Skip to main content

Advertisement

SpringerLink
Log in

A Continuous Correlation Between Intracranial Pressure and Cerebral Blood Flow Velocity Reflects Cerebral Autoregulation Impairment During Intracranial Pressure Plateau Waves

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

Abstract

Background

In the healthy brain, small oscillations in intracranial pressure (ICP) occur synchronously with those in cerebral blood volume (CBV), cerebrovascular resistance, and consequently cerebral blood flow velocity (CBFV). Previous work has shown that the usual synchrony between ICP and CBFV is lost during intracranial hypertension. Moreover, a continuously computed measure of the ICP/CBFV association (Fix index) was a more sensitive predictor of outcome after traumatic brain injury (TBI) than a measure of autoregulation (Mx index). In the current study we computed Fix during ICP plateau waves, to observe its behavior during a defined period of cerebrovascular vasodilatation.

Methods

Twenty-nine recordings of arterial blood pressure (ABP), ICP, and CBFV taken during ICP plateau waves were obtained from the Addenbrooke’s hospital TBI database. Raw data was filtered prior to computing Mx and Fix according to previously published methods. Analyzed data was segmented into three phases (pre, peak, and post), and a median value of each parameter was stored for analysis.

Results

ICP increased from a median of 22–44 mmHg before falling to 19 mmHg. Both Mx and Fix responded to the increase in ICP, with Mx trending toward +1, while Fix trended toward −1. Mx and Fix correlated significantly (Spearman’s R = −0.89, p < 0.000001), however, Fix spanned a greater range than Mx. A plot of Mx and Fix against CPP showed a plateau (Mx) or trough (Fix) consistent with a zone of “optimal CPP”.

Conclusions

The Fix index can identify complete loss of cerebral autoregulation as the point at which the normally positive CBF/CBV correlation is reversed. Both CBF and CBV can be monitored noninvasively using near-infrared spectroscopy (NIRS), suggesting that a noninvasive method of monitoring autoregulation using only NIRS may be possible.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Diehl RR, Diehl B, Sitzer M, Hennerici M. Spontaneous oscillations in cerebral blood flow velocity in normal humans and in patients with carotid artery disease. Neurosci Lett. 1991;127:5–8.

    Article  CAS  PubMed  Google Scholar 

  2. Lang EW, Diehl RR, Timmermann L, et al. Spontaneous oscillations of arterial blood pressure, cerebral and peripheral blood flow in healthy and comatose subjects. Neurol Res. 1999;21:665–9.

    CAS  PubMed  Google Scholar 

  3. Lewis PM, Smielewski P, Pickard JD, Czosnyka M. Slow oscillations in middle cerebral artery cerebral blood flow velocity and aging. Neurol Res. 2007;29:260–3.

    Article  PubMed  Google Scholar 

  4. Lundar T, Lindegaard KF, Nornes H. Continuous recording of middle cerebral artery blood velocity in clinical neurosurgery. Acta Neurochir (Wien). 1990;102:85–90.

    Article  CAS  Google Scholar 

  5. 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 

  6. Castellani G, Zweifel C, Kim DJ, et al. Plateau waves in head injured patients requiring neurocritical care. Neurocrit Care. 2009;11:143–50.

    Article  PubMed  Google Scholar 

  7. Aalkjaer C, Boedtkjer D, Matchkov V. Vasomotion—what is currently thought? Acta Physiol (Oxf). 2011;202:253–69.

    Article  CAS  Google Scholar 

  8. Auer LM, Sayama I. Intracranial pressure oscillations (B-waves) caused by oscillations in cerebrovascular volume. Acta Neurochir (Wien). 1983;68:93–100.

    Article  CAS  Google Scholar 

  9. Droste DW, Krauss JK, Berger W, Schuler E, Brown MM. Rhythmic oscillations with a wavelength of 0.5–2 min in transcranial Doppler recordings. Acta Neurol Scand. 1994;90:99–104.

    Article  CAS  PubMed  Google Scholar 

  10. Newell DW, Aaslid R, Stooss R, Reulen HJ. The relationship of blood flow velocity fluctuations to intracranial pressure B waves. J Neurosurg. 1992;76:415–21.

    Article  CAS  PubMed  Google Scholar 

  11. 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 

  12. Reinhard M, Roth M, Guschlbauer B, et al. Dynamic cerebral autoregulation in acute ischemic stroke assessed from spontaneous blood pressure fluctuations. Stroke. 2005;36:1684–9.

    Article  CAS  PubMed  Google Scholar 

  13. Rosner MJ. The vasodilatory cascade and intracranial pressure. In: Miller JD, Teasdale GM, Rowan JO, Galbraith SL, Mendelow AD, editors. Intracranial pressure IV. Berlin: Springer; 1986.

