Abstract
Background
The continuous electroencephalogram (cEEG) monitoring is recommended for critical ill patients with altered mental status, The cEEG detects seizure activity and nonconvulsive status epilepticus (NCSE) more efficiently than routine electroencephalogram (rEEG). Yet, cEEG is not widely available in many neurological intensive care units (NICU) in limited resource countries. Ideal study duration, and whether cEEG is useful and cost-effective in terms of patient outcome compared to (rEEG), is still questions under research. The main objective in our study was the relative diagnostic yield of the 2 h, prolonged EEG recording, compared to the 30-min rEEG recording in the NICU.
Results
There was no significant diagnostic yield for the 2-h electroencephalogram (EEG) over the 30-min EEG for patient with altered mental status in the NICU. Being with altered mental state in an NICU carries a poor outcome, we found that death occurred in 68.9% of patients. Acute ischemic stroke is the most common cause of altered mental status in NICU by about 53.3% of patients. Less than half of the patients (42.2%) were receiving anti-seizure medications (ASM).
Conclusions
As long as the cEEG is not available in the NICU, the 30-min EEG has a good diagnostic yield and it is almost equivalent to the prolonged 2-h EEG, and if the EEG is recommended for a longer duration, we recommend a long-term EEG more than 2 h.
Similar content being viewed by others
Explore related subjects
Find the latest articles, discoveries, and news in related topics.Background
The incidence of seizures in critically ill patients is ranged from 8% to 34% based on continuous electroencephalogram (cEEG) [1] The most common conditions associated with seizure in critical illness include a pre-existing history of epilepsy, direct central nervous system (CNS) insults, metabolic derangements, and drug withdrawal or intoxication [2] In critically ill patients with seizures, status epilepticus (SE) must be anticipated [3]. The cEEG detects seizure activity and nonconvulsive status epilepticus (NCSE) more efficiently than routine electroencephalogram (rEEG) [4]. Both European Society of Intensive Care Medicine [2] and American Clinical Neurophysiology Society [5] suggest cEEG for critically ill patients with altered consciousness [5]. There are a lot of unanswered questions related to cEEG monitoring, including the ideal study duration, whether therapy of particular EEG patterns without clinical correlation is necessary, and whether cEEG is useful and cost-effective in terms of patient outcome [6]. Such efforts and costs may be justified if the results of cEEG lead to treatment modifications and why not it might improve the outcome [7]. Therefore, on the basis of being in a limited resource, country and the cEEG are not available, yet in our neurological intensive care unit (NICU), the main objective in our study was about the relative diagnostic yield of the 2 h, prolonged EEG recording, compared to the 30-min rEEG recording in the NICU.
Methods
The study is cross-sectional analytic study of 45 consecutive patients, between 16 November 2021 and 25 July 2022, who suffered from altered mental status, whether at the presentation or during the hospital stay, defined as any deviation from the baseline level of consciousness ranged from mild confusion till deep coma, of any age and sex, excluding patients who were on sedation during the 24 h before the EEG recording as it will affect the EEG results. A written informed consent was obtained from patients’ first degree relative. The scales used in the clinical assessment of altered mental state are Glasgow coma scale (GCS), Full Outline of Un-Responsiveness score (FOUR score), and Modified Rankin score on discharge (mRS) in patients with ischemic stroke. All the patients underwent a 30-min EEG followed by a 2-h EEG under the same settings (once the EEG was available). All recorded EEGs were evaluated according to the latest standardized American Clinical Neurophysiology Society guidelines (ACNS) for the EEG terminology in the critical care settings, 2021 Version [8], by an expert clinical-neurophysiologist blinded to the clinical data. EEG was recorded digitally using Nicolet vEEG system (Viasys Neurocare ISO 13485) with V32 Amplifier (16 bits digital converter, 32 channel input, bandwidth 0.5–70 Hz, channel crosstalk < 40 dB). 21 scalp electrodes placed according to the international 10–20 system. Data were analyzed using Statistical Package for the Social Sciences (SPSS) version 28. Numerical data were summarized as mean ± standard deviation or median (range), while qualitative data were presented as percentage number (%). Comparisons between EEG ½ and EEG 2 h were done using McNemar test. Probability value (p value) equal to or less than 0.05 is considered significant.
