Hemodynamic characterization of intracranial pressure plateau waves in head-injured patients

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Object. Plateau waves of intracranial pressure (ICP) are often recorded during intensive care monitoring of severely head injured patients. They are traditionally interpreted as meaningful secondary brain insults because of the dramatic decrease in cerebral perfusion pressure (CPP). The aim of this study was to investigate both the hemodynamic profile and the clinical consequences of plateau waves.

Methods. One hundred sixty head-injured patients were studied using continuous monitoring of ICP; almost 20% of these patients exhibited plateau waves. In 96 patients arterial pressure, ICP, and transcranial Doppler (TCD) blood flow velocity were studied daily for 20 minutes to 3 hours. Sixteen episodes of plateau waves in eight patients were recorded and analyzed.

The dramatic increase in ICP was followed by a profound fall in CPP (by 45%). In contrast, flow velocity fell by only 20%. Autoregulation was documented to be intact both before and after plateau but was disturbed during the wave (p < 0.05). Pressure-volume compensatory reserve was always depleted before the wave. Cerebrovascular resistance decreased during the wave by 60% (p <0.05) and TCD pulsatility increased (p <0.05). Plateau waves did not increase the probability of an unfavorable outcome following injury.

Conclusions. The authors have confirmed that the plateau waves are a hemodynamic phenomenon associated with cerebrovascular vasodilation. They are observed in patients with preserved cerebral autoregulation but reduced pressure-volume compensatory reserve.

Article Information

Address reprint requests to: Marek Czosnyka, Ph.D., Academic Neurosurgical Unit, P. O. Box 167, Addenbrooke's Hospital, Cambridge CB2 2QQ, United Kingdom. email: MC141@MEDSCHL.CAM.AC.UK.

© AANS, except where prohibited by US copyright law.

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Figures

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    Examples of recordings of ABP, ICP, and blood FV obtained in two head-injured patients developing ICP plateau waves. A: The plateau wave was initiated by a short-term decrease in ABP. B: The ABP before the wave was stable, but ICP waves (B-waves) were recorded.

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    Tracings of plateau waves with parallel changes in indices describing cerebral autoregulation (Mx), vascular reactivity (PRx), and pressure—volume compensatory reserve (RAP). The tracings show decreases in both autoregulatory and reactivity capacity (Mx and Prx both increase). The compensatory reserve is exhausted (RAP close to +1).

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    Tracings showing the dynamic behavior of pulse amplitudes of blood FV (FVa) and intracranial pressure (ICPa) during a plateau wave.

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    Recordings showing the distinctive changes in ICP and FV pulsatile components before (left) and on the top (right) of a plateau wave.

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    Scatterplots of pooled 1-minute averages from all 16 plateau waves analyzed with the best-fit polynomial regression models (5th order, r2 > 0.75). a: The ICP pulse amplitude compared with the mean ICP. b: The ICP pulse amplitude compared with the mean CPP.

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    Tracings showing deep vasogenic waves of ICP that are not plateau waves. a: Passive transmission of rapid variation of ABP to ICP. b: Active response of ICP to changes in ABP (note the inverse direction of changes in ABP and ICP). c: Increase in ICP caused by temporary hyperemia, as it is revealed by a rise in the FV.

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    Tracings showing the rare occurrence of a very deep plateau wave, when blood FV decreases by more than 60% of baseline. Notice the decrease in heart rate (HR) and the hyperemic increase in FV after the ICP wave subsided.

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    Recording of early termination of a plateau wave by manual hyperventilation lasting 74 seconds (indicated by a short thick horizontal bar), during which end-tidal CO2 decreased from 32 to 25 mm Hg. Note the immediate decrease in systolic blood FV in response to hyperventilation, with diastolic still being close to zero.

References

  • 1.

    Avezaat CJvan Eijndhoven JH: Clinical observations on the relationship between cerebrospinal fluid pulse pressure and intracranial pressure. Acta Neurochir 79:13291986Avezaat CJ van Eijndhoven JH: Clinical observations on the relationship between cerebrospinal fluid pulse pressure and intracranial pressure. Acta Neurochir 79:13–29 1986

  • 2.

    Avezaat CJJvan Eijndhoven JHM: Cerebrospinal Fluid Pulse Pressure and Craniospinal Dynamics. A Theoretical Clinical and Experimental Study. Thesis. The Hague: A Jongbloed1984Avezaat CJJ van Eijndhoven JHM: Cerebrospinal Fluid Pulse Pressure and Craniospinal Dynamics. A Theoretical Clinical and Experimental Study. Thesis. The Hague: A Jongbloed 1984

  • 3.

