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Key Words: EEG, Nasopharyngeal electrode, Electric source imaging, Temporal lobe epilepsy
Abstract
Purpose:
To investigate the different regions covered by nasopharyngeal (NPEs) and anterior temporal (anterior temporal electrodes [ATEs]) electrodes in assessing temporal lobe epilepsy, to overcome the limitations of the 10 to 20 electroencephalography (EEG) in diagnosing the basal and mesial temporal regions.
Methods:
EEG data from 229 patients diagnosed with temporal lobe epilepsy were simultaneously analyzed with attached NPEs and ATEs. In case of discrepancies in EEG interpretation, a consensus interpretation was reached among three epilepsy experts. Spike detection was conducted using the Curry9 program for secondary analysis of electric source localization, with source location performed using standard brain MRI data.
Results:
In total, 2,721 interictal epileptiform discharges (IEDs) from 175 patients were analyzed. Of these, 734 IEDs from 48 patients were detected exclusively with NPEs, while 1,987 IEDs from 127 patients were detected simultaneously by both NPEs and the standard international 10 to 20 electrodes system supplemented with ATEs, respectively. The former IEDs exhibited clustering dipoles in the basal and mesial temporal regions, while the latter were localized solely to the frontotemporal and lateral temporal regions.
Conclusions:
Nasopharyngeals can identify IEDs in the mesial and basal temporal region that cannot be detected by ATEs. Nasopharyngeals offer additional diagnostic value in regions not confirmed by the existing 10 to 20 EEG electrode system, including those covered by ATE.
Introduction
The international 10 to 20 electroencephalography (EEG) electrode placement guideline is considered standard in the performance of scalp EEG in both clinical practice and academic research. However, the traditional 10 to 20 electrode EEG electrode placement has several limitations in the detection of epileptiform discharges (interictal epileptiform discharges [IEDs]) arising from the inferior and mesial temporal lobes.1–3 As such, several additional electrodes, including anterior temporal (anterior temporal electrodes [ATEs]), nasopharyngeal (NPE) electrodes, sphenoidal, minisphenoidal, foramen ovale, anterior cheek, and inferior temporal electrodes have been introduced to facilitate adequate detection of temporal lobe epilepsy (TLE).4–10 Among these additional electrodes, noninvasive forms should be actively used, because they can enhance the diagnostic sensitivity of the standard 10 to 20 electrodes system simply and cost-effectively.
The combination of ATEs and NPEs with the standard 10 to 20 electrodes system can improve the diagnostic sensitivity for TLE.11 The authors previously reported that incorporating ATEs and NPEs into the 10 to 20 electrode placement system not only enhances its diagnostic sensitivity but also improves the consistency of EEG interpretations among interpreters. Specifically, visual EEG interpretation using NPEs demonstrated remarkable diagnostic sensitivity, particularly for cases of mesial TLE, such as hippocampal sclerosis or amygdala enlargement, and for nonlesional TLE.12 In addition, other researchers have reported that the detection coverage area of ATEs and NPEs is somewhat different during simultaneous subdural recording.13
Electric source imaging (ESI) is a noninvasive method with high sensitivity and specificity for localizing the epileptogenic zone, which is crucial in the evaluation preceding surgical treatment for focal brain lesions in epilepsy.14–17
Building on existing research, this study aimed to evaluate the diagnostic coverage of the ATEs and NPEs by analyzing the IEDs detected in patients with TLE using an ESI method. In addition, the detection capabilities of NPEs were compared with those of ATEs, which are widely applied in clinical practice, to assess the accuracy and effectiveness of NPEs in identifying epileptogenic zones.
METHODS
Patient's EEG Recordings
This study recruited patients diagnosed with TLE who consecutively visited the outpatient epilepsy clinic at Severance Hospital between March 2010 and March 2016. All patients were selected by a single physician (K.H.), and all TLE diagnoses were established based on ictal semiology, EEG, and brain MRI findings. Subsequently, patients were classified into presumed mesial, neocortical TLE, nonlesional TLE, or undetermined TLE subgroups according to seizure semiology, MRI characteristics, and multidisciplinary clinical consensus by the epilepsy team. Electroencephalography recordings were obtained using an EEG (AS40PLUS Amplifier System, GRASS Comet-PLUS, RI). Nasopharyngeals, flexible and insulated wires terminating in a 3-mm gold-plated ball (GRASS Technologies, RI) were used. Nasopharyngeals were placed by skillful technicians using standard placement techniques.18 Nasopharyngeal was not used in patients who were unable to cooperate, such as those with intellectual disability, pediatric patients, and psychological problems, or in patients with technical difficulties due to nasal cavity deformity, who were expected to have unsatisfactory EEG recordings. All EEG recordings were performed for >40 minutes, with ATEs and NPEs in place. One of the 230 patients who underwent the procedure complained of discomfort during NPE tracing, so the patient dropped out of the study. Therefore, 229 patients conducted EEG with NPE and ATE attached.