Results
The study included 45 patients, 40% were males and 60% were females. The median age of the participants was 63 years ranging from 19 to 84 years (Table 1). Almost all of the participants (82.8%) were non-smokers. About one-third of the participants were diabetic and hypertensive. Thirteen percent of the participants suffered from metabolic syndrome mostly of renal origin. Previous psychiatric illness and cognitive impairment were present only in a small percentage of cases 6.7% and 13.3%, respectively. While, history of ischemic heart disease was present in about 17.8%; half of them had a history of myocardial infarction (MI) or coronary artery stenting. Finally, Atrial fibrillation was detected in about 20% of the participants. The most common aetiology among participants was ischemic stroke (53.3%), followed by post ictal state in patients presented by serial fits with altered consciousness (13%), less commonly, CNS inflammatory condition, haemorrhagic stroke, cerebral venous thrombosis, metabolic derangement and neuromuscular respiratory failure (Fig. 1). Glasgow coma scale (GCS) during the EEG revealed that more than two-third of the patients (66.7%) were classified as GCS ≥ 8 and the Full Outline of Un-Responsiveness score (FOUR score) showed a median of 13 points (range 0–16). Computerized tomography (CT) brain was done for almost all patients (91.1%). Abnormal CT brain finding was detected among 80.5% of the patients (Fig. 2). Right and left middle cerebral artery (MCA) with oedema was the most common reported CT brain abnormality (18.2%). Regarding treatment history during the hospital stay less than half of the patients (42.2%) were on anti-seizure medications, mostly combined 52.6%, monotherapy in 47.4% (levetiracetam 36.8%, carbamazepine 5.3%, or phenytoin 5.3%, 15.6% of the patients received specific immune therapy, 93.3% were receiving intravenous antibiotics due to recurrent chest or urinary tract infections. Less than half of the patients (46.7%) were investigated by magnetic resonance imaging (MRI) brain and abnormal finding of MRI was detected in (90.5%) of the participants. The median duration of intensive care unit (ICU) stay was 15 days, ranging from 2 to 70 days. The median duration to obtain an EEG recording for patient with altered mental status (AMS) was 4 days. Regarding modified Rankin score on discharge (mRS), about two-third of the participants 68.9% were dead on discharge. The good outcome (mRS 0:1) was obtained in 8.9% of patients and the rest (about 22.2%) of the patients were discharged with variable degrees of disability. The comparison between the 30-min EEG and the 2-h EEG revealed that, there was no significant difference between the 30-min EEG and 2-h EEG regarding symmetry, posterior dominant alpha with eye closure, voltage EEG and anterior-to-posterior (AP) gradient p value (1.000, 1.000, 0.233 and 0.607, respectively) (Table 2). Regarding Predominant background frequency, 30-min EEG detects predominant Beta activity in 11.1% of patients and Delta activity in 6.7%, while 2-h EEG detects Beta activity in 2.2% and Delta activity in 24.4% of patients with statistically significant differences (p value = 0.036) (Fig. 3).The 30-min EEG showed absent state change in 88.9% of patients and state change without stage N2 sleep in 8.9% of the patients, while the 2-h EEG showed absent state change in 66.9% and state change without stage N2 sleep in 26.7%; with statistically significant difference (p value = 0.037) in eliciting the state change without stage N2 sleep (Fig. 4). Regarding continuity of the background: during the 30-min EEG, the background was continuous in 95.6% and suppressed in 4.4% of patients, while the 2-h EEG revealed that the background was continuous in 93.3% and suppressed in 2.2%, it also showed a burst attenuation of the background in 2.2% (only 1 patient) and attenuation in 2.2%, Regarding reactivity: it was tested only during the 2-h EEG, we found that our patients were classified as unclear in 22.2%, Reactive in 20%, Unreactive in 20%, and Unknown in 37.8% of the patients. The study did not detect any of the following: sporadic epileptiform discharges (ED), rhythmic and periodic patterns (RPPs), electrographic and electroclinical seizures/status epilepticus, brief potentially ictal rhythmic discharges (BIRDs), ictal interictal continuum (IIC) whether in the 2-h EEG or the 30-min EEG, the majority of EEGs showed variable degrees of generalized slowing.
