Overcoming traps and pitfalls leading to misinterpretation of normal EEG variants and variation of the background activity.

Normal EEG variants, especially the epileptiform variants, can be challenging to interpret because they often have sharp contours and may be confused with "epileptic" interictal activities. However, they can be recognized by the fact that "most spikes or sharp wave discharges of clinical import are followed by a slow wave or a series of slow deflections" (Maulsby, 1971). If there is no wave after the spike, electroencephalographers should be suspicious of artifacts and normal EEG variants. Most normal EEG variants display a single rhythm with the same frequency within the pattern and the morphology remains stable throughout the entire EEG recording with repetition of the same pattern. In case of doubt or difficulties with a standard EEG, it is recommended to undergo an EEG that includes sleep stages with or without sleep deprivation. Finally, epileptiform is an ambiguous term corresponding to an electroencephalographic trait. Epileptiform does not imply a pathological condition, including epilepsy. The clinical context remains the most paramount in the diagnosis of epilepsy. In this article, we propose a set of rules and guidelines to identify normal EEG variants in EEG tracings and normal variation of the background activity. It is not easy to accurately assign a specific/precise name to all EEG activity, but with an orderly approach to EEG that involves using a set of criteria, nonepileptic activity can be identified.

Stimulus-induced arousal with transient electroencephalographic improvement distinguishes nonictal from ictal generalized periodic discharges.

In the case of suspicion of nonconvulsive status epilepticus (NCSE), reactivity on electroencephalograms (EEGs) can provide valuable diagnostic information. Reactivity refers to responses to auditory or somatosensory stimulation, with changes in amplitude and frequency of background activity. Because of self-perpetuating processes and the failure of self-terminating mechanisms, status epilepticus is unlikely to cease when patients spontaneously move, and it cannot typically be stopped by external stimulation (i.e., auditory and tactile stimuli). The defining EEG characteristic of absence status epilepticus is the presence of bilateral, synchronous, symmetric, rhythmic paroxysmal activity that shows little or no reactivity to sensory stimulation. On the other hand, in metabolic/toxic or multifactorial encephalopathies, triphasic waves (TWs) are influenced by the level of vigilance. TWs may be transiently abolished when patients increase their level of alertness from a drowsy/lethargic state to a state of wakefulness. This reactivity is only observed when patients can be aroused by a somatosensory or auditory stimulus. This reactivity tends to disappear with increasing severity of the disease and in comatose patients. In patients without preexisting developmental and epileptic encephalopathy, this pattern of stimulus-induced wakefulness with transient improvement of the EEG is a major criterion in determining that the EEG patterns are not ictal. This criterion of reactivity on EEGs, beyond the classical clinical/EEG criteria of NCSE (Salzburg criteria), should now be systematically added.

Epilepsy with eyelid myoclonia (Jeavons syndrome): Generalized, focal, or combined generalized and focal epilepsy syndrome?

Epilepsy with eyelid myoclonia (EM) or Jeavons syndrome (JS) is an epileptic syndrome related to the spectrum of genetic generalized epilepsies (GGE). We report two untreated children on which EEGs were performed several hours after a generalized tonic-clonic seizure (GTCS). These showed a unilateral, nearly continuous posterior slowing. This slow-wave activity was associated with contralateral epileptiform activity in one case, while in the second case, it was associated with an ipsilateral activity. However, in the latter child, a few months later an independent focus on the contralateral side was observed. A diagnosis of focal occipital lobe epilepsy was proposed in both cases, and one child underwent a left occipital lobectomy at 3.5 years of age. Despite surgery, absences with EM persisted in this child, and a marked photosensitivity to photic stimulation was observed two years later. The focal slow wave activity of one occipital lobe several hours after a GTCS in these two subjects was in favor of a focal onset preceding the generalization. The EEG evidence for independent left and right posterior focus in these two cases, the persistence of EM, and the development of a marked photosensitivity to photic stimulation in the child who underwent an occipital lobectomy, allow us to suggest that JS is associated with a network of bi-occipital hyperexcitability that rapidly engages bilaterally to produce generalized seizures.

