Temporal resolution deficits in patients with refractory complex partial seizures and mesial temporal sclerosis (MTS)

Temporal resolution deficits in patients with refractory complex partial seizures and mesial temporal sclerosis (MTS)

Epilepsy & Behavior 24 (2012) 126–130 Contents lists available at SciVerse ScienceDirect Epilepsy & Behavior journal homepage: www.elsevier.com/loca...

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Epilepsy & Behavior 24 (2012) 126–130

Contents lists available at SciVerse ScienceDirect

Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh

Temporal resolution deficits in patients with refractory complex partial seizures and mesial temporal sclerosis (MTS) Rajasekaran Aravindkumar a, N. Shivashankar a, P. Satishchandra b, Sanjib Sinha b,⁎, J. Saini c, D.K. Subbakrishna d a

Department of Speech Pathology and Audiology, National Institute of Mental Health and Neurosciences, Bangalore, India Department of Neurology, National Institute of Mental Health and Neurosciences, Bangalore, India Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences, Bangalore, India d Department of Biostatistics, National Institute of Mental Health and Neurosciences, Bangalore, India b c

a r t i c l e

i n f o

Article history: Received 10 October 2011 Revised 5 March 2012 Accepted 6 March 2012 Available online 14 April 2012 Keywords: Epilepsy Gaps-In-Noise test Mesial temporal sclerosis Temporal resolution

a b s t r a c t We studied the temporal resolution ability in patients with refractory complex partial seizures and mesial temporal sclerosis (MTS) using Gaps-In-Noise (GIN) test in a prospective cross-sectional study. Thirteen patients with right MTS (age: 31± 7.67 years; M:F = 8:5) and 13 patients with left MTS (age: 25.76 ± 8.26 years; M: F = 9:4) having normal hearing and mini-mental state examination (MMSE) score of >23/30 were recruited. Fifty healthy volunteers (26.3± 5.17 years; M:F = 28:22) formed the control group. Gaps-In-Noise test demonstrated impaired temporal resolution: 69.2% of patients with right MTS (RMTS) and 76.9% of patients with left MTS (LMTS) had abnormal scores in the right ear for gap detection threshold (GDT) measure. Similarly, 53.8% of patients in the RMTS group and 76.9% of patients in the LMTS group had abnormal scores in the left ear. In percentage of correct identification (PCI), 46.1% of patients with RMTS and 69.2% of patients with LMTS had poorer scores in the right ear, whereas 46.1% of patients with RMTS and 61.5% of patients with LMTS had poorer scores in the left ear. Both patient groups, viz., RMTS and LMTS, demonstrated bilateral temporal resolution deficits. © 2012 Elsevier Inc. All rights reserved.

1. Introduction The temporal lobe plays a vital role in auditory processing. It encompasses primary and secondary auditory areas that are responsible for perception, assimilation and interpretation of the auditory signals. Epileptogenic foci in the temporal lobe, hence, may adversely affect the auditory processing mechanism. Temporal lobe epilepsy (TLE) could be classified into two types, viz., medial and lateral [1,2]. Engel [3] while reviewing the hospital-based study of Semah et al. [4], observed that 74% of all patients with epilepsy (n = 2200) had localization-related epilepsy, and among them, 66% had TLE. Further, considering the patients in whom MRI was performed, about 53% of TLE patients had evidence of hippocampal sclerosis. Temporal resolution is the ability of the auditory system to respond to rapid changes in the envelope of a sound stimulus over time [5]. Psychophysical gap detection is the most common method of assessing auditory temporal resolution wherein the subjects are required to detect gaps within a continuous auditory stimulus [6]. Gap detection has been found to correlate with speech perception acuity [7,8] and poor speech discrimination in noise [9]. Poor gap detection scores, viz., high gap detection threshold or low percentage of correct ⁎ Corresponding author at: Department of Neurology, National Institute of Mental Health and Neurosciences, Bangalore 560029, India. Fax: + 91 80 26564830. E-mail address: [email protected] (S. Sinha). 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.03.004

