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Reliability of the witness descriptions of epileptic seizures and psychogenic nonepileptic attacks: a comparative analysis Aleksandar J. Ristic´1, Maja Drasˇkovic´2, Zoran Bukumiric´3, Dragoslav Sokic´1 1
Neurology Clinic, Clinical Center of Serbia, University of Belgrade, Serbia, 2Medical School, University of Belgrade, Serbia, 3Institute of Medical Statistics and Informatics, Medical School, University of Belgrade, Serbia
Background: The diagnosis of epilepsy primarily depends on description of the observed seizure. The aim of this study was to determine the reliability of witness’ description among groups with different medical education. Methods: A group of 44 respondents (15 laymen, 15 medical students, and 14 doctors at neurology residency program) were shown video footages of focal epileptic seizure (ES) with secondary generalization and psychogenic non-epileptic seizure (PNES) of the same patient. The ability to describe ES and PNES characteristics, to estimate duration of seizures, and to detect of accurate seizure type was evaluated using a questionnaire. For the analysis of primary data obtained from questionnaires, we used descriptive statistical methods and methods for testing statistical hypotheses. Results: The sensitivity (Sn) and specificity (Sp) for accurate recognition of ES are different in the examined groups (laymen Sn 5 53.3%, Sp 5 33.3%; medical students Sn 5 100%, Sp 5 13.3%; neurology residents Sn 5 100%, Sp 5 71.4%). Evaluated duration of PNES and ES do not differ between examined groups. The impression that ES and PNES are distinct events is reciprocal for medical students and neurology residents, but not in laymen group. Neurology residents notice the essential characteristics of ES in high percentage. Conclusion: Accurate classification of the attacks is associated with the observers’ level of medical knowledge. Witnesses with specific, neurological knowledge with higher probability, compared to the laity and medical students, differentiate ES from PNES. Keywords: Epilepsy, Psychogenic non-epileptic seizures, Reliability of witnesses, Seizure description
Introduction Epileptic seizures (ESs) are paroxysmal and may include impaired consciousness and motor, sensory, autonomous, and psychic events perceived by the subject or an observer. Psychogenic non-epileptic seizure (PNES) is a sudden change in a person’s behavior, perception, thinking, or feeling that is time limited and resembles, or is mistaken for, epilepsy but does not have the electroencephalographic (EEG) changes that accompanies ES.1 As the patient’s description of the ES has limitations owing to level of consciousness, the observer’s description frequently provides critical information.2 However, the accuracy of seizure descriptions by witnesses is with wide variations.3,4
Correspondence to: Aleksandar J. Ristic´, Neurology Clinic, Clinical Center of Serbia, University of Belgrade, Dr Subotic´a 6, Belgrade 11000, Serbia. Email: [email protected]
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132815Y.0000000009
We determined the ability of accurate recognition of the ES according to degree of the medical education.
Methods Two videos of the patient with epilepsy and PNES comorbidity, obtained during long-term video-EEG monitoring (vEEGM), were projected with video beam to the three separate groups: laymen (15 subjects), students of medicine (MSs) (15 subjects), and doctors at neurology residency program (NRs) (14 subjects). Both videos were pruned from the raw data identically: beginning of the video – 10 seconds prior to first clinical sign; the end of the video – 10 seconds following last clinical sign. Forty-three-year-old male patient, physically abused during childhood, suffered ESs following head trauma with short-lasting loss of consciousness in 31 years of age. Three different antiepileptic drugs failed to render him seizure free. Brain MRI showed left temporal neocortical focal cortical dysplasia. The
Neurological Research
2014
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Ristic´ et al.