Patients whose initial EEGs included ictal activity were excluded. In addition, patients with IEDs in the temporal region, who were later determined to have extra TLE based on long-term EEG monitoring or epilepsy surgery, were also excluded. Finally, 11 patients diagnosed with TLE through long-term EEG monitoring or epilepsy surgery were enrolled in this study. Electroencephalography recordings were performed with ATEs and NPEs, in addition to the electrodes of the 10 to 20 system as the initial evaluation at Severance Hospital.
Visual EEG Interpretation
The EEG interpretation was performed using two different montage configurations. In the first configuration, the montage included only ATEs, in addition to the international 10 to 20 EEG electrode placement system. In the second configuration, the montage incorporated both ATEs and NPEs. Three neurologists independently interpreted the 2 sets of 229 EEG recordings (229 patients; NPEs and non-NPEs): a senior interpreter (K.H.) with 28 years of experience, and two junior interpreters (Y.H.C. and S.H.Y.), each with 4 years of experience. Both junior interpreters were certified in EEG interpretation. After performing individual EEG interpretations, final interpretations were determined through careful analysis and consensus-based discussion.
Moreover, IEDs were defined as spikes, sharp waves, polyspikes, or spike-wave discharges, typically lasting <200 milliseconds,19 which were distinguished from the normal EEG background by their morphology and/or amplitude. Normal EEG variants, including small sharp spikes and wicket spikes, were excluded from consideration as IEDs. In cases of uncertainty, a conservative approach was adopted in the interpretation. When IEDs were detected, their laterality (unilateral or bilateral independent) and the electrodes exhibiting the maximum IED amplitude were evaluated. The IED amplitudes were visually estimated as the peak-to-peak value in the Cz reference montage. Electrodes consistently demonstrating the highest IED amplitude were regarded as electrodes with maximum amplitude. In instances where different electrodes independently exhibited the highest amplitude, those electrodes were differently identified as displaying the maximum IED amplitude. For EEGs with bilateral independent IEDs, electrodes with maximum amplitude were analyzed separately for each hemisphere. In this study, the distribution of maximum amplitude of IEDs in patients with TLE was analyzed, classifying them into those detected exclusively by ATEs, those detected simultaneously by both ATEs and NPEs, those detected exclusively by NPEs, and maximum amplitude of IEDs detected by other electrodes excluding ATEs and NPEs. The authors have compiled 13 pairs of EEGs (see Data, Supplemental Digital Content 1, http://links.lww.com/JCNP/A356).
Dipole Analysis of IEDs by Source Localization
This study is a follow-up to the authors’ previous work published in NPE-related study.12 In this study, EEG data that had initially been reviewed visually in the previous study were reanalyzed using the Curry 9 program (Compumedics, Charlotte, NC) to identify IEDs. Averaging of EEG waveforms was then performed based on the confirmed discharges. Subsequently, ESI was conducted using the Brainstorm toolbox (version 3.230823) in MATLAB version 9.9.0. (R2020b). The identified data were imported into the Brainstorm toolbox, while epochs were extracted within a time window ranging from 50 milliseconds before to 50 milliseconds after the peak amplitude of the IEDs for analysis. Epochs with voltage values exceeding ±100 µV were rejected.
Although the use of a realistic head model based on each patient's individual MRI is preferable for subject-specific analysis, this study aimed to perform group-level comparisons across a large cohort. Therefore, an average MRI template was used for head modeling to ensure methodologic consistency. A standard electrode template was applied in this study to maintain uniformity in source modeling across all participants. The location of NPEs was determined based on coordinate values extracted from computed tomography imaging acquired with the electrode in situ.
The ICBM125 2009c Nonlinear Asymmetric, which is an average template of the MRI, used a default anatomy with Brainstorm. The boundary element method with OpenMEEG was applied to compute the forward model.20,21 Subsequently, the dipole modeling method was applied to estimate a solution to the linear inverse problem, using the identity as the noise covariance. Dipole modeling was applied to each time point within the epoch window to compute distributed source estimates over time. The results were then averaged across all time points for each group. After dipole modeling, dipole scanning was performed across the entire epoch window to identify, for each time sample, the dipole solution with highest goodness-of-fit. To demonstrate the impact of the NPEs, the difference in the absolute value of the distribution of clustered dipoles between the two groups was then tested.
