Skip to main content

Advertisement

Log in

Characterization of the Relationship Between Intracranial Pressure and Electroencephalographic Monitoring in Burst-Suppressed Patients

  • Original Article
  • Published:
Neurocritical Care Aims and scope Submit manuscript

Abstract

Background

The objective of this study is to characterize the relationship between ICP and EEG

Methods

Simultaneous ICP and EEG data were obtained from burst-suppressed patients and segmented by EEG bursts. Segments were categorized as increasing/decreasing and peak/valley to investigate relationship between ICP changes and EEG burst duration. A generalized ICP response was obtained by averaging all segments time-aligned at burst onsets. A vasodilatation index (VDI) was derived from the ICP pulse waveform and calculated on a sliding interval to investigate cerebrovascular changes post-burst.

Results

Data from two patients contained 309 bursts. 246 ICP segments initially increased, of which 154 peaked. 63 ICP segments decreased, and zero reached a valley. The change in ICP (0.54 ± 0.85 mmHg) was significantly correlated with the burst duration (p < 0.001). Characterization of the ICP segments showed a peak at 8.1 s and a return to baseline at 14.7 s. The VDI for increasing segments was significantly elevated (median 0.56, IQR 0.31, p < 0.001) and correlated with burst duration (p < 0.001).

Conclusions

Changes in the ICP and pulse waveform shape after EEG burst suggest that these signals can be related within the context of neurovascular coupling.

Significance

Existence of a physiological relationship between ICP and EEG may allow the study of neurovascular coupling in acute brain injury patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Asgari S, Bergsneider M, Hamilton R, Vespa P, Hu X. Consistent changes in intracranial pressure waveform morphology induced by acute hypercapnic cerebral vasodilatation. Neurocrit Care. 2011;15(1):55–62.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Asgari S, Gonzalez N, Subudhi AW, Hamilton R, Vespa P, Bergsneider M, Roach RC, Hu X. Continuous detection of cerebral vasodilatation and vasoconstriction using intracranial pulse morphological template matching. PLoS One. 2012;7(11):e50795. doi:10.1371/journal.pone.0050795.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Ayata C. Spreading Depression and Neurovascular Coupling. Stroke. 2013;44(6 suppl 1):S87–9. doi:10.1161/strokeaha.112.680264.

    Article  PubMed  Google Scholar 

  4. Baumgartner C, Serles W, Leutmezer F, Pataraia E, Aull S, Czech T, Pietrzyk U, Relic A, Podreka I. Preictal SPECT in temporal lobe epilepsy: regional cerebral blood flow is increased prior to electroencephalography-seizure onset. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine, 1998;39(6):978–82. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9627329.

  5. Bouma GJ, Muizelaar JP, Choi SC, Newlon PG, Young HF. Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg. 1991;75(5):685–93. doi:10.3171/jns.1991.75.5.0685.

    Article  CAS  PubMed  Google Scholar 

  6. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 2011;17(4):439–47.

    Article  CAS  PubMed  Google Scholar 

  7. Füchtemeier M, Leithner C, Offenhauser N, Foddis M, Kohl-Bareis M, Dirnagl U, Lindauer U, Royl G. Elevating intracranial pressure reverses the decrease in deoxygenated hemoglobin and abolishes the post-stimulus overshoot upon somatosensory activation in rats. NeuroImage, 2010;52(2):445–454. Retrieved from http://www.sciencedirect.com/science/article/pii/S105381191000649X.

  8. Golanov EV, YamamotoS, Reis DJ. Spontaneous waves of cerebral blood flow associated with a pattern of electrocortical activity. American Physiological Society Regulatory, Integrative and Comparative Physiology, 1994;266(1): R204–R214. Retrieved from http://ajpregu.physiology.org/content/266/1/R204.abstract.

  9. Hart RG, Byer JA, Slaughter JR, Hewett JE, Easton DJ. Occurrence and Implications of Seizures in Subarachnoid Hemorrhage Due to Ruptured Intracranial Aneurysms. Neurosurgery, 1981;8(4): 417–421. Retrieved from http://journals.lww.com/neurosurgery/Fulltext/1981/04000/Occurrence_and_Implications_of_Seizures_in.2.aspx.

  10. Hartings JA, Strong AJ, Fabricius M, Manning A, Bhatia R, Dreier JP, Mazzeo AT, Tortella FC, Bullock MR. Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma. 2009;26(11):1857–66.

    Article  PubMed Central  PubMed  Google Scholar 

  11. Hu X, Glenn T, Scalzo F, Bergsneider M, Sarkiss C, Martin N, Vespa P. Intracranial pressure pulse morphological features improved detection of decreased cerebral blood flow. Physiol Meas. 2010;31(5):679–95. doi:10.1088/0967-3334/31/5/006.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Hu X, Xu P, Scalzo F, Vespa P, Bergsneider M. Morpological clustering and analysis of continuous intracranial pressure. IEEE Trans Biomed Eng. 2009;56(3):696–705.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Koide M, Sukhotinsky I, Ayata C, Wellman GC. Subarachnoid hemorrhage, spreading depolarizations and impaired neurovascular coupling. Stroke Research and Treatment. 2013;2013:819340. doi:10.1155/2013/819340.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Lauritzen M, Jørgensen MB, Diemer NH, Gjedde A, Hansen AJ. Persistent oligemia of rat cerebral cortex in the wake of spreading depression. Annals of Neurology. 1982;12(5):469–74. doi:10.1002/ana.410120510.