Can epilepsy affect normal EEG variants? A comparative study between subjects with and without epilepsy.

OBJECTIVES: To compare the prevalence of benign EEG variants (BEVs) between epileptic and non-epileptic subjects. METHODS: A prospective, observational EEG study of 1,163 consecutive patients, using the 10-20 international system with systematically two additional anterior/inferior temporal electrodes. The video-EEG monitoring duration was between 24 h and eight days. RESULTS: We identified 917 (78.9%) epileptic patients (mean age: 33.42 ± 15.5 years; females: 53.4%) and 246 (21.2%) non-epileptic patients (mean age: 35.6 ± 18.75 years; females: 54.9%). Despite a shorter mean duration of the EEG recordings, the prevalence of BEVs was higher in non-epileptic vs. epileptic patients (73.2% vs. 57.8%, p = 0.000011). This statistical difference was confirmed for lambda waves (23.6% in the non-epilepsy group vs. 14.8% in the epilepsy group, p = 0.001), POSTs (50.8% vs. 32.5%, p < 0.000001), wicket spikes (20.3% vs. 13.6%, p = 0.009) in particular in NREM and REM sleep, and 14- and 6-Hz positive bursts (13% vs. 7.1% p = 0.003). Mu rhythm was observed at the same frequency in both groups (21.1% in the non-epilepsy group vs. 22.7% in the epilepsy group). There was no difference between the two groups for rarer rhythms, such as rhythmic mid-temporal theta burst of drowsiness, small sharp spikes, and midline theta rhythm. CONCLUSIONS: There was no increase in any of the BEVs in the epilepsy group. On the contrary, BEVs were more frequent and diversified in the non-epilepsy group. Epilepsy may negatively affect the occurrence of the most common BEVs, with the exception of the mu rhythm, which is present in about one-fifth of the population with or without epilepsy.

Bilateral and synchronous "dents de scie" spikes: A highly specific EEG pattern of young adult Dravet syndrome.

BACKGROUND: In Dravet syndrome (DS), EEGs evolve over time. OBJECTIVE: To describe a peculiar EEG pattern in two adults with a de novo SCN1A gene mutation, in exon 5 (case 1) and 9 (case 2). METHODS: Two female patients underwent a prolonged video EEG (24 h) as part of their epilepsy assessment. RESULTS: In both cases, the EEG showed a very peculiar and stereotypical pattern of bilateral synchronous spikes at about 5-6 Hz. This activity was present during wakefulness and highly activated at sleep onset and in NREM sleep, which could show nearly continuous spike activity. This activity dramatically decreased in REM sleep and after awakening. This pattern of "dents de scie" (sawtooth) spikes maintained the same morphology throughout the entire EEG recording. In both patients, the spikes were favored by passive eye closure. During wakefulness, the spikes could evolve into atypical absences while keeping the same "dents de scie" pattern. Neither patient had tonic or myoclonic seizures at the time of the EEG assessment. Both were moderately retarded, and neither one had a typical DS gait disorder. Previous EEG recordings of case 1 performed at 9.5 and 18.5 years showed spike-waves, but the morphology did not correspond to the EEG recording observed at 22 years. CONCLUSIONS: Both patients have a similar electro-clinical phenotype. This "dents de scie" pattern appears to be very specific and could be pathognomonic in a subgroup of young adults with DS. Results of sleep EEG recording could be added to the diagnostic criteria for this syndrome.

How valid are proxy assessment of mental health and sleep comorbidities of patients with epilepsy using standardized questionnaires?

