). Routine use of basal temporal electrodes (but not sphenoidal, nasopharyngeal, or nasoethmoidal electrodes) is recommended. No consensus was reached regarding use of diagnostic electrode caps. Nor was consensus reached to recommend maximal allowable scalp electrode impedance, although values less than 5 kX have previously been recommended for standard EEG (Seeck et al., 2017; Sinha et al., 2016). Consensus was reached for EMUs performing LTVEM to have the optional technical capability of using invasive electrodes. Polygraphy incorporating eye and limb movement, oximetry, autonomic metrics, and direct current channels usage is an acceptable option during LTVEM and tailored to the specific condition being investigated (Rubboli et al., 2008; Shibasaki and Hallett, 2005; Bubrick et al., 2014; Itoh et al., 2015). All raters agreed that ECG recording was necessary during LTVEM.
LTVEM storage servers require hard drive memory capability to acquire at least 200 GB of data per week per LTVEM recording unit in clinical operation (Scherg et al., 2012). Solid-state multichannel amplifiers need to include an isolation amplifier stage and follow the technical criteria established for minimum standards of recording clinical EEG (Tatum et al., 2018; Sinha et al., 2016). Consensus was reached for analogue to digital converters to use 12-bits or more and sample rates of 256 samples/second or higher. Many commercial systems use at least 16-bit resolution and sample at 512 Hz to minimize aliasing and optimize signal resolution to improve localization. High pass (low frequency) filter settings of 0.5 Hz or less and low pass (high frequency) filter settings of 70 Hz or greater should initially be applied during LTVEM EEG review. Following acquisition, EEG signals should be stored in a central server with long-term archiving performed by a technolo-gist or physician. Consensus supported maintaining all video and EEG files until LTVEM reporting was finalized. A recent retrospective 15-year study (category III) involving 1025 cases showed a trend to normal VEM patient results minimizing the need for detailed archiving (Cho et al., 2019) with polygraphic recordings supplementing EEG in select cases when informative (Barrett, 1992; Oguni et al., 1994; Brown et al., 1999). Despite the similar localizing ability of noninvasive dense EEG arrays to iEEG in patients with focal seizures (Lantz et al., 2003; Holmes et al., 2010), only low level evidence and expert consensus exists to support the use of iEEG in complex patients during presurgical evaluation (Brna et al., 2015; Jayakar et al., 2014).
5.2. Video
Video recording is routine during LTVEM (Lesser, 1996; Cascino, 2002; Chowdhury et al., 2008) in concert with EEG in expanding numbers of EMUs (Sauro et al., 2014; Hamandi et al., 2017; Brunnhuber et al., 2014). One camera is standard for LTVEM, however some centers use two to provide different viewpoints. Prospective multi-rater studies (categories II and III) have shown that compared with LTVEM, video alone may be useful when evaluating the clinical description of patients with observed seizures (Tatum et al., 2020; Beniczky et al., 2012), with similar sensitivity (category III) compared with EEG (Chen et al., 2008) in various patient populations (Watemberg et al., 2005). Implementing video recording added to EEG increases the diagnostic yield over EEG alone (Serles et al., 2000; Bidwell et al., 2015) and details seizure semiology (Lüders et al., 1998). However, no uniform nomenclature and consistent classification system differentiates patients with PNEA from epilepsy by video alone (Blume et al., 2001), although semiologies (Hubsch et al., 2011) allow hierarchical clustering (Gröppel et al., 2000; Seneviratne et al., 2010; Fayerstein et al., 2020). Based on video data alone, a prospective LTVEM study involving 5 epilepsy experts found 7 of 23 (30%) cases by all raters correctly classified epileptic seizures and PNEA (Erba et al., 2016). A prospective study analyzing 120 seizures from 35 consecutive subjects found of 45 signs demonstrated on video, only 3 for epileptic seizures and 3 for PNEA were useful in categorizing seizures, and no single clinical feature was sensitive and specific for either event (Syed et al., 2011). The sequence of seizure phenomenology recorded on video during LTVEM identifies patterns that localize and lateralize signs (Wadwekar et al., 2014). When scalp ictal EEG onset follows clinical onset, a deep or distant generator, often extratemporal in origin, is suggested (Tanaka et al., 2018; Ebersole and Pacia, 1996).
Standard digital audio–video data is acquired provided by standard industry codecs. Precise specification for timesynchronization between video and EEG has been standardized in the DICOM format and MED format, although they are not in broad clinical use (Halford et al., 2021). Split screen synchronized video and dual screen review may be useful to evaluate paroxysmal neurological events (Tinuper et al., 2004). Digital video (and audio) are typically encoded into MPEG, MPEG2, or MPEG4 formats differing in the degree of resolution and compression algorithms used and synchronized with EEG by use of a time marker, but other audio–video formats can be used successfully. 24-hour LTVEM requires up to 30 GB of memory and varies depending upon video resolution, degree of coloration, number of frames/second, and machine data compression algorithm employed. For archiving, relevant LTVEM clips involving events of interest are selected to minimize long-term data storage requirements.
There were 4 class II studies (2 without EEG and 2 with EEG) that consistently showed benefit with the use of video. Confidence in the evidence of using video with EEG monitoring is moderate.
Recommendation: Video should be combined with EEG during LTVEM (strong recommendation).
5.3. Safety
The potential for dangerous consequences exist during LTVEM because patients’ seizures are induced (Nunes et al., 2004). Convulsions and seizure emergencies, falls, injury, and postictal psychosis, among others, are possible safety risks (Kobulashvili et al., 2016; Hamandi et al., 2017). Standardized protocols are recommended for use to ensure basic patient safety (Rubboli et al., 2015; Shafer et al., 2012). Safety and quality data from a meta-analysis of 181,823 patients reporting on 34 different safety variables demonstrate a great deal of variation in reporting safety and quality measures in EMUs (Sauro et al., 2016). No validated protocols are universally available and utilized, and substantial variation in practice for essential aspects of LTVEM exist for performing optimal patient observation, tapering ASMs, and ASM rescue protocols (Atkinson et al., 2012; Buelow et al., 2009; Caplin et al., 2006). Therefore, variation in quality and safety measures may exist during LTVEM, with a pooled proportion of adverse events in 5–9% present in a meta-analysis (Sauro et al., 2016). In addition, practice variability performing LTVEM was found among 32 epilepsy centers in the UK likely reflecting variations in usage for different patient populations (Hamandi et al., 2017).
5.3.1. Clinical safety
Overall, LTVEM is an acceptably safe procedure with appropriate precautions in adults and children (Seeck et al., 2017; Atkinson et al., 2012; Noe and Drazkowski, 2009; Spanaki et al., 2012). Safety issues are more frequently encountered during LTVEM in patients with focal epilepsy undergoing pre-surgical evaluation than for those with GGE undergoing diagnostic evaluations. (De Marchi et al., 2017) Seizure provocation poses potential safety risks to patients represented by category III and IV studies (Atkinson et al., 2012; Espinosa et al., 2009; Shafer et al., 2011). For children, and patients with intellectual, cognitive and behavioral challenges, patient companions during the night are recommended both for safety and for documenting events, assessing awareness, ensuring video integrity, and alerting staff at seizure onset. Immediate family members are more helpful than nonfamily members and always necessary for children less than 5 years of age (Seeck et al., 2017). Even patients with PNEA are prone to adverse events, usually falls, at a significant rate (Atkinson et al., 2012) often while in the bathroom (Spritzer et al., 2015). A large category III study of 976 patients found only 1.9% of patients fell (without injury) despite being freely mobile, a similar finding reported in other centers practicing restricted mobility (Craciun et al., 2017). One comparative study (category III) found alert patients fell in the bathroom within the first 3 days of LTVEM compared to patients hospitalized for mental status changes where falls occurred after 3 days in their rooms (Pati et al., 2013). Novel lift systems, patient education, frequent nursing rounds, use of bed alarms, and assistance when out of bed may limit fall risk. (Spritzer et al., 2015). A category IV study reviewing records from an Epilepsy Foundation database identified 2 of 733 patients with aspiration following a generalized tonic-clonic seizure, and shoulder dislocation in 8 of 806 during seizures, for an overall risk < 1% (DeToledo and Lowe, 2001). Rarely, serious medical consequences associated with seizures may occur such as malignant cardiac arrhythmias, bony fractures, and pneumonia (Noe and
Drazkowski, 2009; Shafer et al., 2011). Prospective comparative studies (category III) show patients with PNEA have increases in heart rate and systolic blood pressure during the ictal phase, potentially predisposing to complications when attacks are prolonged (Tatum et al., 2016). Ictal asystole has been reported in 0.22–0.4% of patients undergoing LTVEM, and a systematic review of 157 cases found females with preexisting heart conditions and males with autonomic dysregulation were predisposed (Tényi et al., 2017). Sudden unexpected death in epilepsy during LTVEM has been noted in retrospective series (category IV) from 160 EMUs throughout the world (Ficker et al., 1998; Ryvlin et al., 2013).
Current practice recommendations reached consensus that informed consent should be obtained before VEM with continuous observation of patients by nursing and professional staff over the monitoring duration as a minimum standard, supplemented with alarm systems and video monitors (Hamandi et al., 2017). A multicenter category II survey study of epilepsy centers in the UK involving 198 adults and 78 children recommended the optimal nurse-to-patient ratio in an EMU should not exceed a ratio of 4:1 to ensure patient safety (Hamandi et al., 2017; Kandler et al., 2013). In a UK pediatric consensus statement, a ratio of 2:1 for scalp EEG was recommended and 1:1 during iEEG (Seeck et al., 2017). Complications involving iEEG electrodes in a prospective population-based observational category II study associated intracranial hemorrhage in a significant minority of epilepsy patients during LTVEM (Hedegärd et al., 2014).
Safety studies involving nurse-to-patient ratio during LTVEM and risk of intracranial hemorrhage with invasive EEG electrodes provide low confidence in the evidence.
Recommendation: The safe, maximal nurse-to-patient ratio to provide constant supervision of patients during LTVEM may be 4:1 (weak recommendation).
5.3.2. Electrical safety
Category IV clinical reports reflect essential safety features during LTVEM (Table 4) (Bettini et al., 2014; Villanueva et al., 2011; Seneviratne et al., 2012; Lazarus et al., 2003; Zanzmera et al., 2019). Electrical safety rules and governance are unique to individual countries and established by the International Electrotechnical Commission. Electrical injury is possible when current passes through a patient from an electrical source or electrode contacts (Starmer et al., 1971; Leitgeb and Schröttner, 2002). Any mainspowered electrical device may ‘‘leak” current and enter the patient through direct contact of a nearby metal object or indirectly by capacitive coupling inside an electrical device from nearby wiring conducted from the transformer to the case. Electrical shocks usually result from chassis leakage current from LTVEM equipment powered by 120 volts, 60 Hz AC current in the United States and 230 volts, 50 Hz AC current in Europe. Safe current limits are set for both normal conditions and for single fault conditions (i.e., a disconnected earth ground). LTVEM safety guidelines exist for individual components of equipment. Biomedical engineering services should check equipment for safe use according to safety standards (Burgess, 2019).