    Batorski LCzosnyka MLaniewski Pet al: Application of advanced forms of intracranial pressure analysis in craniosynostosis in Hoff JTBetz AL (eds): Intracranial Pressure VII. Berlin: Springer-Verlag1989 pp 189192Batorski L Czosnyka M Laniewski P et al: Application of advanced forms of intracranial pressure analysis in craniosynostosis in Hoff JT Betz AL (eds): Intracranial Pressure VII. Berlin: Springer-Verlag 1989 pp 189–192

  • 4.

    Chan KHMiller DJDearden NMet al: The effect of changes in cerebral perfusion pressure upon middle cerebral artery blood flow velocity and jugular bulb venous oxygen saturation after severe brain trauma. J Neurosurg 77:55611992Chan KH Miller DJ Dearden NM et al: The effect of changes in cerebral perfusion pressure upon middle cerebral artery blood flow velocity and jugular bulb venous oxygen saturation after severe brain trauma. J Neurosurg 77:55–61 1992

  • 5.

    Czosnyka MGuazzo EWhitehouse Met al: Significance of intracranial pressure waveform analysis after head injury. Acta Neurochir 138:5315421996Czosnyka M Guazzo E Whitehouse M et al: Significance of intracranial pressure waveform analysis after head injury. Acta Neurochir 138:531–542 1996

  • 6.

    Czosnyka MPiechnik SRichards HKet al: Contribution of mathematical modelling to the interpretation of bedside tests of cerebrovascular autoregulation. J Neurol Neurosurg Psychiatry 63:7217311997Czosnyka M Piechnik S Richards HK et al: Contribution of mathematical modelling to the interpretation of bedside tests of cerebrovascular autoregulation. J Neurol Neurosurg Psychiatry 63:721–731 1997

  • 7.

    Czosnyka MRichards HKWhitehouse HEet al: Relationship between transcranial Doppler-determined pulsatility index and cerebrovascular resistance: an experimental study. J Neurosurg 84:79841996Czosnyka M Richards HK Whitehouse HE et al: Relationship between transcranial Doppler-determined pulsatility index and cerebrovascular resistance: an experimental study. J Neurosurg 84:79–84 1996

  • 8.

    Czosnyka MSmielewski PKirkpatrick Pet al: Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 41:11191997Czosnyka M Smielewski P Kirkpatrick P et al: Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 41:11–19 1997

  • 9.

    Czosnyka MSmielewski PKirkpatrick Pet al: Monitoring of cerebral autoregulation in head-injured patients. Stroke 27:182918341996Czosnyka M Smielewski P Kirkpatrick P et al: Monitoring of cerebral autoregulation in head-injured patients. Stroke 27:1829–1834 1996

  • 10.

    Czosnyka MWhitehouse HSmielewski Pet al: Computer supported multimodal bed-side monitoring in neuro intensive care. Int J Clin Monitor Comput 11:2232321994Czosnyka M Whitehouse H Smielewski P et al: Computer supported multimodal bed-side monitoring in neuro intensive care. Int J Clin Monitor Comput 11:223–232 1994

  • 11.

    Czosnyka MWollk-Laniewski PBatorski L: Analysis of intracranial pressure waveform during infusion test. Acta Neurochir 93:1401451989Czosnyka M Wollk-Laniewski P Batorski L: Analysis of intracranial pressure waveform during infusion test. Acta Neurochir 93:140–145 1989

  • 12.

    Giller CARatcliff BBerger Bet al: An impedance index in normal subjects and in subarachnoid hemorrhage. Ultrasound Med Biol 22:3733821996Giller CA Ratcliff B Berger B et al: An impedance index in normal subjects and in subarachnoid hemorrhage. Ultrasound Med Biol 22:373–382 1996

  • 13.

    Gjerris FBorgesen SEHoppe Eet al: The conductance to outflow of CSF in adults with high-pressure hydrocephalus. Acta Neurochir 64:59671982Gjerris F Borgesen SE Hoppe E et al: The conductance to outflow of CSF in adults with high-pressure hydrocephalus. Acta Neurochir 64:59–67 1982

  • 14.

    Gray WJRosner MJ: Pressure-volume index as a function of cerebral perfusion pressure. Part 1: The effects of cerebral perfusion pressure changes and anesthesia. J Neurosurg 67:3693761987Gray WJ Rosner MJ: Pressure-volume index as a function of cerebral perfusion pressure. Part 1: The effects of cerebral perfusion pressure changes and anesthesia. J Neurosurg 67:369–376 1987

  • 15.

    Hayashi MHanda YKobayashi Het al: Plateau wave phenomenon (I). Correlation between the appearance of plateau waves and CSF circulation in patients with intracranial hypertension. Brain 114:268126911991Hayashi M Handa Y Kobayashi H et al: Plateau wave phenomenon (I). Correlation between the appearance of plateau waves and CSF circulation in patients with intracranial hypertension. Brain 114:2681–2691 1991

  • 16.

