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ORIGINAL ARTICLE
Ahead of print publication  

Reevaluation of the electroencephalogram recordings of patients with nonconvulsive status epilepticus by using salzburg consensus criteria


1 Department of Neurology, Istanbul Medical Faculty, Istanbul University, Istanbul; Department of Neurology, Kocaeli Public Hospital, Kocaeli, Turkey
2 Department of Neurology, Istanbul Medical Faculty, Istanbul University, Istanbul; Department of Neurology, Medical Faculty, Van Yüzüncü Yıl University, Van, Turkey
3 Department of Neurology, Istanbul Medical Faculty, Istanbul University, Istanbul; Department of Neurology, Medical Faculty, Uludağ University, Bursa, Turkey
4 Department of Neurology, Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey

Date of Submission27-Jul-2020
Date of Decision16-Aug-2020
Date of Acceptance06-Sep-2020
Date of Web Publication07-Sep-2021

Correspondence Address:
Emin Timer,
Department of Neurology, Kocaeli Public Hospital, 41300, Kocaeli
Turkey
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/NSN.NSN_127_20

  Abstract 


Objective: Nonconvulsive status epilepticus (NCSE) is a challenge to diagnose in some cases, and recently, Salzburg consensus criteria for NCSE (SCC-NCSE) were developed to contribute to clinical practice. We aimed to investigate their validity and usefulness by reevaluating the electroencephalogram (EEG) examinations of our patients in this study. Materials and Methods: We retrospectively evaluated all EEG recordings of patients diagnosed with NCSE by experienced clinical neurophysiologists in our EEG laboratory over a period of 2 years. Two neurologists trained in EEG reanalyzed all EEG data and categorized these patients as NCSE, possible NCSE, or non-NCSE using the SCC-NCSE. Results: Twenty-nine patients with a mean age of 31.5 ± 25.9 were reanalyzed. According to the SCC-NCSE, 24 patients (82.7%) were diagnosed as NCSE. Eighteen patients (62%) who fulfilled all SCC-NCSE were diagnosed as NCSE, whereas six patients (20.7%) were diagnosed only as possible NCSE. Five patients (17.3%) did not fulfill SCC-NCSE; the reasons are the lack of additional secondary criteria in 2 patients with encephalopathy, the absence of full compliance with the criteria in other 2 patients, and a diagnosis of electrical status epilepticus during sleep in the last patient. Conclusion: The results of our study show that SCC-NCSE is highly consistent with clinical practice to decide for the diagnosis of NCSE. The evaluation of NCSE according to a set of new standardized criteria is thought to be difficult in practice, but it provides a more objective assessment. Therefore, we believe that its use should be encouraged to increase experience and the possibility of correct diagnosis.

Keywords: Electroencephalogram, nonconvulsive status epilepticus, Salzburg consensus criteria



How to cite this URL:
Timer E, Yılgor A, Oguz-Akarsu E, Bebek N, Baykan B. Reevaluation of the electroencephalogram recordings of patients with nonconvulsive status epilepticus by using salzburg consensus criteria. Neurol Sci Neurophysiol [Epub ahead of print] [cited 2021 Sep 18]. Available from: http://www.nsnjournal.org/preprintarticle.asp?id=325651




  Introduction Top


Nonconvulsive status epilepticus (NCSE) is defined as a continuous epileptic activity in electroencephalogram (EEG) accompanied by altered behavior and mental state that can be distinguished from baseline without prominent motor symptoms.[1],[2],[3]

Establishing the diagnosis of NCSE correctly and manage the treatment appropriately is quite complicated as it depends on many factors such as etiology, EEG findings, and the clinical circumstances of patients. In addition, it is not always well-defined to what extent the EEG activity contributes to the clinical deterioration or ongoing neuronal activity; it may be simply a bystander of other pathophysiological processes. Therefore, the criteria of NCSE have been altered frequently in the course of time.[4],[5],[6]

A committee on epileptic seizures and status epilepticus convened at the fourth London-Innsbruck Colloquium in Salzburg (2013) and as a result of consensus, a set of criteria for the diagnosis of NCSE (Salzburg Consensus Criteria for NCSE, [SCC-NCSE]) were suggested.[7] In 2015, the American Clinical Neurophysiology Association standardized EEG terminology[8] was added to these criteria to decrease the frequency of the false-positive diagnosis of NCSE, and modified SCC-NCSE was developed.[9]