Discussion
Both European Society of Intensive Care Medicine [2] and American Clinical Neurophysiology Society suggest cEEG for critically ill patients with altered consciousness [5]. However, it may be difficult to apply in centers lacking human and technical resources which explains why such procedure may still be underused. Although its use increased by 10 folds recently but it accounts about 0.3% of the critically ill population EEG recording [9]. The ideal study duration of cEEG is still debatable [10]. In our study, the aetiology of AMS was variable; the most common cause was acute ischemic stroke in more than half of our participants (53.3%), followed by post ictal state, accounting for 13.3% of patients, matched with the etiology of critically patients with AMS (a similar population) admitted to a neurology unit [11, 12]. The abnormal CT brain findings were detected in 80.5% of our patients in our NICU and that is close to an 89% abnormality found by Rai and colleagues in a similar population with an AMS [11]. The median duration for the length of stay (LOS) in our NICU, through our population of different aetiologies, was 15 days, ranging from 2 to 70 days, with an in-hospital mortality 68.9%. The good outcome (mRS 0:1) was obtained in 8.9% of patients, and the rest (about 22.2%) of the patients were discharged with variable degrees of disability and it was close enough to the findings of rai and colleagues [11]. The main objective for this work was to find if there is a diagnostic yield for the prolonged 2-h EEG over the routine 30-min EEG, in 45 consecutive patients with altered mental status, and we found that there is no significant diagnostic yield. The majority of our EEGs showed variable degrees of generalized slowing, indicative for a diffuse cerebral dysfunction or diffuse encephalopathy, yet it is a nonspecific feature unrelated to the underlying aetiology [13]. We failed to record any sporadic epileptiform discharges, rhythmic and periodic patterns (RPPs), electrographic and electroclinical seizures/status epilepticus, brief potentially ictal rhythmic discharges (BIRDs), ictal interictal continuum (IIC) whether in the 2-h EEG or the 30-min EEG. Generalized slowing is one of the most common findings in the critical care settings [14], even it might be the most frequent finding [15]. It is considered as one of the nine categories of the baseline EEG pattern according to cEEG monitoring [16] and it is present in half of the requested emergent EEG in the ICU [17]. It should be noted that patient with generalized slowing during the initial EEG recording are unlikely to develop seizure in the subsequent cEEG monitoring [18] and usually carries a better prognosis in comparison with low voltage EEG [13]. Therefore, our EEG findings were different that might be explained by the different methodology; in our study, we did an EEG recording for any patient suffering from AMS (whether at the presentation or during the hospital stay), so we perhaps did an EEG recording for patients who might not be otherwise indicated for EEG, and who might have a clear primary cause for their AMS. These finding were concordant with the study conducted by rai and his coworkers who underwent 1-h EEG versus 72-h EEG, there was no NCSE in any one of the 1-h EEG records and the generalized periodic epileptiform discharges (GPEDs) were seen only in 1% the patients [11]. Another study for patients with AMS in an adult (medical/surgical) ICU who underwent 30-min EEG versus 24 h of continuous video-EEG (cvEEG) monitoring; no epileptiform findings was found during the first 30 min cvEEG monitoring in 66% of patients [10]. In addition, it is still debatable if electrographic seizures, periodic discharge (PD) or NCSE indicate the severity of an underlying disease or whether these abnormalities independently correlate towards an unfavorable patient outcome [7, 19]. Keeping in mind that seizures, independent of the illness severity, are associated with increased morbidity, but not mortality [7]. The current literature suggests that longer duration of EEG recording increases the yield of detecting interictal epileptiform discharges, there is a retrospective study revealed that 2-h EEG has a similar yield as 30-min EEG to detect epileptiform discharges in patients with a normal 30-min rEEG, and it was 3.3% in the 30-min EEG group and 4.2% in the 2-h EEG group. Another study comparing the continuous video-EEG (cvEEG) monitoring and 30-min EEG in an adult (medical/surgical), ICU patient demonstrated that if the cvEEG is not feasible, and a 30-min EEG in the ICU has a high diagnostic yield, providing the majority of epileptiform abnormalities to be detected [10]. In our study, the comparison between the 2-h EEG and the 30-min EEG among patient receiving ASM (42.2% of cases) showed no significant difference. A more recent multicenter study underwent in Switzerland at 4 tertiary hospitals, for critically ill patients with altered consciousness and no recent seizure; cEEG leads to enhanced seizure detection and adjustment of antiseizure medication, but not improved the outcome compared the rEEG. The investigators concluded that in the absence of bigger research, rEEG might be a viable alternative to cEEG in settings with limited resources[18]. In a harmony with our study, this can be applied in NICU settings of limited resources. On the other hand, research was conducted to predict the prognosis of individuals who had altered level of consciousness owing to neurological reasons, found that cEEG (at least 72h) is useful for detecting subclinical seizures, predicting outcomes, and perhaps monitoring the clinical status and responsiveness to therapies such as intravenous antiseizure medication in patients with altered consciousness. This makes cEEG a superior tool for detecting and managing nonconvulsive seizures than single rEEG or serial rEEG recordings [11]. Another more recent research revealed that, the odds of in-hospital death were lower in the cEEG group compared to controls but was not associated with a lower risk of in-hospital death. Taking in consideration that, the use of cEEG was linked to a higher median total hospitalization fee and a longer median hospital stay [9] Although the EEG is an important tool for determining prognosis after cardiac arrest, cEEG has no advantage over intermittent rEEG in terms of outcome in cardiac arrest patients and has no effect on the time to death [17]. In our study, there were 7 patients with GCS 3/15 and FOUR score zero at the initiation of EEG recording, analysis of their EEG showed no difference in the diagnostic yield between the 30-min EEG and the 2-h EEG, yet the small number of those patients limited our ability to illustrate such data statistically.
