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Cerebral Vascular Changes During Acute Intracranial Pressure Drop

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Abstract

Objective

This study applied a new external ventricular catheter, which allows intracranial pressure (ICP) monitoring and cerebral spinal fluid (CSF) drainage simultaneously, to study cerebral vascular responses during acute CSF drainage.

Methods

Six patients with 34 external ventricular drain (EVD) opening sessions were retrospectively analyzed. A published algorithm was used to extract morphological features of ICP recordings, and a template-matching algorithm was applied to calculate the likelihood of cerebral vasodilation index (VDI) and cerebral vasoconstriction index (VCI) based on the changes of ICP waveforms during CSF drainage. Power change (∆P) of ICP B-waves after EVD opening was also calculated. Cerebral autoregulation (CA) was assessed through phase difference between arterial blood pressure (ABP) and ICP using a previously published wavelet-based algorithm.

Results

The result showed that acute CSF drainage reduced mean ICP (P = 0.016) increased VCI (P = 0.02) and reduced ICP B-wave power (P = 0.016) significantly. VCI reacted to ICP changes negatively when ICP was between 10 and 25 mmHg, and VCI remained unchanged when ICP was outside the 10–25 mmHg range. VCI negatively (r = − 0.44) and VDI positively (r = 0.82) correlated with ∆P of ICP B-waves, indicating that stronger vasoconstriction resulted in bigger power drop in ICP B-waves. Better CA prior to EVD opening triggered bigger drop in the power of ICP B-waves (r = − 0.612).

Conclusions

This study demonstrates that acute CSF drainage reduces mean ICP, and results in vasoconstriction which can be detected through an index, VCI. Cerebral vessels actively respond to ICP changes or cerebral perfusion pressure (CPP) changes in a certain range; beyond which, the vessels are insensitive to the changes in ICP and CPP.

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References

  1. Rangel-Castillo L, Robertson CS. Management of intracranial hypertension. Crit Care Clin. 2006;26:713–32.

    Article  Google Scholar 

  2. Lane PL, Skoretz TG, Doig G, Girotti MJ. Intracranial pressure monitoring and outcomes after traumatic brain injury. Can J Surg. 2000;43:442–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Czosnyka M, Smielewski P, Timofeev I, Lavinio A, Guazzo E, Hutchinson P, et al. Intracranial pressure: more than a number. Neurosurg Focus. 2007;22:E10.

    PubMed  Google Scholar 

  4. Czosnyka Z, Czosnyka M. Long-term monitoring of intracranial pressure in normal pressure hydrocephalus and other CSF disorders. Acta Neurochir (Wien). 2017;159:1979–80.

    Article  Google Scholar 

  5. Chari A, Dasgupta D, Smedley A, Craven C, Dyson E, Matloob S, et al. Intraparenchymal intracranial pressure monitoring for hydrocephalus and cerebrospinal fluid disorders. Acta Neurochir (Wien). 2017;159:1967–78.

    Article  Google Scholar 

  6. Kirkman MA, Smith M. Intracranial pressure monitoring, cerebral perfusion pressure estimation, and icp/cpp-guided therapy: a standard of care or optional extra after brain injury? Br J Anaesth. 2014;112:35–46.

    Article  CAS  Google Scholar 

  7. Muralidharan R. External ventricular drains: management and complications. Surg Neurol Int. 2015;6:271.

    Article  Google Scholar 

  8. Kirmani A, Sarmast A, Bhat A. Role of external ventricular drainage in the management of intraventricular hemorrhage; its complications and management. Surg Neurol Int. 2015;6:188.

    Article  Google Scholar 

  9. Staykov D, Kuramatsu JB, Bardutzky J, Volbers B, Gerner ST, Kloska SP, et al. Efficacy and safety of combined intraventricular fibrinolysis with lumbar drainage for prevention of permanent shunt dependency after intracerebral hemorrhage with severe ventricular involvement: A randomized trial and individual patient data meta-analysis. Ann Neurol. 2017;81:93–103.

    Article  CAS  Google Scholar 

  10. Kerr ME, Weber BB, Sereika SM, Wilberger J, Marion DW. Dose response to cerebrospinal fluid drainage on cerebral perfusion in traumatic brain-injured adults. Neurosurg Focus. 2001;11:E1.

    Article  CAS  Google Scholar 

  11. Cruz J. Combined continuous monitoring of systemic and cerebral oxygenation in acute brain injury: preliminary observations. Crit Care Med. 1993;21:1225–32.