Microshock is of greatest concern to patients undergoing LTVEM with scalp electrodes, created by a low-resistance pathway to the body (Burgess, 2019). Susceptibility is maximal when electrical frequency reaches 60 Hz and is especially concerning when patients have an intravenous (IV) cannula, because it provides a very low-resistance pathway to the heart (Burgess, 2019). Currents of 5-10A can induce ventricular fibrillation (Starmer et al., 1971) as a function of body habitus, current intensity, duration, and pathway (Leitgeb and Schröttner, 2002; Cooper, 1995; Geddes and Roeder, 2004). Similarly, when patients undergo LTVEM and have cardiac pacemakers, the leads create a potential for electrically induced arrhythmia. Ground loops are critical to avoid during LTVEM. Current flowing from one ground to another on separate parts of a patient’s body produce magnetic fields through inductive coupling of nearby powerline wiring and may pose potential electrical safety risk to patients.
There is no evidence for or against methods to ensure electrical safety in patients undergoing LTVEM. Ethical constraints prevent studies of this nature from being performed.
5.4. Practice and personnel
Despite the use of LTVEM as a gold standard for seizure diagnoses, limited appreciation of this technique is held by some general neurologists, psychiatrists, hospital administrators, and insurance carriers managing people with paroxysmal neurological disorders (Table 5) (Shih et al., 2018). The current practice of LTVEM has been outlined in a European multi-center web-based survey study (Kobulashvili et al., 2016).
5.4.1. Seizure monitoring
Considerable variation in the practice and organization of EMUs was found in a web-based survey study involving 25 centers across 22 European countries, and authors subsequently recommended development and implementation of evidence-based LTVEM practices (Kobulashvili et al., 2016). Delayed response to seizure alarms may occur due to high false-positive rates of detection (Shin et al., 2012). A retrospective multicenter study found the average response time from caregivers was twice as fast as the response by EMU-based personnel. In addition, staff uncovering patients during seizures to evaluate semiology found 40% of patients were fully or partially obscured for more than 30 seconds during the event, compromising visualization (Malloy et al., 2018). Hence, presence of a parent or caregiver is encouraged, especially at night, while monitoring young children, and patients with intellectual and developmental disabilities. Encouraging observers to report and describe seizures in a log is useful. Implementing standardized protocol for testing patients during seizures can potentially improve the quality of the data recorded during LTVEM. A task force appointed by the ILAE Commission on European Affairs and the European Epilepsy Monitoring Unit Association prospectively studied (category II) testing paradigms during seizures in 152 consecutive patients (250 seizures) at 10 epilepsy centers; interictal, ictal, and post-ictal testing adaptive paradigms during seizures were successfully implemented in 93% of patients, limited only by seizures of short duration (Beniczky et al., 2016). A European survey showed 91% of EMUs performed ictal or postictal testing, however, there was no standardization of the procedure, and many EMUs lacked institutional guidelines for testing patients during seizure monitoring (Rubboli et al., 2015). Retrospective comparative assessment of seizures in 33 adult or pediatric patients captured during VEM found behavioral testing during seizures could be performed in only 50% of patients, whereas automated videorecorded behavioral tasks activated by computer-based seizure detection provided reliable behavioral assessment (Touloumes et al., 2016). Overall, the one category II study was unable to demonstrate superiority of a particular testing paradigm during LTVEM. Confidence in evidence is therefore low. Testing during seizures in patients with cognitive and behavioral disorders is highly variable and individualized.
Recommendation: A written, standardized protocol may be used in each LTVEM unit for managing and testing patients during seizures (weak recommendation).
5.4.2. Services
Guidelines for facilities, personnel and essential LTVEM services are established by experts in referral hospitals to comply with national and international standards (Gumnit and Walczak, 2001). Partnerships between epilepsy specialists in full-service epilepsy centers performing LTVEM and referring clinicians should exist to form care networks ensuring continued best practices and follow-up patient management (Shih et al., 2018; Labiner et al., 2010).
5.4.3. LTVEM personnel
Patients undergoing LTVEM are subject to various personnel and staffing models (Spritzer et al., 2014; Labiner et al., 2010; Bingham and Patterson, 2002). Available standards applied to personnel and their role caring for a variety of complex patients during LTVEM are resource dependent, with significant variability throughout the world. We obtained consensus for some aspects of personnel working in LTVEM units (Table 3B). Staffing models for a LTVEM laboratory (American Clinical Neurophysiology Society, 2008) and American standards for individual qualifications and responsibilities for personnel performing neurodiagnostic procedures have previously been outlined (ASET, 2013). Monitoring personnel should be comprised of dedicated staff with expertise in performing LTVEM, with expertise in seizure management, rescue medication, and behavioral testing. One retrospective category III study found implementing peri-ictal nursing intervention shortened the duration of postictal generalized EEG suppression (Wu et al., 2016), but oxygen supplementation did not. Ictal SPECT requires multidisciplinary personnel to be successful. A survey study in the United States found 68.8% of participants provided continuous patient observation during LTVEM (Shafer et al., 2011). A European survey study reported 80% of participants provided continuous observation, with 10% only during daytime hours of operation and 10% performing observation intermittently in conjunction with automated seizure and spike detection algorithms (Rubboli et al., 2015). Despite limited evidence, continuous EEG monitoring is recommended to be performed by appropriately trained, certified, and supervised neurodiagnostic technologists in the EMU and ICU (Herman et al., 2015).
5.4.4. Duration of recording
Wide variability exists among epilepsy centers regarding the duration of LTVEM, which is dependent upon the reason for admission (Benbadis et al., 2004; Moseley et al., 2016). One category III diagnostic LTVEM study of 226 patients found most patients undiagnosed following outpatient EEG were diagnosed in the first day (Bettini et al., 2014). Other prospective studies (category III) required a second day of LTVEM (Villanueva et al., 2011), and other category IV studies were split between 1–2 days (Foong and Seneviratne, 2016). In contrast, a category IV study of 439 LTVEM cases found 3 days was necessary to record at least one seizure in 90% of patients with epilepsy (2 days with PNEA) (Al Kasab et al., 2016). By 5 days of LTVEM, a retrospective study (category IV) reported a 98% recovery rate for the targeted clinical event (Foong and Seneviratne, 2016).
In patients diagnosed with PNEA, category III and IV studies suggest LTVEM could be averted by diagnostic outpatient shortterm VEM (Benbadis et al., 2004; Seneviratne et al., 2012; Lazarus et al., 2003; Zanzmera et al., 2019). However, one single center category III study of 865 patients noted a higher readmission rate when short duration LTVEM was initially performed (Caller et al., 2014).
A minimum of 72 hours of LTVEM is therefore necessary for patients with drug-resistant epilepsy, whereas those with PNEA are typically diagnosed in the first 1–2 days (Hupalo et al., 2016). A longer duration of monitoring is required for epilepsy patients to ensure appropriate seizure recording, supported by a retrospective category III review of 596 admissions (Moseley et al., 2016). Accurate identification of the seizure-onset zone through iEEG LTVEM requires an extended period of time (Liu et al., 2018). For surgery, at least 3 seizures are sought as representative in uncomplicated cases. In complicated cases with more than one seizureonset zone, the average duration to record the first electrographic seizure from a second focus can be more than 1 month (category III) (King-Stephens et al., 2015). In pediatric patients, a retrospective (category III) LTVEM study of 1000 children (mean age 7 years) usually monitored for 1.5 days investigators found longer sessions had higher rates of epilepsy using ILAE classification, and fewer inconclusive sessions in adolescents. This resulted in recommendations for LTVEM durations of more than 3 days when events were less than daily (Asano et al., 2009). Because the duration of LTVEM depends on the indication and the seizure frequency, a standard duration is variable.
Recommendation: The duration of LTVEM will vary relative to the indication for performance and number of seizures and events captured (conditional recommendation).
5.4.5. Activation
Activation protocols provide relative degrees of usefulness in patients with epilepsy (Leach et al., 2006). Two prospective multicenter studies (category II) support safety and efficacy of activation procedures (Kane et al., 2014; Craciun et al., 2015). General methods of activation including hyperventilation, photic stimulation and sleep deprivation are recommended in guidelines to elicit abnormalities (Sinha et al., 2016; Flink et al., 2002; National Institute for Health and Care Excellence, 2012). In addition, exercise, stress, and dietary influences may precipitate seizures in some patients with epilepsy (da Silva et al., 2005; Pedersen and Petersen, 1998). A random sample of 1000 standard EEGs in the UK verified the additive effect of activation to routine EEG in 11% of cases (Angus-Leppan, 2007). In patients with epilepsy, standard EEG from category II and III studies demonstrates sleep as a potent form of activation to trigger seizures and IEDs (Beniczky et al., 2012; Guaranha et al., 2009). Sleep-deprivation during LTVEM has previously demonstrated diagnostic value in activating IEDs (Pratt et al., 1968; Degen, 1980) as an acceptable practice in the United States and Europe (Sinha et al., 2016; Kasteleijn-Nolst Trenité, 2012) to increase the yield (Carpay et al., 1997; Gustafsson et al., 2015). In contrast, a class III study of acute whole night sleep deprivation every day during LTVEM found no change in precipitating focal to bilateral tonic-clonic seizures (Rossi et al., 2020). Similarly, a recent systematic review found no effect from sleep deprivation suggesting usage may be over-rated during LTVEM (Malow et al., 2002). The ACNS, ILAE, and National Institute for Health and Care Excellence recommend that hyperventilation is performed as part of a standard EEG (Kasteleijn-Nolst Trenité, 2012; Carpay et al., 1997). Hyperventilation with breath counting and intermittent photic stimulation are most useful in patients with GGE to clarify specific epilepsy syndromes (Koutroumanidis et al., 2008). A prospective study (category I) of 52 seizures recorded over 247 days of LTVEM demonstrated the rate of activated seizures was nine times higher than the rate of control seizures and demonstrated value of instituting repeated hyperventilation as an activation technique combined with ASM withdrawal (Jonas et al., 2011a). One category II study found hyperventilation in activating temporal lobe seizures in 25% of patients during LTVEM (Guaranha et al., 2005). A category III study in focal epilepsies found the rate of activated seizures was nine times higher with hyperventilation (Jonas et al., 2011b). Unique methods of activation during LTVEM may provoke seizures in some patients with reflex epilepsies using individualized stimuli (e.g., reading, writing, eating, performing arithmetic, and somatosensory stimulation) (Guaranha et al., 2009; Koepp et al., 2016).