    Article  CAS  PubMed  Google Scholar 

  15. Leao AAP. Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol, 1944; 7(6):391–396. Retrieved from http://jn.physiology.org/content/7/6/391.citation.

  16. Lescot T, Naccache L, Bonnet MP, Abdennour L, Coriat P, Puybasset L. The relationship of intracranial pressure Lundberg waves to electroencephalograph fluctuations in patients with severe head trauma. Acta Neurochirurgica. 2005;147(2):125–9. doi:10.1007/s00701-004-0355-8.

    Article  CAS  PubMed  Google Scholar 

  17. Liu X, Zhu X-H, Zhang Y, Chen W. Neural origin of spontaneous hemodynamic fluctuations in rats under burst suppression anesthesia condition. Cereb Cortex. 2011;21(2):374–84. doi:10.1093/cercor/bhq105.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Mayevsky A, Doron A, Manor T, Meilin S, Zarchin N, Ouaknine GE. Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Research, 1996;740(1):268–274. Retrieved from http://www.sciencedirect.com/science/article/pii/S0006899396008748.

  19. Mayevsky A, Weiss HR. Cerebral blood flow and oxygen consumption in cortical spreading depression. Journal of Cerebral Blood Flow and Metabolism. 1991;11(5):829–36. doi:10.1038/jcbfm.1991.142.

    Article  CAS  PubMed  Google Scholar 

  20. Miller JD, Becker DP, Ward JD, Sullivan HG, Adams WE, Rosner MJ. Significance of intracranial hypertension in severe head injury. J Neurosurg. 1977;47(4):503–16. doi:10.3171/jns.1977.47.4.0503.

    Article  CAS  PubMed  Google Scholar 

  21. Roche-Labarbe N, Wallois F, Ponchel E, Kongolo G, Grebe R. Coupled oxygenation oscillation measured by NIRS and intermittent cerebral activation on EEG in premature infants. NeuroImage, 2007; 36(3), 718–727. Retrieved from http://www.sciencedirect.com/science/article/pii/S1053811907003059.

  22. Shin HK, Dunn AK, Jones PB, Boas DA, Moskowitz MA, Ayata C. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. Journal of Cerebral Blood Flow and Metabolism. 2006;26(8):1018–30. doi:10.1038/sj.jcbfm.9600252.

    Article  PubMed  Google Scholar 

  23. Steiner LA, Andrews PJD. Monitoring the injured brain: ICP and CBF. Br J Anaesth. 2006;97(1):26–38. doi:10.1093/bja/ael110.

    Article  CAS  PubMed  Google Scholar 

  24. Stover JF, Pleines UE, Morganti-Kossmann MC, Stocker R, Kossmann T. Thiopental attenuates energetic impairment but fails to normalize cerebrospinal fluid glutamate in brain-injured patients. Critical Care Medicine, 1999; 27(7), 1351–7. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10446831.

  25. Strong AJ, Anderson PJ, Watts HR, Virley DJ, Lloyd A, Irving EA, Nagafuji T, Ninomiya M, Nakamura H, Dunn AK, Graf R. Brain. 2007;130(4):995–1008. doi:10.1093/brain/awl392.

    Article  PubMed  Google Scholar 

  26. Vespa PM, Nuwer MR, Nenov V, Ronne-Engstrom E, Hovda DA, Bergsneider M, Kelly DF, Martin NA, Becker DP. Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic brain injury as detected by continuous electroencephalographic monitoring. J Neurosurg. 1999;91(5):750–60. doi:10.3171/jns.1999.91.5.0750.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Westbrook LE, Devinsky O, Geocadin R. Nonepileptic seizures after head injury. Epilepsia. 1998;39(9):978–82. doi:10.1111/j.1528-1157.1998.tb01447.x.

    Article  CAS  PubMed  Google Scholar 

  28. Winer JW, Rosenwasser RH, Jimenez F. Electroencephalographic activity and serum and cerebrospinal fluid pentobarbital levels in determining the therapeutic end point during barbiturate coma. Neurosurgery, 1991; 29(5), 739–41; discussion 741–2. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1961405.

  29. Winkler MKL, Chassidim Y, Lublinsky S, Revankar GS, Major S, Kang E-J, Oliveira-Ferreira AI, Woitzik J, Sandow N, Scheel M, Friedman A, Dreier JP. Impaired neurovascular coupling to ictal epileptic activity and spreading depolarization in a patient with subarachnoid hemorrhage: possible link to blood-brain barrier dysfunction. Epilepsia. 2012;53(6):22–30. doi:10.1111/j.1528-1167.2012.03699.x.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Woitzik J, Dreier JP, Hecht N, Fiss I, Sandow N, Major S, Winkler M, Dahlem YA, Manville J, Diepers M, Muench E, Kasuya H, Schmiedek P, Vajkoczy P. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2012;32(2):203–12. doi:10.1038/jcbfm.2011.169.

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

XH support from the National Institutes of Health Award Number NS076738 and the University of California, San Francisco Institute of Computational Health Sciences. NRG support from National Institute of neurological Disorders and Stroke of the National Institutes of Health under Award Number K23NS079477.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiao Hu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Connolly, M., Vespa, P., Pouratian, N. et al. Characterization of the Relationship Between Intracranial Pressure and Electroencephalographic Monitoring in Burst-Suppressed Patients. Neurocrit Care 22, 212–220 (2015). https://doi.org/10.1007/s12028-014-0059-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-014-0059-8

Keywords

Navigation