A Handy EEG Electrode Set for patients suffering from altered mental state
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1 J Clin Monit Comput (2015) 29: DOI /s ORIGINAL RESEARCH A Handy EEG Electrode Set for patients suffering from altered mental state Pasi Lepola Sami Myllymaa Juha Töyräs Taina Hukkanen Esa Mervaala Sara Määttä Reijo Lappalainen Katja Myllymaa Received: 29 April 2014 / Accepted: 24 December 2014 / Published online: 10 January 2015 Springer Science+Business Media New York 2015 Abstract Although electroencephalography (EEG) is an important diagnostic tool for investigating patients with unexplained altered mental state (AMS), recording of emergency EEG is not a clinical routine. This is mainly due to the cumbersome electrode solutions. A Handy EEG Electrode Set consists of ten EEG, two EOG, two ground and two commutative reference hydrogel-coated silver wire electrodes attached to a thin polyester carrier film. The clinical usefulness of the Handy EEG Electrode Set was tested in 13 patients (five females, eight males) with AMS. EEG recordings were conducted at the same time with a standard electrode set. The registration in the first patient case without the behind-ear electrodes (T9 and T10), indicated that these electrodes are very crucial to provide clinically relevant information from posterior regions of brain. In following 12 cases, the sensitivity and specificity for detecting EEG abnormality based on the Handy EEG Electrode Set recordings were 83 and 100 %, respectively. The Handy EEG Electrode Set proved to be P. Lepola (&) J. Töyräs T. Hukkanen E. Mervaala S. Määttä K. Myllymaa Department of Clinical Neurophysiology, Kuopio University Hospital, POB 100, Kuopio, Finland pasi.lepola@uef.fi P. Lepola S. Myllymaa J. Töyräs R. Lappalainen Department of Applied Physics, University of Eastern Finland, POB 1627, Kuopio, Finland S. Myllymaa R. Lappalainen SIB Labs, University of Eastern Finland, POB 1627, Kuopio, Finland E. Mervaala Institute of Clinical Medicine, Faculty of Health Sciences, University of Eastern Finland, POB 100, Kuopio, Finland easy to use and to provide valuable information for the neurophysiological evaluation of a patient suffering from AMS. However, further studies with larger number of patients are warranted to clarify the true diagnostic accuracy and applicability of this approach. Keywords EEG Electrode Hydrogel Emergency EEG Altered mental state Status epilepticus 1 Introduction The electroencephalogram (EEG) is the method of choice for revealing abnormalities in brain electrical activity. Particularly, it is considered specific in the diagnostics of epilepsies [1]. Furthermore, recording of emergency EEG is a clinically crucial tool e.g., in patients with an unexplained confusion state or acute impairment of consciousness [2 7]. Emergency EEG has an important role together with other imaging modalities in many clinical situations including diagnostics of non-convulsive status epilepticus (SE) after treatment of convulsive status, breakthrough seizures after treated SE, as well as evaluations in patients with chronic epilepsy, acute head trauma, and psychogenic seizures [8]. The early application of continuous electroencephalography (ceeg) is of special importance in the detection and treating of non-convulsive seizures after a brain injury, because typically these kinds of seizures occur within the first 48 h after injury [9 11]. Furthermore, mortality has been reported to increase with the duration of seizure activity [12]. Since more than 90 % of seizures in comatose patients are non-convulsive, it has been recommended that ceeg monitoring should be a part of the routine evaluation of comatose patients [13, 14]. Towne et al. [14] detected non-convulsive SE in 8 % of 236
2 698 J Clin Monit Comput (2015) 29: patients, with coma but without any clinical signs of seizure, who underwent EEG within 3 days of coma onset. Quantitative EEG measurements can help to detect regional ischemia and in that way EEG can help in the prognosis after cardiac arrest [15, 16]. In addition, EEG has been claimed to be useful in the acute triage evaluation as soon as the patient is admitted to the emergency room (ER) [3]. Although the clinical importance of EEG has been proven, there are impediments to the routine use of emergency EEG due to impractical electrode solutions. Most commercially available electrodes require special expertise and skills, as well as skin preparation in order to achieve a sufficient signal quality