In the diagnosis of PNEA, activation techniques had a marked methodological heterogeneity and low level of evidence in a systematic review including 11 prospective studies (Popkirov et al., 2015). Standard EEG and short-term outpatient video-EEG studies (Burgess, 2001; Benbadis et al., 2004; Kane et al., 2014; Craciun et al., 2015) have performed activation to achieve a diagnosis of PNEA using techniques that are similar to those used during LTVEM, either alone (Kane et al., 2014; Craciun et al., 2015) or in combination with photic stimulation (Benbadis et al., 2004) to provide evidence of suggestibility (Abubakr et al., 2010). Temple compression and tuning fork application were found in one retrospective (category IV) study to be most effective (Goyal et al., 2014). However, controversy exists regarding ethical use (Benbadis et al., 2009; Devinsky and Fisher, 1996; Gates, 2001;
Leeman, 2009). Nonetheless, sensitivity ranges from 77% to 84% (Lancman et al., 1994; Walczak et al., 1994; Benbadis et al., 2000; Barry et al., 2000) and specificity approaches 100% (Lancman et al., 1994) for diagnosis. In older comparative trials (category III and IV), using placebo (e.g., saline injection, application of color patches, alcohol patches or tuning fork) elicited PNEA in most patients (Walczak et al., 1994). Atypical events or epileptic seizures occur in a minority of patients and result in an incorrect diagnosis (Lancman et al., 1994). Provocation without placebo such as combined hyperventilation and photic stimulation has demonstrated comparable sensitivity to placebo without the disadvantages of deception, given it’s routine use in standard EEG (Devinsky and Fisher, 1996) demonstrating non-inferiority (Leeman, 2009). Provocation methods potentially reduce costs by shortening the duration of LTVEM and expedite diagnosis for patients with infrequent events (Lancman et al., 1994).
There is moderate confidence in evidence that hyperventilation was successful in conjunction with ASM withdrawal as an activating procedure to provoke seizures in patients. Expert opinionbased recommendations suggest patient-specific provocation methods be performed in patients with reflex epilepsies.
Recommendation: Patients should undergo hyperventilation in conjunction with ASM withdrawal as an effective activating procedure (strong recommendation).
5.4.6. Drug reduction
ASM is routinely reduced during LTVEM to increase the likelihood of event capture. A judicious speed of reduction should be balanced against ineffective or prolonged hospitalization (Al Kasab et al., 2016). Current practices of ASM reduction are highly variable, and studies provide a wide range of evidence across epilepsy centers performing LTVEM. Rapid withdrawal may potentially obscure localizing information at seizure onset in the EEG during LTVEM (Kobulashvili et al., 2016; Novitskaya et al., 2018). Introducing a scheduled taper of ASM according to a preprescribed protocol facilitates a standardized approach to safe seizure provocation (Shafer et al., 2012). However, no standardized protocols for reduction of ASM during LTVEM exist (Dworetzky and Kapur, 2017) and current practices are highly variable across centers (Buelow et al., 2009). Overly aggressive ASM taper may result in capturing non-habitual seizure semiology, obscure localizing information on ictal EEG, or produce seizure clustering and status epilepticus. Formal protocols focused on ASM taper were shown to have fewer seizure clusters during LTVEM (Rose et al., 2003). Various study methodologies and small sample sizes have limited reliable conclusions regarding the optimal rate of ASM taper during VEM (Di Gennaro et al., 2012). In a comparative study (level II) ictal EEG localization did not change during ASM withdrawal during reduction of lamotrigine and carbamazepine during LTVEM performed during pre-surgical evaluation (Wang-Tilz et al., 2005). Two prospective studies have provided high level evidence for the withdrawal of ASM during LTVEM (Kumar et al., 2018; Rizvi et al., 2014). One randomized controlled (category I) trial, using open-label treatment but blinded outcome, assessed ASM reduction in 2 arms of 70 patients each, comparing fast taper by 30– 50% (fast) and slow taper by 15–30%, in patients without a prior history of status epilepticus or frequent daily seizures and concluded fast taper of ASMs was safe and effective aside from an increase in 4-hour seizure clusters (Kumar et al., 2018). A second prospective study of 158 patients with no control arm (Category II) found that rapid taper of ASM combined with sleep deprivation during LTVEM was safe and effective in adults relative to time of first seizure resulting in reduced time spent in the EMU (Rizvi et al., 2014). This compares favorably with other retrospective, single-center, observational studies (Henning et al., 2014). In contrast, rapid ASM tapering within one day was associated with longer EMU admissions and greater seizure frequency during LTVEM (Al Kasab et al., 2016). Rapid ASM taper in a category III study did not produce a significant adverse effect on the electrocardiogram or heart rate variability (Stefani et al., 2013). Tapering carbamazepine was found to influence ictal semiology, intensifying seizure frequency and severity compared to valproate in a category III study (Zhou et al., 2002). In category IV studies involving barbiturates and benzodiazepines, taper triggered seizures in some people without epilepsy (Shih et al., 2017). Patients completely discontinued from ASM appear more likely to experience focal to bilateral tonic-clonic seizures than those in whom ASM was partly discontinued (Guld et al., 2017). Slowly tapering ASM at home prior to inpatient LTVEM starting 1 week or more prior to admission has been reported to be safe in a retrospective observational cohort of 273 patients (category III) without complications (van Griethuysen et al., 2018).
In patients without a prior history of status epilepticus or frequent daily seizures, ASM taper by 30–50% (fast) and slow taper by 15–30% were safe.
Recommendation: In patients without a history of status epilepticus or frequent daily seizures, a fast taper of 30–50% daily should be considered (strong recommendation).
5.4.7. Automated analyses
Automated analyses are used to identify IEDs and electrographic seizures in an attempt to condense large volumes of data requiring physician review for time efficient interpretation (Tzallas et al., 2009). Relying solely on automation alone is not recommended. Commercially available automated software is used to detect and validate epileptiform activity, and to classify and quantify EEG abnormalities (Gotman, 1999). Software systems available for seizure detection have been tested in a prospective multicenter study (Fürbass et al., 2015) and retrospectively (Fürbass et al., 2015; Kelly et al., 2010; Scheuer et al., 2017). Algorithms for automated seizure detection during scalp LTVEM have a greater sensitivity than IED detection. These may exceed 75.0% detection with low false positive rates (Saab and Gotman, 2005), thus supplementing patient and witness identified seizures. In a study of 159 patients with TLE, 794 seizures were analyzed with a sensitivity of 87.3% and 0.22 false det.ections per hour (Hopfengärtner et al., 2014). However, this has not been confirmed in extratemporal seizures or generalized seizures of a short duration. In a recent study, 14 seizure detection algorithms from 120 patients found performance of the system was comparable to three human experts with a sensitivity of 78% and false positive rate of 1 per day (Scheuer et al., 2017). Most commercially available systems will only detect seizures when the ictal EEG has a duration of 12 seconds or longer. Employing computer-based automated analyses for seizure detection is estimated to save 1.3 hospital days per patient admission, based on the percentage of seizure detections captured solely by the computer (Salinsky, 1997). Better algorithms with greater sensitivity and specificity and a lower number of false positive detections are evolving.
Recommendation: Automated algorithms for spike and seizure detection may provide complementary aid to expert assessment (weak recommendation).
5.4.8. Rescue medication
Fortunately, seizure emergencies rarely occur during LTVEM (Dobesberger et al., 2011), and consequences are reduced when slow reduction of ASM is combined with a benzodiazepine rescue protocol (Shih et al., 2018; Dobesberger et al., 2017). In children and adults, class 1 evidence included in an evidence-based guideline demonstrates both intravenous lorazepam and intravenous diazepam as efficacious initial therapy in convulsive status epilepticus, though ASM usage and new routes of administration have proven efficacy (Glauser et al., 2016; Maglalang et al., 2018). A retrospective LTVEM study (category III) reported different seizure durations guided the use of rescue medication for patients with focal and generalized seizures (Dobesberger et al., 2015). No universal approach or standardized protocol exists for use of rescue medications (Tsai et al., 2016). The National Association of Epilepsy Centers recommends standing orders for both IV and non-IV emergency ASM to be used for seizures lasting more than 5 minutes (National Association of Epilepsy Centers, 2018).
5.5. Reporting
The LTVEM report has traditionally been a qualitative description of waveform interpretation using a free text format (Kaplan and Benbadis, 2013; Tatum et al., 2016). LTVEM interpretative reports, like standard EEG, are becoming increasingly automated (Beniczky et al., 2017). Providing graphic display of EEG samples (Sterne et al., 2001) enhances reproducibility of interictal and ictal EEG portions of the LTVEM report to facilitate patient management and clinical research (Kaplan and Benbadis, 2013). Updated terminology (Berg et al., 2010; Blume et al., 2001) and newer classification systems (Fisher et al., 2017) provide a current framework for the report. Despite established American guidelines (Tatum et al., 2016) and European consensus (Beniczky et al., 2017), significant variation in LTVEM reporting exists. Moderate interobserver variability plagues EEG interpretation, which may be in part due to inconsistencies and lack of standardization for reporting style and terminology utilized (Kaplan and Benbadis, 2013; Tatum et al., 2016; Beniczky et al., 2017; Hirsch et al., 2013). In 2017, the second International version of SCORE (Standardized computer-based organized reporting of EEG), initially published as a European consensus, established a template for automated LTVEM reporting (Beniczky et al., 2017). It was endorsed as a guideline by the IFCN in a susequent version adapting IFCN, ILAE, and ACNS classification systems and glossary of terms to enhance the initial European version (Beniczky et al., 2017). Instituting electronic databases with a list of pre-established terms may result in higher inter-rater agreement of EEG features (Beniczky et al., 2017; Gaspard et al., 2014; Stroink et al., 2006). Both semiology and ictal EEG reporting should follow a chronological order using standardized terminology (IFCN Glossary for EEG; ILAE Glossary for semiology).
