Study of the cognition in patients with benign epilepsy of childhood with centrotemporal spikes by using the ReHo, ALFF, fALFF of RS-fMRI_Journal of Epilepsy

Authors：

QU Bingqian ¹ ,  YU Qing ¹ , YAN Xinxin ¹ , YANG Qianqian ¹ , LI Nana ¹ , ZHANG Qingqing ¹ , PANG Jie ¹ , CHEN Ying ¹ , YAO Xiaojuan ¹ , YANG Weidong ² , CHEN Zhijuan ² , YIN Jianzhong ³ , LIU Na ³ , TAN Ke ⁴

1. Department of Neurology, Tianjin Medical University General Hospital, Tianjin 300052, China;
2. Department of Neurosurgery, Tianjin Medical University General Hospital Tianjin, 300052, China;
3. Department of Radiology, Tianjin First Central Hospital, Tianjin 300192, China;
4. Department of Behavior and Psychology, Tianjin Normal University, Tianjin 300387, China;

Corresponding author：

YU Qing, Email: yq_yuqing@163.com

Keywords：

Benign epilepsy of childhood with centrotemporal spikes; Resting-state function magnetic resonance imaging; Spike-wave index; Cognition

DOI：

10.7507/2096-0247.20180076

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Objective The ReHo, ALFF, fALFF of resting-state functional magnetic resonance imaging (RS-fMRI) technology were used to study the influencing factors and neural mechanism of cognitive dysfunction in patients with benign epilepsy of childhood with centrotemporal spikes (BECT). Methods Fourteen patients were enrolled (from April 2015 to March 2018) from epilepsy specialist outpatients and Functional Department of Neurosurgery of Tianjin Medical University General Hospital. They underwent the long term VEEG monitoring (one sleep cycle was included at least), the Wechsler Intelligence Scale (China Revised), the head MRI and RS-fMRI examinations. Spike-wave index (SWI), FIQ, VIQ, PIQ scores were calculated. According to full-scale IQ (FIQ), they were divided into two groups: FIQ<90 (scores range from 70 to 89, the average score was 78.3±8.9, 6 cases) and FIQ≥90 (scores range from 90 to 126, the average score was 116.6±12.9, 8 cases). SPSS21.0 statistical software was used to compare the general clinical data and SWI of the two groups, and the correlation between clinical factors and the evaluation results of Wechsler Intelligence Scale was analyzed. The RS-fMRI images were preprocessed and the further data were analysed by two independent samplest-test under the whole brain of regional homogeneity (ReHo), amplitude of low frequency fluctuation (ALFF) and fractional of ALFF (fALFF) methods. The differences of brain activation regions in RS-fMRI between the two groups were observed, and the results of general clinical data, SWI and cognitive function test were compared and analyzed comprehensively. Results The differences of SWI were statistically significant (P<0.05): FIQ<90 group were greater than FIQ≥90 group. The FIQ, VIQ and PIQ of two groups were negatively correlated with SWI (P<0.05). And the FIQ and PIQ were negatively correlated with the total number of seizures (P<0.05). Compared with FIQ≥90 group by two samplet-test based on whole level ReHo, ALFF, fALFF methods, deactivation of brain regions of FIQ<90 group include bilateral precuneus, posterior cingulate and occipital lobe, and enhanced activation of brain regions include left prefrontal cortex, bilateral superior frontal gyrus medial and right precentral gyrus, supplementary motor area, angular gyrus, supramarginal gyrus, middle temporal gyrus, bilateral insular lobe and subcortical gray matter structures. Conclusions Frequent epileptic discharges during slow wave sleep and recurrent clinical episodes were risk factors for cognitive impairment in BECT patients. Repeated clinical seizures and frequent subclinical discharges could cause dysfunction of local brain areas associated with cognition and the default network, resulting in patients with impaired cognitive function.

Citation： QU Bingqian, YU Qing, YAN Xinxin, YANG Qianqian, LI Nana, ZHANG Qingqing, PANG Jie, CHEN Ying, YAO Xiaojuan, YANG Weidong, CHEN Zhijuan, YIN Jianzhong, LIU Na, TAN Ke. Study of the cognition in patients with benign epilepsy of childhood with centrotemporal spikes by using the ReHo, ALFF, fALFF of RS-fMRI. Journal of Epilepsy, 2018, 4(6): 473-479. doi: 10.7507/2096-0247.20180076 Copy