for recording [2, 8]. Furthermore, fullmontage EEG electrode sets cannot be attached if the patient is suffering from open head trauma or if the patient s head is unmovable, e.g., due to acute head or neck injury. This is a major drawback as head or neck injuries are often clinically suspected in an unconscious patient arriving to ER. It is also complicated to attach full-montage EEG set in patients with craniotomy and in patients with other implanted measuring instruments (e.g., brain pressure measurement or cerebral microdialysis). To solve these problems, below hairline EEG recording solutions have been introduced. For example, Young et al. [13] introduced a four-channel and Kolls and Hussain [17] a six-channel below hairline EEG set. However, we suppose that in some situations, six electrodes may be too few for accurate diagnosis (e.g., detection of hemispheric asymmetry) [18]. In our recent paper, a forehead EEG electrode set was introduced [18] with ten EEG electrodes, two EOG electrodes and an ECG electrode. We tested it successfully in two patients with suspected Creutzfeld Jacob disease and SE. In this paper, we introduce a further development, a more comprehensive electrode set for emergency EEG. In particular, we wanted to examine the possibility of recording EEG signals from the posterior part of the brain with extra electrodes behind the ears. Due to these posterior electrodes we have no longer only a forehead electrode set, and therefore it is now referred to as the Handy EEG Electrode Set. Finally, we evaluated the performance and the usefulness of the Handy EEG Electrode Set in the diagnosis and management of 13 clinical patients with altered mental state (AMS) in the ER and the intensive care unit (ICU). 2 Materials and methods 2.1 Handy EEG Electrode Set The Handy EEG Electrode Set was developed and iterated into a fully functional device during a 3-year trial period. The detailed description of the original electrode construction and its initial development has been presented in our earlier paper [18]. However, the electrode layout was optimized for this study based on discussions with several specialists in clinical neurophysiology working in Kuopio University Hospital (KUH). This electrode set consists of ten EEG, two EOG, two ground and two reference hydrogel-coated silver wire electrodes attached to a solid, thin polyester carrier film (Fig. 1). Electrocardiogram was recorded with a separate electrode attached to the patient s chest. The electrodes were constructed by attaching pieces of pure silver wire (Ag 99.9 %, Ø: 0.4 mm) to cables widely used in biosignal monitoring (Ambu A/S, Ballerup, Denmark). The ends of the silver wires were covered with round-shaped pieces of hydrogel membrane (AG602, Amgel Technologies, Fallbrock, CA, USA), 18 mm in diameter, to improve the skin electrode contact. Although hydrogel adheres tightly to the skin, the attachment was sometimes ensured with Omnifix medical grade tape (Hartmann Inc., Rock Hill, SC, USA). 2.2 EEG recordings The EEG recordings were carried out in the Departments of Anesthesiology and Intensive Care, Clinical Neurophysiology, Emergency and Neurology in Kuopio University Hospital (Kuopio, Finland) by an experienced EEG technician. The recordings were performed during a 1-year time period in randomly selected days and the first patient of the day referred for emergency EEG was selected to this study. Thirteen patients (five females, eight males) with AMS were randomly selected for the study. Three different commercial EEG monitoring devices, SystemPlus LTM (Micromed S.p.A., Treviso, Italy), Comet XL (Grass Technology, West Warwick, RI, USA) and Aura (Grass Technology) were applied. A conventional full-montage EEG recorded with twenty-one gold-over-silver scalp surface electrodes (Grass Technology) positioned according to the international set and affixed with EC2 Genuine Grass Electrode Cream was used for comparison. The Handy EEG Electrode Set was attached simultaneously with the set, being positioned below the hairline of the patient. Both electrode sets included separate ground and reference electrodes. The ground electrode of the set was on forehead and the reference electrode was on vertex (Fcz), while with Handy EEG Electrode Set reference and ground electrodes were on forehead (Fig. 1). However, using the different reference electrodes is not critical for comparison of the set and the Handy EEG Electrode Set, since bipolar montages were used. Before attachment of the Handy EEG Electrode Set the skin of the patient was cleaned by wiping it gently with an ethanol soaked cotton pad. The electrode impedances were monitored and the quality of the raw signal was determined by visual inspection on the computer screen. The same