Retrospectively, Leitinger et al. showed that SCC-NCSE has great diagnostic accuracy and reliability with a high interrater concurrence. They reported that SCC-NCSE shows a high diagnostic accuracy for NCSE with high sensitivity (98%) and specificity (90%).[10] Afterward, external validation studies evaluating SCC-NCSE were published.[11],[12],[13],[14] A retrospective analysis assessing SCC-NCSE in critically ill patients showed that SCC-NCSE is highly concordant with clinical practice.[11] On the contrary, Goselink et al. showed a lower accuracy and interrater consistency in a study that retrospectively investigated SCC-NCSE.[12] Othman et al. reported high conformity between the EEG diagnosis of NCSE made by their treating neurologist and the SCC in the definite and non-NCSE, however discordance was observed in possible-NCSE.[13]

In this study, our purpose was to research the validity, usefulness, and contributions of the SCC-NCSE in clinical practice by reevaluating the EEG examinations of patients with NCSE diagnosed in our EEG laboratory over a period of 2 years.


  Materials and Methods Top


We retrospectively reviewed all routine and emergency EEG recordings of patients admitted to our EEG laboratory over a period of 2 years, between January 2015 and February 2017. The patients who have diagnosed with NCSE by experienced clinical neurophysiologists in our EEG laboratory were included in the study. The clinical neurophysiologists were all blind to the SCC when they were reporting EEG's in the above mentioned period.

All EEGs were recorded conforming to the International 10–20 System by experienced EEG technicians. Clinical information was collected from EEG request forms, medical files, and discharge summaries. If we were able to access video recordings during reanalyzing, we also examined them.

Two neurologists trained in EEG and epilepsy reanalyzed all the EEG data using the SCC-NCSE and categorized patients as definite NCSE, possible NCSE, or non-NCSE. The diagnosis was made with a consensus for each EEG recording.

If epileptiform discharges (EDs) are >2.5 Hz per s and continue at least 10 s, a diagnosis of “NCSE” is made directly. If EDs are present at the worst 10 s at a frequency of ≤2.5 Hz, or when EDs are not detected, but continuous (semi-) rhythmic delta-theta activity (RDTA) between 0.5 and 4.0 Hz is present, secondary criteria have to be present: (a) typical spatiotemporal evolution or (b) subtle clinical phenomena or (c) response after intravenous (IV) antiepileptic drug (AED) both in terms of clinical and EEG features. If there is only fluctuation in frequency, morphology, or locations of the EDs or RDTA without a clear pattern with evolution, or if there is only EEG improvement without clinical improvement after IV AEDs, only “possible NCSE” could be diagnosed. In all the other circumstances, the diagnosis of NCSE is excluded if there is a pattern of RDTA at a frequency of <0.5 Hz or the patterns do not evolve or fluctuate. An additional criterion is necessary for the diagnosis of NCSE in patients with epileptic encephalopathy: either clinical and EEG improvement after administration of IV AEDs; or the increase in frequency or prominence of defining graphoelements; and as a third option clinical deterioration when compared to baseline are needed in these cases to support the NCSE diagnosis.


  Results Top


The demographic characteristics of patients with the diagnosis of NCSE are presented in [Table 1]. Among 6050 EEG recordings over a period of 2 years, EEG recordings of 29 patients who had been diagnosed as NCSE were analyzed retrospectively using the SCC-NCSE.
Table 1: Clinical characteristics of the patients with a diagnosis of nonconvulsive status epilepticus

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According to SCC-NCSE, 24 of our patients (82.7%) had NCSE.

Among them, 18 patients (62%) fulfilled all SCC-NCSE and diagnosed as definite NCSE. EEG findings of 11 patients met the first criterion of >2.5 Hz EDs per s. EDs ≤2.5/s with typical spatiotemporal evolution were detected in two patients; EDs ≤2.5/s with subtle ictal clinical phenomena were observed in further two patients; and EDs ≤2.5/s together with clinical and EEG improvement after IV AEDs were detected in the remaining three patients, as shown in [Figure 1]. AEDs were detected in the remaining three patients.
Figure 1: Distribution of the electroencephalogram findings of our patients according to Salzburg consensus criteria-nonconvulsive status epilepticus

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There were 6 patients (20.7%) who diagnosed as possible NCSE. Two of these patients had RDTA with only EEG response without clinical improvement after IV AEDs; three of them had EDs ≤2.5/s with only EEG response but without clinical improvement after IV AEDs, and the last one of them had EDs ≤2.5/s and RDTA with only fluctuation but without spatiotemporal evolution.

