Impaired pulsation absorber mechanism in idiopathic normal pressure hydrocephalus

Laboratory investigation

Eun-Hyoung Park Ph.D.1, Per Kristian Eide M.D., Ph.D.2,4, David Zurakowski Ph.D.3, and Joseph R. Madsen M.D.1
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  • 1 Departments of Neurosurgery and
  • | 3 Anesthesiology, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts;
  • | 2 Department of Neurosurgery, Oslo University Hospital–Rikshospitalet, Oslo; and
  • | 4 Faculty of Medicine, University of Oslo, Norway
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Object

The pathophysiology of normal pressure hydrocephalus (NPH), and the related problem of patient selection for treatment of this condition, have been of great interest since the description of this seemingly paradoxical condition nearly 50 years ago. Recently, Eide has reported that measurements of the amplitude of the intracranial pressure (ICP) can both positively and negatively predict response to CSF shunting. Specifically, the fraction of time spent in a “high amplitude” (> 4 mm Hg) state predicted response to shunting, which may represent a marker for hydrocephalic pathophysiology. Increased ICP amplitude might suggest decreased brain compliance, meaning a static measure of a pressure-volume ratio. Recent studies of canine data have shown that the brain compliance can be described as a frequency-dependent function. The normal canine brain seems to show enhanced ability to absorb the pulsations around the heart rate, quantified as a cardiac pulsation absorbance (CPA), with properties like a notch filter in engineering. This frequency dependence of the function is diminished with development of hydrocephalus in dogs. In this pilot study, the authors sought to determine whether frequency dependence could be observed in humans, and whether the frequency dependence would be any different in epochs with high ICP amplitude compared with epochs of low ICP amplitude.

Methods

Systems analysis was applied to arterial blood pressure (ABP) and ICP waveforms recorded from 10 patients undergoing evaluations of idiopathic NPH to calculate a time-varying transfer function that reveals frequency dependence and CPA, the measure of frequency-dependent compliance previously used in animal experiments. The ICP amplitude was also calculated in the same samples, so that epochs with high (> 4 mm Hg) versus low (≤ 4 mm Hg) amplitude could be compared in CPA and transfer functions.

Results

Transfer function analysis for the more “normal” epochs with low amplitude exhibits a dip or notch in the physiological frequency range of the heart rate, confirming in humans the pulsation absorber phenomenon previously observed in canine studies. Under high amplitude, however, the dip in the transfer function is absent. An inverse relationship between CPA index and ICP amplitude is evident and statistically significant. Thus, elevated ICP amplitude indicates decreased performance of the human pulsation absorber.

Conclusions

The results suggest that the human intracranial system shows frequency dependence as seen in animal experiments. There is an inverse relationship between CPA index and ICP amplitude, indicating that higher amplitudes may occur with a reduced performance of the pulsation absorber. Our findings show that frequency dependence can be observed in humans and imply that reduced frequency-dependent compliance may be responsible for elevated ICP amplitude observed in patients who respond to CSF shunting.

Abbreviations used in this paper:

ABP = arterial blood pressure; CPA = cardiac pulsation absorbance; GEE = generalized estimating equations; ICP = intracranial pressure; ICPa = ICP amplitude; NPH = normal pressure hydrocephalus; VP = ventriculoperitoneal.

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Contributor Notes

Address correspondence to: Joseph R. Madsen, M.D., Department of Neurosurgery, Boston Children's Hospital, Harvard Medical School, Hunnewell 244, 300 Longwood Avenue, Boston, Massachusetts 02115. email: joseph.madsen@childrens.harvard.edu.

Please include this information when citing this paper: published online October 12, 2012; DOI: 10.3171/2012.9.JNS121227.

  • 1

    Adams RD, , Fisher CM, , Hakim S, , Ojemann RG, & Sweet WH: Symptomatic occult hydrocephalus with “normal” cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med 273:117126, 1965

    • Search Google Scholar
    • Export Citation
  • 2

    Bering EA Jr: Circulation of the cerebrospinal fluid. Demonstration of the choroid plexuses as the generator of the force for flow of fluid and ventricular enlargement. J Neurosurg 19:405413, 1962

    • Search Google Scholar
    • Export Citation
  • 3

    Di Rocco C, , Maira G, , Rossi GF, & Vignati A: Cerebrospinal fluid pressure studies in normal pressure hydrocephalus and cerebral atrophy. Eur Neurol 14:119128, 1976

    • Search Google Scholar
    • Export Citation
  • 4

    Di Rocco C, , Pettorossi VE, , Caldarelli M, , Mancinelli R, & Velardi F: Experimental hydrocephalus following mechanical increment of intraventricular pulse pressure. Experientia 33:14701472, 1977

    • Search Google Scholar
    • Export Citation
  • 5

    Eide PK: Assessment of childhood intracranial pressure recordings using a new method of processing intracranial pressure signals. Pediatr Neurosurg 41:122130, 2005

    • Search Google Scholar
    • Export Citation
  • 6

    Eide PK: Comparison of simultaneous continuous intracranial pressure (ICP) signals from ICP sensors placed within the brain parenchyma and the epidural space. Med Eng Phys 30:3440, 2008