3 J Clin Monit Comput (2015) 29: Fig. 1 A schematic illustration of the whole electrode set consisting of ten EEG, two EOG, two ground and two reference hydrogel-coated silver wire electrodes attached to a solid, thin polyester carrier film. Electrocardiogram was recorded with a separate electrode attached to filter parameters ( Hz) were configured on both recording software, effectively diminishing the effect of difference in sampling frequencies of Grass and Micromed devices (200 and 256 Hz). The simultaneously started EEG recordings lasted from 20 min up to 2 days depending on the reason for the referral. Two experienced EEG specialists (EM and SMä) reviewed independently the Handy EEG Electrode Set recordings according to the clinical referral. They were unaware of findings in routine EEG recordings. The clinical referral questions for EEG were known. For the EEG interpretation, they used SystemPlus Evolution (Micromed S.p.A., Treviso, Italy) and Twin EEG (Grass Technology, West Warwick, RI, USA) softwares enabling notch and band-pass filters. The EEG recordings were analysed and interpreted along normal clinical guidelines. The whole data sets were analysed regardless of their duration. First, they reviewed all the Handy EEG Electrode Set recordings and a few days later all recordings with the set. EEG findings obtained with the set were compared from patient to patient in order to determine the inter-rater agreement. This procedure ensures that both of the specialists had made the same findings with the set, the patient s chest (a), a close-up image of an individual electrode (Sp1) (b), the sites of electrode placements on the patient s head (c) and a model wearing the Handy EEG Electrode Set (d) which was used as a reference. The essential EEG findings from both EEG sets were collected into separate tables. Subsequently, they compared the obtained findings. Findings with the Handy EEG Electrode Set were true positive (TP) if a positive finding was correctly identified when comparing with the findings obtained with the reference set. They were true negative (TN) if correctly identified as negative. If a finding was incorrectly identified, it was designated as a false positive (FP) or false negative (FN). The results were used in the calculation of average sensitivity and specificity for EEG abnormality. The study protocol was reviewed by the local ethical committee (Kuopio University Hospital Ethical Committee, favorable opinion 10/2011) and VALVIRA (Finnish National Supervisory Authority for Welfare and Health, permission 166/2011). 3 Results With the standard set 100 % inter-rater agreement was reached. The EEG specialists were able to reply correctly to the referral question in 11 or 12 cases out of 12
4 700 J Clin Monit Comput (2015) 29: based on the Handy EEG Electrode Set recordings (Table 1, cases #2 #13). The average sensitivity and specificity for detecting EEG abnormality based on the Handy EEG Electrode Set recordings were 83 and 100 %, respectively. Note that there were no FP cases. If there was difference between findings, it was mentioned in the EEG interpretations and notes column of the Table 1. The registration in case #1 differs from others because the reduced electrode set without T9/T10 electrodes was used. Posterior quadrant EEG discharges were missed because the setup used in this registration did not have the electrodes placed behind the ear. Several EEG phenomena and disturbances could be detected with the Handy EEG Electrode Set: hemispheric asymmetry, diffuse slowing of background activity, spike-slow-wave complexes, periodic lateralizing epileptiform discharges (PLED), triphasic waves and burstsuppression pattern (Table 1). The longest SE monitoring lasted 48 h. According to the visual observation of the EEG specialist signal quality remained excellent over the whole 48 h monitoring period. In several of the referrals, the most important clinical issue was to clarify or rule-out whether a patient was in SE. In all cases except for case #1 (in which the reduced EEG electrode set was used); the specialists were able to diagnose or exclude SE based on the Handy EEG Electrode Set recording (Fig. 2). A typical SE finding is presented in Fig. 3 (case #11). In case #6, it was impossible