Statistical Analysis
A chi-square test of independence was used to evaluate the association between TLE subtype (e.g., mesial vs. neocortical) and the distribution of maximum amplitude of IEDs across different electrode types (NPE max, ATE max, mixed, and others). To assess the diagnostic utility of NPE across TLE subgroups, the proportion of NPE involvement—defined as either “only NPE max” or “mixed NPE and ATE max”—was compared using chi-square tests. Pairwise comparisons between subgroups (e.g., mesial vs. neocortical TLE) were also performed using chi-square analysis. In addition, a logistic regression analysis was conducted to determine whether TLE subtype was associated with increased likelihood of diagnosis through only NPE max. All tests were two-tailed, and statistical significance was defined as P < 0.05. All statistical analyses were performed using R version 4.3.0 (R Foundation for Statistical Computing, Vienna, Austria).
IRB Approval
This study was conducted in compliance with the principles of the Declaration of Helsinki. The study protocol was reviewed and approved by the institutional review board of Severance Hospital (IRB No. 1-2017-0044).
RESULTS
Demographics and Characteristics of the Enrolled Patients with TLE
This study included 229 patients (229 EEGs), with 1 EEG excluded because of movement artifacts related to the use of NPEs. The mean age of patients at the time of the initial EEG recording was 45.0 ± 17.2 years (range: 13–88), while the mean age at disease onset was 34.0 ± 21.0 years. Among the 229 patients, interictal spikes were detected in 175 patients, who were subsequently divided into 2 groups: those with spikes detected on the standard 10 to 20 electrode system supplemented with ATEs and those in whom they were detected using NPEs.
Spectrum of the Maximum Amplitude of IEDs in Enrolled TLE
A total of 2,721 IEDs across 175 patients were identified in the study. These data were separated into two groups: IEDs detected exclusively with NPEs (734 spikes, n = 48) and IEDs detected simultaneously using both NPEs and the standard 10 to 20 electrodes system supplemented with ATEs (1,987 spikes, n = 127). Within the latter group, a subset was identified in which IEDs were observed through both ATEs and NPEs (1,659 spikes, n = 104) (Fig. 1).
FIG. 1.
Spectrum of the maximum IEDs in patients with TLE (total 2,721 spikes, N = 175). The maximum amplitude of IEDs is categorized as follows: IEDs detected exclusively by ATEs (266 spikes, n = 17), mixed maximum amplitude of IEDs detected by both ATEs and NPE electrodes (NPEs) (1,659 spikes, n = 104), IEDs detected exclusively by NPEs (734 spikes, n = 48), and maximum amplitude of IEDs detected by other electrodes, excluding ATEs and NPEs (62 spikes, n = 6). ATEs, anterior temporal electrodes; IEDs, interictal epileptiform discharges; NPE, nasopharyngeal; TLE, temporal lobe epilepsy.
In addition, IEDs were identified exclusively using NPEs and ATEs in 48 and 17 patients, respectively. The pathologic types among the 48 patients with IEDs identified only using NPEs were as follows: nonlesional (n = 17), hippocampal sclerosis (n = 10), amygdala enlargement (n = 9), cerebral encephalomalacia (n = 3), cavernous malformation (n = 3), focal cortical dysplasia (n = 2), dual pathology (n = 2), and foreign tissue lesions (n = 2). The pathologic types among the 17 patients with IEDs identified only using ATEs were as follows: hippocampal sclerosis (n = 5), nonlesional (n = 5), cerebral encephalomalacia (n = 3), amygdala enlargement (n = 2), vascular malformation (n = 1), and tuberous sclerosis (n = 1).
Distribution of Maximum Amplitude of IEDs According to TLE Subtype
Among the 175 patients with identifiable IEDs, 88 (50.3%) were classified as having mesial TLE, 29 (16.6%) as neocortical TLE, 44 (25.1%) as nonlesional epilepsy, and 14 (8.0%) as undetermined TLE.