Our research was limited by the unavailability of cEEG monitoring and video EEG monitoring in our NICU, that’s why we tried to check whether the prolonged 2-h EEG is more informative than the rEEG and what is the diagnostic relative yield of the prolonged 2-h EEG compared to rEEG. This study, however, may represent a "real-life" clinical practice at several institutions lacking such necessary resources.
Conclusion
There was no significant diagnostic yield for the 2-h EEG over the 30-min EEG for patient with altered mental status in the NICU. Therefore, as long as the cEEG is not available in the NICU, the 30-min EEG has a good diagnostic yield and it is almost equivalent to the prolonged 2-h EEG and if the EEG is recommended for a longer duration, we recommend to ask for a long-term EEG more than 2 h.
Availability of data and materials
The data sets generated and/or analyzed during the current study are not publicly available due to the current Cairo University regulations and Egyptian legislation but they are available by a reasonable request from the corresponding author.
Abbreviations
- ACNS:
-
American Clinical Neurophysiology Society guidelines
- AMS:
-
Altered mental status
- AP:
-
Anterior–posterior
- ASM:
-
Anti-seizure medication
- BIRDs:
-
Brief potentially ictal rhythmic discharges
- cEEG:
-
Continuous electroencephalogram
- CNS:
-
Central nervous system
- CT:
-
Computed Tomography
- CVT:
-
Cerebral venous thrombosis
- cvEEG:
-
Continuous video-EEG
- ED:
-
Epileptiform discharges
- EEG:
-
Electroencephalogram
- FOUR:
-
Full Outline of UnResponsiveness
- GCS:
-
Glasgow Coma Scale
- GPEDs:
-
Generalized periodic epileptiform discharges
- ICU:
-
Intensive care unit
- IIC:
-
Ictal interictal continuum
- LOS:
-
The length of stay
- MCA:
-
Middle Cerebral artery
- MI:
-
Myocardial infarction
- MRI:
-
Magnetic resonance imaging
- mRS:
-
Modified Rankin score
- NCSE:
-
Non-convulsive status epilepticus
- NICU:
-
Neurological intensive care unit
- p value:
-
Probability-value number
- PD:
-
Periodic discharges
- PCA:
-
Posterior cerebral artery
- rEEG:
-
Routine electroencephalogram
- RPPs:
-
Rhythmic and periodic patterns
- RT:
-
Right
- SE:
-
Status epilepticus
- SPSS:
-
Statistical Package for the Social Sciences
- %:
-
Percentage number
References:
Westover MB, Shafi MM, Bianchi MT, Moura LM, O’Rourke D, Rosenthal ES, et al. The probability of seizures during EEG monitoring in critically ill adults. Clin Neurophysiol. 2015;126(3):463–71.
Claassen J, Mayer SA, Kowalski RG, Emerson RG, Hirsch LJ. Detection of electrographic seizures with continuous EEG monitoring in critically ill patients. Neurology. 2004;62(10):1743–8.
Strein M, Holton-Burke JP, Smith LR, Brophy GM. Prevention, treatment, and monitoring of seizures in the intensive care unit. J Clin Med. 2019;8(8):1177.
Sutter R, Fuhr P, Grize L, Marsch S, Rüegg S. Continuous video-EEG monitoring increases detection rate of nonconvulsive status epilepticus in the ICU. Epilepsia. 2011;52(3):453–7.
