Relationship of EEG sources of neonatal seizures to acute perinatal brain lesions seen on MRI: A pilot study

Even though it is known that neonatal seizures are associated with acute brain lesions, the relationship of electroencephalographic (EEG) seizures to acute perinatal brain lesions visible on magnetic resonance imaging (MRI) has not been objectively studied. EEG source localization is successfully used for this purpose in adults, but it has not been sufficiently explored in neonates. Therefore, we developed an integrated method for ictal EEG dipole source localization based on a realistic head model to investigate the utility of EEG source imaging in neonates with postasphyxial seizures. We describe here our method and compare the dipole seizure localization results with acute perinatal lesions seen on brain MRI in 10 full‐term infants with neonatal encephalopathy. Through experimental studies, we also explore the sensitivity of our method to the electrode positioning errors and the variations in neonatal skull geometry and conductivity. The localization results of 45 focal seizures from 10 neonates are compared with the visual analysis of EEG and MRI data, scored by expert physicians. In 9 of 10 neonates, dipole locations showed good relationship with MRI lesions and clinical data. Our experimental results also suggest that the variations in the used values for skull conductivity or thickness have little effect on the dipole localization, whereas inaccurate electrode positioning can reduce the accuracy of source estimates. The performance of our fused method indicates that ictal EEG source imaging is feasible in neonates and with further validation studies, this technique can become a useful diagnostic tool. Hum Brain Mapp 34:2402–2417, 2013. © 2012 Wiley Periodicals, Inc.

[1]  D. A. Driscoll,et al.  Current Distribution in the Brain From Surface Electrodes , 1968, Anesthesia and analgesia.

[2]  T. Kemper,et al.  The propagation of focal paroxysmal activity in the Macaca mulatta at birth and at 24 months. , 1973, Brain : a journal of neurology.

[3]  Parasagittal cerebral injury in neonatal hypoxic-ischemic encephalopathy: Clinical and neuroradiologic features , 1977 .

[4]  M. Kato,et al.  Local cerebral glucose utilization in newborn and pubescent monkeys during focal motor seizures , 1980, Annals of neurology.

[5]  K. Hara,et al.  Behavioral state cycles, background EEGs and prognosis of newborns with perinatal hypoxia. , 1980, Electroencephalography and clinical neurophysiology.

[6]  E. Grant,et al.  Variation with age of the dielectric properties of mouse brain cerebrum , 1984, Physics in medicine and biology.

[7]  M. Phelps,et al.  Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. , 1986, Science.

[8]  J. F. Kaiser,et al.  On a simple algorithm to calculate the 'energy' of a signal , 1990, International Conference on Acoustics, Speech, and Signal Processing.

[9]  L. Quesney.  Preoperative Electroencephalographic Investigation in Frontal Lobe Epilepsy: Electroencephalographic and Electrocorticographic Recordings , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[10]  S. Saha,et al.  Electric and dielectric properties of wet human cortical bone as a function of frequency , 1992, IEEE Transactions on Biomedical Engineering.

[11]  M J Painter,et al.  Electrographic seizures in preterm and full-term neonates: clinical correlates, associated brain lesions, and risk for neurologic sequelae. , 1993, Pediatrics.

[12]  S. Sato,et al.  How well does a three-sphere model predict positions of dipoles in a realistically shaped head? , 1993, Electroencephalography and clinical neurophysiology.

[13]  T. Rasmussen,et al.  Reevaluation of Surgical Failures and the Role of Reoperation in 39 Patients with Frontal Lobe Epilepsy , 1994, Epilepsia.

[14]  A M Bye,et al.  Spatial and Temporal Characteristics of Neonatal Seizures , 1995, Epilepsia.

[15]  B.N. Cuffin,et al.  EEG localization accuracy improvements using realistically shaped head models , 1996, IEEE Transactions on Biomedical Engineering.

[16]  David R. Wozny,et al.  The electrical conductivity of human cerebrospinal fluid at body temperature , 1997, IEEE Transactions on Biomedical Engineering.

[17]  J. Pernier,et al.  A systematic evaluation of the spherical model accuracy in EEG dipole localization. , 1997, Electroencephalography and clinical neurophysiology.

