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Language and central temporal auditory processing in childhood epilepsies
Epilepsy & Behavior 53 (2015) 180–183
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Language and central temporal auditory processing in childhood epilepsies Mirela Boscariol a,⁎, Raquel L. Casali b, M. Isabel R. Amaral b, Luciane L. Lunardi a, Carla G. Matas c, M. Francisca Collela-Santos b, Marilisa M. Guerreiro a a b c
Department of Neurology, University of Campinas (UNICAMP), Campinas, Brazil Department of Human Development and Rehabilitation, University of Campinas (UNICAMP), Campinas, Brazil Department of Physiotherapy, Communication Science & Disorders, University of São Paulo (USP), São Paulo, Brazil
a r t i c l e
i n f o
Article history: Received 2 September 2015 Revised 13 October 2015 Accepted 16 October 2015 Available online xxxx Keywords: Rolandic epilepsy Temporal lobe epilepsy Children Language Auditory processing
a b s t r a c t Because of the relationship between rolandic, temporoparietal, and centrotemporal areas and language and auditory processing, the aim of this study was to investigate language and central temporal auditory processing of children with epilepsy (rolandic epilepsy and temporal lobe epilepsy) and compare these with those of children without epilepsy. Thirty-five children aged between eight and 14 years old were studied. Two groups of children participated in this study: a group with childhood epilepsy (n = 19), and a control group without epilepsy or linguistic changes (n = 16). There was a significant difference between the two groups, with the worst performance in children with epilepsy for the gaps-in-noise test, right ear (p b 0.001) and left ear (p b 0.001) tests, and duration pattern test — naming (p = 0.002) and humming (p = 0.002). In auditory P300, there was no significant difference in latency (p = 0.343) and amplitude (p = 0.194) between the groups. There was a significant difference between the groups, with the worst performance in children with epilepsy, for the auditory-receptive vocabulary (PPVT) (p b 0.001) and phonological working memory (nonwords repetition task) tasks (p = 0.001). We conclude that the impairment of central temporal auditory processing and language skills may be comorbidities in children with rolandic epilepsy and temporal lobe epilepsy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction
2. Material and methods
The occurrence of epileptic seizures in the developing brain may impair neurophysiological maturation of neural networks involved in the acquisition of cognitive skills that are fundamental to the learning process. The dysfunction may be due to an abnormal cortical processing, neuronal organization, and functional specialization of the brain [1]. Language and auditory processing areas are mainly located around the Sylvian fissure comprising both rolandic and temporal lobe cortices [2]. Because of the relationship between rolandic, temporoparietal, and centrotemporal areas and language and auditory processing, the aim of this study was to investigate language and centrotemporal auditory processing of children with epilepsy and compare these with those of children without epilepsy. We hypothesized that language and auditory processing dysfunctions may be a comorbidity of rolandic epilepsy and temporal lobe epilepsy due to a maturational deficit caused by epileptic activity in the related brain areas.
This was a cross-sectional comparative study performed at the Department of Neurology and the Laboratory of Audiology of our university. The study was approved by the Ethics Committee (354/2010) and was conducted between 2010 and 2013. Parents agreed to have their children participate, signed a consent form, and answered questions regarding the overall development of the child, the family history of language disorders, and variables of epilepsy (date of seizure onset, clinical features, and treatment).
⁎ Corresponding author at: Department of Neurology, FCM, UNICAMP, 13083-887 Campinas, SP, Brazil. Tel.: +55 19 3521 7372; fax: +55 19 3521 7483. E-mail address: [email protected] (M. Boscariol).
http://dx.doi.org/10.1016/j.yebeh.2015.10.015 1525-5050/© 2015 Elsevier Inc. All rights reserved.
2.1. Participants The study included 35 children of both genders, aged between eight and 14 years old. Children were divided into two groups: a group with childhood epilepsy (n = 19, 14 males, mean age ± SD: 11.56 ± 1.79) and a control group (n = 16, eight males, mean age ± SD: 10.52 ± 1.92) without epilepsy or linguistic changes. We included children with both rolandic epilepsy (n = 12) and temporal lobe epilepsy (n = 7). Eligibility criteria were: children from public elementary school, normal neurological examination, IQ N 80, and normal hearing — based on the findings on otoscopic exam, and an average of pure tone threshold within b15 dB of hearing level at frequencies of 500 Hz and
M. Boscariol et al. / Epilepsy & Behavior 53 (2015) 180–183
181
1, 2, and 4 kHz and “A” type tympanogram. Children of the control group were selected from regular schools according to the same economic background as those with epilepsy and with good school performance according to their teachers.
at 1 Hz. We analyzed the latency and amplitude of the P300 wave in the curve of the rare stimulus.
2.2. Procedures
We applied a protocol of language skills using the Peabody Picture Vocabulary Test (PPVT), Brazilian standardization [8], to evaluate auditory receptive vocabulary and phonological working memory (nonword repetition task) [9].