    Article  CAS  Google Scholar 

  12. Fortune JB, Feustel PJ, Graca L, Hasselbarth J, Kuehler DH, Wilberger JE, et al. Effect of hyperventilation, mannitol, and ventriculostomy drainage on cerebral blood flow after head injury. J Trauma—Inj Infect Crit Care. 1995;39:1091–9.

    Article  CAS  Google Scholar 

  13. Papo I, Caruselli G. Long-term intracranial pressure monitoring in comatose patients suffering from head injuries. A critical survey. Acta Neurochir (Wien). 1977;39:187–200.

    Article  CAS  Google Scholar 

  14. Zweckberger K, Sakowitz OW, Unterberg AW, Kiening KL. Intracranial pressure-volume relationship. Physiology and pathophysiology. Anaesthesist. 2009;58:392–7.

    Article  CAS  Google Scholar 

  15. Kerr EM, Marion D, Sereika MS, Weber BB, Orndoff AP, Henker R, et al. The effect of cerebrospinal fluid drainage on cerebral perfusion in traumatic brain injured adults. J Neurosurg Anesthesiol. 2000;12:324–33.

    Article  CAS  Google Scholar 

  16. Slazinkski T, Anderson T, Cattell E, Eigsti J, Heimsoth S. Care of the patient undergoing intracranial pressure monitoring/external ventricular drainage or lumbar drainage. AANN Clin Pract Guidel Ser. 2011:1–38.

  17. Integra Design Verification Report for Camino Flex Ventricular Catheter. 49–51.

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

    Article  Google Scholar 

  19. Asgari S, Gonzalez N, Subudhi AW, Hamilton R, Vespa P, Bergsneider M, et al. Continuous detection of cerebral vasodilatation and vasoconstriction using intracranial pulse morphological template matching. PLoS One. 2012;7:e52795.

    Article  Google Scholar 

  20. 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;15:55–62.

    Article  Google Scholar 

  21. Kempley ST, Gamsu HR. Changes in cerebral artery blood flow velocity after intermittent cerebrospinal fluid drainage. Arch Dis Child. 1993;69:74–6.

    Article  CAS  Google Scholar 

  22. Asgari S, Vespa P, Bergsneider M, Hu X. Lack of consistent intracranial pressure pulse morphological changes during episodes of microdialysis lactate/pyruvate ratio increase. Physiol Meas. 2011;32:1639–51.

    Article  Google Scholar 

  23. Connolly M, Vespa P, Hu X. Characterization of cerebral vascular response to EEG bursts using ICP pulse waveform template matching. Acta Neurochir Suppl. 2016;122:291–4.

    Article  Google Scholar 

  24. Bouma GJ, Muizelaar JP, Bandoh K, Marmarou A. Blood pressure and intracranial pressure-volume dynamics in severe head injury: relationship with cerebral blood flow. J Neurosurg. 1992;77:15–9.

    Article  CAS  Google Scholar 

  25. Rangel-Castilla L, Gasco J, Nauta HJW, Okonkwo DO, Robertson CS. Cerebral pressure autoregulation in traumatic brain injury. Neurosurg Focus. 2008;25:E7.

    Article  Google Scholar 

  26. Kainerstorfer JM, Sassaroli A, Tgavalekos KT, Fantini S. Cerebral autoregulation in the microvasculature measured with near-infrared spectroscopy. J Cereb Blood Flow Metab. 2015;35:959–66.

    Article  CAS  Google Scholar 

  27. Salehi A, Zhang JH, Obenaus A. Response of the cerebral vasculature following traumatic brain injury. J Cereb Blood Flow Metab. 2017;37:2320–39.

    Article  Google Scholar 

  28. Liu X, Donnelly J, Czosnyka M, Aries MJH, Brady K, Cardim D, et al. Cerebrovascular pressure reactivity monitoring using wavelet analysis in traumatic brain injury patients: a retrospective study. PLOS Med. 2017;14:7.

    Article  CAS  Google Scholar 

  29. Tian F, Tarumi T, Liu H, Zhang R, Chalak L. Wavelet coherence analysis of dynamic cerebral autoregulation in neonatal hypoxic-ischemic encephalopathy. NeuroImage Clin. 2016;11:124–32.

    Article  Google Scholar 

  30. Peng T, Rowley AB, Ainslie PN, Poulin MJ, Payne SJ. Wavelet phase synchronization analysis of cerebral blood flow autoregulation. IEEE Trans Biomed Eng. 2010;57:960–8.