responses in gap detection tests, might indicate the underlying temporal resolution deficits. Studies have reported impaired temporal resolution in aging [10] and in disease conditions, such as auditory neuropathy [11], multiple sclerosis [12], brainstem and cortical lesions [13], insular lesions [14], as well as in patients post-temporal lobectomy [15]. (Central) auditory processing disorders [(C) APD] in patients with TLE might not be an overt symptom [16]. Boatman et al. [16] evaluated speech recognition in patients with focal intractable epilepsy who underwent surgical resections in the non-dominant (right) hemisphere. All patients demonstrated normal auditory recognition of words and environmental sounds before and after surgery. However, when real-world listening conditions were simulated by using acoustically degraded (filtered) words, patients with TLE performed significantly worse than patients with frontal or parieto-occipital lobe epilepsy, before and after surgery (p b 0.0001). Dichotic tests [17], staggered spondaic word test [18], filtered speech test [16], duration pattern test and non-verbal dichotic test [19] have all demonstrated [C] APD in patients with TLE. In another study, Han et al. [20], employing several behavioral measures [frequency pattern test, duration pattern test and dichotic digits test] had demonstrated [C] APD in 28 patients with TLE (right TLE = 15, left TLE = 10 and bilateral = 3). Gaps-In-Noise (GIN) is a test of temporal resolution and is highly feasible [21]. Shinn et al. [21] opined that GIN test puts low demand

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on cognition, is immune to hearing loss at specific frequencies, is easy to administer, could be performed using common equipments and could be used for a wide age range (beginning from 7 years of age). Musiek et al. [13] administered the GIN test to patients with confirmed lesions of the central auditory pathway, viz., brain stem lesions (n = 9) and cortical lesions (n = 9). Fourteen males and 36 females (age range: 13 to 46 years and mean age: 24.6 years) constituted the control group, and 14 males and 4 females (age range: 20 to 65 years and mean age: 46.4 years) constituted the patient group. They reported that the patient group had longer gap detection threshold (GDT) and less percentage of correct responses (PCR) when compared to the control group. Interestingly, though limited by the number and type of patients taken, this test was found to be more sensitive for cortical lesions. Similarly, Bamiou et al. [14] reported bilaterally abnormal GIN scores in their study on 8 patients (five men and three women; age range: 36 to 79 years; mean age: 63 years) with insular stroke with (n = 4) and without (n = 4) involvement of auditory areas. There was contralateral impairment of GIN scores in three patients (one involving right-sided lesion and the other two involving left-sided lesion), and five patients had poor scores bilaterally. The aim of the current study was to evaluate the temporal resolution abilities in patients with refractory complex partial seizure and mesial temporal sclerosis (MTS) by employing the Gaps-In-Noise test.

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2.1. Gaps-In-Noise test The GIN test developed by Musiek et al. [13] was adopted for the present study to probe auditory temporal resolution. In this test, segments (6 s) of white noise containing 0–3 silent intervals or gaps per noise segment were administered monaurally. Duration of gaps were 2, 3, 4, 5, 6, 10, 12, 15 and 20 ms. Each time, the test material (one list for each ear) was randomly selected among the four test lists available in the GIN test. Each list had a total of 60 gaps. The test in itself had random presentations of gaps for location, number, and duration per noise segment. The subjects were asked to respond by pressing the response switch whenever they were able to detect a gap. Practice items were administered before the actual testing to ensure that a patient understood the test procedure. Two types of scores were calculated, viz., percentage of correct identification (PCI) and the gap detection threshold (GDT). The GDT was defined as the shortest gap duration that the subject was able to identify at least four out of six times. The PCI was derived using the formula: number of correct responses (NCR) / total number of gaps × 100. However, for all statistical measures, the raw data, viz., NCR, were used. Further, to identify the abnormal scores in individual patients, a 2-standard deviation (SD) cut-off criterion was adopted [13]. Musiek et al. [13] had arrived at the cut-off values by adding 2 SD values to the mean GDT and subtracting 2 SD values from the mean percentage of correct responses. The cut-off criteria yielded for GDT and percentage of correct responses were 7 ms and 54%, respectively for both ears.