[18]  E. Mercuri,et al.  Abnormal Magnetic Resonance Signal in the Internal Capsule Predicts Poor Neurodevelopmental Outcome in Infants With Hypoxic-Ischemic Encephalopathy , 1998, Pediatrics.

[19]  D. Vigneron,et al.  Prediction of neuromotor outcome in perinatal asphyxia: evaluation of MR scoring systems. , 1998, AJNR. American journal of neuroradiology.

[20]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[21]  T Oostendorp,et al.  Interictal spike localization using a standard realistic head model: simulations and analysis of clinical data , 1999, Clinical Neurophysiology.

[22]  Deepak Khosla,et al.  Spatial mislocalization of EEG electrodes – effects on accuracy of dipole estimation , 1999, Clinical Neurophysiology.

[23]  Thom F. Oostendorp,et al.  The conductivity of the human skull: results of in vivo and in vitro measurements , 2000, IEEE Transactions on Biomedical Engineering.

[24]  Michael Unser,et al.  Optimization of mutual information for multiresolution image registration , 2000, IEEE Trans. Image Process..

[25]  R H Bayford,et al.  Two-dimensional finite element modelling of the neonatal head. , 2000, Physiological measurement.

[26]  R. Guillet,et al.  Electrographic seizures in neonates correlate with poor neurodevelopmental outcome , 2000, Neurology.

[27]  J Gotman,et al.  Dipole modeling of scalp electroencephalogram epileptic discharges: correlation with intracerebral fields , 2001, Clinical Neurophysiology.

[28]  Jean Gotman,et al.  The influence of electrode location errors on EEG dipole source localization with a realistic head model , 2001, Clinical Neurophysiology.

[29]  David R. Haynor,et al.  Nonrigid multimodality image registration , 2001, SPIE Medical Imaging.

[30]  G. Cioni,et al.  Combined use of electroencephalogram and magnetic resonance imaging in full-term neonates with acute encephalopathy. , 2001, Pediatrics.

[31]  J. Gotman,et al.  Modeling of post-surgical brain and skull defects in the EEG inverse problem with the boundary element method , 2002, Clinical Neurophysiology.

[32]  G. Holmes,et al.  Neonatal seizures: characteristics of EEG ictal activity in preterm and fullterm infants , 2003, Brain and Development.

[33]  F. Tortella,et al.  Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent rhythmic delta activity in rat focal ischemia , 2003, Experimental Neurology.

[34]  G. Bydder,et al.  Origin and timing of brain lesions in term infants with neonatal encephalopathy , 2003 .

[35]  Fetsje Bijma,et al.  In vivo measurement of the brain and skull resistivities using an EIT-based method and realistic models for the head , 2003, IEEE Transactions on Biomedical Engineering.

[36]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[37]  W. Sutherling,et al.  Conductivities of Three-Layer Live Human Skull , 2004, Brain Topography.

[38]  Bart Vanrumste,et al.  The Validation of the Finite Difference Method and Reciprocity for Solving the Inverse Problem in EEG Dipole Source Analysis , 2004, Brain Topography.

[39]  W. Drongelen,et al.  Estimation of in vivo human brain-to-skull conductivity ratio from simultaneous extra- and intra-cranial electrical potential recordings , 2005, Clinical Neurophysiology.

[40]  Y. D'Asseler,et al.  A finite difference method with reciprocity used to incorporate anisotropy in electroencephalogram dipole source localization , 2005 .

[41]  John H. Gilmore,et al.  Automatic segmentation of MR images of the developing newborn brain , 2005, Medical Image Anal..

[42]  P. W. Murray.  Field calculations in the head of a newborn infant and their application to the interpretation of transcephalic impedance measurements , 1981, Medical and Biological Engineering and Computing.

[43]  I. Lemahieu,et al.  Influence of measurement noise and electrode mislocalisation on EEG dipole-source localisation , 2000, Medical and Biological Engineering and Computing.

[44]  I. Lemahieu,et al.  Dipole location errors in electroencephalogram source analysis due to volume conductor model errors , 2000, Medical and Biological Engineering and Computing.

[45]  L. Geddes,et al.  The specific resistance of biological material—A compendium of data for the biomedical engineer and physiologist , 1967, Medical and biological engineering.