to use the standard set because of large hemispheric craniotomy which had been performed due to massive brain swelling. Nonetheless, the Handy EEG Electrode Set was capable of recording the EEG from this patient (Fig. 4). This patient did not suffer SE, but displayed a diffuse slowing of background activity. Since the Handy EEG Electrode Set consists of ten EEG channels, it was also possible to detect and recognize hemispheric asymmetry (cases #2, #8 and #13). Interesting observations were made in case #13, in which the standard set did not reveal any EEG discharges, but with the Handy EEG Electrode Set discharge-like activity was seen in the area of the Af7 electrode, an electrode position not included in the standard set. Based on the subjective estimations of the experienced EEG specialists the Handy EEG Electrode Set provides the same signal quality as the standard set and recorded EEG does not contain significantly more artifacts. 4 Discussion The present study describes the further development and clinical evaluation of a novel disposable Forehead EEG Electrode Set introduced previously [18] and now used in ER and ICU. Based on the present results the major advantages of the Handy EEG Electrode Set include: it is very easy and fast to apply, and it does not require specialist level neurophysiological expertise to attach, but provides the same signal quality as the standard scalp EEG. We demonstrated that experienced EEG specialists were able to diagnose almost all of the referred clinical cases purely based on the data obtained from the Handy EEG Electrode Set recordings. In case #1, the posterior quadrant EEG discharges were missed, because the version of the Handy EEG Electrode Set applied in that patient did not include electrodes being placed behind the ears. Subsequently, the behind-ear electrodes were incorporated into the Handy EEG Electrode Set. Due to the poor signal quality caused by power-line interference, interpretations differed and both specialists would have required re-registration in case #3 to ensure interpretation. The power-line interference was probably resulted from high impedance of the aged hydrogel electrodes. Although experienced EEG specialists reviewed recordings with both EEG sets, it should be noted that the Handy EEG Electrode Set recordings were reviewed first. In addition, the reviewers were unaware of the possible findings in routine EEG, nor the patients ultimate clinical diagnosis. The present results indicate that the Handy EEG Electrode Set may be a useful screening tool when evaluating patients with AMS in ER. We also demonstrated that the Handy EEG Electrode Set was practical for long-term monitoring of SE and for assessing the therapeutic burst-suppression pattern (case #10) in the ICU. The significance of short-term emergency EEG in ER for patients with an unexplained confusion state has been recognized in a number of recent publications [2 7]. For example, Ricardo et al. [5] studied 65 patients with acute impairment of consciousness in the ER and ICU, and found epileptic activity in the EEG from almost half of them (44.7 %). Even though there is a high prevalence of epileptic activity in patients with acute impairment of consciousness, EEG is underused in acute emergency situations. Importantly, Ricardo et al. [5] reported that treatment was changed in 72.2 % of the patients after inspection of the EEG recording. Although EEG recording will not always change the patient s planned treatment, it has been claimed that it will definitely help to speed up the diagnosis and the patient s access to the appropriate treatment [7]. It has been shown that the EEG registration for as short a time as 5 min in many cases is sufficient to improve patient treatment in emergency care [7]. Recently, commercially available full-montage quick electrode sets have been introduced for emergency use (e.g., Hydrodot EzeNet and Statnet ). The short installation times achieved with those approaches is based on the use of pre-gelled electrodes requiring no special skin
