A meta-analysis on progressive atrophy in intractable temporal lobe epilepsy

Objective: It remains unclear whether drug-resistant temporal lobe epilepsy (TLE) is associated with cumulative brain damage, with no expert consensus and no quantitative syntheses of the available evidence. Methods: We conducted a systematic review and meta-analysis of MRI studies on progressive atrophy, searching PubMed and Ovid MEDLINE databases for cross-sectional and longitudinal quantitative MRI studies on drug-resistant TLE. Results: We screened 2,976 records and assessed eligibility of 248 full-text articles. Forty-two articles met the inclusion criteria for quantitative evaluation. We observed a predominance of cross-sectional studies, use of different clinical indices of progression, and high heterogeneity in age-control procedures. Meta-analysis of 18/1 cross-sectional/longitudinal studies on hippocampal atrophy (n = 979 patients) yielded a pooled effect size of r = −0.42 for ipsilateral atrophy related to epilepsy duration (95% confidence interval [CI] −0.51 to −0.32; p < 0.0001; I2 = 65.22%) and r = −0.35 related to seizure frequency (95% CI −0.47 to −0.22; p < 0.0001; I2 = 61.97%). Sensitivity analyses did not change the results. Narrative synthesis of 25/3 cross-sectional/longitudinal studies on whole brain atrophy (n = 1,504 patients) indicated that >80% of articles reported duration-related progression in extratemporal cortical and subcortical regions. Detailed analysis of study design features yielded low to moderate levels of evidence for progressive atrophy across studies, mainly due to dominance of cross-sectional over longitudinal investigations, use of diverse measures of seizure estimates, and absence of consistent age control procedures. Conclusions: While the neuroimaging literature is overall suggestive of progressive atrophy in drug-resistant TLE, published studies have employed rather weak designs to directly demonstrate it. Longitudinal multicohort studies are needed to unequivocally differentiate aging from disease progression.

[1]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

[2]  A. Connelly,et al.  The Relationship Between Quantitative MRI and Neuropsychological Functioning in Temporal Lobe Epilepsy , 1998, Epilepsia.

[3]  J. Sander,et al.  Hippocampal damage caused by seizures in temporal lobe epilepsy , 1998, The Lancet.

[4]  A W Toga,et al.  Three-dimensional preoperative maps of hippocampal atrophy predict surgical outcomes in temporal lobe epilepsy , 2005, Neurology.

[5]  Aaron Carass,et al.  Longitudinal changes in cortical thickness associated with normal aging , 2010, NeuroImage.

[6]  K O Lim,et al.  Cortical and Hippocampal Volume Deficits in Temporal Lobe Epilepsy , 1997, Epilepsia.

[7]  G. Cavalleri,et al.  A cross-sectional MRI study of brain regional atrophy and clinical characteristics of temporal lobe epilepsy with hippocampal sclerosis , 2012, Epilepsy Research.

[8]  C. Decarli,et al.  Relationship of Seizure Frequency to Hippocampus Volume and Metabolism in Temporal Lobe Epilepsy , 2000, Epilepsia.

[9]  B. Hermann,et al.  MRI volume loss of subcortical structures in unilateral temporal lobe epilepsy , 2007, Epilepsy & Behavior.

[10]  Alan C. Evans,et al.  Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy , 2009, Neurology.

[11]  L. Westlye,et al.  Differential Longitudinal Changes in Cortical Thickness, Surface Area and Volume across the Adult Life Span: Regions of Accelerating and Decelerating Change , 2014, The Journal of Neuroscience.

[12]  R. Ackermann,et al.  Brain Mediation of Anolis Social Dominance Displays , 2001, Brain, Behavior and Evolution.

[13]  A. R. Gilpin Table for Conversion of Kendall'S Tau to Spearman'S Rho Within the Context of Measures of Magnitude of Effect for Meta-Analysis , 1993 .

[14]  Frederick Andermann,et al.  Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy , 1999, Annals of neurology.

[15]  F Cendes,et al.  Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy , 2009, Neurology.

[16]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[17]  U. Wieshmann,et al.  Eugene Jamot (1879–1937) , 2002, Journal of neurology, neurosurgery, and psychiatry.

[18]  Bruce Hermann,et al.  Thalamic atrophy and cognition in unilateral temporal lobe epilepsy , 2008, Journal of the International Neuropsychological Society.

[19]  D C Reutens,et al.  Morphometric Analysis of the Temporal Lobe in Temporal Lobe Epilepsy , 1998, Epilepsia.

[20]  Benjamin N. Conrad,et al.  Increasing structural atrophy and functional isolation of the temporal lobe with duration of disease in temporal lobe epilepsy , 2015, Epilepsy Research.

[21]  Howard Balshem,et al.  GRADE guidelines: 3. Rating the quality of evidence. , 2011, Journal of clinical epidemiology.

[22]  A. Pitkänen,et al.  Hippocampal and amygdaloid damage in partial epilepsy A cross-sectional MRI study of 241 patients , 2001, Epilepsy Research.

[23]  C R Jack,et al.  MRI hippocampal volumes and memory function before and after temporal lobectomy , 1993, Neurology.

[24]  Eric Halgren,et al.  MRI analysis in temporal lobe epilepsy: Cortical thinning and white matter disruptions are related to side of seizure onset , 2011, Epilepsia.