On the other hand, 5 patients (17.3%) diagnosed previously as NCSE by EEG experts did not fulfill the SCC-NCSE. In two cases with epileptic encephalopathy, the diagnosis of NCSE was suspicious because the necessary additional secondary criteria could not be clearly obtained from the medical records. Two patients did not fulfill the criteria, although clinically suggesting NCSE. The last patient fulfilled the SCC-NCSE, but EEG findings as well as clinical findings are compatible with electrical status epilepticus during sleep. The distribution of patients according to SCC-NCSE is shown in [Figure 1].


  Discussion Top


Our study in 29 patients with a previous diagnosis of NCSE by clinical neurophysiologists showed that SCC-NCSE criteria are highly accordant with clinical practice to decide for NCSE diagnosis. We reevaluated EEG recordings of these patients using the SCC-NCSE, and NCSE was easily diagnosed in 24 patients (%82.7). Various combinations of SCC-NCSE were fulfilled by most of the patients.

There are some difficulties when analyzing EEGs with SCC-NCSE criteria. “Evolution in frequency” is described in SCC-NCSE as minimum two consecutive changes in the same direction by at least 0.5/s, and in order to qualify as evolution is present, a single frequency or location must continue minimum 3 cycles.[7] The EEG of a patient in our study showed that EDs frequency increased from 1 to 2/s and persisted at least 4 sec [Figure 2]a and [Figure 2]b. We think that this created confusion as to whether this pattern fulfilled the definition of evolution in one direct step or not.
Figure 2: (a and b) A representative electroencephalogram recording from patient 1 with progressive myoclonic epilepsy (PME) is shown. Epileptiform discharges frequency increased from 1 to 2/s, persisted at least 4 sec, then decreased to 1/s, (c) no electroencephalogram or clinical improvement after intravenous antiepileptic drugs but minor twitching of the mouth of this patient was stopped

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One criterion of the SCC-NCSE was the assessment of clinical findings and EEG features after IV AED treatments. In the modified SCC, it is stated that clinical and EEG changes after IV AEDs should be seen within 10 min after the administration of AEDs. Clinical improvement is described as better performance in 1 of the 5 verbal or motor commands. If no answer, the commands are repeated after tactile stimuli. EEG improvement is described as reduction to “occasional occurrence,” i.e., 1%–9% of the epoch.[8] We believe that these specifications are helpful to clinicians when documenting the response to IV AEDs. However, when we were evaluating the EEG of one patient, we observed that minor twitching of the mouth of the patient which was thought to be a subtle ictal phenomenon for us was stopped after IV AEDs in video recording [Figure 2]c. Thereafter, we wondered if this drug response of subtle ictal phenomena could be considered as a “clinical” response, too. Another thing creating confusion was the required duration of the clinical and EEG improvement which is usually not permanent. No information was given about the duration of the clinical and EEG improvement in the original paper. In some patients, we observed that clinical and EEG improvement to AED was very short [Figure 3]a,[Figure 3]b,[Figure 3]c. In such cases, clinicians may not be sure easily whether this response is a real improvement from IV AEDs.
Figure 3: (a) The electroencephalogram sample of the patient 2 who is a 9-year-old boy with mental and language problems shows epileptiform discharges ≤ 2.5/s, (b) electroencephalogram with clinical improvement was observed within 1 min after intravenous antiepileptic drugs, (c) similar electroencephalogram and clinical findings were reappeared within 3 min

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One of our intriguing patients had short-lasting but frequent episodes of loss of consciousness obtained from the medical records. The EEG revealed >2.5 Hz EDs per s, but it was not continuous for 10 s [Figure 4]a and [Figure 4]b. Therefore, the criterion of 10 s continuous EDs was not fulfilled, and absence status epilepticus could not be diagnosed according to SCC-NCSE. However, discontinuous absence SE was communicated as an exception for modified SCC-NCSE.[9] Thus, we concluded the NCSE diagnosis in this patient.
Figure 4: (a and b) In the electroencephalogram recordings from patient 3 who had frequent episodes of consciousness with a history of carbon monoxide poisoning, epileptiform discharges >2.5/s but not continuous 10 s is shown

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When compared with previous reports, there are some differences in our study. In previous studies usually, all EEGs from patients with clinically suspected NCSE were included, and the degree of concordance between the standard references and the retrospective application of the SCC-NCSE was evaluated.[12],[13] In this study, we did not aim this, we only wanted to investigate the usefulness and contributions of the SCC-NCSE in clinical practice. Therefore, we evaluated only patients who have already diagnosed with NCSE. We want to emphasize that NCSE should not be neglected with its wide clinical margins, and its EEG findings and diagnostic criteria should be evaluated with wisdom by experts. At the current state of the art, we should initially diagnose NCSE patients by a standardized means and plan their rational management as “primum nil nocere.”[15]

Our study has some limitations. It was an observational, retrospective study, and we had a small size of group with NCSE. Furthermore, there were no patients in coma or monitored in the intensive care unit. Thus, we could not provide information about the usefulness of these criteria in these patients.


