Clusters of Cortical Spreading Depolarizations in a Patient with Intracerebral Hemorrhage: A Multimodal Neuromonitoring Study
- 361 Downloads
- 9 Citations
Abstract
Background
Spontaneous intracerebral hemorrhage (ICH) is associated with high morbidity and mortality. Cortical spreading depolarizations (CSDs) increase brain matrix metalloproteinase (MMP)-9 activity leading to perihematomal edema expansion in experimental ICH.
Methods
The purpose of this report is to describe cerebral metabolic changes and brain extracellular MMP-9 levels in a patient with CSDs and perihematomal edema expansion after ICH.
Results
We present a 66-year-old male patient with ICH who underwent craniotomy for hematoma evacuation. Multimodal neuromonitoring data of the perihematomal region revealed metabolic distress and increased MMP-9 levels in the brain extracellular fluid during perihematomal edema progression. At the same time, subdural electrocorticography showed clusters of CSDs, which disappeared after ketamine anesthesia on day six. Perihematomal edema regression was associated with decreasing cerebral MMP-9 levels.
Conclusions
This novel association between clusters of CSDs, brain metabolic distress, and increased MMP-9 levels expands our knowledge about secondary brain injury after ICH. The role of ketamine after this devastating disorder needs further studies.
Keywords
Cortical spreading depolarizations Intracerebral hemorrhage Matrix metalloproteinase-9 Ketamine Perihematomal edema MicrodialysisNotes
Acknowledgments
We would like to thank the nursing staff and all physicians of our neurointensive care unit for their overall support of this study. RH and AS are supported by a grant of the Austrian National Bank (OeNB-Nr.: 14082).
Conflict of interest
The authors declare that they have no competing interests.
Supplementary material
References
- 1.Balami JS, Buchan AM. Complications of intracerebral haemorrhage. Lancet Neurol. 2012;11:101–18.CrossRefPubMedGoogle Scholar
- 2.Zazulia AR, Videen TO, Powers WJ. Transient focal increase in perihematomal glucose metabolism after acute human intracerebral hemorrhage. Stroke. 2009;40:1638–43.CrossRefPubMedGoogle Scholar
- 3.Kim-Han JS, Kopp SJ, Dugan LL, Diringer MN. Perihematomal mitochondrial dysfunction after intracerebral hemorrhage. Stroke. 2006;37:2457–62.CrossRefPubMedGoogle Scholar
- 4.Butcher KS, Baird T, MacGregor L, Desmond P, Tress B, Davis S. Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke. 2004;35:1879–85.CrossRefPubMedGoogle Scholar
- 5.Rosenberg GA, Estrada EY, Mobashery S. Effect of synthetic matrix metalloproteinase inhibitors on lipopolysaccharide-induced blood-brain barrier opening in rodents: differences in response based on strains and solvents. Brain Res. 2007;1133:186–92.CrossRefPubMedCentralPubMedGoogle Scholar
- 6.Fabricius M, Fuhr S, Bhatia R, et al. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain. 2006;129:778–90.CrossRefPubMedGoogle Scholar
- 7.Strong AJ, Fabricius M, Boutelle MG, et al. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke. 2002;33:2738–43.CrossRefPubMedGoogle Scholar
- 8.Dreier JP, Woitzik J, Fabricius M, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129:3224–37.CrossRefPubMedGoogle Scholar
- 9.Hartings JA, Bullock MR, Okonkwo DO, et al. Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol. 2011;10:1058–64.CrossRefPubMedGoogle Scholar
- 10.Dohmen C, Sakowitz OW, Fabricius M, et al. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol. 2008;63:720–8.CrossRefPubMedGoogle Scholar
- 11.Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al. Cortical spreading depression activates and upregulates MMP-9. J Clin Investig. 2004;113:1447–55.CrossRefPubMedCentralPubMedGoogle Scholar
- 12.Alvarez-Sabin J, Delgado P, Abilleira S, et al. Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: relationship to clinical and radiological outcome. Stroke. 2004;35:1316–22.CrossRefPubMedGoogle Scholar
- 13.Hashemi P, Bhatia R, Nakamura H, et al. Persisting depletion of brain glucose following cortical spreading depression, despite apparent hyperaemia: evidence for risk of an adverse effect of Leao’s spreading depression. J Cereb Blood Flow Metab. 2009;29:166–75.CrossRefPubMedGoogle Scholar
- 14.Orakcioglu B, Uozumi Y, Kentar MM, Santos E, Unterberg A, Sakowitz OW. Evidence of spreading depolarizations in a porcine cortical intracerebral hemorrhage model. Acta Neurochir Suppl. 2012;114:369–72.CrossRefPubMedGoogle Scholar
- 15.Largo C, Cuevas P, Somjen GG, Martin del Rio R, Herreras O. The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival. J Neurosci. 1996;16:1219–29.PubMedGoogle Scholar
- 16.Hertle DN, Dreier JP, Woitzik J, et al. Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain. 2012;135:2390–8.CrossRefPubMedGoogle Scholar
- 17.Vespa PM. Metabolic penumbra in intracerebral hemorrhage. Stroke. 2009;40:1547–8.CrossRefPubMedGoogle Scholar
- 18.Ayata C. Spreading depression and neurovascular coupling. Stroke. 2013;44:S87–9.CrossRefPubMedGoogle Scholar