Electrographic seizures after subarachnoid hemorrhage lead to derangement of brain homeostasis in humans

Abstract

Introduction Nonconvulsive seizures (NCSz) are common after acute brain injury and associated with poor outcome. Underlying mechanisms are poorly understood but in animals periods of inadequate perfusion during seizures have been documented. In the present study we hope to gain better understanding of the relationship between NCSz and brain homeostasis in subarachnoid hemorrhage (SAH) patients. Methods Between 6/06 and 6/10, 51 poor grade SAH patients underwent multimodality monitoring with microdialysis, brain oxygen tension (pbtO2), regional cerebral blood flow (rCBF), and intracranial pressure monitoring; 69% (N=36) also with intracortical EEG (ICE; 8-contact depth electrode). Each minute of EEG was categorized into non-ictal, ictal-interictal continuum, or seizures. We identified seizure onsets and extracted monitoring data 30 minutes pre and post seizure onset. Physiologic profiles based on standard error of the means plots were generated using high frequency time series physiologic measurements. Results Depth NCSz were recorded in 36% (13/36) of patients with ICE recordings (11,017 minutes of depth seizures). NCSz were preceded by increasing rCBF starting 15 minutes before onset of depth NCSz which remained elevated. Heart rate, mean arterial, intracranial, and cerebral perfusion pressures were elevated surrounding NCSZs. There was a small transient drop in pbtO2 and a drop in jugular bulb oxygen saturation between 1-3 minutes following seizure onset. There was a small rise in brain temperature but no change in bladder temperature associated with the NCSZs, but water temperature of the cooling device dropped following seizure onset. Conclusions These findings confirm in comatose human beings that NCSz detected by ICE are associated with hyperemia, increased metabolism, and possibly brain tissue hypoxia, which serve as surrogates for secondary brain injury. Future research should implement novel approaches for ICU time series data analysis, evaluate surface seizures, and utilize other surrogates of brain metabolism such as microdialysis.