5 J Clin Monit Comput (2015) 29: Table 1 Clinical characteristics and referral of patients. Possibility to answer to the clinical referral on the basis of data obtained with the Handy EEG Electrode Set. Essential EEG findings with the Handy EEG Electrode Set, related relevant notes and correspondence of interpretation between the set are also commented in the EEG interpretation and notes column. Differences between EEG interpretations are marked with numbers ( 1 4 ) Case # /unit Age Gender Length of EEG Clinical referral The Handy EEG Electrode Set findings (Reviewer 1/Reviewer 2) EEG interpretation and notes 1/ICU 83 M 20 min Subarachnoid haemorrhage. Altered mental state and occasional left hand and eyelid jerks. Rule out SE 2/ICU 50 M 15 h In EEG-confirmed SE, treated, SE resolved? 3/ICU 50 M 19 min Clinically in SE, treated, SE resolved? 4/ICU 69 M 45 h Clinically in SE, treated with general anesthesia, SE resolved? 5/ND 79 F 20 min Alzheimer s disease with rightsided ICH. Rule out SE 6/ICU 62 F 30 min Large subarachnoid haemorrhage. Craniotomy, posterior fossa decompression. Rule out SE 7/ND 64 M 15 min Previous SE a month ago. Found in asystole, resuscitated. Left cheek fasciculation. Rule out SE 8/ICU 34 M 26 min Infratentorial glioma operated, shunt. Rule out SE 9/ER 74 F 20 min Left limbs weak, in CT right acute ischemic lesion. Rule out SE 10/ICU 62 M 20 min Parkinson s disease. Resuscitated, ROSC 28 min. Hypothermic treatment. Rule out isoelectric EEG 11/ND 80 F 21 min Acute confusion, intermittent eye deviation. Rule out SE 12/ER 81 M 21 min Intermittent aphasia or jargon. Rule out SE 13/ER 55 F 20 min Operated frontal malignant tumor, speech difficulties. Rule out SE FN 1 /FN 1 TP/FN 2 TN 3 /TN 3 TP/TP TP/TP TN 4 /TN 4 Abnormal, diffuse slowing of background activity. No evidence of SE set: discharges at occipital regions that were not seen with the reduced Handy EEG Electrode Set without the behind-ear electrodes Diffuse slowing of background activity, periodic bursts or theta/delta activity. Hemispheric asymmetry. No SE anymore Reviewer 1: Strongly abnormal. Continuous discharge at T9. Still in SE 2 Reviewer 2: Too bad signal to noise ratio to rule out SE. Due the power-line interference, both specialists would have required a re-registration to ensure interpretation set: Still in SE Long-term EEG monitoring. Diffuse slowing of background activity. No SE set: The same EEG interpretation Diffuse slowing, encephalopathic abnormalities, no discharges. No SE Diffuse slowing of background activity. No SE set: impossible to perform due to craniotomy 3 The Handy EEG Electrode Set was the only way to measure EEG Monotonic GPED. Anoxic brain injury, but not SE Diffuse slowing of background activity and hemispheric asymmetry. No SE Diffuse slowing of background activity. No SE Burst-suppression EEG, with left-sided attenuation. Jerks during bursts Continuous bilateral epileptic discharges. Reacts to medication (i.v. benzodiazepine). Confirms SE Diffuse slowing of EEG. No SE Hemispheric asymmetry, frontally slowing over left side. No definite SE 4, but the Handy EEG Electrode Set s Af7 showed abnormal waveforms, which did not appear with set. Possibly it is cerebral origin CT computed tomography, EEG electroencephalography, ER emergency room, F female, FN false negative, FP false positive, GPED generalized periodic epileptiform discharge, ICH intracerebral hemorrhage, ICU intensive care unit, M male, ND department of neurology, ROSC return of spontaneous circulation, SAH subarachnoid hemorrhage, SE status epilepticus, TN true negative and TP true positive
6 702 J Clin Monit Comput (2015) 29: Fig. 2 Recorded EEG samples of 83 year old man (case #1) with set (a) and the Handy EEG Electrode Set (b). Discharges at posterior quadrant regions (framed areas) that were detected with the set were not seen with the Handy EEG Electrode Set. Note also preparation. These electrodes have a solid structure being mounted for standard fitting with a flexible body adapting easily to the shape of the skull. However, the pregelled electrodes may be prone to electrode contact related shortcomings. Firstly, it may be difficult to maintain good electrode contact through the hair for an extended period of time. Secondly, since the electrodes are not glued to the the cardiac dysrhythmia in the ECG channel. This is an example how useful it is to present the ECG with the EEG. After this registration, electrodes behind the ears and ECG electrode were added to the Handy EEG Electrode Set skin they may move easily out of their correct positions, especially in the case of restless patients. Thirdly, fullmontage sets may not be suitable for patients with craniotomy or in a patient who has other implanted measuring instruments in the head area (e.g., intracranial pressure measurement or cerebral microdialysis). Furthermore, if the patient s head is unmovable, e.g., due to suspicion of