2. Methods 3. Results The study was carried out in a tertiary care hospital for neuropsychiatric disorders in south India. Twenty-six patients with refractory complex partial seizures and MRI evidence of mesial temporal sclerosis (MTS) were divided into two groups, viz., right mesial temporal sclerosis (RMTS = 13; age: 31 ± 7.67 years; M:F= 8:5) and left mesial temporal sclerosis (LMTS = 13; age: 25.76 ± 8.26 years; M:F = 9:4). The control group consisted of 50 healthy volunteers (mean: 26.3 ± 5.17 years; M:F = 28:22). The study had the approval of the ethics committee of the study center. All enrolled patients had uncontrolled seizures (i.e., at least 1 to 2 seizures a month for >2 years) while on ≥2 antiepileptic drugs (AEDs). All had demonstrated normal hearing bilaterally [22] on air conduction testing (≤25 dB HL at octave frequencies from 250 Hz to 8 kHz) and were right-handed [23]. They scored >23 on the mini-mental state examination (MMSE), ensuring no cognitive deficits [24]. The MMSE is a tool that can be used to assess the mental status and consist of 11-questions that tests five areas of cognitive function: orientation, registration, attention and calculation, recall, and language. The exclusion criteria were (a) patients who were lefthanded/ambidextrous, (b) patients who had pre-morbid neurological/ psychiatric disorders and (c) patients who had non-mesial TLE. The patients were first identified and evaluated by the neurologist. The neurological evaluation included recording of detailed clinical history, including MMSE, inter-ictal EEG and scalp video–EEG. The MRI was carried out on a 3-T machine (Philips Achieva), and imaging observations, viz., volume loss, signal changes, loss of normal architecture, and loss of hippocampal internal digitization, were taken into account for the diagnosis of MTS. Radiological interpretation was done by a neuroradiologist (JS). Following the neurological evaluation, the patients underwent audiological testing, which comprised pure tone audiometry and the Gaps-In-Noise (GIN) test. Pure tone audiometry (GSI 61 clinical audiometer) was performed to ascertain normal hearing sensitivity based on Goodman's classification [22]. Following the pure tone audiometry, they were administered the GIN test. The pre-recorded GIN stimuli were presented using a standard CD player (Rising SL 1998A) routed through the GSI 61 clinical audiometer. The tests were carried out in a sound-treated double room. The same audiological test protocol was used to test the control group subjects.

The mean gap detection threshold in the control group for the right ear [5.22 (1.11) ms] and the left ear [5.06 (1.0) ms] was found to be lower (better) when compared to the patient group. The mean GDT for the right ear was 8.15 (2.34) and 9.54 (3.67) ms in the RMTS and the LMTS group, respectively, and similarly, for the left ear, it was 7.85 (3.0) ms and 10.15 (4.06) ms, respectively (Table 1). Similarly, the mean percentage of correct identification (PCI) in the control group was found to be higher [69.77 (8.98)% for the right ear and 71.1 (8.89)% for the left ear] than in the patient group. The right ear PCI for the RMTS and the LMTS group was 55.13 (14.47)% and 47.82 (12.7)%, respectively, and for the left ear, it was 51.92 (17.96)% and 48.72 (12.49)%, respectively (Table 1). The GDT and PCI scores of patients with RMTS are depicted as scatter plots in Figs. 1(a) and (b), respectively. A similar depiction of LMTS group

Table 1 Mean and standard deviation scores of test measures across groups. Test measures

Subjects

N

Mean

SD

GDT Rt (ms)

Control RMTS LMTS Control RMTS LMTS Control RMTS LMTS Control RMTS LMTS Control RMTS LMTS Control RMTS LMTS

50 13 13 50 13 13 50 13 13 50 13 13 50 13 13 50 13 13

5.22 8.15 9.54 5.06 7.85 10.15 41.86 33.08 28.69 42.66 31.15 29.23 69.77 55.13 47.82 71.10 51.92 48.72

1.11 2.34 3.67 1.00 3.00 4.06 5.39 8.68 7.62 5.33 10.78 7.5 8.98 14.47 12.7 8.89 17.96 12.49

GDT Lt (ms)

NCR Rt

NCR Lt

PCI Rt (%)

PCI Lt (%)

GDT — gap detection threshold; NCR — number of correct responses; PCI: percentage of correct identification; Rt — right ear; Lt — left ear; RMTS — right mesial temporal sclerosis; LMTS — left mesial temporal sclerosis.

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Fig. 1. (a) Gap detection thresholds of the RMTS group in comparison to a 2-SD reference value of the control group; (b) gap detection thresholds of the LMTS group in comparison to a 2-SD reference value of the control group.

was provided in Figs. 2(a) and (b). To differentiate the normal vs. abnormal scores, a cut-off criterion of two SD [13] from the mean scores of the control group was considered. Accordingly, it was 7.44 ms (right) and 7.06 ms (left) for GDT, which was approximated to 7 ms for both the ears. Similarly, for PCI, two SD scores were 51.8% (right ear) and 53.33% (left ear), which was again approximated to 52% and 53% for the right ear and the left ear, respectively. These cut-off values were similar to the ones reported in the literature, which were 7 ms and 54% for GDT and percentage of correct responses, respectively [13]. The scores were considered abnormal in GDT when it was above (higher threshold) 7 ms and in PCI when it was below (lower identification) 52% and 53% for the right ear and the left ear, respectively. With reference to the above criteria, it was found that 69.23% of patients with RMTS, viz., 9 out of 13 (9/13) patients, and 76.92% of patients with LMTS, viz., 10/13 patients, demonstrated abnormal scores for the GDT right measure. Similarly, for the GDT left measure, 53.85% of patients with RMTS, i.e., 7/13 patients, and 76.92% of patients with LMTS, i.e., 10/13 patients, had abnormal scores. In PCI, 46.15% (6/13 patients) of patients in the RMTS group and 69.23% (9/13 patients) of patients in the LMTS group had abnormal scores in the right ear, whereas 46.15% (6/13 patients) of patients in the RMTS group and 61.54% (8/13 patients) of patients in the LMTS group had abnormal scores in the left ear. Further, the data were evaluated to unravel the bilateral deficits exhibited by the RMTS and the LMTS group. It was arrived through