Within the mesial TLE subgroup (n = 88), NPEs-maximum IEDs were observed in 20 patients, mixed NPEs- and ATEs-maximum IEDs in 60 patients, ATEs-maximum IEDs in 6 patients, and other electrodes-maximum IEDs in 2 patients. In contrast, in the neocortical TLE subgroup (n = 29), 7 patients exhibited ATEs-maximum IEDs, 5 had NPEs-maximum IEDs, 14 showed mixed NPEs and ATEs IEDs, and 3 had maximum IEDs recorded from other electrodes. The proportions of NPE involvement (defined as either “only NPE max” or “mixed NPE and ATE max”) were as follows: 90.9% in mesial TLE (80/88), 65.5% in neocortical TLE (19/29), 93.2% in nonlesional TLE (41/44), and 86.7% in undetermined TLE (13/15).
A χ2 test revealed a statistically significant difference in NPE involvement among the subgroups (χ2 = 24.83, df = 3, P = 0.0024), indicating that NPEs were more frequently involved in mesial and nonlesional TLE compared with other subgroups. The highest proportions were noted in nonlesional (93.2%) and mesial TLE (90.9%), suggesting increased diagnostic sensitivity of NPEs in these subtypes. And a chi-square test comparing NPE diagnostic involvement between mesial and neocortical TLE showed a statistically significant difference (χ2 = 8.94, P = 0.0028), indicating that NPEs contributed more frequently to the diagnosis in mesial TLE. These findings support the hypothesis that NPEs demonstrate higher diagnostic sensitivity particularly in mesial and nonlesional TLE. A χ2 test demonstrated a significant difference in the proportion of only NPEs-maximum IEDs (P = 0.033). In logistic regression analysis, nonlesional TLE showed a trend toward a higher likelihood of being diagnosed by only NPEs compared with neocortical TLE (OR = 3.02, 95% CI: 0.97–9.44, P = 0.057), indicating a potential subtype-specific diagnostic advantage.
Comparison of the Distribution of Clustered Dipoles Between Conventional Scalp EEG With and Without NPEs
The identified IEDs were analyzed based on dipole theory. Clustered dipoles in simultaneously detected IEDs using both NPEs and the standard 10 to 20 electrodes system supplemented with ATEs (1,987 spikes, n = 127) were primarily distributed in the frontotemporal and lateral temporal regions, excluding the mesial and basal temporal lobes. In contrast, clustered dipoles for IEDs detected exclusively through NPEs (734 spikes, n = 48) were predominantly distributed in the basal and mesial temporal regions (Fig. 2).
FIG. 2.
Comparison of the clustered dipole distribution patterns. These figures compare the distribution of clustered dipoles between scalp EEG with and without electrodes (NPEs). Clustered dipoles from IEDs detected simultaneously by both the standard international 10 to 20 electrodes system supplemented with ATEs and NPEs (1,987 spikes, n = 127) are primarily distributed in the frontotemporal and lateral temporal regions, excluding the mesial and basal temporal lobes (A–D). In contrast, the clustered dipoles for IEDs detected exclusively on NPEs (734 spikes, n = 48) are predominantly distributed in the basal and mesial temporal regions (E–F). ATEs, anterior temporal electrodes; EEG, electroencephalography; IEDs, interictal epileptiform discharges; NPE, nasopharyngeal.
Comparison of the Distribution of Clustered Dipoles Between Only ATEs and Only NPEs
The identified IEDs were analyzed through ESI. Clustered dipoles in IEDs identified only using ATEs (266 spikes, n = 17) were primarily distributed in the lateral temporal region, excluding the mesial and basal temporal lobes. In contrast, clustered dipoles for IEDs detected only through NPEs (734 spikes, n = 48) were primarily distributed in the basal and mesial temporal regions (Fig. 3). The red areas indicate regions where the maximum amplitude of IEDs was detected exclusively by NPEs. The yellow areas represent regions in which the maximum amplitude of IEDs was detected exclusively by ATEs. Supplemental Digital Content 1 (see Data, http://links.lww.com/JCNP/A356) includes four illustrative cases of individual ESI.
FIG. 3.

Comparison of the distribution of clustered dipoles between only ATEs and only electrodes (NPEs). The yellow regions correspond to IEDs detected exclusively by ATEs (266 spikes, n = 17). The red regions correspond to those detected exclusively by NPEs (734 spikes, n = 48). Clustered dipoles in IEDs identified exclusively by ATEs are primarily distributed in the lateral temporal region, excluding the mesial and basal temporal lobes. In contrast, clustered dipoles for IEDs detected exclusively by NPEs are predominantly distributed in the basal and mesial temporal regions. The red regions indicate only epileptiform discharges of NPEs electrodes maximum. The yellow regions represent only epileptiform discharges of ATEs maximum. ATEs, anterior temporal electrodes; IEDs, interictal epileptiform discharges; NPE, nasopharyngeal.