1.	Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia, 1989, 30(4): 389-399.
2.	Camfield P, Camfield C. Epileptic syndromes in childhood: clinical features, outcomes, and treatment. Epilepsia, 2002, 43(Suppl 3): 27-32.
3.	Blom S, Heijbel J. Benign epilepsy of children with centrotemporal EEG foci: a follow-up study in adulthood of patients initially studied as children. Epilepsia, 1982, 23(6): 629-632.
4.	Datta AN, Oser N, Bauder F, et al. Cognitive impairment and cortical reorganization in children with benign epilepsy with centrotemporal spikes. Epilepsia, 2013, 54(3): 487-494.
5.	Verrotti A, Filippini M, Matricardi S, et al. Memory impairment and Benign Epilepsy with centrotemporal spike (BECTS): a growing suspicion. Brain Cogn, 2014, 84(1): 123-131.
6.	Vannest J, Tenney JR, Gelineau-Morel R, et al. Cognitive and behavioral outcomes in benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav, 2015, 45: 85-91.
7.	Gobbi G, Boni A, Filippini M. The spectrum of idiopathic Rolandic epilepsy syndromes and idiopathic occipital epilepsies: from the benign to the disabling. Epilepsia, 2006, 47(Suppl 2): 62-66.
8.	Engel JJ. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia, 2001, 42(6): 796-803.
9.	Overvliet GM, Aldenkamp AP, Klinkenberg S, et al. Impaired language performance as a precursor or consequence of Rolandic epilepsy? J Neurol Sci, 2011, 304(1-2): 71-74.
10.	Neri ML, Guimaraes CA, Oliveira EP, et al. Neuropsychological assessment of children with rolandic epilepsy: executive functions. Epilepsy Behav, 2012, 24(4): 403-407.
11.	Deltour L, Quaglino V, Barathon M, et al. Clinical evaluation of attentional processes in children with benign childhood epilepsy with centrotemporal spikes (BCECTS). Epileptic Disord, 2007, 9(4): 424-431.
12.	Tang YL, Ji GJ, Yu Y, et al. Altered regional homogeneity in rolandic epilepsy: a resting-state FMRI study. Biomed Res Int, 2014, 2014: 960395.
13.	Kanemura H, Hata S, Aoyagi K, et al. Serial changes of prefrontal lobe growth in the patients with benign childhood epilepsy with centrotemporal spikes presenting with cognitive impairments/behavioral problems. Brain Dev, 2011, 33(2): 106-113.
14.	Lin JJ, Riley JD, Hsu DA, et al. Striatal hypertrophy and its cognitive effects in new-onset benign epilepsy with centrotemporal spikes. Epilepsia, 2012, 53(4): 677-685.
15.	Friston K. Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Annu Rev Neurosci, 2002, 25: 221-250.
16.	McIntosh AR. Towards a network theory of cognition. Neural Netw, 2000, 13(8-9): 861-870.
17.	Oser N, Hubacher M, Specht K, et al. Default mode network alterations during language task performance in children with benign epilepsy with centrotemporal spikes (BECTS). Epilepsy Behav, 2014, 33: 12-17.
18.	Zeng H, Ramos CG, Nair VA, et al. Regional homogeneity (ReHo) changes in new onset versus chronic benign epilepsy of childhood with centrotemporal spikes (BECTS): A resting state fMRI study. Epilepsy Res, 2015, 116: 79-85.

1. Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia, 1989, 30(4): 389-399.
2. Camfield P, Camfield C. Epileptic syndromes in childhood: clinical features, outcomes, and treatment. Epilepsia, 2002, 43(Suppl 3): 27-32.
3. Blom S, Heijbel J. Benign epilepsy of children with centrotemporal EEG foci: a follow-up study in adulthood of patients initially studied as children. Epilepsia, 1982, 23(6): 629-632.
4. Datta AN, Oser N, Bauder F, et al. Cognitive impairment and cortical reorganization in children with benign epilepsy with centrotemporal spikes. Epilepsia, 2013, 54(3): 487-494.
5. Verrotti A, Filippini M, Matricardi S, et al. Memory impairment and Benign Epilepsy with centrotemporal spike (BECTS): a growing suspicion. Brain Cogn, 2014, 84(1): 123-131.
6. Vannest J, Tenney JR, Gelineau-Morel R, et al. Cognitive and behavioral outcomes in benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav, 2015, 45: 85-91.
7. Gobbi G, Boni A, Filippini M. The spectrum of idiopathic Rolandic epilepsy syndromes and idiopathic occipital epilepsies: from the benign to the disabling. Epilepsia, 2006, 47(Suppl 2): 62-66.
8. Engel JJ. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia, 2001, 42(6): 796-803.
9. Overvliet GM, Aldenkamp AP, Klinkenberg S, et al. Impaired language performance as a precursor or consequence of Rolandic epilepsy? J Neurol Sci, 2011, 304(1-2): 71-74.
10. Neri ML, Guimaraes CA, Oliveira EP, et al. Neuropsychological assessment of children with rolandic epilepsy: executive functions. Epilepsy Behav, 2012, 24(4): 403-407.
11. Deltour L, Quaglino V, Barathon M, et al. Clinical evaluation of attentional processes in children with benign childhood epilepsy with centrotemporal spikes (BCECTS). Epileptic Disord, 2007, 9(4): 424-431.
12. Tang YL, Ji GJ, Yu Y, et al. Altered regional homogeneity in rolandic epilepsy: a resting-state FMRI study. Biomed Res Int, 2014, 2014: 960395.
13. Kanemura H, Hata S, Aoyagi K, et al. Serial changes of prefrontal lobe growth in the patients with benign childhood epilepsy with centrotemporal spikes presenting with cognitive impairments/behavioral problems. Brain Dev, 2011, 33(2): 106-113.
14. Lin JJ, Riley JD, Hsu DA, et al. Striatal hypertrophy and its cognitive effects in new-onset benign epilepsy with centrotemporal spikes. Epilepsia, 2012, 53(4): 677-685.
15. Friston K. Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Annu Rev Neurosci, 2002, 25: 221-250.
16. McIntosh AR. Towards a network theory of cognition. Neural Netw, 2000, 13(8-9): 861-870.
17. Oser N, Hubacher M, Specht K, et al. Default mode network alterations during language task performance in children with benign epilepsy with centrotemporal spikes (BECTS). Epilepsy Behav, 2014, 33: 12-17.
18. Zeng H, Ramos CG, Nair VA, et al. Regional homogeneity (ReHo) changes in new onset versus chronic benign epilepsy of childhood with centrotemporal spikes (BECTS): A resting state fMRI study. Epilepsy Res, 2015, 116: 79-85.

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