6. Conclusions
This CPG provides a comprehensive synthesis of the currently available evidence for performing inpatient LTVEM. In addition to the level of evidence, practical implementation of LTVEM recommendations such as the wise use of resources, preferences of the patients / healthcare personnel, and potential outcome benefit for patients will modify practical usage. There is strong evidence that LTVEM should be used to differentiate between epileptic and non-epileptic events in adults and children when seizures remain uncontrolled despite appropriate treatment. LTVEM is a standard to help classify patients with epilepsy. The ability to quantify seizures in patients with epilepsy is possible for patients with sufficient seizure-frequency to be captured during monitoring (1–2 weeks). There is strong evidence that LTVEM should be used as part of the presurgical evaluation for TLE patients, although for extratemporal epilepsies, low confidence in evidence exists to support LTVEM in the presurgical evaluation, but this does not obviate the current standards of practice. Video should be combined with EEG during LTVEM for greater yield. Activating procedures should be used in conjunction with ASM withdrawal in concert with local practice dictating adaptive testing paradigms during LTVEM. In patients without a history of status epilepticus or frequent daily seizures, tapering ASM by 30–50% daily should be considered. As a new era in EEG monitoring unfolds, home video recordings and subscalp devices for ultra-long-term recording could be an alternative for patients less amenable to LTVEM, but their efficacy still needs to be determined (Dunn-Henriksen et al., 2020).
We found limited high-level evidence exists across published international studies, although this does not preclude the numerous reports, national and international guidelines, and position statements from providing guidance to perform inpatient LTVEM. Significant gaps in knowledge exist due to substantial study heterogeneity and narrow spectrum conclusions involving selected features of LTVEM, therefore further research is needed. Formal CPG (strong and weak) recommendations are not intended to replace sound clinical judgment, and must be adapted for use in limited resource settings. It remains to be proven whether the standards of performance have a direct relationship to meaningful use and outcome. This CPG will require revision as technology, science, and evidence evolve. Nevertheless, experience gained from selective aspects of LTVEM provides insight into current uses and emphasizes the need for conducting comprehensive high-level studies in areas with limited information to further clinical and research development.
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.
References
Abubakr A, Ifeayni I, Wambacq I. The efficacy of routine hyperventilation for seizure activation during prolonged video-electroencephalography monitoring. J Clin Neurosci 2010;17:1503–5.
Acharya JN, Hani AJ, Cheek J, et al. American clinical neurophysiology society guideline 2: guidelines for standard electrode position nomenclature. Neurodiagn J 2016;56:245–52.
Aghaei-Lasboo A, Fisher RS. Methods for measuring seizure frequency and severity. Neurol Clin 2016;34:383–94.
Al Kasab S, Dawson RA, Jaramillo JL, et al. Correlation of seizure frequency and medication down-titration rate during video-EEG monitoring. Epilepsy Behav 2016;64:51–6.
Aliberti V, Grünewald R, Panayiotopoulos C, et al. Focal electroencephalographic abnormalities in juvenile myoclonic epilepsy. Epilepsia 1994;35:297–301.
Alix JJ, Kandler RH, Mordekar SR. The value of long term EEG monitoring in children:
a comparison of ambulatory EEG and video telemetry. Seizure 2014;23:662–5.
Alsaadi TM, Thieman C, Shatzel A, et al. Video-EEG telemetry can be a crucial tool for neurologists experienced in epilepsy when diagnosing seizure disorders. Seizure 2004;13:32–4.
Alving J, Beniczky S. Diagnostic usefulness and duration of the inpatient long-term video-EEG monitoring: findings in patients extensively investigated before the monitoring. Seizure 2009;18:470–3.
American Clinical Neurophysiology Society. Guideline twelve: guidelines for longterm monitoring for epilepsy. J Clin Neurophysiol 2008;25:170–80.
Angus-Leppan H. Seizures and adverse events during routine scalp electroencephalography: a clinical and EEG analysis of 1000 records. Clin Neurophysiol 2007;118:22–30.
Antony AR, Abramovici S, Krafty RT, et al. Simultaneous scalp EEG improves seizure lateralization during unilateral intracranial EEG evaluation in temporal lobe epilepsy. Seizure 2019;64:8–15.
Arain AM, Song Y, Bangalore-Vittal N, et al. Long term video/EEG prevents unnecessary vagus nerve stimulator implantation in patients with psychogenic nonepileptic seizures. Epilepsy Behav 2011;21:364–6.
Asadi-Pooya AA, Tinker J, Fletman E. Semiological classification of psychogenic nonepileptic seizures. Epilepsy Behav 2016;64:1–3.
Asadi-Pooya AA, Stewart GR, Abrams DJ, et al. Prevalence and incidence of drugresistant mesial temporal lobe epilepsy in the United States. World Neurosurg 2017;99:662–6.
Asano E, Juhasz C, Shah A, et al. Role of subdural electrocorticography in prediction of long-term seizure outcome in epilepsy surgery. Brain 2009;132:1038–47.
ASET - The Neurodiagnostic Society. Minimum education and credentialing recommendations for performing neurodiagnostic procedures. https://www.
aset.org/i4a/pages/index.cfm?pageid=4179. 2013. Accessed 30 Jun 2020.
Atkinson M, Shah A, Hari K, et al. Safety considerations in the epilepsy monitoring unit for psychogenic nonepileptic seizures. Epilepsy Behav 2012;25:176–80.
Atkinson M, Hari K, Schaefer K, et al. Improving safety outcomes in the epilepsy monitoring unit. Seizure 2012;21:124–7.
Baheti NN, Radhakrishnan A, Radhakrishnan K. A critical appraisal on the utility of long-term video-EEG monitoring in older adults. Epilepsy Res 2011;97:12–9.
Barrett G. Jerk-locked averaging: technique and application. J Clin Neurophysiol 1992;9:495–508.
Barry JJ, Atzman O, Morrell MJ. Discriminating between epileptic and nonepileptic events: the utility of hypnotic seizure induction. Epilepsia 2000;41:81–4.
Bautista RED, Spencer DD, Spencer SS. EEG findings in frontal lobe epilepsies. Neurology 1998;50:1765–71.
Benbadis SR. The EEG in nonepileptic seizures. J Clin Neurophysiol 2006;23: 340–52.
Benbadis SR. Errors in EEGs and the misdiagnosis of epilepsy: importance, causes, consequences, and proposed remedies. Epilepsy Behav 2007;11:257–62.
Benbadis S, Johnson K, Anthony K, et al. Induction of psychogenic nonepileptic seizures without placebo. Neurology 2000;55:1904–5.
Benbadis SR, Lin K. Errors in EEG interpretation and misdiagnosis of epilepsy. Eur Neurol 2008;59:267–71.
Benbadis SR, O’Neill E, Tatum WO, et al. Outcome of prolonged video-EEG monitoring at a typical referral epilepsy center. Epilepsia 2004;45:1150–3.
Benbadis SR, LaFrance W, Papandonatos G, et al. Interrater reliability of EEG-video monitoring. Neurology 2009;73:843–6.
Benbadis S, Siegrist K, Tatum W, et al. Short-term outpatient EEG video with induction in the diagnosis of psychogenic seizures. Neurology
Benbadis SR, Tatum WO. Overintepretation of EEGs and misdiagnosis of epilepsy. J Clin Neurophysiol 2003;20:42–4.
Benbadis SR, Thomas P, Pontone G. A prospective comparison between two seizure classifications. Seizure 2001;10:247–9.
Beniczky SA, Fogarasi A, Neufeld M, et al. Seizure semiology inferred from clinical descriptions and from video recordings. How accurate are they? Epilepsy Behav 2012;24:213–5.
Beniczky S, Neufeld M, Diehl B, et al. Testing patients during seizures: A European consensus procedure developed by a joint taskforce of the ILAE–Commission on European Affairs and the European Epilepsy Monitoring Unit Association. Epilepsia 2016;57:1363–8.
Beniczky S, Aurlien H, Brøgger JC, et al. Standardized computer-based organized reporting of EEG: SCORE-Second version. Epilepsia 2017;128(11):2334–46.
Bennett-Back O, Uliel-Siboni S, Kramer U. The yield of video-EEG telemetry evaluation for non-surgical candidate children. Eur J Paediatr Neurol 2016;20:848–54.
Berg AT, Berkovic SF, Brodie MJ, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 2010;51:676–85.
Bettini L, Croquelois A, Maeder-Ingvar M, et al. Diagnostic yield of short-term videoEEG monitoring for epilepsy and PNESs: a European assessment. Epilepsy Behav 2014;39:55–8.
Bidwell J, Khuwatsamrit T, Askew B, et al. Seizure reporting technologies for epilepsy treatment: A review of clinical information needs and supporting technologies. Seizure 2015;32:109–17.
Bingham E, Patterson V. Nurse led epilepsy clinics: a telemedicine approach. (ABN Abstracts). J Neurol Neurosurg Psychiatry 2002;73:216–7.
Binnie C, Rowan A, Overweg J, et al. Telemetric EEG and video monitoring in epilepsy. Neurology 1981;31:298–303.
Blum D, Eskola J, Bortz J, et al. Patient awareness of seizures. Neurology 1996;47:260–4.
Blume WT, Lüders HO, Mizrahi E, et al. Glossary of descriptive terminology for ictal semiology: report of the ILAE task force on classification and terminology. Epilepsia 2001;42:1212–8.
Boon P, Santos SF, Jansen AC, et al. Recommendations for the treatment of epilepsy in adult and pediatric patients in Belgium: 2020 update. Acta Neurol Belg 2021;121:241–57.
Bossuyt PM, Reitsma JB, Bruns DE, et al. Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. Radiology 2003;226: 24–8.
Bossuyt PM, Reitsma JB, Bruns DE, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. Clin Chem 2015;61:1446–52.
Bragin A, Mody I, Wilson CL, et al. Local generation of fast ripples in epileptic brain. J Neurosci 2002;22:2012–21.
Brna P, Duchowny M, Resnick T, et al. The diagnostic utility of intracranial EEG monitoring for epilepsy surgery in children. Epilepsia 2015;56:1065–70.
Brown P, Farmer S, Halliday D, et al. Coherent cortical and muscle discharge in cortical myoclonus. Brain 1999;122:461–72.
Brunnhuber F, Amin D, Nguyen Y, et al. Development, evaluation and implementation of video-EEG telemetry at home. Seizure 2014;23:338–43.
Bubrick EJ, Yazdani S, Pavlova MK. Beyond standard polysomnography: advantages and indications for use of extended 10–20 EEG montage during laboratory sleep study evaluations. Seizure 2014;23:699–702.
Buelow JM, Privitera M, Levisohn P, et al. A description of current practice in epilepsy monitoring units. Epilepsy Behav 2009;15:308–13.
Burgess RC. Design and evolution of a system for long-term electroencephalographic and video monitoring of epilepsy patients. Methods 2001;25:231–48.
Burgess RC. Electrical safety. Handbook of clinical neurology: Elsevier; 2019. p. 67–81.