Reliability of the witness descriptions
patient was admitted for presurgical evaluation. One PNES and one focal complex seizure with secondary generalization were recorded during vEEGM. From January 2007 to December 2012, we detected nine patients with PNES and epilepsy comorbidity. This patient was chosen because of similar semiological features in both recorded events. First video presents PNES that lasted 5 minutes. Clinical onset of the PNES was determined as unresponsiveness to EEG technician while lying down. This is followed by gradual onset of the asynchronous mild whole body jerking that lasted 90 seconds. The PNES continued with more violent upper limb movements and excessive pelvic thrusting in waxing and waning fashion. During the whole PNES, patient had his eyes vigorously closed, and he resisted to the attempt of eyes opening by investigator. The PNES ended spontaneously. Second video presents focal ES with secondary generalization that lasted 1 minute 40 seconds. Clinical onset of the ES was determined as the start of oral automatisms while lying down with eyes wide open and non-forced head turn to the left. At that moment, patient was unresponsive to EEG technician demands. The ES continued with left face and arm clonic jerking and head version to the left. This was followed by tonic extension of the legs, and asymmetric tonic posturing of the arms (left arm extended). The ES finished in symmetrical bilateral clonic jerking. Prior to PNES-video projection, subjects were informed that questionnaire 1 (Q1) regarding the content will be distributed. Immediately following the PNES-video review, subjects were asked to fill out the questionnaire. The same procedure was applied with the ES-video and questionnaire 2 (Q2). Subjects reviewed both videos just once. The simplified questionnaire used in different study5 was utilized with permission from the publisher (Supplementary Material 1 http://dx.doi.org/10.1179/ 1743132815Y.0000000009.s1). Q1/Q2 included different questions about the reviewed seizure: state of consciousness, patient’s ability to respond to EEG technician demands, eyes and head position, seizure duration, and course. Subjects were asked to determine the nature of the event (ES/non-ES) in questionnaires. Q2 consisted additional question about the difference between two reviewed events (Yes/No/Do not know). The descriptive statistics were used to characterize the study sample. Differences between groups in
Figure 1 Subject’s impression about difference of the reviewed events.
continuous and categorical variables were analyzed using one-way ANOVA followed by Tukey’s post hoc test, Kruskal–Wallis test, and Pearson chi-square test. Sensitivity (Sn), specificity (Sp), and likelihood ratio positive and negative (LRz/LR2) were used to assess the ability of participants to determining ES. Statistical analyses were performed using SPSS for Windows, version 22. In all analyses, the significance level was set at 0.05. This research has been approved by Ethical Committee of Clinical Center of Serbia. Informed consent was obtained from the patient and each subject.
Results Sensitivity, Sp, and positive/negative likelihood ratio of the accurate appreciation of ES in all groups are presented in Table 1. The median of the estimated PNES duration was not different among groups: laymen 5.0 (3.0–7.0), MSs 5.0 (2.0–15.0), and NRs 5.0 (5.0–10.0) minutes (P 5 0.45). The mean of the estimated ES duration was not different among groups: laymen 2.9 ¡ 1.2, MSs 2.1 ¡ 1.2, and NRs 2.2 ¡ 0.7 minutes (P 5 0.07). We found significant difference in impression about the difference of events in analyzed groups (x2; P 5 0.04) (Fig. 1). Estimated alertness during PNES in groups showed significant difference: laymen (alert/not alert – 6/9), MSs (alert/not alert/do not know – 1/13/1), and NRs (alert/not alert/do not know – 10/3/1) (x2; P 5 0,006). Similarly, significant difference was
Table 1 Sensitivity, specificity, and positive/negative likelihood ratio (zLR/2LR) for accurate appreciation of the epileptic seizure in all analyzed groups
2
Subject’s groups
Sensitivity (95%CI)
(zLR)
Specificity (95%CI)
(2LR)
Laymen Medical students Neurology residents
53.3% (26.5–78.7) 100% (78.2–100) 100% (76.8–100)
0.79 1.14 3.4
33.3% (11.8–61.6) 13.3% (1.6–40.4) 71.4% (41.9–91.6)
1.42 0 0
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found for the estimated alertness during ES in groups: laymen (alert/not alert – 6/9), MSs (alert/ not alert – 4/11), and NRs (alert/not alert – 1/13) (x2; P 5 0.008). Closed eyes during PNES/opened eyes in ES accurately appreciated in 6.7%/73.3% of laymen, 20%/46.7% of MSs, and 57.1%/50% of NRs. Waxing–waning course of the PNES/continuous course of the ES was accurately appreciated in 86.7%/ 13.3% of laymen, 100%/40% of MSs, and 92.9%/50% of NRs. Ability to maintain communication with the patient during PNES/ES was estimated positive in 20%/46.7% of laymen, 0%/26.7% of MSs, and 14.3%/ 0% of NRs. Absence of the sustained head deviation in PNES/ sustained left head version in ES was accurately appreciated in 6.7%/0% of laymen, 26%/6.7% of MSs, and 21.4%/78.6% of NRs.