The diagnosis of epilepsy was performed by a child neurologist and took into account clinical, electroencephalogram, and MRI findings, following ILAE classification [3]. Brain MRI was performed in all children with epilepsy in order to rule out secondary causes of language impairment or other comorbidities. Children of the control group did not undergo MRI; we performed clinical evaluation to rule out language impairment. After the diagnosis of epilepsy, children underwent an assessment of intellectual level with the Wechsler Intelligence Scale for Children — III [4], peripheral audiological evaluation, central auditory processing evaluation by behavioral and electrophysiological auditory tests, and language assessment. Children of the control group underwent peripheral audiological evaluation, central auditory processing evaluation, and language assessment. Peripheral audiological evaluation included pure tone audiometry, speech audiometry, and tympanometry with an AC-30 audiometer and AT235h Interacoustics tympanometer. 2.3. Behavioral auditory testing We performed centrotemporal auditory processing tests with a twochannel AC 40 Interacoustics audiometer to a CD player. The auditory processing tests were: the gaps-in-noise test [5] and duration pattern test (naming and humming) [6]. The gaps-in-noise test evaluates auditory temporal resolution ability. The stimuli were presented at 40 dBSL. The gaps-in-noise test materials consisted of a series of 6-second white noise stimuli in which 0 to 3 silence gaps of different durations (2–6,8,10,12,15,20 ms) were embedded within each segment. The occurrence of gap duration and location within noise segments is pseudorandomized. Every gap appears six times on each list, totalling 60 gaps per ear. The task required was for the child to raise their hand whenever they were able to identify the silence gaps, in milliseconds (ms), distributed along the white noise presentation. The gap detection threshold was defined as the shortest gap duration that the patient was able to identify at least four out of six times [5]. The duration pattern test evaluates the ability of temporal ordering. The presentation level was 40 dBSL. The frequency of tones is held constant at 1000 Hz with two 300-ms intertone intervals, and the duration of tones is the factor to be identified. Short — S (250 ms) and long — L (500 ms) pure tones were presented in six possible combinations of a three-tone sequence (LLS, LSL, LSS, SLS, SLL, and SSL). Thirty sequences were applied in two modalities to each ear: a verbal description of the sequence (naming) and humming. The score calculated was the percentage of correct responses [6]. 2.4. Auditory-evoked potentials We used the EP-25 equipment for assessment of auditory eventrelated potentials (cognitive potential — P300). The P300 was carried out in an electric and sound-attenuated testing room. The electrodes were positioned according to the international electrode system (IES 10–20) on the vertex (Fz), forehead (Fpz), and the right and left ears (A2 and A1) [7]. Electrode impedances were kept less than 5 kΩ. The oddball paradigm was used in the P300 recordings. The child was instructed to pay attention to rare stimuli (2000 Hz) that appeared randomly within a series of frequent stimuli (1000 Hz) and count the number of times that the rare event occurred. The stimulus was a tone burst at 75 dBnHL. A rate of 1.1 tone bursts per second was used (total of 300 sweeps), with the low filter setup at 30 Hz and the high filter
2.5. Language testing
2.6. Data analysis Statistical analysis was conducted using the Statistical Analysis System (SAS) version 9.4. Comparison between the two groups (group with epilepsy and control group) was done by Mann–Whitney test and analysis of variance (ANOVA). The significance level was set at 0.05. 3. Results Table 1 presents the demographic and clinical data of 19 children with epilepsy: 12 with rolandic epilepsy, and seven with temporal lobe epilepsy. There were no significant differences between the group with epilepsy and control group regarding age (p = 0.111) and gender (p = 0.178). Table 2 shows the mean, standard deviation, and significance level of the group with epilepsy and control group in behavioral auditory tests, including the gaps-in-noise test — threshold and percentage of correct answers (right and left ears) — and duration pattern test — naming and humming (right and left ears). For the behavioral auditory tests evaluated, we analyzed the difference between the group with epilepsy and control group and possible differences between right and left ears for each test. We found a significant difference between groups for threshold in the gaps-in-noise test (p b 0.001) and percentage of correct answers in the gaps-in-noise test (p b 0.001). For the duration pattern test — naming (p = 0.002) and humming (p = 0.002), we also found significant differences between the groups. When comparing the left and right ears, we found no significant difference. Table 3 shows the auditory event-related potentials (P300). There was no significant difference in latency (p = 0.34) and amplitude (p = 0.19) when comparing the two groups. There was also no significant difference when comparing the left and right ears for latency (p = 0.56) and amplitude (p = 0.66) in P300. The analysis of the auditory receptive vocabulary test and phonological working memory, when comparing the two groups, showed
Table 1 Demographic and clinical data of children with epilepsy. Pt/Gender
Age
IQ
Seizure onset
Diagnosis
1/M 2/F 3/F 4/M 5/M 6/F 7/M 8/M 9/F 10/M 11/M 12/M 13/M 14/M 15/M 16/F 17/M 18/M 19/M
9 years 6 months 9 years 8 months 9 years 8 months 9 years 10 months 10 years 8 months 11 years 5 months 11 years 6 months 11 years 9 months 12 years 3 months 13 years 11 months 14 years 14 years 11 months 8 years 6 months 9 years 6 months 12 years 1 month 12 years 1 month 12 years 3 months 12 years 9 months 13 years 5 months
91 110 102 106 112 102 108 110 83 140 137 80 103 115 112 91 112 109 117
5 years 7 months 2 years 6 months 4 years 7 months 8 years 10 months 8 years 4 months 1 year 7 months 1 year 6 months 1 year 6 months 1 year 4 months 9 months 4 years 7 months 9 years 2 years 3 years 10 months 1 year 4 months 7 years 5 years 7 years 9 months
RE RE RE RE RE RE RE RE RE RE RE RE TLE TLE TLE TLE TLE TLE TLE
Pt = patient, RE = rolandic epilepsy, TLE = temporal lobe epilepsy.