BACKGROUND: The study aimed to determine the level of agreement between patients with epilepsy and their proxies when assessing psychiatric comorbidities, sleep disorders, and medication adherence using standardized questionnaires. METHODS: This agreement study is an ancillary analysis of the PRERIES study, a matched case-control study exploring SUDEP risk factors. Controls aged 15 years and older, with active epilepsy or in remission for less than 5 years were recruited between 01/01/2011 and 03/31/2019. An interview was carried out by a trained psychologist on both the patient and a proxy-respondent. During these independent interviews, the following comorbidities were explored: psychiatric comorbidities using the MINI, the STAI- Y2 and NDDI-E scales, sleep disorders with the SDQ-SA and Epworth scales and medication adherence. Level of agreement between patient and their proxy was estimated using Gwet's AC1&2. RESULTS: Among the 107 patient-proxy dyads recruited, proxy respondents were mainly family members (65.4%) or spouses (30.8%). Exploration of present major depression showed excellent agreement at 0.81 [0.65;0.97], as well as exploration of dysthymia at 0.96 [0.61;1]. Suicidal risk evaluation had a lesser agreement at 0.77 [0.60;0.94]. Agreement on anxiety was moderate 0.5 [0.38;0.62]. For sleep disorder, SDQ-SA presented a better agreement than the Epworth questionnaire with respectively 0.73 [0.51;0.95] and 0.45 [0.26;0.63]. For medication adherence, the overall agreement rate was excellent (0.90 [0.78;1]). CONCLUSION: Exploration of potential risk factors through families can give valuable and relatively robust information, especially if the respondent lives with the patient, and should be retrieved, when possible, in usual clinical setting.

Determining ICU EEG periodic patterns and why it matters.

Historically, periodic EEG patterns were described as any pattern with stereotyped paroxysmal complexes occurring at regular intervals, i.e., the period (T). T is the sum of the duration of the waveform (t1) and, eventually, the duration of the interval between two consecutive waves (t2). The American Clinical Neurophysiology Society introduced the concept of a clearly discernible inter-discharge interval between consecutive waveforms (i.e., t2). As this definition was not applied to what have previously been termed triphasic waves and in some cases of lateralized periodic discharges, we propose reconsideration of terminology that includes historical use of definitions. This will allow the development and usage of the concept for periodic EEG patterns as any runs of stereotyped paroxysmal waveforms separated by nearly identical intervals and prolonged repetitive complexes on the EEG. Prolonged expression means EEG is recorded for a sufficient period of time to prove that the pattern is repetitive, thus resulting in a monomorphic/monotonous pattern. More important than the inter-discharge interval (t2), periodic EEG patterns occur at time regular intervals (T). As a result, periodic EEG activity should be considered along a continuum and not the opposite of rhythmic EEG activity where no interval activity exists between consecutive waveforms.

Stratifying sudden death risk in adults with drug-resistant focal epilepsy: The SUDEP-CARE score.

BACKGROUND AND PURPOSE: A clinical risk score for sudden unexpected death in epilepsy (SUDEP) in patients with drug-resistant focal epilepsy could help improve prevention. METHODS: A case-control study was conducted including (i) definite or probable SUDEP cases collected by the French National Sentinel Mortality Epilepsy Network and (ii) control patients from the French national research database of epilepsy monitoring units. Patients with drug-resistant focal epilepsy were eligible. Multiple logistic regressions were performed. After sensitivity analysis and internal validation, a simplified risk score was developed from the selected variables. RESULTS: Sixty-two SUDEP cases and 620 controls were included. Of 21 potential predictors explored, seven were ultimately selected, including generalized seizure frequency (>1/month vs. <1/year: adjusted odds ratio [AOR] 2.6, 95% confidence interval [CI] 1.25-5.41), nocturnal or sleep-related seizures (AOR 4.49, 95% CI 2.68-7.53), current or past depression (AOR 2.0, 95% CI 1.19-3.34) or the ability to alert someone of an oncoming seizure (AOR 0.57, 95% CI 0.33-0.98). After internal validation, a clinically usable score ranging from -1 to 8 was developed, with high discrimination capabilities (area under the receiver operating curve 0.85, 95% CI 0.80-0.90). The threshold of 3 has good sensitivity (82.3%, 95% CI 72.7-91.8), whilst keeping a good specificity (82.7%, 95% CI 79.8-85.7). CONCLUSIONS: These results outline the importance of generalized and nocturnal seizures on the occurrence of SUDEP, and show a protective role in the ability to alert someone of an oncoming seizure. The SUDEP-CARE score is promising and will need external validation. Further work, including paraclinical explorations, could improve this risk score.