Discussion Our results show wide variation in the description accuracy of ES and PNES, linearly dependent on the degree of medical education. It was recently shown that education level of the observers correlated with the accuracy of the description.2 However, in the study consisted of MSs (with/without epilepsy training), non-MSs, and junior doctors on neurological ward (20 subjects), this correlation was not found.3 This is opposite to our results as we notified that NRs are best descriptors of the paroxysmal events. MSs in our study were able to depict major characteristics of the reviewed events, and laymen population was the least consistent in their report. Possibly, the reason for such discrepancy was the applied method. Hence, we used questionnaire with predefined answers that may facilitate the description, and participants in the previous work used open-format questionnaire.3 Also, difference in observation conditions might influence the perception and recollection of ictal phenomena. In two studies, witnesses were asked to describe video-taped seizures.3,5 In other studies, data from video-tape recordings were compared to witness descriptions of seizures observed at home,2,4 thus in a less comfortable and more stressful ambient.
Reliability of the witness descriptions
Although it is very important to verify the reliability of the description, there are surprisingly rare reports on this topic.2–5 Main advantage of our method is utilization of PNES, as the major ‘distractor’ in the routine practice. To our knowledge, there is no study to report Sn/Sp between ES and PNES among observers, which could provide physicians appropriate reference for their data reliability. We demonstrate that Sn/Sp to distinct ES from PNES is very low in laymen, which is contrary to the MSs and NRs. According to the observation that reliability of the witness description depends on the medical education, we show that NRs have high Sn, which is different from the MSs. Most likely, this is due to better observation of the most significant ES characteristics (eyes appearance, head version, etc.) Our results indicate that witness’s seizure depiction accuracy is dependent on the medical knowledge, which further supports earlier ‘warnings’ about the observer’s description reliability. Correct distinction of the ES from different paroxysmal events depends on more specific, neurological familiarity.
Disclaimer Statements Contributors Aleksandar Ristic: study design, data analysis, and manuscript draft. Maja Draskovic: study design and data analysis. Zoran Bukumiric: data analysis. Dragsolav Sokic: study design, data analysis, and manuscript draft. Funding Conflicts of interest The authors declare no conflict of interest. Ethics approval
References 1 Betts T. Psychiatric aspects of nonepileptic seuzures. In: Engel JJ, Pedley T, editors. Epilepsy: a comprehensive text book. Philadelphia, NY: Lippincot-Raven; 1997. p. 2101–16. 2 Heo J, Kim D, Lee S, Cho J, Lee S, Nam H. Reliability of semiology description. Neurologist. 2008;14:7–11. 3 Mannan J, Wieshmann U. How accurate are witness descriptions of epileptic seizures? Seizure. 2003;12:444–7. 4 Besocke A, Rojas J, Valiensi S, Cristiano E, Garcia MC. Interview accuracy in partial epilepsy. Epilepsy Behav. 2009;16(3):551–4. 5 Rugg-Gunn F, Harrison N, Duncan J. Evaluation of the accuracy of seizure descriptions by the relatives of patients with epilepsy. Epilepsy Res. 2001;43:193–9.