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M. Boscariol et al. / Epilepsy & Behavior 53 (2015) 180–183
Table 2 Characteristics of auditory processing data.
Table 4 Characteristics of language skills.
Tests
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
Tests
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
GIN (RE) GIN (LE) GIN % (RE) GIN % (LE) DPT — naming (RE) DPT — naming (LE) DPT — humming (RE) DPT — humming (LE)
8.21 ± 2.37 7.47 ± 2.01 62.89 ± 13.37 59.91 ± 10.58 61.19 ± 24.94 54.89 ± 26.44 65.77 ± 22.29 65.94 ± 23.85
4.75 ± 2.37 4.38 ± 0.62 77.81 ± 6.05 78.96 ± 7.52 83.83 ± 9.69 82.00 ± 11.57 88.04 ± 12.28 86.20 ± 10.24
b0.001⁎
PPVT Phonological working memory
76.11 ± 20.01 66.21 ± 9.57
100.06 ± 14.17 75.44 ± 3.61
b0.001⁎ 0.001⁎
b0.001⁎ 0.002⁎ 0.002⁎
RE: right ear, LE: left ear, DPT: duration pattern test, GIN: gaps-in-noise. ⁎ Statistically significant difference.
significant differences in receptive vocabulary (p b 0.001) and phonological working memory (p = 0.001). The mean, standard deviation, and significance level obtained in the tests of language skills are shown in Table 4. There was no qualitative difference between the two groups with epilepsy when receptive vocabulary and phonological working memory were analyzed. Nevertheless, we have not performed statistical analysis of the epilepsy groups because of the small number of children per group: rolandic epilepsy = 12 and temporal lobe epilepsy = 7. 4. Discussion We sought to investigate the comorbidity between two types of epilepsy (rolandic epilepsy and temporal lobe epilepsy) and language and auditory processing in children. When comparing behavioral auditory tests, we observed a significant difference in auditory processing skills with worse performance in the group with epilepsy in the gaps-in-noise test and duration pattern test (naming and humming). Poor performance in temporal abilities in children with epilepsy may be due to the proximity of the rolandic and centrotemporal areas with the Heschl gyrus. The primary auditory cortex plays an important role in fine discrimination of frequencies (cortical tonotopic organization). The auditory function may be altered if there is a maturational deficit caused by epileptic activity in this brain area [10]. The gaps-in-noise test is a temporal resolution test and is sensitive to the presence of cortical lesions in the temporal lobe and in the central auditory nervous system [5]. It refers to the shortest interval of time that an individual is able to discriminate between two stimuli. Our study showed that children with epilepsy may have more difficulty in identifying smaller intervals of silence, when compared with the control group, leading to difficulty in speech understanding and learning abilities. Based on our results, we propose that the brains of children with epilepsy may harbor subtle changes in the contralateral auditory pathways. The ability to recognize, identify, and perform a sequence of auditory patterns requires integration of information from both hemispheres, and the duration pattern test is sensitive to hemispheric lesions and interhemispheric dysfunction [11]. Furthermore, poor performance in the duration pattern test (naming and humming) is related to difficulty in recognizing and naming temporal patterns, and difficulty in prosody, nonverbal aspects, and suprasegmental speech [12]. Table 3 Data of auditory event-related potentials — P300.
Latency (RE) Latency (LE) Amplitude (RE) Amplitude (LE) RE: right ear, LE: left ear.
PPVT: Peabody picture vocabulary test. ⁎ Statistically significant difference.
