Abstract
Background
Spreading depolarization (SD) is a fundamental pathophysiological mechanism of both pannecrotic and selective neuronal lesions following deprivation of energy. SD with brain injury has been reported including in one patient during an intracranial operation. However, the incidence of SDs in operative resections is unknown.
Methods
We performed (a) retrospective analysis of intraoperative AC-recordings of 69 patients and (b) a prospective study using intraoperative near-DC recording. All patients had the diagnosis of pharmaco-resistant epilepsy. Both studies were designed to determine the incidence and characteristics of SDs intraoperatively. In the retrospective analysis, we used intraoperative electrocorticography (iECoG) recordings obtained from AC-recording of 69 patients. In the prospective analysis, we used an Octal Bio Amp and Power Lab ECoG recorder with near-DC range.
Results
In the retrospective study, we included 69 patients with a mean of 1 h 3 min of iECoG recordings. In the prospective study, we recruited 20 patients with near DC recordings. A total of 35 h 41 min of iECoG recordings with mean of 2 h 32 min/patient were analyzed. We did not find SD in either study.
Conclusions
SDs were not detected during intraoperative recordings of epilepsy surgery using AC- or DC-amplifiers.
Similar content being viewed by others
References
Ayata C (2013) Pearls and pitfalls in experimental models of spreading depression. Cephalalgia 33(8):604–613
Carlson AP, Carter RE, Shuttleworth CW (2012) Vascular, electrophysiological, and metabolic consequences of cortical spreading depression in a mouse model of simulated neurosurgical conditions. Neurol Res 34(3):223–231
Carlson AP, William Shuttleworth C, Mead B, Burlbaw B, Krasberg M, Yonas H (2017) Cortical spreading depression occurs during elective neurosurgical procedures. J Neurosurg 126(1):266–273
Dohmen C, Sakowitz OW, Fabricius M et al (2008) Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 63(6):720–728
Dreier JP (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 17(4):439–447
Dreier JP, Reiffurth C (2015) The stroke-migraine depolarization continuum. Neuron 86(4):902–922
Dreier JP, Major S, Manning A et al (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain J Neurol 132(Pt 7:1866–1881
Dreier JP, Major S, Pannek H-W et al (2012) Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain J Neurol 135(Pt 1:259–275
Dreier JP, Fabricius M, Ayata C et al (2017) Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: review and recommendations of the COSBID research group. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 37(5):1595–1625
Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, Hartings JA, Bullock R, Strong AJ, Lauritzen M (2008) Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 119(9):1973–1984
Hartings JA, Watanabe T, Bullock MR et al (2011) Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain J Neurol 134(Pt 5:1529–1540
Hartings JA, Wilson JA, Hinzman JM, Pollandt S, Dreier JP, DiNapoli V, Ficker DM, Shutter LA, Andaluz N (2014) Spreading depression in continuous electroencephalography of brain trauma. Ann Neurol 76(5):681–694
Hartings JA, Shuttleworth CW, Kirov SA et al (2016) The continuum of spreading depolarizations in acute cortical lesion development: examining Leão’s legacy. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. https://doi.org/10.1177/0271678X16654495
Helbok R, Schiefecker AJ, Friberg C et al (2017) Spreading depolarizations in patients with spontaneous intracerebral hemorrhage: association with perihematomal edema progression. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 37(5):1871–1882
Hertle DN, Dreier JP, Woitzik J et al (2012) Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain J Neurol 135(Pt 8:2390–2398
Jordan KG (2004) Emergency EEG and continuous EEG monitoring in acute ischemic stroke. J Clin Neurophysiol Off Publ Am Electroencephalogr Soc 21(5):341–352
Klass A, Sánchez-Porras R, Santos E (2018) Systematic review of the pharmacological agents that have been tested against spreading depolarizations. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 271678X18771440
Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 31(1):17–35
Sakowitz OW, Santos E, Nagel A, Krajewski KL, Hertle DN, Vajkoczy P, Dreier JP, Unterberg AW, Sarrafzadeh AS (2013) Clusters of spreading depolarizations are associated with disturbed cerebral metabolism in patients with aneurysmal subarachnoid hemorrhage. Stroke J Cereb Circ 44(1):220–223
Sánchez-Porras R, Zheng Z, Sakowitz OW (2015) Pharmacological modulation of spreading depolarizations. Acta Neurochir Suppl 120:153–157
San-juan D, Tapia CA, Claudia AT et al (2011) The prognostic role of electrocorticography in tailored temporal lobe surgery. Seizure 20(7):564–569
Santos E, Sánchez-Porras R, Dohmen C, Hertle D, Unterberg AW, Sakowitz OW (2012) Spreading depolarizations in a case of migraine-related stroke. Cephalalgia 32(5):433–436
Santos E, Schöll M, Sanchez-Porras R, Kentar M, Orakcioglu B, Unterberg A, Dickhaus H, Sakowitz OW (2013) Cortical spreading depression dynamics can be studied using intrinsic optical signal imaging in gyrencephalic animal cortex. Acta Neurochir Suppl 118:93–97
Santos E, Schöll M, Sánchez-Porras R, Dahlem MA, Silos H, Unterberg A, Dickhaus H, Sakowitz OW (2014) Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. NeuroImage 99:244–255
Santos E, León F, Silos H, Sanchez-Porras R, Shuttleworth CW, Unterberg A, Sakowitz OW (2016) Incidence, hemodynamic, and electrical characteristics of spreading depolarization in a swine model are affected by local but not by intravenous application of magnesium. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 36(12):2051–2057
Santos E, Sánchez-Porras R, Sakowitz OW, Dreier JP, Dahlem MA (2017) Heterogeneous propagation of spreading depolarizations in the lissencephalic and gyrencephalic brain. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 37(7):2639–2643
Schöll MJ, Santos E, Sanchez-Porras R et al (2016) Large field-of-view movement-compensated intrinsic optical signal imaging for the characterization of the haemodynamic response to spreading depolarizations in large gyrencephalic brains. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. https://doi.org/10.1177/0271678X16668988
Strong AJ, Fabricius M, Boutelle MG, Hibbins SJ, Hopwood SE, Jones R, Parkin MC, Lauritzen M (2002) Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke J Cereb Circ 33(12):2738–2743
Vespa PM, Nenov V, Nuwer MR (1999) Continuous EEG monitoring in the intensive care unit: early findings and clinical efficacy. J Clin Neurophysiol Off Publ Am Electroencephalogr Soc 16(1):1–13
Vespa PM, O’Phelan K, Shah M et al (2003) Acute seizures after intracerebral hemorrhage: a factor in progressive midline shift and outcome. Neurology 60(9):1441–1446
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (name of institute/committee) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Functional Neurosurgery - Epilepsy
Rights and permissions
About this article
Cite this article
Santos, E., Dávila-Rodríguez, D.O., Márquez-Gonzalez, K. et al. Screening spreading depolarizations during epilepsy surgery. Acta Neurochir 161, 911–916 (2019). https://doi.org/10.1007/s00701-019-03870-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-019-03870-z