    Google Scholar 

  14. Czosnyka M, Smielewski P, Piechnik S, et al. Hemodynamic characterization of intracranial pressure plateau waves in head-injury patients. J Neurosurg. 1999;91:11–9.

    Article  CAS  PubMed  Google Scholar 

  15. Goh D, Minns RA, Pye SD, Steers AJ. Cerebral blood-flow velocity and intermittent intracranial pressure elevation during sleep in hydrocephalic children. Dev Med Child Neurol. 1992;34:676–89.

    Article  CAS  PubMed  Google Scholar 

  16. Czosnyka M, Smielewski P, Piechnik S, Steiner LA, Pickard JD. Cerebral autoregulation following head injury. J Neurosurg. 2001;95:756–63.

    Article  CAS  PubMed  Google Scholar 

  17. Lewis PM, Smielewski P, Rosenfeld JV, Pickard JD, Czosnyka M. Monitoring of the association between cerebral blood flow velocity and intracranial pressure. Acta Neurochir Suppl. 2012;114:147–51.

    Article  PubMed  Google Scholar 

  18. Budohoski KP, Czosnyka M, de Riva N, et al. The relationship between cerebral blood flow autoregulation and cerebrovascular pressure reactivity after traumatic brain injury. Neurosurgery. 2012;71:652–60 discussion 60–1.

    Article  PubMed  Google Scholar 

  19. Kim DJ, Kasprowicz M, Carrera E, et al. The monitoring of relative changes in compartmental compliances of brain. Physiol Meas. 2009;30:647–59.

    Article  CAS  PubMed  Google Scholar 

  20. Lassen NA. Cerebral blood flow and oxygen consumption in man. Physiol Rev. 1959;39:183–238.

    CAS  PubMed  Google Scholar 

  21. Weerakkody RA, Czosnyka M, Zweifel C, et al. Slow vasogenic fluctuations of intracranial pressure and cerebral near infrared spectroscopy–an observational study. Acta Neurochir (Wien). 2010;152:1763–9.

    Article  Google Scholar 

  22. Risberg J, Ancri D, Ingvar DH. Correlation between cerebral blood volume and cerebral blood flow in the cat. Exp Brain Res. 1969;8:321–6.

    Article  CAS  PubMed  Google Scholar 

  23. Barzo P, Doczi T, Csete K, Buza Z, Bodosi M. Measurements of regional cerebral blood flow and blood flow velocity in experimental intracranial hypertension: infusion via the cisterna magna in rabbits. Neurosurgery. 1991;28:821–5.

    Article  CAS  PubMed  Google Scholar 

  24. Grubb RL Jr, Raichle ME, Phelps ME, Ratcheson RA. Effects of increased intracranial pressure on cerebral blood volume, blood flow, and oxygen utilization in monkeys. J Neurosurg. 1975;43:385–98.

    Article  PubMed  Google Scholar 

  25. Miller JD, Stanek A, Langfitt TW. Concepts of cerebral perfusion pressure and vascular compression during intracranial hypertension. Prog Brain Res. 1972;35:411–32.

    Article  CAS  PubMed  Google Scholar 

  26. Wolff HG, Forbes HS. The cerebral circulation v: observations of the pial circulation during changes in intracranial pressure. Arch Neurol Psych. 1928;20:1035–47.

    Article  Google Scholar 

  27. Vignes JR, Dagain A, Guerin J, Liguoro D. A hypothesis of cerebral venous system regulation based on a study of the junction between the cortical bridging veins and the superior sagittal sinus. Laboratory investigation. J Neurosurg. 2007;107:1205–10.

    Article  PubMed  Google Scholar 

  28. Cushing HMD. Some experimental and clinical observations concerning states of increased intracranial tension. Am J Med Sci. 1902;124:375–400.

    Article  Google Scholar 

  29. Nakagawa Y, Tsuru M, Yada K. Site and mechanism for compression of the venous system during experimental intracranial hypertension. J Neurosurg. 1974;41:427–34.

    Article  CAS  PubMed  Google Scholar 

  30. Luce JM, Huseby JS, Kirk W, Butler J. A starling resistor regulates cerebral venous outflow in dogs. J Appl Physiol Respir Environ Exerc Physiol. 1982;53:1496–503.

    CAS  PubMed  Google Scholar 

  31. Johnston IH, Rowan JO. Raised intracranial pressure and cerebral blood flow. 3. Venous outflow tract pressures and vascular resistances in experimental intracranial hypertension. J Neurol Neurosurg Psychiatry. 1974;37:392–402.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Marmarou A, Maset AL, Ward JD, et al. Contribution of CSF and vascular factors to elevation of ICP in severely head-injured patients. J Neurosurg. 1987;66:883–90.