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
330.84 ± 30.18 323.05 ± 29.37 4.63 ± 2.99 4.90 ± 2.78
317.50 ± 28.17 318.50 ± 28.13 5.88 ± 2.18 5.67 ± 2.61
0.343 0.194
As for the cognitive potential P300, our study found no difference between the groups. Other studies comparing children with temporal lobe epilepsy and healthy controls also found no difference in auditory P300 [13,14]. Concerning language, we observed a statistically significant difference in phonological working memory (nonwords repetition task) and auditory-receptive vocabulary (Peabody Picture Vocabulary Test — PPVT). The auditory-receptive vocabulary (PPVT) evaluates the level of understanding when hearing the words in various categories. It requires the use of inferences about the meaning of familiar or unfamiliar words [8]. We found significant differences between children with epilepsy and the control group, showing an impairment in receptive vocabulary in children with epilepsy. This finding is in keeping with others [15]. Phonological working memory is the ability to maintain, manipulate, and retrieve short-term verbal information. The working memory involves perceptual and memory encoding, maintenance, and retrieval. Intracerebral EEG studies in patients with epilepsy showed an increase of gamma band activity in regions associated with the phonological loop, such as Broca's area and the auditory cortex, the prefrontal cortex, the pre- and postcentral gyri, the hippocampus, and the fusiform gyrus [16]. Our study showed an impairment in phonological working memory (nonwords repetition task), suggesting that involvement in the perisylvian and centrotemporal regions can impair working memory. Our study also showed an impairment in tasks involving interhemispheric transfer (corpus callosum) and the primary auditory cortex, also related to an impairment in working memory, association, and recognition of reading. In rolandic epilepsy, electrical discharges concentrate in the central region, predominantly in the low rolandic area and perisylvian region, and may extend to the adjacent temporoparietal region, resulting in an impairment in language and auditory processing [17,18]. In temporal lobe epilepsy, deficits in language and auditory processing may be associated with temporal damage and dysfunction of extratemporal regions. Abnormalities in the extratemporal region (reduction of gray matter) and functional alterations in these children can be correlated with dysfunction in neural networks due to early brain injury in areas important for cognitive development [19]. Other studies have shown that patients with temporal lobe epilepsy showed poor performance in temporal ordering, dichotic listening, and processing of rapid auditory information [20,21], as well as impairment of phonological, semantic, and verbal working memories [22]. 5. Conclusion Our findings showed that children with epilepsy may present with impairment in language skills and central auditory processing. Longitudinal studies with larger populations may help us better understand the difficulties of language and auditory processing in these children and to guide more effective rehabilitation planning. Acknowledgments Mirela Boscariol received a scholarship from FAPESP (grant number # 2010/07438-3). Luciane L. Lunardi, Maria Isabel Ramos do Amaral, and Raquel Leme Casali received a scholarship from CAPES Foundation.
M. Boscariol et al. / Epilepsy & Behavior 53 (2015) 180–183
Conflict of interest statement The authors declare no conflict of interest. References [1] Flax JF, Realpe-Bonilla T, Hirsch LS, Brzustowicz LM, Bartlett CW, Tallal P. Specific language impairment in families: evidence for co-occurrence with reading impairments. J Speech Lang Hear Res 2003;46:530–43. [2] Damasio AR, Damasio H. Aphasia and the neural basis of language. In: Mesulam M-M, editor. Principles of behavioral and cognitive neurology. 2nd ed. Oxford: Oxford University Press; 2000. p. 294–315. [3] Berg AT, Berkovic S, Brodie MJ, Buchhalter J, Cross JH, van Emde Boas W, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 2010;51:676–85. [4] Wechsler D. WISC III: Wechsler Intelligence Scale for Children — manual. 3rd ed.; 1991. Adaptação e padronização de uma amostra brasileira. Figueiredo VLM. São Paulo: Casa do Psicólogo; 2002. [5] Musiek FE, Shinn JB, Jirsa R, Bamiou DE, Baran JA, Zaidan E. GIN (gaps-in-noise) test performance in subjects with confirmed central auditory nervous system involvement. Ear Hear 2005;26:608–18. [6] Musiek F. Frequency (pitch) and duration pattern tests. J Am Acad Audiol 1994;5: 265–8. [7] Klem GH, Lüders HO, Jasper HH, Elger C. The ten–twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52:3–6. [8] Capovilla FC, Capovilla AGS. Desenvolvimento linguístico na criança brasileira, dos dois aos seis anos: tradução e estandardização do Peabody Picture Vocabulary Test e da Language Development Survey de Rescorla. Ciênc Cogn 1997;1:353–80. [9] Grivol MA, Hage SRV. Phonological working memory: a comparative study between different age groups. J Soc Bras Fonoaudiol 2011;23:245–51.