two steps. Firstly, the number of patients who exhibited abnormal scores in either of the ears was calculated for RMTS and LMTS groups. Secondly, the number of patients who had abnormal scores in both ears among the patients who were identified in the first step was calculated. This provided the number of patients who revealed bilateral deficits among the patients who had abnormal scores in either of the ears. In the RMTS group, 10 patients had abnormal GDT in at least one ear, and among them, 6 (60%) had bilateral involvement. Similarly, of the 7 patients with abnormal PCI scores, 5 (71.43%) had bilateral involvement. In the LMTS group, all 13 patients had abnormal GDT scores, and among them, 7 (53.85%) had bilateral deficits. Further, in 10 patients who had abnormal PCI scores in either ear, 8 patients (80%) had bilateral deficits. However, considering all patients (n = 13) in each patient group, 6/13 (46.15%) and 5/13 (38.46%) of patients with RMTS had bilateral deficits in GDT and PCI measures, respectively. Similarly, 5/13 (53.85%) and 8/13 (61.54%) of the patients with LMTS revealed bilateral deficits. The mean GDT scores and the number of correct responses (NCR) were further analyzed using one-way ANOVA (Table 2), and the analysis revealed significant differences (p = 0.000*) between the groups. Further, post-hoc (Dunnett's) analysis also revealed significant differences (p = 0.000*) in all test measures when the patient groups were compared with the control group. An independent t-test was performed to evaluate for the differences between the RMTS and the LMTS group (Table 3). The results revealed that there were no significant differences in any of the test measures between the groups. It

Fig. 2. (a) Percentage of correct identification of the RMTS group in comparison to a 2-SD reference value of the control group; (b) percentage of correct identification of the LMTS group in comparison to a 2-SD reference value of the control group.

R. Aravindkumar et al. / Epilepsy & Behavior 24 (2012) 126–130 Table 2 Results of one-way ANOVA measure.

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Table 4 Between-the-ears comparison (paired t-test).

Test measures

ANOVA

df

F

Sig.

Test measure

Groups

t

df

Sig. (2-tailed)

GDT Rt

Between groups Within groups Between groups Within groups Between groups Within groups Between groups Within groups

2 73 2 73 2 73 2 73

30.14

0.000⁎

30.93

0.000⁎

GDT Rt vs. Lt

26.36

0.000⁎

1.085 0.574 − 0.553 − 1.534 1.052 − 0.547

49 12 12 49 12 12

0.322 0.576 0.590 0.154 0.313 0.594

28.29

0.000⁎

Control RMTS LMTS Control RMTS LMTS

GDT Lt NCR Rt NCR Lt

GDT — gap detection threshold; NCR — number of correct responses; Rt — right ear; Lt — left ear; RMTS — right mesial temporal sclerosis; LMTS — left mesial temporal sclerosis. ⁎ The mean difference is significant at the .01 level.

was also found that on performing paired sample t-test, there was no significant difference between the right and the left ear either in the control group or in the patient groups (RMTS and LMTS groups) (Table 4). 4. Discussion Auditory temporal resolution, one of the (central) auditory processing mechanisms [(C) AP], refers to the ability of the central auditory system to detect rapid changes in the auditory stimuli. It requires anatomical and functional integrity of the central auditory nervous system. It is thought that the gap detection abilities provide information about the integrity of the central auditory system [25]. Reduction in the ability to detect the gaps has been reported to be associated with aging [10], auditory neuropathy [11] and multiple sclerosis [12]. The present study examined the gap detection ability in patients with refractory complex partial seizures and MTS using the GIN test. On comparison with the control group, the mean GDT right and left scores of the RMTS group were poorer by 2.93 and 2.79 ms, and the LMTS groups were poorer by 4.32 and 5.09 ms, respectively. Similarly, in the PCI measure, the difference (poorer) was 14.64 and 19.18% and 21.95 and 22.38% for RMTS and LMTS groups, respectively, compared to the control group. This suggested an impaired temporal resolution in patients with MTS. It appears that the effect of MTS on the central nervous system makes it vulnerable to temporal processing deficits. Further, it has to be noted that the GIN test was found to be sensitive to cortical lesions [13]. In the current study, among the patients with deficits, more than 50% in the GDT measure and more than 70% in the PCI measure exhibited bilateral deficits. These percentages were arrived at by calculating the number of patients having deficits in both ears among the patients who had abnormal scores in at least one ear. Bi-hemispheric abnormality, viz., physiological and anatomical, had been documented in patients with TLE. Adam et al. [26] reported contralateral propagation of seizures in patients with mesial temporal lobe epilepsy (MTLE) using intracranial EEG recording. They proposed that the seizure activity emerging from the anterior paralimbic regions could propagate to the contralateral medial temporal lobe via the anterior commissure. Further widespread neocortical damage had been reported in patients with MTLE [27,28].