DISCUSSION
The results demonstrated that the dipole areas detected by NPEs and ATEs correspond to anatomically distinct locations. Specifically, the distributions of dipole location in ATEs were clustered in the lateral temporal region, while those for NPEs were concentrated in the mesial and basal temporal regions. This difference in electrical coverage may provide an important clue to enhance diagnostic sensitivity by identifying IEDs that the standard 10 to 20 electrode system cannot identify by combining EEG with NPEs.
Currently, three representative studies compare diagnostic sensitivity using NPEs and ATEs with the standard 10 to 20 electrode system tracing.11,12,22 Electroencephalography analysis using NPEs demonstrated a high diagnostic sensitivity in all three studies. However, the discrepancies in diagnostic sensitivity between NPEs and non-NPEs ranged from 3% to 39%. The authors reported the clinical value of NPEs in TLE through visual EEG analysis based on a consensus among three EEG experts.12 The detection rate of IEDs using the standard 10 to 20 electrode system supplemented with ATEs without NPEs was 127/229 (55.5%), while with the addition of NPEs, the detection rate was 178/229 (76.4%), indicating a 20.9% increase in diagnostic sensitivity when NPEs were used. Interestingly, the result aligns closely with the mean value from the two previous studies, which reported differences in diagnostic sensitivity of 39 and 3% when comparing NPEs with the standard 10 to 20 electrode system supplemented with ATEs recordings.23
Although NPEs were originally introduced in 1949, compared with other additional electrodes, such as sphenoidal and ATEs, relatively few studies have focused on them.23 Furthermore, earlier studies evaluating the clinical implications of additional electrodes in TLE often relied on one-dimensional amplitude comparison of identified IEDs.24
Thus far, no prior reports are available that objectively analyze all identified IEDs according to the type of additional electrodes based on the dipole source localization. In this study, the dipole distribution was compared through the source localization by identifying IEDs according to the type of additional electrodes in TLE. The results confirmed that IEDs detected exclusively by ATEs were associated with the lateral aspect of the temporal lobe. In contrast, IEDs detected by NPEs were closely linked to the basal aspect of the temporal lobe, through the use of simultaneous additional electrodes under the subdural EEG monitoring.13 The subtype-specific analysis of TLE further supports the utility of NPEs in the evaluation of TLE. The statistically significant association between TLE subtype (mesial vs. neocortical) and the IED distribution pattern highlights the differential sensitivity of NPEs in detecting mesial temporal discharges. In cases of mesial TLE and nonlesional TLE, NPE diagnostic involvement was predominantly observed, whereas neocortical TLE cases showed a more balanced distribution across NPEs, ATEs, and other electrodes maxima. These findings emphasize the importance of using tailored electrode montages to optimize the detection of the epileptogenic zone, particularly in mesial TLE.
The electrical gradient in TLE can be classified into three types, based on the dipole formation.25 The pattern of maximal scalp voltage negativity in the vertical radial prefrontal and lateral temporal areas can be sufficiently interpreted using the typical electrode placement of the standard 10 to 20 electrodes system supplemented with ATEs recordings. However, the tangential vertical electrical gradient located on the temporal base is a pattern that cannot be confirmed using routine scalp EEG recording.
The identified IEDs in this TLE were categorized into three types: identified only in ATE, identified in both ATE and NPE, and identified only in NPE. In this classification, the horizontal radial pattern is more likely to be detected in ATEs. And the horizontal tangential pattern is presumed to have been detected simultaneously in both ATE and NPE. This result aligns with earlier studies that examined dipole patterns through the standard 10 to 20 electrodes system supplemented with ATEs recordings in TLE.26,27
Based on the dipole pattern of IEDs in NPE, the authors believe that the IEDs found in NPE display vertical tangential patterns exclusively.28 The increased sensitivity of NPEs in IEDs formed by a tangential vertical gradient, compared with conventional scalp EEG recordings, is also supported by study using magnetoencephalography.29 In the earlier mentioned magnetoencephalography study, as shown in Supplemental Digital Content 1–5 (see Figures, http://links.lww.com/JCNP/A356), subtle IEDs that appeared as small sharp spikes because of the low amplitude of spikes in scalp EEG were confirmed as definitive IEDs through magnetoencephalography. These results likely reflect the fact that NPEs and magnetoencephalography have a greater diagnostic sensitivity to tangential current than radial dipole current.12,30 Nasopharyngeals and foramen ovale electrodes differ from other additional electrodes and conventional scalp electrodes in that they can monitor electrical signals from the base of the temporal lobe by approaching vertically from below.7 This unique positioning allows them to detect electrical signals that may not be observable with traditional scalp or sphenoid electrodes.3,31 Their vertical electrode structure is advantageous because it enhances the ability to identify IEDs formed by a tangential vertical gradient near the base of the temporal lobe.