Butler CR, Graham KS, Hodges JR, et al. The syndrome of transient epileptic amnesia. Ann Neurol 2007;61:587–98.
Caller TA, Chen JJ, Harrington JJ, et al. Predictors for readmissions after video-EEG monitoring. Neurology 2014;83:450–5.
Caplan JP, Binius T, Lennon VA, et al. Pseudopseudoseizures: conditions that may mimic psychogenic non-epileptic seizures. Psychosomatics 2011;52:501–6.
Caplin DA, Rao JK, Filloux F, et al. Development of performance indicators for the primary care management of pediatric epilepsy: expert consensus recommendations based on the available evidence. Epilepsia 2006;47:2011–9.
Carpay J, De Weerd A, Schimsheimer R, et al. The diagnostic yield of a second EEG after partial sleep deprivation: a prospective study in children with newly diagnosed seizures. Epilepsia 1997;38:595–9.
Cascino GD. Clinical indications and diagnostic yield of videoelectroencephalographic monitoring in patients with seizures and spells. Mayo Clin Proc; 2002: Elsevier. p. 1111-20.
Catarino CB, Vollmar C, Noachtar S. Paradoxical lateralization of non-invasive electroencephalographic ictal patterns in extra-temporal epilepsies. Epilepsy Res 2012;99:147–55.
Chadwick D, Smith D. The misdiagnosis of epilepsy: The rate of misdiagnosis and wide treatment choices are arguments for specialist care of epilepsy. British Medical Journal Publishing Group; 2002.
Chemmanam T, Radhakrishnan A, Sarma SP, et al. A prospective study on the costeffective utilization of long-term inpatient video-EEG monitoring in a developing country. J Clin Neurophysiol 2009;26:123–8.
Chen Z, Brodie MJ, Liew D, et al. Treatment outcomes in patients with newly diagnosed epilepsy treated with established and new antiepileptic drugs: a 30year longitudinal cohort study. JAMA Neurol 2018;75:279–86.
Chen DK, Graber KD, Anderson CT, et al. Sensitivity and specificity of video alone versus electroencephalography alone for the diagnosis of partial seizures. Epilepsy Behav 2008;13:115–8.
Chen DK, Izadyr S, Collins RL, Berge JF, LeMaire AW, Hrachovy RA. Induction of psychogenic nonepileptic events: Success rate influenced by prior induction exposure, ictal semiology, and psychological profiles. Epilepsia 2011;52 (6):1063–70.
Cho YW, Motamedi GK, Kim KT. The clinical utility of non-invasive videoelectroencephalographic monitoring has been diversifying. Neurol Sci 2019;40:2625–31.
Chowdhury F, Nashef L, Elwes R. Misdiagnosis in epilepsy: a review and recognition of diagnostic uncertainty. Eur J Neurol 2008;15:1034–42.
Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 1989;30(4):389–99.
Cooper MA. Emergent care of lightning and electrical injuries. Semin Neurol. 1995;15:268–78.
Craciun L, Varga ET, Mindruta I, et al. Diagnostic yield of five minutes compared to three minutes hyperventilation during electroencephalography. Seizure 2015;30:90–2.
Craciun L, Alving J, Gardella E, et al. Do patients need to stay in bed all day in the Epilepsy Monitoring Unit? Safety data from a non-restrictive setting. Seizure 2017;49:13–6.
Cuthill FM, Espie CA. Sensitivity and specificity of procedures for the differential diagnosis of epileptic and non-epileptic seizures: a systematic review. Seizure 2005;14:293–303.
da Silva Sousa P, Lin K, Garzon E, et al. Self-perception of factors that precipitate or inhibit seizures in juvenile myoclonic epilepsy. Seizure 2005;14:340–6.
De Marchi LR, Corso JT, Zetehaku AC, et al. Efficacy and safety of a video-EEG protocol for genetic generalized epilepsies. Epilepsy Behav 2017;70:187–92.
Deacon C, Wiebe S, Blume W, et al. Seizure identification by clinical description in temporal lobe epilepsy: how accurate are we? Neurology 2003;61:1686–9.
Degen R. A study of the diagnostic value of waking and sleep EEGs after sleep deprivation in epileptic patients on anticonvulsive therapy. Electroencephalogr Clin Neurophysiol 1980;49:577–84.
Derry CP, Harvey AS, Walker MC, et al. NREM arousal parasomnias and their distinction from nocturnal frontal lobe epilepsy: a video EEG analysis. Sleep 2009;32:1637–44.
DeToledo JC, Lowe MR. Seizures, lateral decubitus, aspiration, and shoulder dislocation: time to change the guidelines? Neurology 2001;56:290–1.
Devinsky O, Fisher R. Ethical use of placebos and provocative testing in diagnosing nonepileptic seizures. Neurology 1996;47:866–70.
Di Gennaro G, Picardi A, Sparano A, et al. Seizure clusters and adverse events during pre-surgical video-EEG monitoring with a slow anti-epileptic drug (AED) taper. Clin Neurophysiol 2012;123:486–8.
Dobesberger J, Walser G, Unterberger I, et al. Video-EEG monitoring: safety and adverse events in 507 consecutive patients. Epilepsia 2011;52:443–52.
Dobesberger J, Ristic´ AJ, Walser G, et al. Duration of focal complex, secondarily generalized tonic–clonic, and primarily generalized tonic–clonic seizures—A video-EEG analysis. Epilepsy Behav 2015;49:111–7.
Dobesberger J, Höfler J, Leitinger M, et al. Personalized safety measures reduce the adverse event rate of long-term video EEG. Epilepsia Open 2017;2:400–14.
DuBois J, Boylan L, Shiyko M, et al. Seizure prediction and recall. Epilepsy Behav 2010;18:106–9.
Dunn-Henriksen J, Baud M, Richardson MP, et al. A new era in electroencephalographic monitoring? Subscalp devices for ultra-long term recording. Epilepsia 2020;61(9):1805–17.
Dwivedi R, Ramanujam B, Chandra PS, et al. Surgery for drug-resistant epilepsy in children. N Engl J Med 2017;377:1639–47.
Dworetzky BA, Kapur J. Gaining perspective on SUDEP: the new guideline. AAN Enterprises 2017.
Dworetzky BA, Mortati KA, Rossetti AO, et al. Clinical characteristics of psychogenic nonepileptic seizure status in the long-term monitoring unit. Epilepsy Behav 2006;9:335–8.
Ebersole JS. Non-invasive pre-surgical evaluation with EEG/MEG source analysis. Electroencephalogr Clin Neurophysiol Suppl 1999;50:167.
Ebersole JS, Pacia SV. Localization of temporal lobe foci by ictal EEG patterns.
Eddy CM, Cavanna AE. Video-electroencephalography investigation of ictal alterations of consciousness in epilepsy and nonepileptic attack disorder: Practical considerations. Epilepsy Behav 2014;30:24–7.
Elger CE, Hoppe C. Diagnostic challenges in epilepsy: seizure under-reporting and seizure detection. Lancet Neurol 2018;17:279–88.
Engel Jr J. Report of the ILAE classification core group. Epilepsia 2006;47: 1558–68.
Engel Jr J, Wiebe S, French J, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Epilepsia 2003;44:741–51.
Engel J, McDermott MP, Wiebe S, et al. Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA 2012;307:922–30.
England MJ, Liverman CT, Schultz AM, et al. Summary: a reprint from epilepsy across the spectrum: promoting health and understanding. Epilepsy Curr 2012;12:245–53.
Erba G, Giussani G, Juersivich A, et al. The semiology of psychogenic nonepileptic seizures revisited: can video alone predict the diagnosis? Preliminary data from a prospective feasibility study. Epilepsia 2016;57:777–85.
Espinosa P, Lee J, Tedrow U, et al. Sudden unexpected near death in epilepsy:
malignant arrhythmia from a partial seizure. Neurology 2009;72:1702–3.
Fayerstein J, McGonigal A, Pizzo F, et al. Quantitative analysis of hyperkinetic seizures and correlation with seizure onset zone. Epilepsia 2020;61:1019–26.
Feigin VL, Nichols E, Alam T, et al. Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 2019;18:459–80.
Ficker DM, So E, Shen W, et al. Population-based study of the incidence of sudden unexplained death in epilepsy. Neurology 1998;51:1270–4.
Fisher RS, Acevedo C, Arzimanoglou A, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014;55:475–82.
Fisher RS, Cross JH, French JA, et al. Operational classification of seizure types by the International League Against Epilepsy: Position Paper of the ILAE Commission for Classification and Terminology. Epilepsia 2017;58:522–30.
Fitzsimons M, Browne G, Kirker J, et al. An international survey of long-term video/ EEG services. J Clin Neurophysiol 2000;17:59–67.
Flink R, Pedersen B, Guekht A, et al. Guidelines for the use of EEG methodology in the diagnosis of epilepsy: International League Against Epilepsy: Commission Report Commission on European Affairs: Subcommission on European Guidelines. Acta Neurol Scand 2002;106:1–7.
Foldvary N, Klem G, Hammel J, et al. The localizing value of ictal EEG in focal epilepsy. Neurology 2001;57:2022–8.
Foong M, Seneviratne U. Optimal duration of video-electroencephalographic monitoring to capture seizures. J Clin Neurosci 2016;28:55–60.
Fowle AJ, Binnie CD. Uses and abuses of the EEG in epilepsy. Epilepsia 2000;41: S10–8.
Friedman DE, Hirsch LJ. How long does it take to make an accurate diagnosis in an epilepsy monitoring unit? J Clin Neurophysiol 2009;26:213–7.
Fürbass F, Ossenblok P, Hartmann M, et al. Prospective multi-center study of an automatic online seizure detection system for epilepsy monitoring units. Clin Neurophysiol 2015;126:1124–31.
Gaspard N, Hirsch LJ, LaRoche SM, et al. Interrater agreement for critical care EEG terminology. Epilepsia 2014;55:1366–73.
Gates JR. Provocative testing should not be used for nonepileptic seizures. Arch Neurol 2001;58:2065–6.
Gavaret M, Maillard L, Jung J. High-resolution EEG (HR-EEG) and magnetoencephalography (MEG). Neurophysiol Clin 2015;45:105–11.
Geddes L, Roeder R. Direct-current injury: electrochemical aspects. J Clin Monit Comput 2004;18:157–61.
Ghougassian DF, d’Souza W, Cook MJ, et al. Evaluating the utility of inpatient videoEEG monitoring. Epilepsia 2004;45:928–32.
Glauser T, Shinnar S, Gloss D, et al. Evidence-based guideline: treatment of convulsive status epilepticus in children and adults: report of the Guideline Committee of the American Epilepsy Society. Epilepsy Curr 2016;16:48–61.