    Hayashi MKobayashi HHanda Yet al: Brain blood volume and blood flow in patients with plateau waves. J Neurosurg 63:5565611985Hayashi M Kobayashi H Handa Y et al: Brain blood volume and blood flow in patients with plateau waves. J Neurosurg 63:556–561 1985

  • 17.

    Hayashi MKobayashi HKawano Het al: Cerebral blood flow and ICP patterns in patients with communicating hydrocephalus after aneurysm rupture. J Neurosurg 61:30361984Hayashi M Kobayashi H Kawano H et al: Cerebral blood flow and ICP patterns in patients with communicating hydrocephalus after aneurysm rupture. J Neurosurg 61:30–36 1984

  • 18.

    Hayashi MKobayashi HKawano Het al: ICP patterns and isotope cisternography in patients with communicating hydrocephalus following rupture of intracranial aneurysm. J Neurosurg 62:2202261985Hayashi M Kobayashi H Kawano H et al: ICP patterns and isotope cisternography in patients with communicating hydrocephalus following rupture of intracranial aneurysm. J Neurosurg 62:220–226 1985

  • 19.

    Ishii HHanda YKobayashi Het al: Role of the medullary vasomotor centre in the development of plateau waves. Neurol Res 11:1861901989Ishii H Handa Y Kobayashi H et al: Role of the medullary vasomotor centre in the development of plateau waves. Neurol Res 11:186–190 1989

  • 20.

    Janny P: La Pression Intracranienne Chez l'Homme. Thesis. Paris: 1950Janny P: La Pression Intracranienne Chez l'Homme. Thesis. Paris: 1950

  • 21.

    Kontos HAWei EPNavari RMet al: Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 234:H371H3831978Kontos HA Wei EP Navari RM et al: Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 234:H371–H383 1978

  • 22.

    Legarth JNolsoe C: Doppler blood velocity waveforms and the relation to peripheral resistance in the brachial artery. J Ultrasound Med 9:4494531990Legarth J Nolsoe C: Doppler blood velocity waveforms and the relation to peripheral resistance in the brachial artery. J Ultrasound Med 9:449–453 1990

  • 23.

    Lundberg N: Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Neurol Scand 36 (Suppl 149):11931960Lundberg N: Continuous recording and control of ventricular fluid pressure in neurosurgical practice. Acta Psychiatr Neurol Scand 36 (Suppl 149):1–193 1960

  • 24.

    Matsuda MYoneda SHanda Het al: Cerebral hemodynamics changes during plateau waves in brain-tumor patients. J Neurosurg 50:4834881979Matsuda M Yoneda S Handa H et al: Cerebral hemodynamics changes during plateau waves in brain-tumor patients. J Neurosurg 50:483–488 1979

  • 25.

    Miller JDBecker DP: Secondary insults to the injured brain. J R Coll Surg Edinb 27:2922981982Miller JD Becker DP: Secondary insults to the injured brain. J R Coll Surg Edinb 27:292–298 1982

  • 26.

    Miller JDPickard JD: Intracranial volume-pressure studies in patients with head injury. Injury 5:2652681974Miller JD Pickard JD: Intracranial volume-pressure studies in patients with head injury. Injury 5:265–268 1974

  • 27.

    Newell DWAaslid RStooss Ret al: Evaluation of hemodynamic responses in head injury patients with transcranial Doppler monitoring. Acta Neurochir 139:8048171997Newell DW Aaslid R Stooss R et al: Evaluation of hemodynamic responses in head injury patients with transcranial Doppler monitoring. Acta Neurochir 139:804–817 1997

  • 28.

    Nornes HAaslid RLindegaard KF: Intracranial pulse pressure dynamics in patients with intracranial hypertension. Acta Neurochir 38:1771861977Nornes H Aaslid R Lindegaard KF: Intracranial pulse pressure dynamics in patients with intracranial hypertension. Acta Neurochir 38:177–186 1977

  • 29.

    Piper IRMiller JDDearden NMet al: System analysis of cerebrovascular pressure transmission: an observational study in head-injured patients. J Neurosurg 73:8718801990Piper IR Miller JD Dearden NM et al: System analysis of cerebrovascular pressure transmission: an observational study in head-injured patients. J Neurosurg 73:871–880 1990

  • 30.

    Price DJSaxena ACzosnyka M: The relationship of vasogenic waves to ICP and cerebral perfusion pressure in head injured patients. Acta Neurochir Suppl 71:2972991998Price DJ Saxena A Czosnyka M: The relationship of vasogenic waves to ICP and cerebral perfusion pressure in head injured patients. Acta Neurochir Suppl 71:297–299 1998

  • 31.