Scalp ictal EEG rhythms in TLE are also identified differently, according to the dipole pattern,32 because the direction of the dipole is formed differently depending on the lesional location in the temporal lobe. For instance, the earliest recognizable scalp ictal rhythm tends to differ depending on the region affected, such as the temporal basal region for hippocampal lesions, the temporal tip for entorhinal cortex lesions, and the lateral aspect for lateral neocortical lesions.
Interictal epileptiform discharges detected using both the ATEs and NPEs suggested a shared area between two additional electrodes. In contrast, isolated IEDs detected by either the ATEs or NPEs indicate the presence of distinct, separate regions. These findings are consistent with those of a previous study investigating ATEs and NPEs,1 which identified that, even though IEDs with the highest amplitudes were observed in the ATEs, other discharges were also detected with the highest amplitude in the NPEs. These results suggest that the inclusion of NPEs may enhance diagnostic sensitivity by detecting pathologic electrical signals from the basal temporal lobe.
Several factors may explain the limited use of NPEs. First, a common belief is that NPEs result in patient discomfort because of their insertion through the nostril, while many operators have the preconception that their diagnostic yield is negligible. However, NPEs are generally safe and pose no risk of nasal deformity. Moreover, as EEG technicians gain proficiency, the rate of incomplete EEG tracing significantly decreases. Furthermore, concluding that NPEs are not beneficial based on earlier studies is premature,22 because subsequent research has demonstrated that the combination of ATEs and NPEs with the 10 to 20 electrode positioning system can greatly enhance diagnostic sensitivity.11,33,34 In addition, NPEs have demonstrated superior detection capabilities in the mesiobasal temporal region, which is commonly overlooked by ATEs alone.13
This study has several limitations. First, simultaneous subdural EEG monitoring, which requires an invasive procedure, must be accompanied by precise evaluation to accurately assess the distribution of IEDs detected by ATEs and NPEs. In this study, only 11 enrolled patients underwent long-term EEG monitoring for ictal findings or epilepsy surgery. Subdural EEG monitoring of six patients in a prior study revealed that NPEs primarily detected electrical activity in the basal temporal region, while ATEs detected activity in the lateral temporal region.13 These findings closely align with the results of this study in many aspects.
Second, although high-density EEG arrays are commonly used in addition to the standard international 10 to 20 system for ESI to localize the epileptogenic zone in patients with epilepsy,35 this study used a targeted montage. Specifically, the standard 10 to 20 system was used, supplemented with ATEs and NPEs, to enhance the detection of mesial temporal discharges. This approach is consistent with recent evidence suggesting that ESI based on targeted electrode montages can achieve high concordance with high-density EEG in presurgical evaluations.36 Furthermore, the inclusion of inferior temporal electrodes in long-term EEG monitoring has been reported to improve interictal discharge localization in approximately half of patients.37 Although the EEG recordings were of relatively short duration (about 40 minutes), the strategic placement of ATEs and NPEs proved effective in enhancing the detection of mesial temporal IEDs.
CONCLUSIONS
This study demonstrates that NPEs provide significant diagnostic value in detecting IEDs in the mesial and basal temporal regions, areas commonly missed by ATEs and the standard 10 to 20 EEG system. Electric source imaging confirmed that NPEs are particularly effective at localizing activity in these deep regions, while ATEs are more suited to identifying discharges in the lateral temporal region. The combination of NPEs and ATEs enhances diagnostic sensitivity and provides comprehensive coverage of TLE. These findings highlight the importance of incorporating NPEs into standard clinical EEG protocols to improve diagnostic accuracy and localization in TLE.
Supplementary Material
Footnotes
The authors have no funding or conflicts of interest to disclose.
This research was supported by the Ulsan University Research Fund.
All authors contributed to the study's conception and design. S. H. Yim, Y. H. Choi, and K. Heo prepared the material, collected the data, and analyzed the data. S. H. Yim wrote the first draft of the article. T. Jang analyzed the secondary processing of EEG using MATLAB. Moreover, all authors commented on previous versions of the article and read and approved the final article.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.clinicalneurophys.com).
Contributor Information
Yun Ho Choi, Email: recluse21@naver.com.