[25]  B. Bernhardt,et al.  Mapping thalamocortical network pathology in temporal lobe epilepsy , 2012, Neurology.

[26]  Bernd Weber,et al.  Morphometric MRI alterations and postoperative seizure control in refractory temporal lobe epilepsy , 2015, Human brain mapping.

[27]  C. Yasuda,et al.  Memory impairment is not necessarily related to seizure frequency in mesial temporal lobe epilepsy with hippocampal sclerosis , 2014, Epilepsia.

[28]  S. Wiebe Burden of intractable epilepsy. , 2006, Advances in neurology.

[29]  Asla Pitkänen,et al.  Quantitative MRI volumetry of the entorhinal cortex in temporal lobe epilepsy , 2000, Seizure.

[30]  O. Witte,et al.  Bilateral reductions of hippocampal volume, glucose metabolism, and Wada hemispheric memory performance are related to the duration of mesial temporal lobe epilepsy , 1999, Journal of Neurology.

[31]  M. Cook,et al.  Degree of hippocampal atrophy is not related to a history of febrile seizures in patients with proved hippocampal sclerosis , 2000, Journal of neurology, neurosurgery, and psychiatry.

[32]  Bernd Weber,et al.  Thalamotemporal alteration and postoperative seizures in temporal lobe epilepsy , 2015, Annals of neurology.

[33]  I. Fried,et al.  Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. , 2012, JAMA.

[34]  R. Johnson,et al.  Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis , 2001, Neurology.

[35]  Aashit Shah,et al.  Hippocampal sclerosis is a progressive disorder: A longitudinal volumetric MRI study , 2003, Annals of neurology.

[36]  W H Theodore,et al.  Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures , 1999, Neurology.

[37]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[38]  J. Stockman Early Surgical Therapy for Drug-Resistant Temporal Lobe Epilepsy: A Randomized Trial , 2013 .

[39]  Agatha D. Lee,et al.  Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. , 2007, Cerebral cortex.

[40]  C. Yasuda,et al.  Frequent Seizures Are Associated with a Network of Gray Matter Atrophy in Temporal Lobe Epilepsy with or without Hippocampal Sclerosis , 2014, PloS one.

[41]  Bruce Hermann,et al.  Ipsilateral and Contralateral MRI Volumetric Abnormalities in Chronic Unilateral Temporal Lobe Epilepsy and their Clinical Correlates , 2005, Epilepsia.

[42]  Smith,et al.  Epilepsy and other Chronic Convulsive Diseases, Their Causes, Symptoms and Treatment , 1902 .

[43]  Michal Mikl,et al.  Correlation study of optimized voxel‐based morphometry and 1H MRS in patients with mesial temporal lobe epilepsy and hippocampal sclerosis , 2009, Human brain mapping.

[44]  Jullie W Pan,et al.  Decreased hippocampal volume on MRI is associated with increased extracellular glutamate in epilepsy patients , 2008, Epilepsia.

[45]  Neda Bernasconi,et al.  MRI volumetry of the thalamus in temporal, extratemporal, and idiopathic generalized epilepsy , 2003, Neurology.

[46]  E. Halgren,et al.  Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation , 2008, Epilepsy Research.

[47]  Neda Bernasconi,et al.  Cortical thickness analysis in temporal lobe epilepsy , 2010, Neurology.

[48]  Eric Halgren,et al.  Regional neocortical thinning in mesial temporal lobe epilepsy , 2008, Epilepsia.

[49]  Li Min Li,et al.  Gray matter atrophy associated with duration of temporal lobe epilepsy , 2006, NeuroImage.

[50]  J. Régis,et al.  The role of corticothalamic coupling in human temporal lobe epilepsy. , 2006, Brain : a journal of neurology.

[51]  A. Garg,et al.  Disparities in surgery among patients with intractable epilepsy in a universal health system , 2016, Neurology.

[52]  L Lemieux,et al.  Extrahippocampal temporal lobe atrophy in temporal lobe epilepsy and mesial temporal sclerosis. , 2001, Brain : a journal of neurology.

[53]  Bernd Weber,et al.  Concomitant Fractional Anisotropy and Volumetric Abnormalities in Temporal Lobe Epilepsy: Cross-Sectional Evidence for Progressive Neurologic Injury , 2012, PloS one.

[54]  N. Roberts,et al.  Voxel‐based morphometry of temporal lobe epilepsy: An introduction and review of the literature , 2008, Epilepsia.

[55]  Norman Delanty,et al.  Asymmetric cortical surface area and morphology changes in mesial temporal lobe epilepsy with hippocampal sclerosis , 2012, Epilepsia.

[56]  Boris C. Bernhardt,et al.  Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy , 2008, NeuroImage.

[57]  J L Lancaster,et al.  MR imaging volumetry of subcortical structures and cerebellar hemispheres in temporal lobe epilepsy. , 2006, AJNR. American journal of neuroradiology.

[58]  A. Pitkänen,et al.  Recurrent seizures may cause hippocambal damage in temporal lobe epilepsy , 1998, Neurology.

[59]  M. Brodie,et al.  Definition of drug resistant epilepsy: Consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies , 2011 .

[60]  L. Wilkins Referral pattern for epilepsy surgery after evidence-based recommendations: A retrospective study , 2010, Neurology.