    Renier DSainte-Rose CMarchac Det al: Intracranial pressure in craniostenosis. J Neurosurg 57:3703771982Renier D Sainte-Rose C Marchac D et al: Intracranial pressure in craniostenosis. J Neurosurg 57:370–377 1982

  • 32.

    Risberg JLundberg NIngvar DH: Regional cerebral blood volume during acute transient rises of intracranial pressure (plateau waves). J Neurosurg 31:3033101969Risberg J Lundberg N Ingvar DH: Regional cerebral blood volume during acute transient rises of intracranial pressure (plateau waves). J Neurosurg 31:303–310 1969

  • 33.

    Rosner MJ: Pathophysiology and management of increased intracranial pressure in Andrews BT (ed): Neurosurgical Intensive Care. New York: McGraw Hill1993 pp 57112Rosner MJ: Pathophysiology and management of increased intracranial pressure in Andrews BT (ed): Neurosurgical Intensive Care. New York: McGraw Hill 1993 pp 57–112

  • 34.

    Rosner MJBecker DP: Origin and evolution of plateau waves. Experimental observations and a theoretical model. J Neurosurg 60:3123241984Rosner MJ Becker DP: Origin and evolution of plateau waves. Experimental observations and a theoretical model. J Neurosurg 60:312–324 1984

  • 35.

    Signorini DFAndrews PJDJones PAet al: Adding insult to injury: the prognostic value of early secondary insults for survival after traumatic brain injury. J Neurosurg Neurol Psychiatry 66:26311999Signorini DF Andrews PJD Jones PA et al: Adding insult to injury: the prognostic value of early secondary insults for survival after traumatic brain injury. J Neurosurg Neurol Psychiatry 66:26–31 1999

  • 36.

    Smielewski PCzosnyka MZabolotny Wet al: A computing system for the clinical and experimental investigation of cerebrovascular reactivity. Int J Clin Monitor Comput 14:1851981997Smielewski P Czosnyka M Zabolotny W et al: A computing system for the clinical and experimental investigation of cerebrovascular reactivity. Int J Clin Monitor Comput 14:185–198 1997

  • 37.

    Stochetti NRossi SCacerelli Pet al: The pattern of ICP after bolus injection as an indicator of intracranial disturbances in Nagai HKamiya KIshii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag1994 pp 172174Stochetti N Rossi S Cacerelli P et al: The pattern of ICP after bolus injection as an indicator of intracranial disturbances in Nagai H Kamiya K Ishii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag 1994 pp 172–174

  • 38.

    Symon LDorsch NWC: Use of long-term intracranial pressure measurement to assess hydrocephalic patients prior to shunt surgery. J Neurosurg 42:2582731975Symon L Dorsch NWC: Use of long-term intracranial pressure measurement to assess hydrocephalic patients prior to shunt surgery. J Neurosurg 42:258–273 1975

  • 39.

    Thiel AZickmann BStertmann WAet al: Cerebrovascular carbon dioxide reactivity in carotid artery disease. Relation to intraoperative cerebral monitoring results in 100 carotid endarterectomies. Anesthesiology 82:6556611995Thiel A Zickmann B Stertmann WA et al: Cerebrovascular carbon dioxide reactivity in carotid artery disease. Relation to intraoperative cerebral monitoring results in 100 carotid endarterectomies. Anesthesiology 82:655–661 1995

  • 40.

    Tuor UIFarrar JK: Pial vessel caliber and cerebral blood flow during hemorrhage and hypercapnia in the rabbit. Am J Physiol 247:H40H511984Tuor UI Farrar JK: Pial vessel caliber and cerebral blood flow during hemorrhage and hypercapnia in the rabbit. Am J Physiol 247:H40–H51 1984

  • 41.

    Ursino MDiGiammarco P: A mathematical model of the relationship between cerebral blood volume and intracranial pressure changes: the generation of plateau waves. Ann Biomed Eng 19:15421991Ursino M DiGiammarco P: A mathematical model of the relationship between cerebral blood volume and intracranial pressure changes: the generation of plateau waves. Ann Biomed Eng 19:15–42 1991

  • 42.

    Zabolotny WCzosnyka MSmielewski P: Portable software for intracranial pressure recording and waveform analysis in Nagai HKamiya KIshii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag1994 pp 439440Zabolotny W Czosnyka M Smielewski P: Portable software for intracranial pressure recording and waveform analysis in Nagai H Kamiya K Ishii S (eds): Intracranial Pressure IX. Tokyo: Springer-Verlag 1994 pp 439–440

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