Coffee consumption and seizure frequency in patients with drug-resistant focal epilepsy.

OBJECTIVE: To assess the relation between coffee consumption and seizure frequency in patients with drug-resistant focal epilepsy. METHODS: Cross-sectional analysis of data collected in the SAVE study, which included patients with drug-resistant focal epilepsy during long-term EEG monitoring. Patients in whom both coffee consumption and data about seizure frequency, including focal to bilateral tonic-clonic seizures (FBTCS), were available were selected. Coffee consumption was collected using a standardized self-report questionnaire and classified into four groups: none, rare (from less than 1 cup/week to up 3 cups/week), moderate (from 4 cups/week to 3 cups/day), and high (more than 4 cups/day). RESULTS: Six hundred and nineteen patients were included. There was no relation between coffee consumption and total seizure frequency (p = 0.902). In contrast, the number of FBTCS reported over the past year was significantly associated with usual coffee consumption (p = 0.029). Specifically, number of FBCTS in patients who reported moderate coffee consumption was lower than in others. In comparison with patients with moderate coffee consumption, the odds ratio (95%CI) for reporting at least 1 FBTCS per year was 1.6 (1.03-2.49) in patients who never take coffee, 1.62 (1.02-2.57) in those with rare consumption and 2.05 (1.24-3.4) in those with high consumption. Multiple ordinal logistic regression showed a trend toward an association between coffee consumption and number of FBTCS (p = 0.08). CONCLUSIONS AND RELEVANCE: Our data suggest that effect of coffee consumption on seizures might depend on dose with potential benefits on FBTCS frequency at moderate doses. These results will have to be confirmed by prospective studies.

Recommendations for risk management and better living with epilepsy. Phenomenological study of the experience of patients, relatives, and bereaved families.

OBJECTIVE: To understand the lived experience of people with epilepsy (PWE) and their relatives, the risks associated with epilepsy, the information received from healthcare professionals, and the reaction to this information. METHODS: Qualitative phenomenological study conducted between 2016 and 2018. Individual semi-directive in-depth interviews were performed based on a triangulation of sources in three study groups: PWE, relatives of PWE, and bereaved families. Interviews were analyzed continuously, using a semiopragmatic method until data saturation. RESULTS: Interviews with PWE (N = 16), relatives of PWE (N = 8), and bereaved families (N = 10) led to several observations: (i) The stigmatizing representations of epilepsy and its constraints lead to a feeling of abnormality which determines the behavior of patients and their relatives; (ii) The global uncertainty surrounding epilepsy is an obstacle to the delivery of clear and personalized information by professionals, and, consequently, to empowerment; (iii) The communication skills of the physician have an impact on the lived experiences of patients and relatives; (iv) Better knowledge on direct mortal epilepsy-related risk could influence the perception of danger to oneself, and help find a balance between overprotection and trivialization. The experience of the patients and relatives led them to formulate concrete recommendations: (i) for the general public: to run information campaigns in order to limit stigmatization; (ii) for caregivers: to provide personalized and detailed information without minimizing the risks, in order to enable patients to "live by setting these risks"; (iii) for patients: to have a trusted person who is informed and trained in seizure management, to join patient associations. CONCLUSION: Our study points out that stigma, uncertainty, and lack of clarity of information are all barriers to patient empowerment. In order to provide prompt and personalized information on how to live with epilepsy while managing the risks, physicians need to develop person-centered communication skills. Future research is also required for the development of tools to facilitate this communication.

Stimulus-Induced Rhythmic or Periodic Intermittent Discharges (SIRPIDs) in patients with triphasic waves and Creutzfeldt-Jakob disease.