Table 3 Comparison between RMTS and LMTS (independent t-test). Test measures

t

df

Sig. (2-tailed)

GDT Rt GDT Lt NCR Rt NCR Lt

− 1.148 − 1.649 1.368 0.528

20.386 22.082 23.601 21.409

0.264 0.113 0.184 0.603

GDT — gap detection threshold; NCR — number of correct responses; Rt — right ear; Lt — left ear; RMTS — right mesial temporal sclerosis; LMTS — left mesial temporal sclerosis.

NCR Rt vs. Lt

GDT — gap detection threshold; NCR — number of correct responses; Rt — right ear; Lt — left ear; RMTS — right mesial temporal sclerosis; LMTS — left mesial temporal sclerosis.

In a radiological volumetric MRI and cortical reconstruction study on 21 patients with MTLE, McDonald et al. [28] reported bilateral thinning of Heschl's gyrus and ipsilateral thinning of superior and middle temporal gyri, which were not otherwise appreciated on standard imaging. Thus, long-lasting seizure activity may cause indelible damage along the areas it propagates. Hence, bilaterally impaired gap detection abilities as evident from the current study may be due to bi-hemispheric damage as a result of seizure propagation between the hemispheres. The exact reason for bilateral deficits in patients with unilateral MTS is unknown, but this could be due to occult pathology, kindling phenomena or genetic susceptibility. The statistical analysis yielded significant differences (p = 0.000*) in both GDT and NCR measures when the patient groups were compared with the control group. These findings are similar to the earlier studies [13,14]. Attention deficit has been reported to be a co-morbid condition in 30 to 40% of patients with epilepsy [14,29]. The GIN test administered in the current study required the subjects to attend to the gaps and respond. Hence, poorer response by the patient group may be related to attention deficit. To know the effect of this confounding factor, the results of the subtask 4 (attention and calculation) in the MMSE were examined separately. The mean score on this subtask was 3.69 (1.49) and 4 (1.29) for RMTS and LMTS groups, respectively out of the maximum score of 5. The criterion used by Shigemori et al. [30] was adopted in the current study for analyzing the data. Accordingly, individuals scoring 2 points below the maximum in any independent domain (except design copying) was considered as impaired. Hence, a score ≤ 3 was considered abnormal for attention and calculation subtask. Based on this criterion, both RMTS and LMTS groups were further classified into two sub-groups, viz., one with a score of ≤3 and the other with a score of >3. The scores of the right and the left ear were considered separately. Both GDT and NCR were compared among them. Independent t-test revealed no significant difference between the criterion-based sub-groups (Table 5). It may be cautiously inferred that attention deficit may not have a significant role for the impaired GIN performance among the MTS group. However,

Table 5 Within-the-group comparison with reference to the MMSE subtest (attention) score — independent sample t-test. Group

Test measure

t

df

Sig. (2-tailed)

RMTS

GDT_Rt GDT_Lt NCR_Rt NCR_Lt GDT_Rt GDT_Lt NCR_Rt NCR_Lt

− 0.774 − 0.324 1.389 0.553 0.340 0.373 − 0.245 − 0.713

11 11 11 11 11 11 11 11

0.455 0.752 0.192 0.591 0.740 0.716 0.811 0.491

LMTS

GDT — gap detection threshold; NCR — number of correct responses; Rt — right ear; Lt — left ear; RMTS — right mesial temporal sclerosis; LMTS — left mesial temporal sclerosis.

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the role of attention needs to be further ascertained by incorporating a more detailed assessment of the attentional factor. A limitation of the current study is not analyzing the effect of duration and frequency of seizures and antiepileptic drugs. To summarize, this study highlighted the nature of temporal processing deficits in patients with MTS characterized by lack of difference between ears or between those with left or right MTS. Also, there were bilateral deficits in people with unilateral pathology, indicating a bilateral effects.

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