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Reliability of the witness descriptions of epileptic seizures and psychogenic nonepileptic attacks: a comparative analysis Aleksandar J. Ristic´1, Maja Drasˇkovic´2, Zoran Bukumiric´3, Dragoslav Sokic´1 1
Neurology Clinic, Clinical Center of Serbia, University of Belgrade, Serbia, 2Medical School, University of Belgrade, Serbia, 3Institute of Medical Statistics and Informatics, Medical School, University of Belgrade, Serbia
Background: The diagnosis of epilepsy primarily depends on description of the observed seizure. The aim of this study was to determine the reliability of witness’ description among groups with different medical education. Methods: A group of 44 respondents (15 laymen, 15 medical students, and 14 doctors at neurology residency program) were shown video footages of focal epileptic seizure (ES) with secondary generalization and psychogenic non-epileptic seizure (PNES) of the same patient. The ability to describe ES and PNES characteristics, to estimate duration of seizures, and to detect of accurate seizure type was evaluated using a questionnaire. For the analysis of primary data obtained from questionnaires, we used descriptive statistical methods and methods for testing statistical hypotheses. Results: The sensitivity (Sn) and specificity (Sp) for accurate recognition of ES are different in the examined groups (laymen Sn 5 53.3%, Sp 5 33.3%; medical students Sn 5 100%, Sp 5 13.3%; neurology residents Sn 5 100%, Sp 5 71.4%). Evaluated duration of PNES and ES do not differ between examined groups. The impression that ES and PNES are distinct events is reciprocal for medical students and neurology residents, but not in laymen group. Neurology residents notice the essential characteristics of ES in high percentage. Conclusion: Accurate classification of the attacks is associated with the observers’ level of medical knowledge. Witnesses with specific, neurological knowledge with higher probability, compared to the laity and medical students, differentiate ES from PNES. Keywords: Epilepsy, Psychogenic non-epileptic seizures, Reliability of witnesses, Seizure description
Introduction Epileptic seizures (ESs) are paroxysmal and may include impaired consciousness and motor, sensory, autonomous, and psychic events perceived by the subject or an observer. Psychogenic non-epileptic seizure (PNES) is a sudden change in a person’s behavior, perception, thinking, or feeling that is time limited and resembles, or is mistaken for, epilepsy but does not have the electroencephalographic (EEG) changes that accompanies ES.1 As the patient’s description of the ES has limitations owing to level of consciousness, the observer’s description frequently provides critical information.2 However, the accuracy of seizure descriptions by witnesses is with wide variations.3,4
Correspondence to: Aleksandar J. Ristic´, Neurology Clinic, Clinical Center of Serbia, University of Belgrade, Dr Subotic´a 6, Belgrade 11000, Serbia. Email: [email protected]
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132815Y.0000000009
We determined the ability of accurate recognition of the ES according to degree of the medical education.
Methods Two videos of the patient with epilepsy and PNES comorbidity, obtained during long-term video-EEG monitoring (vEEGM), were projected with video beam to the three separate groups: laymen (15 subjects), students of medicine (MSs) (15 subjects), and doctors at neurology residency program (NRs) (14 subjects). Both videos were pruned from the raw data identically: beginning of the video – 10 seconds prior to first clinical sign; the end of the video – 10 seconds following last clinical sign. Forty-three-year-old male patient, physically abused during childhood, suffered ESs following head trauma with short-lasting loss of consciousness in 31 years of age. Three different antiepileptic drugs failed to render him seizure free. Brain MRI showed left temporal neocortical focal cortical dysplasia. The
Neurological Research
2014
VOL .
0
NO .
0
1
Ristic´ et al.