Since the term Stimulus-Induced Rhythmic, Periodic, or Ictal Discharges (SIRPIDs) was introduced into the vocabulary of electrophysiologists/neurologists, there has been an ongoing debate about its significance, as well as its correlation with outcomes. SIRPIDs are frequently seen in patients who are critically ill from various causes. The literature reflects the findings of triphasic morphology, with the generalized periodic discharge (GPD) classification in many patients with SIRPIDs: toxic/metabolic encephalopathies, septic, and hypoxemic/hypercapnic encephalopathies, but also sharp periodic complexes in Creutzfeldt-Jakob disease and advanced Alzheimer's disease. In these settings, GPDs disappear when patients fall asleep and reappear when patients spontaneously wake up, or are awoken by an external stimulus, or sometimes because of a respiratory event, with the possibility of the appearance of GPDs with a cyclic alternating pattern. SIRPIDs may be seen as a transitional pattern between sleep and waking states, corresponding to a postarousal/awakening phenomenon. As SIRPIDs are a transient phenomenon and can usually be recorded repeatedly with each stimulation, the word "Ictal" could be replaced by "Intermittent": Stimulus-Induced Rhythmic or Periodic Intermittent Discharges. However, considering that SIRPIDs may be "potentially ictal" or on an "ictal-interictal continuum" in some situations, the "plus" modifier may be added: SIRPIDs-plus.

Lateralized Periodic Discharges: Which patterns are interictal, ictal, or peri-ictal?

There is an ongoing debate if Lateralized Periodic Discharges (LPDs) represent an interictal pattern reflecting non-specific but irritative brain injury, or conversely, is an ictal pattern. The challenge is: how to correctly manage these patients? Between this apparent dichotomous distinction, there is a pattern lying along the interictal-ictal continuum (IIC) that we may call "peri-ictal". Peri-ictal means that LPDs are temporally associated with epileptic seizures (although not necessarily in the same recording). Their recognition should lead to careful EEG monitoring and longer periods of video-EEG to detect seizure activity (clinical and/or subclinical seizures). In order to distinguish which kind of LPDs should be considered as representing interictal/irritative brain injury versus ictal/peri-ictal LPDs, a set of criteria, with both clinical/neuroimaging and EEG, is proposed. Among them, the dichotomy LPDs-proper versus LPDs-plus should be retained. Spiky or sharp LPDs followed by associated slow after-waves or periods of flattening giving rise to a triphasic morphology should be included in the definition of LPDs-plus. We propose defining a particular subtype of LPDs-plus that we call "LPDs-max". The LPDs-max pattern corresponds to an ictal pattern, and therefore, a focal non-convulsive status epilepticus, sometimes associated with subtle motor signs and epileptic seizures. LPDs-max include periodic polyspike-wave activity and/or focal burst-suppression-like patterns. LPDs-max have a posterior predominance over the temporo-parieto-occipital regions and are refractory to antiseizure drugs. Interpretations of EEGs in critically ill patients require a global clinical approach, not limited to the EEG patterns. The clinical context and results of neuroimaging play key roles.

Benign EEG variants in the sleep-wake cycle: A prospective observational study using the 10-20 system and additional electrodes.

OBJECTIVES: To study the prevalence of benign EEG variants (BEVs) in the sleep-wake cycle among 1163 consecutive patients. METHODS: Prospective, observational EEG study using the 10-20 system with systematically two additional anterior-temporal electrodes. Depending on clinical indications, other electrodes were added. REM sleep identification was based on its characteristic EEG grapho-elements and rapid eye movements, clearly detectable with the additional anterior-temporal and fronto-polar electrodes due to eye proximity. The video-EEG monitoring duration was between 24hours and eight days. RESULTS: We identified 710 patients (61%) with BEVs. Positive occipital sharp transients of sleep (POSTs) were observed in 36.4% of participants, mu rhythm in 22.4%, lambda waves in 16.7%, wicket spikes (WS) in 15%, 14- and 6-Hz positive bursts in 8.3%, benign sporadic sleep spikes (BSSS) in 3.3%, rhythmic mid-temporal theta burst of drowsiness (RMTD) in 2.15%, midline theta rhythm in 2.1% and six-Hz spike and wave (SW) bursts in 0.1%. WS and RMTD were present during wakefulness, NREM (14.1%, 1.3%, respectively) and REM sleep (3.3%, 1.1%, respectively). Mu rhythm was also observed during NREM (1.5%) and REM sleep (7.7%). Fourteen- and 6-Hz positive bursts were present during NREM (4.5%) and REM sleep (6.5%). BSSS and six-Hz SW bursts were only observed during NREM sleep. CONCLUSIONS: The prevalence of BEVs is much higher than current estimates. POSTs and WS can no longer be considered as unusual patterns but physiological patterns of NREM sleep. RMTD and mu rhythm may be observed during NREM and REM sleep.