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[10] Lundberg S, Frylmark A, Eeg-Olofsson O. Children with rolandic epilepsy have abnormalities of oromotor and dichotic listening performance. Dev Med Child Neurol 2005;47:603–8. [11] Musiek F, Baran J, Pinheiro M. Duration pattern recognition in normal subjects and patients with cerebral and cochlear lesions. Audiology 1990;29:304–13. [12] Banai K, Kraus N. Neurobiology of (central) auditory processing disorder and language-based learning disability. In: Musiek FE, Chermak GD, editors. Handbook of (central) auditory processing disorder: auditory neuroscience and diagnosis. San Diego: Singular Publishing Group; 2007. p. 89–116. [13] Sunaga Y, Hikima A, Otsuka T, Nagashima K, Kuroume T. P300 event-related potentials in epileptic children. Clin Electroencephalogr 1994;25:13–7. [14] Chayasirisobhon WV, Chayasirisobhon S, Tin SN, Leu N, Tehrani K, McGuckin JS. Scalp-recorded auditory P300 event-related potentials in new-onset untreated temporal lobe epilepsy. Clin EEG Neurosci 2007;38:168–71. [15] Verrotti A, D'Egidio C, Agostinelli S, Parisi P, Chiarelli F, Coppola G. Cognitive and linguistic abnormalities in benign childhood epilepsy with centrotemporal spikes. Acta Paediatr 2011;100:768–72. [16] Mainy N, Kahane P, Minotti L, Hoffmann D, Bertrand O, Lachaux JP. Neural correlates of consolidation in working memory. Hum Brain Mapp 2007;28:183–93. [17] Staden U, Isaacs E, Boyd SG, Brandl U, Neville BG. Language dysfunction in children with rolandic epilepsy. Neuropediatrics 1998;29:242–8. [18] Wong PK. Source modelling of the rolandic focus. Brain Topogr 1991;4:105–12. [19] Guimarães CA, Min LL, Rzezak P, Fuentes D, Franzon RC, Montenegro MA, et al. Temporal lobe epilepsy in childhood: comprehensive neuropsychological assessment. J Child Neurol 2007;22:836–40. [20] Ehrlé N, Samson S, Baulac M. Processing of rapid auditory information in epileptic patients with left temporal lobe damage. Neuropsychologia 2001;39:525–31. [21] Meneguello J, Leonhardt FD, Pereira LD. Auditory processing in patients with temporal lobe epilepsy. Braz J Otorhinolaryngol 2006;72:496–504. [22] Chaix Y, Laguitton V, Lauwers-Cancès V, Daquin G, Cancès C, Démonet JF, et al. Reading abilities and cognitive functions of children with epilepsy: influence of epileptic syndrome. Brain Dev 2006;28:122–30.
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Language and central temporal auditory processing in childhood epilepsies Mirela Boscariol a,⁎, Raquel L. Casali b, M. Isabel R. Amaral b, Luciane L. Lunardi a, Carla G. Matas c, M. Francisca Collela-Santos b, Marilisa M. Guerreiro a a b c
Department of Neurology, University of Campinas (UNICAMP), Campinas, Brazil Department of Human Development and Rehabilitation, University of Campinas (UNICAMP), Campinas, Brazil Department of Physiotherapy, Communication Science & Disorders, University of São Paulo (USP), São Paulo, Brazil
a r t i c l e
i n f o
Article history: Received 2 September 2015 Revised 13 October 2015 Accepted 16 October 2015 Available online xxxx Keywords: Rolandic epilepsy Temporal lobe epilepsy Children Language Auditory processing
a b s t r a c t Because of the relationship between rolandic, temporoparietal, and centrotemporal areas and language and auditory processing, the aim of this study was to investigate language and central temporal auditory processing of children with epilepsy (rolandic epilepsy and temporal lobe epilepsy) and compare these with those of children without epilepsy. Thirty-five children aged between eight and 14 years old were studied. Two groups of children participated in this study: a group with childhood epilepsy (n = 19), and a control group without epilepsy or linguistic changes (n = 16). There was a significant difference between the two groups, with the worst performance in children with epilepsy for the gaps-in-noise test, right ear (p b 0.001) and left ear (p b 0.001) tests, and duration pattern test — naming (p = 0.002) and humming (p = 0.002). In auditory P300, there was no significant difference in latency (p = 0.343) and amplitude (p = 0.194) between the groups. There was a significant difference between the groups, with the worst performance in children with epilepsy, for the auditory-receptive vocabulary (PPVT) (p b 0.001) and phonological working memory (nonwords repetition task) tasks (p = 0.001). We conclude that the impairment of central temporal auditory processing and language skills may be comorbidities in children with rolandic epilepsy and temporal lobe epilepsy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction
2. Material and methods
The occurrence of epileptic seizures in the developing brain may impair neurophysiological maturation of neural networks involved in the acquisition of cognitive skills that are fundamental to the learning process. The dysfunction may be due to an abnormal cortical processing, neuronal organization, and functional specialization of the brain [1]. Language and auditory processing areas are mainly located around the Sylvian fissure comprising both rolandic and temporal lobe cortices [2]. Because of the relationship between rolandic, temporoparietal, and centrotemporal areas and language and auditory processing, the aim of this study was to investigate language and centrotemporal auditory processing of children with epilepsy and compare these with those of children without epilepsy. We hypothesized that language and auditory processing dysfunctions may be a comorbidity of rolandic epilepsy and temporal lobe epilepsy due to a maturational deficit caused by epileptic activity in the related brain areas.