Goldenholz DM, Jow A, Khan OI, et al. Preoperative prediction of temporal lobe epilepsy surgery outcome. Epilepsy Res 2016;127:331–8.
Gotman J. Automatic detection of seizures and spikes. J Clin Neurophysiol 1999;16:130–40.
Goyal G, Kalita J, Misra UK. Utility of different seizure induction protocols in psychogenic nonepileptic seizures. Epilepsy Res 2014;108:1120–7.
Gronseth GS, Woodroffe LM, Getchius TS. Clinical practice guideline process manual. St Paul, MN: American Academy of Neurology 2011.
Gröppel G, Kapitany T, Baumgartner C. Cluster analysis of clinical seizure semiology of psychogenic nonepileptic seizures. Epilepsia 2000;41:610–4.
Guaranha MSB, Da Silva Sousa P, De Araújo-Filho GM, et al. Provocative and inhibitory effects of a video-EEG neuropsychologic protocol in juvenile myoclonic epilepsy. Epilepsia 2009;50:2446–55.
Guaranha MS, Garzon E, Buchpiguel CA, et al. Hyperventilation revisited: physiological effects and efficacy on focal seizure activation in the era of video-EEG monitoring. Epilepsia 2005;46:69–75.
Guld A, Sabers A, Kjaer T. Drug taper during long-term video-EEG monitoring: efficiency and safety. Acta Neurol Scand 2017;135:302–7.
Gustafsson G, Broström A, Ulander M, et al. Occurrence of epileptiform discharges and sleep during EEG recordings in children after melatonin intake versus sleep-deprivation. Clin Neurophysiol 2015;126:1493–7.
Gumnit RJ, Walczak TS. National Association of Epilepsy Centers. Guidelines for essential services, personnel, and facilities in specialized epilepsy centers revised 2010 guidelines. Epilepsia 2001;42:804–14.
Halford JJ, Clunie DA, Brinkmann BH, Krefting D, Rémi J, Rosenow F, Husain AM, Fürbass F, Ehrenberg JA, Winkler S. Standardization of Neurophysiology Signal Data into the DICOM Standard. Clin Neurophysiol. 2021;32(4):993–7.
Hall-Patch L, Brown R, House A, et al. Acceptability and effectiveness of a strategy for the communication of the diagnosis of psychogenic nonepileptic seizures. Epilepsia 2010;51:70–8.
Hamandi K, Beniczky S, Diehl B, et al. Current practice and recommendations in UK epilepsy monitoring units. Report of a national survey and workshop. Seizure 2017;50:92–8.
Hedegärd E, Bjellvi J, Edelvik A, et al. Complications to invasive epilepsy surgery workup with subdural and depth electrodes: a prospective population-based observational study. J Neurol Neurosurg Psychiatry 2014;85:716–20.
Helmstaedter C, Kurthen M, Lux S, et al. Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Ann Neurol 2003;54:425–32.
Henning O, Baftiu A, Johannessen S, et al. Withdrawal of antiepileptic drugs during presurgical video-EEG monitoring: an observational study for evaluation of current practice at a referral center for epilepsy. Acta Neurol Scand 2014;129:243–51.
Heo K, Han SD, Lim SR, et al. Patient awareness of complex partial seizures. Epilepsia 2006;47:1931–5.
Herman ST, Abend N, Bleck T, et al. Consensus statement on continuous EEG in critically Ill adults and children, Part II: personnel, technical specifications, and clinical practice. J Clin Neurophysiol. 2015;32(2):96–108.
Hirfanoglu T, Serdaroglu A, Cansu A, et al. Semiological seizure classification: before and after video-EEG monitoring of seizures. Pediatr Neurol 2007;36:231–5.
Hirsch L, LaRoche S, Gaspard N, et al. American clinical neurophysiology society’s standardized critical care EEG terminology: 2012 version. J Clin Neurophysiol 2013;30:1–27.
Holmes MD, Brown M, Tucker DM. Are ‘‘generalized” seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 2004;45:1568–79.
Holmes MD, Tucker DM, Quiring JM, et al. Comparing noninvasive dense array and intracranial electroencephalography for localization of seizures. Neurosurgery 2010;66:354–62.
Hopfengärtner R, Kasper BS, Graf W, et al. Automatic seizure detection in long-term scalp EEG using an adaptive thresholding technique: a validation study for clinical routine. Clin Neurophysiol 2014;125:1346–52.
Hoppe C, Poepel A, Elger CE. Epilepsy: accuracy of patient seizure counts. Arch Neurol 2007;64:1595–9.
Hubsch C, Baumann C, Hingray C, et al. Clinical classification of psychogenic nonepileptic seizures based on video-EEG analysis and automatic clustering. J Neurol Neurosurg Psychiatry 2011;82:955–60.
Hupalo M, Smigielski JW, Jaskolski DJ. Optimal time of duration of a long-term video-EEG monitoring in paroxysmal events–A retrospective analysis of 282 sessions in 202 patients. Neurol Neurochir Pol 2016;50:331–5.
Itoh Y, Oguni H, Hirano Y, et al. Study of epileptic drop attacks in symptomatic epilepsy of early childhood–Differences from those in myoclonic-astatic epilepsy. Brain Dev 2015;37:49–58.
Jayakar P, Gaillard WD, Tripathi M, et al. Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia 2014;55:507–18.
Je˛drzegczak J, Owczarek K, Majkowski J. Psychogenic pseudoepileptic seizures: clinical and electroencephalogram (EEG) video-tape recordings. Eur J Neurol 1999;6:473–9.
Jokeit H, Ebner A. Long term effects of refractory temporal lobe epilepsy on cognitive abilities: a cross sectional study. J Neurol Neurosurg Psychiatry 1999;67:44–50.
Jonas J, Vignal J-P, Baumann C, et al. Effect of hyperventilation on seizure activation: potentiation by antiepileptic drug tapering. J Neurol Neurosurg Psychiatry 2011a;82:928–30.
Jonas J, Vignal J-P, Baumann C, Anxionnat J-F, Muresan M, Vespignani H, Maillard L. Effect of hyperventilation on seizure activation: potentiation by antiepileptic drug tapering. J Neurol Neurosurg Psychiatry 2011b;82(8):928–30.
Kandler R, Lai M, Ponnusamy A, et al. The safety of UK video telemetry units: results of a national service evaluation. Seizure 2013;22:872–6.
Kane N, Grocott L, Kandler R, et al. Hyperventilation during electroencephalography: safety and efficacy. Seizure 2014;23:129–34.
Kanner AM, Stagno S, Kotagal P, et al. Postictal psychiatric events during prolonged video-electroencephalographic monitoring studies. Arch Neurol 1996;53:258–63.
Kaplan PW, Benbadis SR. How to write an EEG report: dos and don’ts. Neurology 2013;80:S43–6.
Kasteleijn-Nolst Trenité DG. Provoked and reflex seizures: surprising or common? Epilepsia 2012;53:105–13.
Kelly K, Shiau D, Kern R, et al. Assessment of a scalp EEG-based automated seizure detection system. Clin Neurophysiol 2010;121:1832–43.
Keränen T, Rainesalo S, Peltola J. The usefulness of video-EEG monitoring in elderly patients with seizure disorders. Seizure 2002;11:269–72.
Kerling F, Mueller S, Pauli E, et al. When do patients forget their seizures? An electroclinical study. Epilepsy Behav 2006;9:281–5.
King-Stephens D, Mirro E, Weber PB, et al. Lateralization of mesial temporal lobe epilepsy with chronic ambulatory electrocorticography. Epilepsia 2015;56:
Kipervasser S, Neufeld M. Video-EEG monitoring of paroxysmal events in the elderly. Acta Neurol Scand 2007;116:221–5.
Knox A, Arya R, Horn PS, et al. The diagnostic accuracy of video electroencephalography without event capture. Pediatr Neurol 2018;79:8–13.
Kobulashvili T, Höfler J, Dobesberger J, et al. Current practices in long-term videoEEG monitoring services: A survey among partners of the E-PILEPSY pilot network of reference for refractory epilepsy and epilepsy surgery. Seizure 2016;38:38–45.
Kobulashvili T, Kuchukhidze G, Brigo F, et al. Diagnostic and prognostic value of noninvasive long-term video-electroencephalographic monitoring in epilepsy surgery: A systematic review and meta-analysis from the E-PILEPSY consortium. Epilepsia 2018;59:2272–83.
Koepp MJ, Caciagli L, Pressler RM, et al. Reflex seizures, traits, and epilepsies: from physiology to pathology. Lancet Neurol 2016;15:92–105.
Koutroumanidis M, Aggelakis K, Panayiotopoulos CP. Idiopathic epilepsy with generalized tonic–clonic seizures only versus idiopathic epilepsy with phantom absences and generalized tonic–clonic seizures: One or two syndromes? Epilepsia 2008;49:2050–62.
Krauss G, Abdallah A, Lesser R, et al. Clinical and EEG features of patients with EEG wicket rhythms misdiagnosed with epilepsy. Neurology 2005;64: 1879–83.
Kumar S, Ramanujam B, Chandra P, et al. Randomized controlled study comparing the efficacy of rapid and slow withdrawal of antiepileptic drugs during longterm video-EEG monitoring. Epilepsia 2018;59:460–7.
Kumar-Pelayo M, Oller-Cramsie M, Mihu N, et al. Utility of video-EEG monitoring in a tertiary care epilepsy center. Epilepsy Behav 2013;28:501–3.
Kwan P, Brodie MJ. Early identification of refractory epilepsy. N Engl J Med 2000;342:314–9.
Labiner DM, Bagic AI, Herman ST, et al. Essential services, personnel, and facilities in specialized epilepsy centers–revised 2010 guidelines. Epilepsia 2010;51:2322–33.
LaFrance Jr WC, Baker GA, Duncan R, et al. Minimum requirements for the diagnosis of psychogenic nonepileptic seizures: a staged approach: a report from the International League Against Epilepsy Nonepileptic Seizures Task Force. Epilepsia 2013;54:2005–18.
Lancman ME, Asconapé JJ, Craven WJ, et al. Predictive value of induction of psychogenic seizures by suggestion. Ann Neurol 1994;35:359–61. Langston ME, Tatum IV WO. Focal seizures without awareness. Epilepsy Res 2015;109:163–8.
Lantz G, De Peralta RG, Spinelli L, et al. Epileptic source localization with high density EEG: how many electrodes are needed? Clin Neurophysiol
Lazarus J, Bhatia M, Shukla G, et al. A study of nonepileptic seizures in an Indian population. Epilepsy Behav 2003;4:496–9.