Epilepsy with eyelid myoclonias (Jeavons syndrome): An electro-clinical study of 40 patients from childhood to adulthood.

PURPOSE: To describe the typical and atypical clinical and electroencephalographic (EEG) features of 40 patients with Jeavons syndrome (JS). METHOD: Retrospective analysis from two French tertiary centers. RESULTS: Forty patients were enrolled (31 females and 9 males; sex ratio F/M = 3.44; mean age at epilepsy onset: 6.2 ± 3.4 years [range: 1-15 years]). A positive family history of generalized genetic epilepsy was reported by 13 patients (32.5 %). Eyelid myoclonias with or without absence were the seizure onset in 29 patients (72.5 %), and generalized tonic-clonic seizures in 11 (27.5 %). Over the course of the disease, all had absences. Intellectual disability and psychiatric disorders were reported in 14 (35 %) and 18 patients (45 %), respectively. Focal EEG abnormalities were observed in 65 % of patients, with a posterior (57.7 %) or anterior (30 %) distribution. Generalized EEG discharges were identified in 37 patients (92.5 %). Epileptiform abnormalities were activated during NREM sleep and increased upon awakening. Response to intermittent light stimulation (ILS) was observed in 34 patients (85 %), with an unusual pattern of epileptiform abnormalities at the same frequency of the flashes in 20 patients. Patients with all seizure types were more likely to have this response (p = 0.017). CONCLUSION: JS is a lifelong genetic epileptic syndrome with onset in childhood, female preponderance, and a positive family history of epilepsy in one-third of the cases. Focal EEG abnormalities are frequent. Response to ILS appears different from other photosensitive syndromes, with an unusual pattern of photo-induced abnormal synchronization. Intellectual disability and psychiatric disorders are not rare.

How to carry out and interpret EEG recordings in COVID-19 patients in ICU?

There are questions and challenges regarding neurologic complications in COVID-19 patients. EEG is a safe and efficient tool for the evaluation of brain function, even in the context of COVID-19. However, EEG technologists should not be put in danger if obtaining an EEG does not significantly advance diagnosis or change management in the patient. Not every neurologic problem stems from a primary brain injury: confusion, impaired consciousness that evolves to stupor and coma, and headaches are frequent in hypercapnic/hypoxic encephalopathies. In patients with chronic pulmonary disorders, acute symptomatic seizures have been reported in acute respiratory failure in 6%. The clinician should be aware of the various EEG patterns in hypercapnic/hypoxic and anoxic (post-cardiac arrest syndrome) encephalopathies as well as encephalitides. In this emerging pandemic of infectious disease, reduced EEG montages using single-use subdermal EEG needle electrodes may be used in comatose patients. A full 10-20 EEG complement of electrodes with an ECG derivation remains the standard. Under COVID-19 conditions, an expedited study that adequately screens for generalized status epilepticus, most types of regional status epilepticus, encephalopathy or sleep may serve for most clinical questions, using simplified montages may limit the risk of infection to EEG technologists. We recommend noting whether the patient is undergoing or has been placed prone, as well as noting the body and head position during the EEG recording (supine versus prone) to avoid overinterpretation of respiratory, head movement, electrode, muscle or other artifacts. There is slight elevation of intracranial pressure in the prone position. In non-comatose patients, the hyperventilation procedure should be avoided. At present, non-specific EEG findings and abnormalities should not be considered as being specific for COVID-19 related encephalopathy.