This was a cross-sectional comparative study performed at the Department of Neurology and the Laboratory of Audiology of our university. The study was approved by the Ethics Committee (354/2010) and was conducted between 2010 and 2013. Parents agreed to have their children participate, signed a consent form, and answered questions regarding the overall development of the child, the family history of language disorders, and variables of epilepsy (date of seizure onset, clinical features, and treatment).
⁎ Corresponding author at: Department of Neurology, FCM, UNICAMP, 13083-887 Campinas, SP, Brazil. Tel.: +55 19 3521 7372; fax: +55 19 3521 7483. E-mail address: [email protected] (M. Boscariol).
http://dx.doi.org/10.1016/j.yebeh.2015.10.015 1525-5050/© 2015 Elsevier Inc. All rights reserved.
2.1. Participants The study included 35 children of both genders, aged between eight and 14 years old. Children were divided into two groups: a group with childhood epilepsy (n = 19, 14 males, mean age ± SD: 11.56 ± 1.79) and a control group (n = 16, eight males, mean age ± SD: 10.52 ± 1.92) without epilepsy or linguistic changes. We included children with both rolandic epilepsy (n = 12) and temporal lobe epilepsy (n = 7). Eligibility criteria were: children from public elementary school, normal neurological examination, IQ N 80, and normal hearing — based on the findings on otoscopic exam, and an average of pure tone threshold within b15 dB of hearing level at frequencies of 500 Hz and
M. Boscariol et al. / Epilepsy & Behavior 53 (2015) 180–183
181
1, 2, and 4 kHz and “A” type tympanogram. Children of the control group were selected from regular schools according to the same economic background as those with epilepsy and with good school performance according to their teachers.
at 1 Hz. We analyzed the latency and amplitude of the P300 wave in the curve of the rare stimulus.
2.2. Procedures
We applied a protocol of language skills using the Peabody Picture Vocabulary Test (PPVT), Brazilian standardization [8], to evaluate auditory receptive vocabulary and phonological working memory (nonword repetition task) [9].
The diagnosis of epilepsy was performed by a child neurologist and took into account clinical, electroencephalogram, and MRI findings, following ILAE classification [3]. Brain MRI was performed in all children with epilepsy in order to rule out secondary causes of language impairment or other comorbidities. Children of the control group did not undergo MRI; we performed clinical evaluation to rule out language impairment. After the diagnosis of epilepsy, children underwent an assessment of intellectual level with the Wechsler Intelligence Scale for Children — III [4], peripheral audiological evaluation, central auditory processing evaluation by behavioral and electrophysiological auditory tests, and language assessment. Children of the control group underwent peripheral audiological evaluation, central auditory processing evaluation, and language assessment. Peripheral audiological evaluation included pure tone audiometry, speech audiometry, and tympanometry with an AC-30 audiometer and AT235h Interacoustics tympanometer. 2.3. Behavioral auditory testing We performed centrotemporal auditory processing tests with a twochannel AC 40 Interacoustics audiometer to a CD player. The auditory processing tests were: the gaps-in-noise test [5] and duration pattern test (naming and humming) [6]. The gaps-in-noise test evaluates auditory temporal resolution ability. The stimuli were presented at 40 dBSL. The gaps-in-noise test materials consisted of a series of 6-second white noise stimuli in which 0 to 3 silence gaps of different durations (2–6,8,10,12,15,20 ms) were embedded within each segment. The occurrence of gap duration and location within noise segments is pseudorandomized. Every gap appears six times on each list, totalling 60 gaps per ear. The task required was for the child to raise their hand whenever they were able to identify the silence gaps, in milliseconds (ms), distributed along the white noise presentation. The gap detection threshold was defined as the shortest gap duration that the patient was able to identify at least four out of six times [5]. The duration pattern test evaluates the ability of temporal ordering. The presentation level was 40 dBSL. The frequency of tones is held constant at 1000 Hz with two 300-ms intertone intervals, and the duration of tones is the factor to be identified. Short — S (250 ms) and long — L (500 ms) pure tones were presented in six possible combinations of a three-tone sequence (LLS, LSL, LSS, SLS, SLL, and SSL). Thirty sequences were applied in two modalities to each ear: a verbal description of the sequence (naming) and humming. The score calculated was the percentage of correct responses [6]. 