Leach JP, Stephen LJ, Salveta C, et al. Which electroencephalography (EEG) for epilepsy? The relative usefulness of different EEG protocols in patients with possible epilepsy. J Neurol Neurosurg Psychiatry 2006;77:1040–2.
Lee Y-Y, Lee M-Y, Chen I, et al. Long-term video-EEG monitoring for paroxysmal events. Chang Gung Med J 2009;32:305–12.
Leeman BA. Provocative techniques should not be used for the diagnosis of psychogenic nonepileptic seizures. Epilepsy Behav 2009;15:110–4.
Leitgeb N, Schröttner J. Electric current perception study challenges electric safety limits. J Med Eng Technol 2002;26:168–72.
Lesser RP. Psychogenic seizures. Neurology 1996;46:1499–507.
Linstone HA, Turoff M. The delphi method. MA: Addison-Wesley Reading; 1975.
Liu S, Gurses C, Sha Z, et al. Stereotyped high-frequency oscillations discriminate seizure onset zones and critical functional cortex in focal epilepsy. Brain 2018;141:713–30.
Louis EKS, Cascino GD. Diagnosis of epilepsy and related episodic disorders. Continuum (Minneap Minn) 2016;22:15–37.
Lüders H, Acharya J, Baumgartner C, et al. Semiological seizure classification. Epilepsia 1998;39:1006–13.
Maglalang PD, Rautiola D, Siegel RA, et al. Rescue therapies for seizure emergencies: new modes of administration. Epilepsia 2018;59:207–15.
Malloy K, Cardenas D, Blackburn A, et al. Time to response and patient visibility during tonic–clonic seizures in the epilepsy monitoring unit. Epilepsy Behav 2018;89:84–8.
Malow B, Passaro E, Milling C, et al. Sleep deprivation does not affect seizure frequency during inpatient video-EEG monitoring. Neurology 2002;59:1371–4.
McBride AE, Shih TT, Hirsch LJ. Video-EEG monitoring in the elderly: a review of 94 patients. Epilepsia 2002;43:165–9.
McGonigal A, Russell AJ, Mallik AK, Oto M, Duncan R. Use of short term video EEG in the diagnosis of attack disorders. J Neurol Neurosurg Psychiatry 2004 May 1;75 (5):771–2.
Merrell RT, Anderson SK, Meyer FB, et al. Seizures in patients with glioma treated with phenytoin and levetiracetam. J Neurosurg 2010;113:1176–81.
Michel CM, Lantz G, Spinelli L, et al. 128-channel EEG source imaging in epilepsy:
clinical yield and localization precision. J Clin Neurophysiol 2004;21:71–83.
Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010;8:336–41.
Moseley BD, Dewar S, Haneef Z, et al. Reasons for prolonged length of stay in the epilepsy monitoring unit. Epilepsy Res 2016;127:175–8. Moshé SL, Perucca E, Ryvlin P, et al. Epilepsy: new advances. Lancet
Mullen SA, Carvill GL, Bellows S, et al. Copy number variants are frequent in genetic generalized epilepsy with intellectual disability. Neurology 2013;81:1507–14.
National Association of Epilepsy Centers. Sample protocol #3: medication reduction to increase seizure yield. 2018. https://www.naec-epilepsy.org/2018-sampleprotocols/. Accessed 12 Jun 2019.
National Institute for Health and Care Excellence. Epilepsies: diagnosis and management (CG137). 2012, https://www.nice.org.uk/Guidance/CG137. Accessed 18 Dec 2012.
Nunes VD, Sawyer L, Neilson J, Sarri G, Cross JH. Diagnosis and management of the epilepsies in adults and children: summary of updated NICE guidance. BMJ 2012;344:e281.
Noe KH, Drazkowski JF. Safety of long-term video-electroencephalographic monitoring for evaluation of epilepsy. Mayo Clin Proc; 2009: Elsevier. p. 495-500.
Noe K, Sulc V, Wong-Kisiel L, et al. Long-term outcomes after nonlesional extratemporal lobe epilepsy surgery. JAMA Neurol 2013;70:1003–8.
Nordli Jr DR. Usefulness of video-EEG monitoring. Epilepsia 2006;47(Suppl 1):26–30.
Novitskaya Y, Hintz M, Schulze-Bonhage A. Rapid antiepileptic drug withdrawal may obscure localizing information obtained during presurgical EEG recordings. Epileptic Disord 2018;20:151–7.
Nuwer MR, Comi G, Emerson R, et al. IFCN standards for digital recording of clinical EEG. Electroencephalogr Clin Neurophysiol 1998;106:259–61.
Oehl B, Götz-Trabert K, Brandt A, et al. Latencies to first typical generalized spikewave discharge in idiopathic generalized epilepsies during video-EEG monitoring. J Clin Neurophysiol 2010;27:1–6.
Oguni H, Mukahira K, Oguni M, et al. Video-polygraphic analysis of myoclonic seizures in juvenile myoclonic epilepsy. Epilepsia 1994;35:307–16.
Oostenveld R, Praamstra P. The five percent electrode system for high-resolution EEG and ERP measurements. Clin Neurophysiol 2001;112:713–9.
Oyegbile T, Dow C, Jones J, et al. The nature and course of neuropsychological morbidity in chronic temporal lobe epilepsy. Neurology 2004;62:1736–42.
Pati S, Kumaraswamy VM, Deep A, et al. Characteristics of falls in the epilepsy monitoring unit: a retrospective study. Epilepsy Behav 2013;29:1–3.
Pedersen S, Petersen K. Juvenile myoclonic epilepsy: clinical and EEG features. Acta Neurol Scand 1998;97:160–3.
Penry JK, Porter RJ, Dreifuss R. Simultaneous recording of absence seizures with video tape and electroencephalography. A study of 374 seizures in 48 patients. Brain 1975;98:427–40.
Perucca E, Covanis A, Dua T. Commentary: epilepsy is a global problem. Epilepsia 2014;55:1326–8.
Pillai J, Sperling MR. Interictal EEG and the diagnosis of epilepsy. Epilepsia 2006;47:14–22.
Popkirov S, Grönheit W, Wellmer J. A systematic review of suggestive seizure induction for the diagnosis of psychogenic nonepileptic seizures. Seizure 2015;31:124–32.
Pratt KL, Mattson RH, Weikers NJ, et al. EEG activation of epileptics following sleep deprivation: a prospective study of 114 cases. Electroencephalogr Clin Neurophysiol 1968;24:11–5.
Pressler RM, Seri S, Kane N, et al. Consensus-based guidelines for video EEG monitoring in the pre-surgical evaluation of children with epilepsy in the UK. Seizure 2017;50:6–11.
Ramantani G, Dümpelmann M, Koessler L, et al. Simultaneous subdural and scalp EEG correlates of frontal lobe epileptic sources. Epilepsia 2014;55:278–88.
Raymond A, Gilmore W, Scott C, et al. Video-EEG telemetry: apparent manifestation of both epileptic and non-epileptic attacks causing potential diagnostic pitfalls. Epileptic Disord 1999;1:101–6.
Risinger M, Engel J, Van Ness P, et al. Ictal localization of temporal lobe seizures with scalp/sphenoidal recordings. Neurology 1989;39:1288-.;39:1288.
Rizvi SA, Hernandez-Ronquillo L, Wu A, et al. Is rapid withdrawal of anti-epileptic drug therapy during video EEG monitoring safe and efficacious? Epilepsy Res 2014;108:755–64.
Rose A, McCabe P, Gilliam F, et al. Occurrence of seizure clusters and status epilepticus during inpatient video-EEG monitoring. Neurology 2003;60:975–8.
Rossi KC, Joe J, Makhija M, et al. Insufficient sleep, electroencephalogram activation, and seizure risk: re-evaluating the evidence. Ann Neurol 2020;87:798–806.
Rubboli G, Bisulli F, Michelucci R, et al. Sudden falls due to seizure-induced cardiac asystole in drug-resistant focal epilepsy. Neurology 2008;70:1933–5.
Rubboli G, Beniczky S, Claus S, et al. A European survey on current practices in epilepsy monitoring units and implications for patients’ safety. Epilepsy Behav 2015;44:179–84.
Rugg-Gunn F, Harrison N, Duncan J. Evaluation of the accuracy of seizure descriptions by the relatives of patients with epilepsy. Epilepsy Res 2001;43:193–9.
Ryvlin P, Nashef L, Lhatoo SD, et al. Incidence and mechanisms of cardiorespiratory arrests in epilepsy monitoring units (MORTEMUS): a retrospective study. Lancet Neurol 2013;12:966–77.
Saab M, Gotman J. A system to detect the onset of epileptic seizures in scalp EEG. Clin Neurophysiol 2005;116:427–42.
Sadleir LG, Scheffer IE, Smith S, et al. EEG features of absence seizures in idiopathic generalized epilepsy: impact of syndrome, age, and state. Epilepsia 2009;50:1572–8.
Salinsky M. A practical analysis of computer based seizure detection during continuous video-EEG monitoring. Electroencephalogr Clin Neurophysiol 1997;103:445–9.
Sammaritano M, de Lotbinière A, Andermann F, et al. False lateralization by surface EEG of seizure onset in patients with temporal lobe epilepsy and gross focal cerebral lesions. Ann Neurol 1987;21:361–9.
Sauro KM, Macrodimitris S, Krassman C, et al. Quality indicators in an epilepsy monitoring unit. Epilepsy Behav 2014;33:7–11.
Sauro KM, Wiebe S, Perucca E, et al. Developing clinical practice guidelines for epilepsy: a report from the ILAE Epilepsy Guidelines Working Group. Epilepsia 2015;56:1859–69.
Sauro KM, Wiebe N, Macrodimitris S, et al. Quality and safety in adult epilepsy monitoring units: A systematic review and meta-analysis. Epilepsia 2016;57:1754–70.
Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE commission for classification and terminology. Epilepsia 2017;58:512–21.
Scherg M, Ille N, Weckesser D, et al. Fast evaluation of interictal spikes in long-term EEG by hyper-clustering. Epilepsia 2012;53:1196–204.
Scheuer ML, Bagic A, Wilson SB. Spike detection: Inter-reader agreement and a statistical Turing test on a large data set. Clin Neurophysiol 2017; 128:243–50.
Scottish Intercollegiate Guidelines Network. SIGN 70: Diagnosis and management of epilepsy in adults. 2003. https://www.sign.ac.uk.archived-guidelines.html. Accessed 7 Jun 2020.
Seeck M, Koessler L, Bast T, et al. The standardized EEG electrode array of the IFCN. Clin Neurophysiol 2017;128:2070–7.