7 J Clin Monit Comput (2015) 29: Fig. 3 Simultaneously recorded EEGs of 80 year old female (Case #11) with set (a) and the Handy EEG Electrode Set (b). Continuous bilateral epileptic discharges were detected with both electrode sets head or neck injury, it may not be possible to attach the standard electrode sets. This represents a major handicap for many of the unconscious patients arriving in the ER. Due to the above mentioned issues, the electrode set placed below the hairline could represent a viable alternative solution. Below hairline EEG sets have been reported to be suitable for detection of various EEG disturbances such as spikes, PLEDs and thus also for detecting non-convulsive SE [13, 17, 19, 20]. Despite the fact that the signal measured below hairline is probably mixed with EEG, EOG and EMG, Young et al. [13] demonstrated 68 % sensitivity (four EEG channels) and Kolls and Husain [17] 72 % sensitivity (six EEG channels) for seizure detection with sub-hairline sets. Despite these promising results, other types of seizures, e.g., occipital seizures, will remain
8 704 J Clin Monit Comput (2015) 29: Fig. 4 EEG of 62 year old female (case #6) with large subarachnoid haemorrhage. The Handy EEG Electrode Set was the only way to measure EEG because of large craniotomy, performed in order to posterior fossa decompression. This patient did not display EEG signs of status epilepticus, but instead a diffuse slowing of background activity could be detected in the recording undetected if only frontal electrodes are used. Since in addition to its eight frontal EEG channels the Handy EEG Electrode Set has two electrodes to be placed behind the ears, it provides information also about EEG discharges restricted to posterior head regions. The fact that there are several electrodes in symmetrical positions is important for detection of hemispheric asymmetry. Without several EEG channels over both sides of the convexity, it would be impossible to judge whether the signal amplitude is decreased due to changes in the brain or is variation in the electrode skin impedances. In contrast to the current below hairline sets, the newly devised Handy EEG Electrode Set also includes ECG and EOG channels, that are useful for the recognition of artifacts. As mentioned above, EEG recorded with below hairline electrodes is easily contaminated by EMG, which is a common problem also in traditional EEG. Spectral and topographical characteristics of contaminated EMG are well known [21] and EMG may be distinguishing from EEG especially by visual inspection. In particular, human review is indispensable when processing clinical EEG [22]. Possible contamination with EMG is important issue to take into account since some of the electrodes in the Handy EEG Electrode Set are located over facial muscles. For example, Sp electrodes are attached over temporomandibular joint and EMG activity of cheek muscles can contaminate EEG when a patient smacks his/ her mouth or grinds. This can complicate interpretation of EEG even when using band-pass filtering. However, the recorded EEG was pure enough to enable to answering the clinical question (e.g., rule out SE). The Handy EEG Electrode Set could be set in less than 5 min in all cases when the setting of the electrode set took min with bridge electrodes. Placement times were estimated by an experienced EEG technician. Rapid attachment is a major advantage for example to a paramedic, who may not have either time or skills to set-up the full set in an emergency situation. Kolls et al. [23] reported that although the BraiNet TM EEG template (Jordan NeuroScience, Inc, Redlands, CA, USA) was used, 71 % of non-technologists were not able to set up the electrode set in less than 30 min. Based on the present results, we believe that the Handy EEG Electrode Set including also posterior electrodes could become a part of routine protocol in the diagnosis and management for patients with acute impairment of consciousness in the ER and ICU, especially in situations when a standard full-montage EEG is not available or applicable. We emphasize that at least ten EEG electrodes should be used and that recording of EOG and ECG is important in order to distinguish actual EEG phenomena from EEG contaminated with eye movement and pulse artifacts. Although the Handy EEG Electrode Set did show clinical potential, we recognize that our present experience is limited to only 13 patient cases. Thus, clinical studies with larger patient populations are warranted to clarify the true diagnostic value and applicability of this approach.