Reliability of the witness descriptions
patient was admitted for presurgical evaluation. One PNES and one focal complex seizure with secondary generalization were recorded during vEEGM. From January 2007 to December 2012, we detected nine patients with PNES and epilepsy comorbidity. This patient was chosen because of similar semiological features in both recorded events. First video presents PNES that lasted 5 minutes. Clinical onset of the PNES was determined as unresponsiveness to EEG technician while lying down. This is followed by gradual onset of the asynchronous mild whole body jerking that lasted 90 seconds. The PNES continued with more violent upper limb movements and excessive pelvic thrusting in waxing and waning fashion. During the whole PNES, patient had his eyes vigorously closed, and he resisted to the attempt of eyes opening by investigator. The PNES ended spontaneously. Second video presents focal ES with secondary generalization that lasted 1 minute 40 seconds. Clinical onset of the ES was determined as the start of oral automatisms while lying down with eyes wide open and non-forced head turn to the left. At that moment, patient was unresponsive to EEG technician demands. The ES continued with left face and arm clonic jerking and head version to the left. This was followed by tonic extension of the legs, and asymmetric tonic posturing of the arms (left arm extended). The ES finished in symmetrical bilateral clonic jerking. Prior to PNES-video projection, subjects were informed that questionnaire 1 (Q1) regarding the content will be distributed. Immediately following the PNES-video review, subjects were asked to fill out the questionnaire. The same procedure was applied with the ES-video and questionnaire 2 (Q2). Subjects reviewed both videos just once. The simplified questionnaire used in different study5 was utilized with permission from the publisher (Supplementary Material 1 http://dx.doi.org/10.1179/ 1743132815Y.0000000009.s1). Q1/Q2 included different questions about the reviewed seizure: state of consciousness, patient’s ability to respond to EEG technician demands, eyes and head position, seizure duration, and course. Subjects were asked to determine the nature of the event (ES/non-ES) in questionnaires. Q2 consisted additional question about the difference between two reviewed events (Yes/No/Do not know). The descriptive statistics were used to characterize the study sample. Differences between groups in
Figure 1 Subject’s impression about difference of the reviewed events.
continuous and categorical variables were analyzed using one-way ANOVA followed by Tukey’s post hoc test, Kruskal–Wallis test, and Pearson chi-square test. Sensitivity (Sn), specificity (Sp), and likelihood ratio positive and negative (LRz/LR2) were used to assess the ability of participants to determining ES. Statistical analyses were performed using SPSS for Windows, version 22. In all analyses, the significance level was set at 0.05. This research has been approved by Ethical Committee of Clinical Center of Serbia. Informed consent was obtained from the patient and each subject.
Results Sensitivity, Sp, and positive/negative likelihood ratio of the accurate appreciation of ES in all groups are presented in Table 1. The median of the estimated PNES duration was not different among groups: laymen 5.0 (3.0–7.0), MSs 5.0 (2.0–15.0), and NRs 5.0 (5.0–10.0) minutes (P 5 0.45). The mean of the estimated ES duration was not different among groups: laymen 2.9 ¡ 1.2, MSs 2.1 ¡ 1.2, and NRs 2.2 ¡ 0.7 minutes (P 5 0.07). We found significant difference in impression about the difference of events in analyzed groups (x2; P 5 0.04) (Fig. 1). Estimated alertness during PNES in groups showed significant difference: laymen (alert/not alert – 6/9), MSs (alert/not alert/do not know – 1/13/1), and NRs (alert/not alert/do not know – 10/3/1) (x2; P 5 0,006). Similarly, significant difference was
Table 1 Sensitivity, specificity, and positive/negative likelihood ratio (zLR/2LR) for accurate appreciation of the epileptic seizure in all analyzed groups
2
Subject’s groups
Sensitivity (95%CI)
(zLR)
Specificity (95%CI)
(2LR)
Laymen Medical students Neurology residents
53.3% (26.5–78.7) 100% (78.2–100) 100% (76.8–100)
0.79 1.14 3.4
33.3% (11.8–61.6) 13.3% (1.6–40.4) 71.4% (41.9–91.6)
1.42 0 0
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found for the estimated alertness during ES in groups: laymen (alert/not alert – 6/9), MSs (alert/ not alert – 4/11), and NRs (alert/not alert – 1/13) (x2; P 5 0.008). Closed eyes during PNES/opened eyes in ES accurately appreciated in 6.7%/73.3% of laymen, 20%/46.7% of MSs, and 57.1%/50% of NRs. Waxing–waning course of the PNES/continuous course of the ES was accurately appreciated in 86.7%/ 13.3% of laymen, 100%/40% of MSs, and 92.9%/50% of NRs. Ability to maintain communication with the patient during PNES/ES was estimated positive in 20%/46.7% of laymen, 0%/26.7% of MSs, and 14.3%/ 0% of NRs. Absence of the sustained head deviation in PNES/ sustained left head version in ES was accurately appreciated in 6.7%/0% of laymen, 26%/6.7% of MSs, and 21.4%/78.6% of NRs.