Semah F, Picot M-C, Adam C, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 1998;51:1256–62.
Seneviratne U, Reutens D, D’Souza W. Stereotypy of psychogenic nonepileptic seizures: Insights from video-EEG monitoring. Epilepsia 2010;51:1159–68.
Seneviratne U, Cook M, D’Souza W. The electroencephalogram of idiopathic generalized epilepsy. Epilepsia 2012;53:234–48.
Seneviratne U, Rahman Z, Diamond A, et al. The yield and clinical utility of outpatient short-term video-electroencephalographic monitoring: a five-year retrospective study. Epilepsy Behav 2012;25:303–6.
Serles W, Caramanos Z, Lindinger G, et al. Combining ictal surfaceelectroencephalography and seizure semiology improves patient lateralization in temporal lobe epilepsy. Epilepsia 2000;41:1567–73.
Shafer P, Buelow J, Ficker D, et al. Risk of adverse events on epilepsy monitoring units: a survey of epilepsy professionals. Epilepsy Behav 2011;20:502–5.
Shafer PO, Buelow JM, Noe K, et al. A consensus-based approach to patient safety in epilepsy monitoring units: recommendations for preferred practices. Epilepsy Behav 2012;25:449–56.
Shibasaki H, Hallett M. Electrophysiological studies of myoclonus. Muscle Nerve 2005;31:157–74.
Shih JJ, Whitlock JB, Chimato N, et al. Epilepsy treatment in adults and adolescents: expert opinion, 2016. Epilepsy Behav 2017;69:186–222.
Shih JJ, Fountain NB, Herman ST, et al. Indications and methodology for videoelectroencephalographic studies in the epilepsy monitoring unit. Epilepsia 2018;59:27–36.
Shin HW, Pennell PB, Lee JW, et al. Efficacy of safety signals in the epilepsy monitoring unit (EMU): Should we worry? Epilepsy Behav 2012;23:
Sinha SR, Sullivan LR, Sabau D, et al. American clinical neurophysiology society guideline 1: minimum technical requirements for performing clinical electroencephalography. Neurodiagn J 2016;56:235–44.
Smith S. EEG in the diagnosis, classification, and management of patients with epilepsy. J Neurol Neurosurg Psychiatry 2005;76:ii2-ii7.
Spanaki MV, McCloskey C, Remedio V, et al. Developing a culture of safety in the epilepsy monitoring unit: a retrospective study of safety outcomes. Epilepsy Behav 2012;25:185–8.
Spritzer SD, Pirotte BD, Agostini SD, et al. The influence of staffing on diagnostic yield of EMU admissions: a comparison study between two institutions. Epilepsy Behav 2014;41:264–7.
Spritzer SD, Riordan KC, Berry J, et al. Fall prevention and bathroom safety in the epilepsy monitoring unit. Epilepsy Behav 2015;48:75–8.
Starmer CF, McIntosh HD, Whalen RE. Electrical hazards and cardiovascular function. N Engl J Med 1971;284:181–6.
Stefan H, Kreiselmeyer G, Kasper B, et al. Objective quantification of seizure frequency and treatment success via long-term outpatient video-EEG monitoring: a feasibility study. Seizure 2011;20:97–100.
Stefani M, Arima H, Mohamed A. Withdrawal of anti-epileptic medications during video EEG monitoring does not alter ECG parameters or HRV. Epilepsy Res 2013;106:222–9.
Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. BMJ
Stroink H, Schimsheimer R-J, de Weerd AW, et al. Interobserver reliability of visual interpretation of electroencephalograms in children with newly diagnosed seizures. Dev Med Child Neurol 2006;48:374–7.
Syed TU, LaFrance Jr WC, Kahriman ES, et al. Can semiology predict psychogenic nonepileptic seizures? A prospective study. Ann Neurol 2011;69:997–1004.
Tanaka H, Khoo HM, Dubeau F, et al. Association between scalp and intracerebral electroencephalographic seizure-onset patterns: A study in different lesional pathological substrates. Epilepsia 2018;59:420–30.
Tanaka H, Gotman J, Khoo HM, et al. Neurophysiological seizure-onset predictors of epilepsy surgery outcome: a multivariable analysis. J Neurosurg 2019;1:1–10.
Tao JX, Ray A, Hawes-Ebersole S, et al. Intracranial EEG substrates of scalp EEG interictal spikes. Epilepsia 2005;46:669–76.
Tao JX, Baldwin M, Ray A, et al. The impact of cerebral source area and synchrony on recording scalp electroencephalography ictal patterns. Epilepsia 2007;48:2167–76.
Tatum IV WO, Winters L, Gieron M, et al. Outpatient seizure identification: results of 502 patients using computer-assisted ambulatory EEG. J Clin Neurophysiol 2001;18:14–9.
Tatum WO, Dworetzky BA, Schomer DL. Artifact and recording concepts in EEG. J Clin Neurophysiol 2011;28:252–63.
Tatum WO, Acton EK, Langston ME, et al. Multimodality peak lctal vital signs during video-EEG monitoring. Seizure 2016;40:15–20.
Tatum WO, Selioutski O, Ochoa J, Munger H, Cheek J, Drislane F, Tsuchida T. American clinical neurophysiology society guideline 7: guidelines for EEG reporting. J Clin Neurophysiol 2016;33(4):328–32.
Tatum WO, Rubboli G, Kaplan PW, et al. Clinical utility of EEG in diagnosing and monitoring epilepsy in adults. Clin Neurophysiol 2018;129:1056–82.
Tatum WO, Hirsch LJ, Gelfand MA, et al. Assessment of the predictive value of outpatient smartphone videos for diagnosis of epileptic seizures. JAMA Neurol 2020.
Tényi D, Gyimesi C, Kupó P, et al. Ictal asystole: a systematic review. Epilepsia 2017;58:356–62.
Thijs RD, Surges R, O’Brien TJ, Sander JW. Epilepsy in adults. Lancet 2019;393 (10172):689–701.
Tian N, Boring M, Kobau R, et al. Active epilepsy and seizure control in adults— United States, 2013 and 2015. MMWR Morb Mortal Wkly Rep 2018;67:437.
Tinuper P, Grassi C, Bisulli F, et al. Split-screen synchronized display. A useful videoEEG technique for studying paroxysmal phenomena. Epileptic Disord 2004;6:27–30.
Touloumes G, Morse E, Chen WC, et al. Human bedside evaluation versus automatic responsiveness testing in epilepsy (ARTiE). Epilepsia 2016;57:e28–32.
Tsai C, Mintzer S, Nei M, et al. A Retrospective Review of Rescue Medications used During Video EEG-Monitoring in the Epilepsy Monitoring Unit (P4. 198). AAN Enterprises; 2016.
Tzallas AT, Tsipouras MG, Fotiadis DI. Epileptic seizure detection in EEGs using time–frequency analysis. IEEE Trans Inf Technol Biomed 2009;13:703–10.
Uldall P, Alving J, Hansen L, et al. The misdiagnosis of epilepsy in children admitted to a tertiary epilepsy centre with paroxysmal events. Arch Dis Child 2006;91:219–21.
US FDA. How drugs are developed and approved. 2019. https://www.fda.gov/drugs/ development-approval-process-drugs/how-drugs-are-developed-andapproved. Accessed 17 Dec 2019.
Usui N, Kotagal P, Matsumoto R, et al. Focal semiologic and electroencephalographic features in patients with juvenile myoclonic epilepsy. Epilepsia 2005;46:1668–76.
van Griethuysen R, Hofstra WA, van der Salm SM, et al. Safety and efficiency of medication withdrawal at home prior to long-term EEG video-monitoring. Seizure 2018;56:9–13.
Vaughan KA, Ramos CL, Buch VP, et al. An estimation of global volume of surgically treatable epilepsy based on a systematic review and meta-analysis of epilepsy. J Neurosurg 2018;130:1127–41.
Velis D, Plouin P, Gotman J, et al. Recommendations regarding the requirements and applications for long-term recordings in epilepsy. Epilepsia 2007;48:379–84.
Villanueva V, Gutierrez A, Garcia M, et al. Usefulness of video-eeg monitoring in patients with drugresistant epilepsy. Neurología 2011;26:6–12.
Wadwekar V, Nair PP, Murgai A, et al. Semiologic classification of psychogenic non epileptic seizures (PNES) based on video EEG analysis: do we need new classification systems? Seizure 2014;23:222–6.
Walczak TS, Williams DT, Berten W. Utility and reliability of placebo infusion in the evaluation of patients with seizures. Neurology 1994.;44:394.
Wang S, Jin B, Yang L, et al. Clinical value and predictors of subclinical seizures in patients with temporal lobe epilepsy undergoing scalp video-EEG monitoring. J Clin Neurosci 2017;44:214–7.
Wang-Tilz Y, Tilz C, Wang B, et al. Changes of seizures activity during rapid withdrawal of lamotrigine. Eur J Neurol 2005;12:280–8.
Watemberg N, Tziperman B, Dabby R, et al. Adding video recording increases the diagnostic yield of routine electroencephalograms in children with frequent paroxysmal events. Epilepsia 2005;46:716–9.
Wetjen NM, Marsh WR, Meyer FB, et al. Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy. J Neurosurg 2009;110:1147–52.
Wiebe S, Blume WT, Girvin JP, et al. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 2001;345:311–8.
Worrell GA, So EL, Kazemi J, et al. Focal ictal b discharge on scalp EEG predicts excellent outcome of frontal lobe epilepsy surgery. Epilepsia 2002;43:277–82.
Wu S, Issa NP, Rose SL, et al. Impact of periictal nurse interventions on postictal generalized EEG suppression in generalized convulsive seizures. Epilepsy Behav 2016;58:22–5.
Yogarajah M, Powell HR, Heaney D, et al. Long term monitoring in refractory epilepsy: the Gowers Unit experience. J Neurol Neurosurg Psychiatry 2009;80:305–10.
Yun CH, Lee SK, Lee SY, et al. Prognostic factors in neocortical epilepsy surgery: multivariate analysis. Epilepsia 2006;47:574–9.
Zanzmera P, Sharma A, Bhatt K, et al. Can short-term video-EEG substitute longterm video-EEG monitoring in psychogenic nonepileptic seizures? A prospective observational study. Epilepsy Behav 2019;94:258–63.
Zeman A, Butler C. Transient epileptic amnesia. Curr Opin Neurol 2010;23:610–6.
Zhou D, Wang Y, Hopp P, et al. Influence on ictal seizure semiology of rapid withdrawal of carbamazepine and valproate in monotherapy. Epilepsia 2002;43:386–93.