Taeik Jang, Email: taeikjang84@gmail.com.
Kyoung Heo, Email: juny0215@naver.com.
REFERENCES
- 1.Binnie CD, Dekker E, Smit A, Van der Linden G. Practical considerations in the positioning of EEG electrodes. Electroencephalogr Clin Neurophysiol 1982;53:453–458. [DOI] [PubMed] [Google Scholar]
- 2.Binnie CD, Marston D, Polkey CE, Amin D. Distribution of temporal spikes in relation to the sphenoidal electrode. Electroencephalogr Clin Neurophysiol 1989;73:403–409. [DOI] [PubMed] [Google Scholar]
- 3.Kissani N, Alarcon G, Dad M, Binnie CD, Polkey CE. Sensitivity of recordings at sphenoidal electrode site for detecting seizure onset: evidence from scalp, superficial and deep foramen ovale recordings. Clin Neurophysiol 2001;112:9. [DOI] [PubMed] [Google Scholar]
- 4.McLean PD. A new nasopharyngeal lead. Electroencephalogr Clin Neurophysiol 1949;1:110–112. [PubMed] [Google Scholar]
- 5.Jones DP. Recording of the basal electroencephalogram with sphe- noidal needle electrodes. Electroencephalogr Clin Neurophysiol 1951;3. [Google Scholar]
- 6.Laxer KD. Mini-sphenoidal electrodes in the investigation of seizures. Electroencephalogr Clin Neurophysiol 1984;58:127–129. [DOI] [PubMed] [Google Scholar]
- 7.Siegfried J, Wieser HG, Stodieck SR. Foramen ovale electrodes: a new technique enabling presurgical evaluation of patients with mesiobasal temporal lobe seizures. Appl Neurophysiol 1985;48:408–417. [DOI] [PubMed] [Google Scholar]
- 8.Krauss GL, Lesser RP, Fisher RS, Arroyo S. Anterior “cheek” electrodes are comparable to sphenoidal electrodes for the identification of ictal activity. Electroencephalogr Clin Neurophysiol 1992;83:333–338. [DOI] [PubMed] [Google Scholar]
- 9.Bach Justesen A, Eskelund Johansen AB, Martinussen NI, et al. Added clinical value of the inferior temporal EEG electrode chain. Clin Neurophysiol 2018;129:291–295. [DOI] [PubMed] [Google Scholar]
- 10.Silverman D. The anterior temporal electrode and the ten-twenty system. Electroencephalogr Clin Neurophysiol 1960;12:735–737. [DOI] [PubMed] [Google Scholar]
- 11.Goodin DS, Aminoff MJ, Laxer KD. Detection of epileptiform activity by different noninvasive EEG methods in complex partial epilepsy. Ann Neurol 1990;27:330–334. [DOI] [PubMed] [Google Scholar]
- 12.Hwan Yim S, Ho Cho K, Ho Choi Y, Ihn Kim H, Cho YJ, Heo K. Nasopharyngeal electrodes in temporal lobe epilepsy: a reappraisal of their diagnostic utility. Clin Neurophysiol 2021;132:1741–1751. [DOI] [PubMed] [Google Scholar]
- 13.Zijlmans M, Huiskamp GM, van Huffelen AC, Spetgens WPJ, Leijten FSS. Detection of temporal lobe spikes: comparing nasopharyngeal, cheek and anterior temporal electrodes to simultaneous subdural recordings. Clin Neurophysiol 2008;119:1771–1777. [DOI] [PubMed] [Google Scholar]
- 14.Brodbeck V, Spinelli L, Lascano AM, et al. Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients. Brain 2011;134:2887–2897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Krings T, Chiappa KH, Cuffin BN, Buchbinder BR, Cosgrove GR. Accuracy of electroencephalographic dipole localization of epileptiform activities associated with focal brain lesions. Ann Neurol 1998;44:76–86. [DOI] [PubMed] [Google Scholar]
- 16.Kaiboriboon K, Luders HO, Hamaneh M, Turnbull J, Lhatoo SD. EEG source imaging in epilepsy--practicalities and pitfalls. Nat Rev Neurol 2012;8:498–507. [DOI] [PubMed] [Google Scholar]
- 17.Lemieux L, Krakow K, Fish DR. Comparison of spike-triggered functional MRI BOLD activation and EEG dipole model localization. Neuroimage 2001;14:1097–1104. [DOI] [PubMed] [Google Scholar]
- 18.Huntington Mavor MKH. Nasopharyngeal electrode recording. Am J EEG Technology 1964;4:8. [Google Scholar]