    Article  Google Scholar 

  31. Spiegelberg A, Preuß M, Kurtcuoglu V. B-waves revisited. Interdiscip Neurosurg. 2016;6:13–7.

    Article  Google Scholar 

  32. Lemaire JJ, Khalil T, Cervenansky F, Gindre G, Boire JY, Bazin JE, et al. Slow pressure waves in the cranial enclosure. Acta Neurochir (Wien). 2002;144:243–54.

    Article  CAS  Google Scholar 

  33. Lundberg N. Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Scand Suppl. 1960;36:1–193.

    CAS  PubMed  Google Scholar 

  34. Hu X, Xu P, Lee DJ, Vespa P, Baldwin K, Bergsneider M. An algorithm for extracting intracranial pressure latency relative to electrocardiogram R wave. Physiol Meas. 2008;29:459–71.

    Article  Google Scholar 

  35. Grinsted A, Moore JC, Jevrejeva S. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process Geophys. 2004;11:561–6.

    Article  Google Scholar 

  36. Keissar K, Davrath LR, Akselrod S. Coherence analysis between respiration and heart rate variability using continuous wavelet transform. Philos Trans A Math Phys Eng Sci. 2009;367:1393–406.

    Article  Google Scholar 

  37. Kvandal P, Sheppard L, Landsverk SA, Stefanovska A, Kirkeboen KA. Impaired cerebrovascular reactivity after acute traumatic brain injury can be detected by wavelet phase coherence analysis of the intracranial and arterial blood pressure signals. J Clin Monit Comput. 2013;27:375–83.

    Article  Google Scholar 

  38. Ps A. The illustrated wavelet transform handbook, introductory theory and applications in science, engineering, medicine and finance. New York: Talor and Francis; 2002.

    Google Scholar 

  39. Addison PS. The illustrated wavelet transform handbook: introductory theory and applications in science, engineering, medicine and finance. 2nd ed. Boca Raton: CRC Press; 2016.

    Google Scholar 

  40. Brady KM, Easley RB, Kibler K, Kaczka DW, Andropoulos D, Fraser CD, et al. Positive end-expiratory pressure oscillation facilitates brain vascular reactivity monitoring. J Appl Physiol. 2012;113:1362–8.

    Article  Google Scholar 

  41. Zhang R, Zuckerman JH, Giller CA, Levine BD. Transfer function analysis of dynamic cerebral autoregulation in humans. Am J Physiol. 1998;274:H233–41.

    CAS  PubMed  Google Scholar 

  42. Muizelaar J, Ward J, Marmarou A, Newlon P, Wachi A. Cerebral blood flow and metabolism in severely head-injured children Part 2: Autoregulation. J Neurosurg. 1989;71:72–6.

    Article  CAS  Google Scholar 

  43. Liu X, Czosnyka M, Donnelly J, Cardim D, Cabeleira M, Hutchinson PJ, et al. Wavelet pressure reactivity index: a validation study. J Physiol. 2018;596(14):2797–2809.

    Article  CAS  Google Scholar 

  44. Rao AR, Hamed K. Multi-taper method of analysis of periodicities in hydrologic data. J Hydrol. 2003;279:125–43.

    Article  Google Scholar 

  45. Jeyaseelan AS, Balaji R. Spectral analysis of wave elevation time histories using multi-taper method. Ocean Eng. 2015;105:242–6.

    Article  Google Scholar 

  46. Aries MJH, Czosnyka M, Budohoski KP, Steiner LA, Lavinio A, Kolias AG, et al. Continuous determination of optimal cerebral perfusion pressure in traumatic brain injury. Crit Care Med. 2012;40:2456–63.

    Article  Google Scholar 

  47. Trauner DA, Brown F, Ganz E, Huttenlocher PR. Treatment of elevated intracranial pressure in reye syndrome. Ann Neurol. 1978;4:275–8.

    Article  CAS  Google Scholar 

  48. Hawthorne C, Piper I. Monitoring of intracranial pressure in patients with traumatic brain injury. Front Neurol. 2014;5:121.

    Article  Google Scholar 

  49. Physics C, Hospital SG, Kingdom U. Pressure autoregulation monitoring and cerebral perfusion pressure target recommendation in patients with severe traumatic brain injury based on minute-by-minute monitoring data. 2014;120:1451–7.

    Google Scholar 

  50. Panerai RB. Cerebral autoregulation: from models to clinical applications. Cardiovasc Eng. 2008;8:42–59.

    Article  Google Scholar 

  51. Larsen FS, Olsen KS, Hansen BA, Paulson OB, Knudsen GM. Transcranial Doppler is valid for determination of the lower limit of cerebral blood flow autoregulation. Stroke. 1994;25:1985–8.