Herman ST, Abend NS, Bleck TP, Chapman KE, Drislane FW, Emerson RG, et al. Critical Care Continuous EEG Task Force of the American Clinical Neurophysiology Society. Consensus statement on continuous EEG in critically ill adults and children, part I: indications. J Clin Neurophysiol. 2015;32(2):87–95.
Holmes GL. To know or not to know: does EEG monitoring in the paediatric intensive care unit add anything besides cost? Brain. 2014;137(Pt 5):1276–7.
Payne ET, Zhao XY, Frndova H, McBain K, Sharma R, Hutchison JS, et al. Seizure burden is independently associated with short term outcome in critically ill children. Brain. 2014;137(Pt 5):1429–38.
Hirsch LJ, Fong MWK, Leitinger M, LaRoche SM, Beniczky S, Abend NS, et al. American Clinical Neurophysiology Society’s Standardized Critical Care EEG Terminology: 2021 Version. J Clin Neurophysiol. 2021;38(1):1–29.
Hill CE, Blank LJ, Thibault D, Davis KA, Dahodwala N, Litt B, et al. Continuous EEG is associated with favorable hospitalization outcomes for critically ill patients. Neurology. 2019;92(1):e9–18.
Khan OI, Azevedo CJ, Hartshorn AL, Montanye JT, Gonzalez JC, Natola MA, et al. A comparison of continuous video-EEG monitoring and 30-minute EEG in an ICU. Epileptic Disord. 2014;16(4):439–48.
Rai V, Jetli S, Rai N, Padma MV, Tripathi M. Continuous EEG predictors of outcome in patients with altered sensorium. Seizure. 2013;22(8):656–61.
Horsting MW, Franken MD, Meulenbelt J, van Klei WA, de Lange DW. The etiology and outcome of non-traumatic coma in critical care: a systematic review. BMC Anesthesiol. 2015;29(15):65.
Poothrikovil RP, Gujjar AR, Al-Asmi A, Nandhagopal R, Jacob PC. Predictive value of short-term EEG recording in critically ill adult patients. Neurodiagn J. 2015;55(3):157–68.
Anderson D, Jirsch JD, Wheatley MB, Brindley PG. Electroencephalogram patterns in critical care: a primer for acute care doctors. J Intensive Care Soc. 2022;23(1):58–69.
Varelas PN, Hacein-Bey L, Hether T, Terranova B, Spanaki MV. Emergent electroencephalogram in the intensive care unit: indications and diagnostic yield. Clin EEG Neurosci. 2004;35(4):173–80.
Swisher CB, Shah D, Sinha SR, Husain AM. Baseline EEG pattern on continuous ICU EEG monitoring and incidence of seizures. J Clin Neurophysiol. 2015;32(2):147–51.
Kurtz P, Gaspard N, Wahl AS, Bauer RM, Hirsch LJ, Wunsch H, et al. Continuous electroencephalography in a surgical intensive care unit. Intensive Care Med. 2014;40(2):228–34.
Rossetti AO, Schindler K, Sutter R, Rüegg S, Zubler F, Novy J, et al. Continuous vs routine electroencephalogram in critically ill adults with altered consciousness and no recent seizure: a multicenter randomized clinical trial. JAMA Neurol. 2020;77(10):1225–32.
Fatuzzo D, Beuchat I, Alvarez V, Novy J, Oddo M, Rossetti AO. Does continuous EEG influence prognosis in patients after cardiac arrest? Resuscitation. 2018;132:29–32.
Acknowledgements
The authors acknowledge subjects for their participation and cooperation in this study.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
NM: data analysis, manuscript writing and reviewing workup, ESB: analyzed research idea, data acquisition, data analysis and interpretation, MFA: performed data acquisition, data analysis and interpretation. AAT: data acquisition and interpretation and manuscript reviewing.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Ethical approval was obtained from the “Research ethical committee (REC) Cairo university Faculty of medicine, Code (MS-612-2021).
Consent for publication
Not applicable.
Competing interests
None of the authors has any conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Mounir, N., Belal, E.S., Abozeina, M.F. et al. The diagnostic yield of a 2-h versus a 30-min electroencephalogram for patients with altered mental status in neurological intensive care unit. Egypt J Neurol Psychiatry Neurosurg 60, 36 (2024). https://doi.org/10.1186/s41983-024-00809-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s41983-024-00809-9