    • Search Google Scholar
    • Export Citation
  • 7

    Eide PK: Intracranial pressure parameters in idiopathic normal pressure hydrocephalus patients treated with ventriculoperitoneal shunts. Acta Neurochir (Wien) 148:2129, 2006

    • Search Google Scholar
    • Export Citation
  • 8

    Eide PK: A new method for processing of continuous intracranial pressure signals. Med Eng Phys 28:579587, 2006

  • 9

    Eide PK: Quantitative analysis of continuous intracranial pressure recordings in symptomatic patients with extracranial shunts. J Neurol Neurosurg Psychiatry 74:231237, 2003

    • Search Google Scholar
    • Export Citation
  • 10

    Eide PK, & Brean A: Intracranial pulse pressure amplitude levels determined during preoperative assessment of subjects with possible idiopathic normal pressure hydrocephalus. Acta Neurochir (Wien) 148:11511156, 2006

    • Search Google Scholar
    • Export Citation
  • 11

    Eide PK, , Due-Tønnessen B, , Helseth E, & Lundar T: Differences in quantitative characteristics of intracranial pressure in hydrocephalic children treated surgically or conservatively. Pediatr Neurosurg 36:304313, 2002

    • Search Google Scholar
    • Export Citation
  • 12

    Eide PK, , Egge A, , Due-Tønnessen BJ, & Helseth E: Is intracranial pressure waveform analysis useful in the management of pediatric neurosurgical patients?. Pediatr Neurosurg 43:472481, 2007

    • Search Google Scholar
    • Export Citation
  • 13

    Eide PK, & Sorteberg W: Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 66:8091, 2010

    • Search Google Scholar
    • Export Citation
  • 14

    Foltz EL, & Aine C: Diagnosis of hydrocephalus by CSF pulsewave analysis: a clinical study. Surg Neurol 15:283293, 1981

  • 15

    Foltz EL, , Blanks JP, & Yonemura K: CSF pulsatility in hydrocephalus: respiratory effect on pulse wave slope as an indicator of intracranial compliance. Neurol Res 12:6774, 1990

    • Search Google Scholar
    • Export Citation
  • 16

    Hakim S, & Adams RD: The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 2:307327, 1965

    • Search Google Scholar
    • Export Citation
  • 17

    Hebb AO, & Cusimano MD: Idiopathic normal pressure hydrocephalus: a systematic review of diagnosis and outcome. Neurosurgery 49:11661186, 2001

    • Search Google Scholar
    • Export Citation
  • 18

    Kuchiwaki H, , Misu N, , Kageyama N, , Ishiguri H, & Takada S: Periodic oscillation of intracranial pressure in ventricular dilation: a preliminary report. Neurol Res 9:218224, 1987

    • Search Google Scholar
    • Export Citation
  • 19

    Langfitt TW, , Weinstein JD, & Kassell NF: Cerebral vasomotor paralysis produced by intracranial hypertension. Neurology 15:622641, 1965

  • 20

    Löfgren J, , von Essen C, & Zwetnow NN: The pressure-volume curve of the cerebrospinal fluid space in dogs. Acta Neurol Scand 49:557574, 1973

    • Search Google Scholar
    • Export Citation
  • 21

    Malm J, & Eklund A: Idiopathic normal pressure hydrocephalus. Pract Neurol 6:1427, 2006

  • 22

    Marmarou A, , Shulman K, & LaMorgese J: Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 43:523534, 1975

    • Search Google Scholar
    • Export Citation
  • 23

    Miller JD, , Garibi J, & Pickard JD: Induced changes of cerebrospinal fluid volume. Effects during continuous monitoring of ventricular fluid pressure. Arch Neurol 28:265269, 1973

    • Search Google Scholar
    • Export Citation
  • 24

    O'Connell J: Vascular factor in intracranial pressure and maintenance of cerebro-spinal fluid circulation. Brain 66:204228, 1943

  • 25

    Park EH, , Dombrowski S, , Luciano M, , Zurakowski D, & Madsen JR: Alterations of pulsation absorber characteristics in experimental hydrocephalus. Laboratory investigation. J Neurosurg Pediatr 6:159170, 2010

    • Search Google Scholar
    • Export Citation
  • 26

    Sorteberg A, , Eide PK, & Fremming AD: A prospective study on the clinical effect of surgical treatment of normal pressure hydrocephalus: the value of hydrodynamic evaluation. Br J Neurosurg 18:149157, 2004

    • Search Google Scholar
    • Export Citation
  • 27

    Vittinghoff E, , Glidden DV, , Shiboski SC, & McCulloch CE: Regression Methods in Biostatistics. Linear, Logistic, Survival, and Repeated Measures Models New York, Springer, 2005. 266303

    • Search Google Scholar
    • Export Citation
  • 28

    Zou R, , Park EH, , Kelly EM, , Egnor M, , Wagshul ME, & Madsen JR: Intracranial pressure waves: characterization of a pulsation absorber with notch filter properties using systems analysis: laboratory investigation. Laboratory investigation. J Neurosurg Pediatr 2:8394, 2008

    • Search Google Scholar
    • Export Citation

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