    Article  CAS  Google Scholar 

  52. Lang EW, Lagopoulos J, Griffith J, Yip K, Yam A, Mudaliar Y, et al. Cerebral vasomotor reactivity testing in head injury: the link between pressure and flow. J Neurol Neurosurg Psychiatry. 2003;74:1053–9.

    Article  CAS  Google Scholar 

  53. Rosner MJ, Rosner SD, Johnson AH. Cerebral perfusion pressure: management protocol and clinical results. J Neurosurg. 1995;83:949–62.

    Article  CAS  Google Scholar 

  54. Hemphill JC, Andrews P, De Georgia M. Multimodal monitoring and neurocritical care bioinformatics. Nat Rev Neurol. 2011;7:451–60.

    Article  Google Scholar 

  55. Addison PS. Identifying stable phase coupling associated with cerebral autoregulation using the synchrosqueezed cross-wavelet transform and low oscillation Morlet wavelets. Conf Proc IEEE Eng Med Biol Soc. 2015;8:5960–3.

    Google Scholar 

  56. Lewis PM, Rosenfeld JV, Diehl RR, Mehdorn HM, Lang EW. Phase shift and correlation coefficient measurement of cerebral autoregulation during deep breathing in traumatic brain injury (TBI). Acta Neurochir (Wien). 2008;150:139–46.

    Article  CAS  Google Scholar 

  57. Donnelly J, Budohoski KP, Smielewski P, Czosnyka M. Regulation of the cerebral circulation: bedside assessment and clinical implications. Crit Care. 2016;20:129.

    Article  Google Scholar 

  58. Lee JK, Kibler KK, Benni PB, Easley RB, Czosnyka M, Smielewski P, et al. Cerebrovascular reactivity measured by near-infrared spectroscopy. Stroke. 2009;40:1820–6.

    Article  Google Scholar 

  59. Liu X, Czosnyka M, Donnelly J, Budohoski KP, Varsos GV, Nasr N, et al. Comparison of frequency and time domain methods of assessment of cerebral autoregulation in traumatic brain injury. J Cereb Blood Flow Metab. 2014;11:1–9.

    Google Scholar 

  60. Steiner LA, Czosnyka M, Piechnik SK. Continuous monitoring of cerebrovascular pressure reactivity allows determination of optimal cerebral perfusion pressure in patients with traumatic brain injury. Crit Care. 2002;30:733–8.

    Article  Google Scholar 

  61. Depreitere B, Güiza F, Van den Berghe G, Schuhmann MU, Maier G, Piper I, et al. Pressure autoregulation monitoring and cerebral perfusion pressure target recommendation in patients with severe traumatic brain injury based on minute-by-minute monitoring data. J Neurosurg. 2014;120:1451–7.

    Article  Google Scholar 

  62. Liu X, Maurits N, Aries M, Czosnyka M, Ercole A, Donnelly J, et al. Monitoring of optimal cerebral perfusion pressure in traumatic brain injured patients using a multi-window weighting algorithm. J Neurotraum`a. 2017;34:3081–8.

    Article  Google Scholar 

  63. Cardim D, Robba C, Bohdanowicz M, Donnelly J, Cabella B, Liu X, et al. Non-invasive Monitoring of Intracranial Pressure Using Transcranial Doppler Ultrasonography: Is It Possible? Neurocrit Care. 2016;25:473–91.

    Article  Google Scholar 

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Funding

This work was partially supported by the UCSF Middle Career Scientist Award, UCSF Institute for Computational Health Sciences, and National Institutes of Health awards (R01NS076738 and NS106905-01A1).

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Authors

Contributions

The concept and study design were formed by X.H., X.Y.L., P.V., L.Z. and X.L.L. Data acquisition was conducted by P.V., N.H. and L.Z. Data analysis was conducted by X.Y.L., N.H., X.L.L and X.H. Drafting of the manuscript and figures was contributed by X.Y.L., X.H., L.Z., P.V., N.H. and X.L.L.

Corresponding author

Correspondence to Xiuyun Liu.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

The institutional review board (IRB) approved the data analysis and waived the need for consenting patients because of the retrospective nature of the study.

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Liu, X., Zimmermann, L.L., Ho, N. et al. Cerebral Vascular Changes During Acute Intracranial Pressure Drop. Neurocrit Care 30, 635–644 (2019). https://doi.org/10.1007/s12028-018-0651-4

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