9 J Clin Monit Comput (2015) 29: Conclusions The Handy EEG Electrode Set showed comparable diagnostic performance with the traditional set and was found to be rapid and easy-to-use. The set consists of 12 recording, two ground and two reference hydrogel-coated silver wire electrodes attached to a solid, thin polyester carrier film. It was found to suit well to be used as a part of the routine protocol in the diagnosis and management for patients with AMS in the ER and ICU. Acknowledgments The authors would like to thank Petro Julkunen, Pekka Tiihonen, Ari Pääkkönen and staff from the Department of Clinical Neurophysiology of the Kuopio University Hospital for their contributions to this work. This study was financially supported, by the Finnish Funding Agency for Technology and Innovation (grant 70019/11, Fabrication and Commercialization of the Forehead EEG Electrode Set ), Kuopio University Hospital (EVO grants and ) and Runar Bäckström Foundation ( Electrode Array for Monitoring Electrical Activity in the Brain (2013) ). KM is supported by the Foundation for Advanced Technology of Eastern Finland, Finnish Cultural Foundation of Northern Savo and Finnish Brain Foundation. PL is supported by the Finnish Brain Research and Rehabilitation Foundation and the Instrumentarium Science Foundation. Conflict of interest The authors declare that they have no conflict of interest and the studies were performed according to current Finnish laws. References 1. Noachtar S, Rémi J. The role of EEG in epilepsy: a critical review. Epilepsy Behav. 2009;15(1): Bearden ST, Nay LB. Utility of EEG in differential diagnosis of adults with unexplained acute alteration of mental status. 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Determinants of mortality in status epilepticus. Epilepsia. 1994;35(1): Pokela M, Jäntti V, Lepola P, Romsi P, Rimpiläinen J, Kiviluoma K, Salomäki T, Vainionpää V, Biancari F, Hirvonen J, Kaakinen T, Juvonen T. EEG burst recovery is predictive of brain injury after experimental hypothermic circulatory arrest. Scand Cardiovasc J. 2003;37(3): Rosenthal ES. The utility of EEG, SSEP, and other neurophysiologic tools to guide neurocritical care. Neurotherapeutics. 2012;9(1): Kolls BJ, Husain AM. Assessment of hairline EEG as a screening tool for nonconvulsive status epilepticus. Epilepsia. 2007;48(5): Myllymaa S, Lepola P, Töyräs J, Hukkanen T, Mervaala E, Lappalainen R, Myllymaa K. New disposable forehead electrode set with excellent signal quality and imaging compatibility. J Neurosci Methods. 2013;215(1): Bridgers SL, Ebersole JS. EEG outside the hairline: detection of epileptiform abnormalities. Neurology. 1988;38(1): Bubrick EJ, Bromfield EB, Dworetzky BA. Utilization of belowthe-hairline EEG in detecting subclinical seizures. Clin EEG Neurosci. 2010;41(1): Goncharova II, McFarland DJ, Vaughan TM, Wolpaw JR. EMG contamination of EEG: spectral and topographical characteristics. Clin Neurophysiol. 2003;114(9): Ma J, Tao P, Bayram A, Svetnik V. Muscle artifacts in multichannel EEG: characteristics and reduction. Clin Neurophysiol. 2012;(8): Kolls BJ, Olson DM, Gallentine WB, Skeen MB, Skidmore CT, Sinha SR. Electroencephalography leads placed by nontechnologists using a template system produce signals equal in quality to technologist-applied, collodion disk leads. J Clin Neurophysiol. 2012;29(1):42 9.
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