- 19.Hirsch LJ, Fong MWK, Leitinger M, et al. American clinical neurophysiology society's standardized critical care EEG terminology: 2021 version. J Clin Neurophysiol 2021;38:1–29. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Gramfort A, Papadopoulo T, Olivi E, Clerc M. OpenMEEG: opensource software for quasistatic bioelectromagnetics. Biomed Eng Online 2010;9:45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Kybic J, Clerc M, Abboud T, Faugeras O, Keriven R, Papadopoulo T. A common formalism for the integral formulations of the forward EEG problem. IEEE Trans Med Imaging 2005;24:12–28. [DOI] [PubMed] [Google Scholar]
- 22.Sperling MR, Engel J, Jr. Electroencephalographic recording from the temporal lobes: a comparison of ear, anterior temporal, and nasopharyngeal electrodes. Ann Neurol 1985;17:510–513. [DOI] [PubMed] [Google Scholar]
- 23.Zijlmans M, van der Salm SMA, Van't Klooster M. Nasopharyngeal electrodes for recording mesiotemporal spikes: post-covid revival?. Clin Neurophysiol 2021;132:1718–1720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Sadler RM, Goodwin J. Multiple electrodes for detecting spikes in partial complex seizures. Can J Neurol Sci 1989;16:326–329. [DOI] [PubMed] [Google Scholar]
- 25.Ebersole JS, Hawes-Ebersole S. Clinical application of dipole models in the localization of epileptiform activity. J Clin Neurophysiol 2007;24:120–129. [DOI] [PubMed] [Google Scholar]
- 26.Ebersole JS, Wade PB. Spike voltage topography identifies two types of frontotemporal epileptic foci. Neurology 1991;41:1425–1433. [DOI] [PubMed] [Google Scholar]
- 27.Young-Soo Kim O-YK, Jung Seokwon, Son Seungnam, et al. Current-source dipole of anterior temporal spikes: clinical significance of orientation. J Korean Neurol Assoc 2011:7. 29;3. [Google Scholar]
- 28.Ebersole JS. Noninvasive localization of epileptogenic foci by EEG source modeling. Epilepsia 2000;41(suppl 3):S24–S33. [DOI] [PubMed] [Google Scholar]
- 29.Agari D, Jin K, Kakisaka Y, et al. Magnetoencephalography to confirm epileptiform discharges mimicking small sharp spikes in temporal lobe epilepsy. Clin Neurophysiol 2021;132:1785–1789. [DOI] [PubMed] [Google Scholar]
- 30.Yang Y, Luo S, Wang W, Gao X, Yao X, Wu T. From bench to bedside: overview of magnetoencephalography in basic principle, signal processing, source localization and clinical applications. Neuroimage Clin 2024;42:103608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Sheth SA, Aronson JP, Shafi MM, et al. Utility of foramen ovale electrodes in mesial temporal lobe epilepsy. Epilepsia 2014;55:713–724. [DOI] [PubMed] [Google Scholar]
- 32.Assaf BA, Ebersole JS. Continuous source imaging of scalp ictal rhythms in temporal lobe epilepsy. Epilepsia 1997;38:1114–1123. [DOI] [PubMed] [Google Scholar]
- 33.Kashnig DM, Celesia GG. Letter: nasopharyngeal electrodes in the diagnosis of partial seizures with complex symptoms. Arch Neurol 1976;33:519–520. [DOI] [PubMed] [Google Scholar]
- 34.Levin R, Leaton EM, Lee SI. The value of nasopharyngeal recording in psychiatric patients. Biol Psychiatry 1986;21:1236–1238. [DOI] [PubMed] [Google Scholar]
- 35.Lantz G, Grave de Peralta R, Spinelli L, Seeck M, Michel CM. Epileptic source localization with high density EEG: how many electrodes are needed?. Clin Neurophysiol 2003;114:63–69. [DOI] [PubMed] [Google Scholar]
- 36.Horrillo-Maysonnial A, Avigdor T, Abdallah C, et al. Targeted density electrode placement achieves high concordance with traditional high-density EEG for electrical source imaging in epilepsy. Clin Neurophysiol 2023;156:262–271. [DOI] [PubMed] [Google Scholar]
- 37.Heers M, Bottcher S, Kalina A, et al. Detection of interictal epileptiform discharges in an extended scalp EEG array and high-density EEG-A prospective multicenter study. Epilepsia 2022;63:1619–1629. [DOI] [PubMed] [Google Scholar]