2.4. Auditory-evoked potentials We used the EP-25 equipment for assessment of auditory eventrelated potentials (cognitive potential — P300). The P300 was carried out in an electric and sound-attenuated testing room. The electrodes were positioned according to the international electrode system (IES 10–20) on the vertex (Fz), forehead (Fpz), and the right and left ears (A2 and A1) [7]. Electrode impedances were kept less than 5 kΩ. The oddball paradigm was used in the P300 recordings. The child was instructed to pay attention to rare stimuli (2000 Hz) that appeared randomly within a series of frequent stimuli (1000 Hz) and count the number of times that the rare event occurred. The stimulus was a tone burst at 75 dBnHL. A rate of 1.1 tone bursts per second was used (total of 300 sweeps), with the low filter setup at 30 Hz and the high filter
2.5. Language testing
2.6. Data analysis Statistical analysis was conducted using the Statistical Analysis System (SAS) version 9.4. Comparison between the two groups (group with epilepsy and control group) was done by Mann–Whitney test and analysis of variance (ANOVA). The significance level was set at 0.05. 3. Results Table 1 presents the demographic and clinical data of 19 children with epilepsy: 12 with rolandic epilepsy, and seven with temporal lobe epilepsy. There were no significant differences between the group with epilepsy and control group regarding age (p = 0.111) and gender (p = 0.178). Table 2 shows the mean, standard deviation, and significance level of the group with epilepsy and control group in behavioral auditory tests, including the gaps-in-noise test — threshold and percentage of correct answers (right and left ears) — and duration pattern test — naming and humming (right and left ears). For the behavioral auditory tests evaluated, we analyzed the difference between the group with epilepsy and control group and possible differences between right and left ears for each test. We found a significant difference between groups for threshold in the gaps-in-noise test (p b 0.001) and percentage of correct answers in the gaps-in-noise test (p b 0.001). For the duration pattern test — naming (p = 0.002) and humming (p = 0.002), we also found significant differences between the groups. When comparing the left and right ears, we found no significant difference. Table 3 shows the auditory event-related potentials (P300). There was no significant difference in latency (p = 0.34) and amplitude (p = 0.19) when comparing the two groups. There was also no significant difference when comparing the left and right ears for latency (p = 0.56) and amplitude (p = 0.66) in P300. The analysis of the auditory receptive vocabulary test and phonological working memory, when comparing the two groups, showed
Table 1 Demographic and clinical data of children with epilepsy. Pt/Gender
Age
IQ
Seizure onset
Diagnosis
1/M 2/F 3/F 4/M 5/M 6/F 7/M 8/M 9/F 10/M 11/M 12/M 13/M 14/M 15/M 16/F 17/M 18/M 19/M
9 years 6 months 9 years 8 months 9 years 8 months 9 years 10 months 10 years 8 months 11 years 5 months 11 years 6 months 11 years 9 months 12 years 3 months 13 years 11 months 14 years 14 years 11 months 8 years 6 months 9 years 6 months 12 years 1 month 12 years 1 month 12 years 3 months 12 years 9 months 13 years 5 months
91 110 102 106 112 102 108 110 83 140 137 80 103 115 112 91 112 109 117
5 years 7 months 2 years 6 months 4 years 7 months 8 years 10 months 8 years 4 months 1 year 7 months 1 year 6 months 1 year 6 months 1 year 4 months 9 months 4 years 7 months 9 years 2 years 3 years 10 months 1 year 4 months 7 years 5 years 7 years 9 months
RE RE RE RE RE RE RE RE RE RE RE RE TLE TLE TLE TLE TLE TLE TLE
Pt = patient, RE = rolandic epilepsy, TLE = temporal lobe epilepsy.
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Table 2 Characteristics of auditory processing data.
Table 4 Characteristics of language skills.
Tests
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
Tests
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
GIN (RE) GIN (LE) GIN % (RE) GIN % (LE) DPT — naming (RE) DPT — naming (LE) DPT — humming (RE) DPT — humming (LE)
8.21 ± 2.37 7.47 ± 2.01 62.89 ± 13.37 59.91 ± 10.58 61.19 ± 24.94 54.89 ± 26.44 65.77 ± 22.29 65.94 ± 23.85
4.75 ± 2.37 4.38 ± 0.62 77.81 ± 6.05 78.96 ± 7.52 83.83 ± 9.69 82.00 ± 11.57 88.04 ± 12.28 86.20 ± 10.24
b0.001⁎
PPVT Phonological working memory
76.11 ± 20.01 66.21 ± 9.57
100.06 ± 14.17 75.44 ± 3.61
b0.001⁎ 0.001⁎
b0.001⁎ 0.002⁎ 0.002⁎
RE: right ear, LE: left ear, DPT: duration pattern test, GIN: gaps-in-noise. ⁎ Statistically significant difference.