[46]  A. Vein,et al.  Prediction of short-term neurological outcome in full-term neonates with hypoxic-ischaemic encephalopathy based on combined use of electroencephalogram and neuro-imaging. , 2007, Neuropediatrics.

[47]  Daniel Rueckert,et al.  Automatic segmentation and reconstruction of the cortex from neonatal MRI , 2007, NeuroImage.

[48]  Patrick Dupont,et al.  Canonical decomposition of ictal scalp EEG reliably detects the seizure onset zone , 2007, NeuroImage.

[49]  G B Boylan,et al.  Defining the gap between electrographic seizure burden, clinical expression and staff recognition of neonatal seizures , 2007, Archives of Disease in Childhood Fetal and Neonatal Edition.

[50]  Samuel R. Atcherson,et al.  Variability of Electrode Positions Using Electrode Caps , 2007, Brain Topography.

[51]  Gregory A. Worrell,et al.  Ictal source analysis: Localization and imaging of causal interactions in humans , 2007, NeuroImage.

[52]  A. Aarabi,et al.  High‐resolution electroencephalography and source localization in neonates , 2008, Human brain mapping.

[53]  M. Cook,et al.  EEG source localization in focal epilepsy: Where are we now? , 2008, Epilepsia.

[54]  Sampsa Vanhatalo,et al.  High-fidelity recording of brain activity in the extremely preterm babies: Feasibility study in the incubator , 2008, Clinical Neurophysiology.

[55]  S. Huffel,et al.  Automated neonatal seizure detection mimicking a human observer reading EEG , 2008, Clinical Neurophysiology.

[56]  S. Huffel,et al.  Neonatal seizure localization using PARAFAC decomposition , 2009, Clinical Neurophysiology.

[57]  Sean Connolly,et al.  Early EEG Findings in Hypoxic-Ischemic Encephalopathy Predict Outcomes at 2 Years , 2009, Pediatrics.

[58]  Maria Luisa Gorno-Tempini,et al.  Neonatal Watershed Brain Injury on Magnetic Resonance Imaging Correlates With Verbal IQ at 4 Years , 2009, Pediatrics.

[59]  M. Lequin,et al.  Imaging patterns of brain injury in term‐birth asphyxia , 2009, Acta paediatrica.

[60]  Simon K. Warfield,et al.  Automatic segmentation of newborn brain MRI , 2009, NeuroImage.

[61]  Dinggang Shen,et al.  Neonatal brain image segmentation in longitudinal MRI studies , 2010, NeuroImage.

[62]  E. Vansteenkiste,et al.  Brain volume segmentation in newborn infants using multi-modal MRI with a low inter-slice resolution , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[63]  Ewout Vansteenkiste,et al.  T1- and T2-weighted spatially constrained fuzzy c-means clustering for brain MRI segmentation , 2010, Medical Imaging.

[64]  W Deburchgraeve,et al.  Time varying neonatal seizure localization. , 2010, Methods of information in medicine.

[65]  Fabrizio Esposito,et al.  Realistic and Spherical Head Modeling for EEG Forward Problem Solution: A Comparative Cortex-Based Analysis , 2010, Comput. Intell. Neurosci..

[66]  M. Borchert,et al.  Neurology of the Newborn, 5th Edition , 2010 .

[67]  Andrew M. White,et al.  Continuous Electroencephalographic Monitoring with Radio-Telemetry in a Rat Model of Perinatal Hypoxia–Ischemia Reveals Progressive Post-Stroke Epilepsy , 2010, The Journal of Neuroscience.

[68]  M. De Vos,et al.  Automated artifact removal as preprocessing refines neonatal seizure detection , 2011, Clinical Neurophysiology.

[69]  Dinggang Shen,et al.  CENTS: Cortical enhanced neonatal tissue segmentation , 2011, Human brain mapping.

[70]  M. De Vos,et al.  Validation of a new automated neonatal seizure detection system: A clinician’s perspective , 2011, Clinical Neurophysiology.

[71]  R. Sadleir,et al.  The conductivity of neonatal piglet skulls. , 2011, Physiological measurement.

[72]  Saeid Sanei,et al.  EEG Source Localization , 2013 .