Discussion Our results show wide variation in the description accuracy of ES and PNES, linearly dependent on the degree of medical education. It was recently shown that education level of the observers correlated with the accuracy of the description.2 However, in the study consisted of MSs (with/without epilepsy training), non-MSs, and junior doctors on neurological ward (20 subjects), this correlation was not found.3 This is opposite to our results as we notified that NRs are best descriptors of the paroxysmal events. MSs in our study were able to depict major characteristics of the reviewed events, and laymen population was the least consistent in their report. Possibly, the reason for such discrepancy was the applied method. Hence, we used questionnaire with predefined answers that may facilitate the description, and participants in the previous work used open-format questionnaire.3 Also, difference in observation conditions might influence the perception and recollection of ictal phenomena. In two studies, witnesses were asked to describe video-taped seizures.3,5 In other studies, data from video-tape recordings were compared to witness descriptions of seizures observed at home,2,4 thus in a less comfortable and more stressful ambient.
Reliability of the witness descriptions
Although it is very important to verify the reliability of the description, there are surprisingly rare reports on this topic.2–5 Main advantage of our method is utilization of PNES, as the major ‘distractor’ in the routine practice. To our knowledge, there is no study to report Sn/Sp between ES and PNES among observers, which could provide physicians appropriate reference for their data reliability. We demonstrate that Sn/Sp to distinct ES from PNES is very low in laymen, which is contrary to the MSs and NRs. According to the observation that reliability of the witness description depends on the medical education, we show that NRs have high Sn, which is different from the MSs. Most likely, this is due to better observation of the most significant ES characteristics (eyes appearance, head version, etc.) Our results indicate that witness’s seizure depiction accuracy is dependent on the medical knowledge, which further supports earlier ‘warnings’ about the observer’s description reliability. Correct distinction of the ES from different paroxysmal events depends on more specific, neurological familiarity.
Disclaimer Statements Contributors Aleksandar Ristic: study design, data analysis, and manuscript draft. Maja Draskovic: study design and data analysis. Zoran Bukumiric: data analysis. Dragsolav Sokic: study design, data analysis, and manuscript draft. Funding Conflicts of interest The authors declare no conflict of interest. Ethics approval
References 1 Betts T. Psychiatric aspects of nonepileptic seuzures. In: Engel JJ, Pedley T, editors. Epilepsy: a comprehensive text book. Philadelphia, NY: Lippincot-Raven; 1997. p. 2101–16. 2 Heo J, Kim D, Lee S, Cho J, Lee S, Nam H. Reliability of semiology description. Neurologist. 2008;14:7–11. 3 Mannan J, Wieshmann U. How accurate are witness descriptions of epileptic seizures? Seizure. 2003;12:444–7. 4 Besocke A, Rojas J, Valiensi S, Cristiano E, Garcia MC. Interview accuracy in partial epilepsy. Epilepsy Behav. 2009;16(3):551–4. 5 Rugg-Gunn F, Harrison N, Duncan J. Evaluation of the accuracy of seizure descriptions by the relatives of patients with epilepsy. Epilepsy Res. 2001;43:193–9.
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