significant differences in receptive vocabulary (p b 0.001) and phonological working memory (p = 0.001). The mean, standard deviation, and significance level obtained in the tests of language skills are shown in Table 4. There was no qualitative difference between the two groups with epilepsy when receptive vocabulary and phonological working memory were analyzed. Nevertheless, we have not performed statistical analysis of the epilepsy groups because of the small number of children per group: rolandic epilepsy = 12 and temporal lobe epilepsy = 7. 4. Discussion We sought to investigate the comorbidity between two types of epilepsy (rolandic epilepsy and temporal lobe epilepsy) and language and auditory processing in children. When comparing behavioral auditory tests, we observed a significant difference in auditory processing skills with worse performance in the group with epilepsy in the gaps-in-noise test and duration pattern test (naming and humming). Poor performance in temporal abilities in children with epilepsy may be due to the proximity of the rolandic and centrotemporal areas with the Heschl gyrus. The primary auditory cortex plays an important role in fine discrimination of frequencies (cortical tonotopic organization). The auditory function may be altered if there is a maturational deficit caused by epileptic activity in this brain area [10]. The gaps-in-noise test is a temporal resolution test and is sensitive to the presence of cortical lesions in the temporal lobe and in the central auditory nervous system [5]. It refers to the shortest interval of time that an individual is able to discriminate between two stimuli. Our study showed that children with epilepsy may have more difficulty in identifying smaller intervals of silence, when compared with the control group, leading to difficulty in speech understanding and learning abilities. Based on our results, we propose that the brains of children with epilepsy may harbor subtle changes in the contralateral auditory pathways. The ability to recognize, identify, and perform a sequence of auditory patterns requires integration of information from both hemispheres, and the duration pattern test is sensitive to hemispheric lesions and interhemispheric dysfunction [11]. Furthermore, poor performance in the duration pattern test (naming and humming) is related to difficulty in recognizing and naming temporal patterns, and difficulty in prosody, nonverbal aspects, and suprasegmental speech [12]. Table 3 Data of auditory event-related potentials — P300.
Latency (RE) Latency (LE) Amplitude (RE) Amplitude (LE) RE: right ear, LE: left ear.
PPVT: Peabody picture vocabulary test. ⁎ Statistically significant difference.
Epilepsy (N = 19) Mean ± SD
Control (N = 16) Mean ± SD
p
330.84 ± 30.18 323.05 ± 29.37 4.63 ± 2.99 4.90 ± 2.78
317.50 ± 28.17 318.50 ± 28.13 5.88 ± 2.18 5.67 ± 2.61
0.343 0.194
As for the cognitive potential P300, our study found no difference between the groups. Other studies comparing children with temporal lobe epilepsy and healthy controls also found no difference in auditory P300 [13,14]. Concerning language, we observed a statistically significant difference in phonological working memory (nonwords repetition task) and auditory-receptive vocabulary (Peabody Picture Vocabulary Test — PPVT). The auditory-receptive vocabulary (PPVT) evaluates the level of understanding when hearing the words in various categories. It requires the use of inferences about the meaning of familiar or unfamiliar words [8]. We found significant differences between children with epilepsy and the control group, showing an impairment in receptive vocabulary in children with epilepsy. This finding is in keeping with others [15]. Phonological working memory is the ability to maintain, manipulate, and retrieve short-term verbal information. The working memory involves perceptual and memory encoding, maintenance, and retrieval. Intracerebral EEG studies in patients with epilepsy showed an increase of gamma band activity in regions associated with the phonological loop, such as Broca's area and the auditory cortex, the prefrontal cortex, the pre- and postcentral gyri, the hippocampus, and the fusiform gyrus [16]. Our study showed an impairment in phonological working memory (nonwords repetition task), suggesting that involvement in the perisylvian and centrotemporal regions can impair working memory. Our study also showed an impairment in tasks involving interhemispheric transfer (corpus callosum) and the primary auditory cortex, also related to an impairment in working memory, association, and recognition of reading. In rolandic epilepsy, electrical discharges concentrate in the central region, predominantly in the low rolandic area and perisylvian region, and may extend to the adjacent temporoparietal region, resulting in an impairment in language and auditory processing [17,18]. In temporal lobe epilepsy, deficits in language and auditory processing may be associated with temporal damage and dysfunction of extratemporal regions. Abnormalities in the extratemporal region (reduction of gray matter) and functional alterations in these children can be correlated with dysfunction in neural networks due to early brain injury in areas important for cognitive development [19]. Other studies have shown that patients with temporal lobe epilepsy showed poor performance in temporal ordering, dichotic listening, and processing of rapid auditory information [20,21], as well as impairment of phonological, semantic, and verbal working memories [22]. 5. Conclusion Our findings showed that children with epilepsy may present with impairment in language skills and central auditory processing. Longitudinal studies with larger populations may help us better understand the difficulties of language and auditory processing in these children and to guide more effective rehabilitation planning. Acknowledgments Mirela Boscariol received a scholarship from FAPESP (grant number # 2010/07438-3). Luciane L. Lunardi, Maria Isabel Ramos do Amaral, and Raquel Leme Casali received a scholarship from CAPES Foundation.
M. Boscariol et al. / Epilepsy & Behavior 53 (2015) 180–183
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