    Article  CAS  PubMed  Google Scholar 

  33. Risberg J, Lundberg N, Ingvar DH. Regional cerebral blood volume during acute transient rises of the intracranial pressure (plateau waves). J Neurosurg. 1969;31:303–10.

    Article  CAS  PubMed  Google Scholar 

  34. Rosner MJ, Becker DP. Origin and evolution of plateau waves. Experimental observations and a theoretical model. J Neurosurg. 1984;60:312–24.

    Article  CAS  PubMed  Google Scholar 

  35. Marmarou A, Signoretti S, Fatouros PP, Portella G, Aygok GA, Bullock MR. Predominance of cellular edema in traumatic brain swelling in patients with severe head injuries. J Neurosurg. 2006;104:720–30.

    Article  PubMed  Google Scholar 

  36. Brady KM, Lee JK, Kibler KK, et al. The lower limit of cerebral blood flow autoregulation is increased with elevated intracranial pressure. Anesth Analg. 2009;108:1278–83.

    Article  PubMed  Google Scholar 

  37. Anile C, De Bonis P, Di Chirico A, Ficola A, Mangiola A, Petrella G. Cerebral blood flow autoregulation during intracranial hypertension: a simple, purely hydraulic mechanism? Childs Nerv Syst. 2009;25:325–35 discussion 37–40.

    Article  CAS  PubMed  Google Scholar 

  38. Avezaat CJJ. Cerebral blood flow autoregulation during intracranial hypertension: a simple, purely hydraulic mechanism? Childs Nerv Syst. 2009;25:339–40.

    Article  Google Scholar 

  39. Wagner EM, Traystman RJ. Cerebrovascular transmural pressure and autoregulation. Ann Biomed Eng. 1985;13:311–20.

    Article  CAS  PubMed  Google Scholar 

  40. Strandgaard S, Paulson OB. Cerebral autoregulation. Stroke. 1984;15:413–6.

    Article  CAS  PubMed  Google Scholar 

  41. Brierley JB, Brown AW, Excell BJ, Meldrum BS. Brain damage in the rhesus monkey resulting from profound arterial hypotension. I. Its nature, distribution and general physiological correlates. Brain Res. 1969;13:68–100.

    Article  CAS  PubMed  Google Scholar 

  42. Wolf M, Ferrari M, Quaresima V. Progress of near-infrared spectroscopy and topography for brain and muscle clinical applications. J Biomed Opt. 2007;12:062104.

    Article  PubMed  Google Scholar 

  43. 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 discussion 46–7.

    Article  CAS  Google Scholar 

  44. Diehl RR, Linden D, Lucke D, Berlit P. Phase relationship between cerebral blood flow velocity and blood pressure. A clinical test of autoregulation. Stroke. 1995;26:1801–4.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  46. Jaeger M, Schuhmann MU, Soehle M, Meixensberger J. Continuous assessment of cerebrovascular autoregulation after traumatic brain injury using brain tissue oxygen pressure reactivity. Crit Care Med. 2006;34:1783–8.

    Article  PubMed  Google Scholar 

  47. Bhuiyan MR, Deb S, Mitchell RA, Teddy PJ, Drummond KJ. The effect of formal training on the clinical utility of transcranial Doppler ultrasound monitoring in patients with aneurysmal subarachnoid haemorrhage. J Clin Neurosci. 2012;19:1255–60.

    Article  PubMed  Google Scholar 

  48. Czosnyka M, Balestreri M, Steiner L, et al. Age, intracranial pressure, autoregulation, and outcome after brain trauma. J Neurosurg. 2005;102:450–4.

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

Marek Czosnyka and Peter Smielewski have a financial interest in a part of the licensing fee for ICM+. Philip M. Lewis, Jeffrey V. Rosenfeld, and John D. Pickard declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Alfred Hospital, 1st Floor, Old Baker Building, Commercial Road, Melbourne, VIC, 3003, Australia

    Philip M. Lewis & Jeffrey V. Rosenfeld

  2. Department of Surgery, Monash University, Melbourne, Australia

    Philip M. Lewis & Jeffrey V. Rosenfeld

  3. Department of Neurosurgery, Addenbrooke’s Hospital, University of Cambridge, Cambridge, UK

    Peter Smielewski, John D. Pickard & Marek Czosnyka

Authors
  1. Philip M. Lewis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Smielewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey V. Rosenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John D. Pickard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marek Czosnyka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip M. Lewis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lewis, P.M., Smielewski, P., Rosenfeld, J.V. et al. A Continuous Correlation Between Intracranial Pressure and Cerebral Blood Flow Velocity Reflects Cerebral Autoregulation Impairment During Intracranial Pressure Plateau Waves. Neurocrit Care 21, 514–525 (2014). https://doi.org/10.1007/s12028-014-9994-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-014-9994-7

Keywords

Search

Navigation