  Conclusion Top


The findings of our study show that SCC-NCSE is strongly consistent with clinical practice to decide for the diagnosis of NCSE. The evaluation of NCSE according to a standardized set of new criteria may be difficult in practice, but it provides a more objective assessment and will increase knowledge, and therefore, the possibility of correct diagnosis increases.

Acknowledgments

The authors thank the EEG technicians and the patients.

Financial support and sponsorship

This work was supported by the grant of the Scientific Research Projects Coordination Unit of Istanbul University (BAP-33450).

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Trinka E, Cock H, Hesdorffer D, Rossetti AO, Scheffer IE, Shinnar S, et al. A definition and classification of status epilepticus – Report of the ILAE Task Force on Classification of Status Epilepticus. Epilepsia 2015;56:15-23.  Back to cited text no. 1
    
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Guberman A, Cantu-Reyna G, Stuss D, Broughton R. Nonconvulsive generalized status epilepticus: Clinical features, neuropsychological testing, and long-term follow-up. Neurology 1986;36:1284-91.  Back to cited text no. 2
    
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Sutter R, Semmlack S, Kaplan PW. Nonconvulsive status epilepticus in adults – Insights into the invisible. Nat Rev Neurol 2016;12:281-93.  Back to cited text no. 3
    
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Shorvon S. What is nonconvulsive status epilepticus, and what are its subtypes? Epilepsia 2007;48:35-8.  Back to cited text no. 5
    
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Beniczky S, Hirsch LJ, Kaplan PW, Pressler R, Bauer G, Aurlien H, et al. Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 2013;54:28-9.  Back to cited text no. 7
    
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Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A, Herman ST, et al. American Clinical Neurophysiology Society's Standardized Critical Care EEG Terminology: 2012 version. J Clin Neurophysiol 2013;30:1-27.  Back to cited text no. 8
    
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Leitinger M, Beniczky S, Rohracher A, Gardella E, Kalss G, Qerama E, et al. Salzburg consensus criteria for non-convulsive status epilepticus – Approach to clinical application. Epilepsy Behav 2015;49:158-63.  Back to cited text no. 9
    
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Leitinger M, Trinka E, Gardella E, Rohracher A, Kalss G, Qerama E, et al. Diagnostic accuracy of the salzburg EEG criteria for non-convulsive status epilepticus: A retrospective study. Lancet Neurol 2016;15:1054-62.  Back to cited text no. 10
    
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Gungor Tuncer O, Altindag E, Ozel Yildiz S, Nalbantoglu M, Acik ME, Tavukcu Ozkan S, et al. Reevaluation of the critically ill patients with nonconvulsive status epilepticus by using salzburg consensus criteria. Clin EEG Neurosci 2018;49:425-32.  Back to cited text no. 11
    
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Goselink RJ, van Dillen JJ, Aerts M, Arends J, van Asch C, van der Linden I, et al. The difficulty of diagnosing NCSE in clinical practice; external validation of the salzburg criteria. Epilepsia 2019;60:e88-e92.  Back to cited text no. 12
    
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Othman AS, Meletti S, Giovannini G. The EEG diagnosis of NCSE: Concordance between clinical practice and salzburg criteria for NCSE. Seizure 2020;79:1-7.  Back to cited text no. 13
    
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Krogstad MH, Høgenhaven H, Beier CP, Krøigård T. Nonconvulsive status epilepticus: Validating the salzburg criteria against an expert EEG examiner. J Clin Neurophysiol 2019;36:141-5.  Back to cited text no. 14
    
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Baykan B. Nonconvulsive status epilepticus: An intriguing, highly heterogeneous neuropsychiatric condition with blurring clinical margins, sharpening EEG criteria and still unsolved background. Noro Psikiyatr Ars 2016;53:192-3.  Back to cited text no. 15
    


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