Cardiac-gated intracranial elastance in a swine model of raised intracranial pressure: a novel method to assess intracranial pressure–volume dynamics

View More View Less
  • 1 Department of Neurosurgery, Hadassah-Hebrew University Medical Center, Jerusalem;
  • 2 Department of Biomedical Engineering, Tel Aviv University, Tel Aviv, Israel;
  • 3 Department of Physiopathology and Transplantation, Milan University and Neuro ICU Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, Milan, Italy; and
  • 4 Department of Neurosurgery, New York University Medical Center, New York, New York
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Previous studies have demonstrated the importance of intracranial elastance; however, methodological difficulties have limited widespread clinical use. Measuring elastance may offer potential benefit in helping to identify patients at risk for untoward intracranial pressure (ICP) elevation from small rises in intracranial volume. The authors sought to develop an easily used method that accounts for the changing ICP that occurs over a cardiac cycle and to assess this method in a large-animal model over a broad range of ICPs.

METHODS

The authors used their previously described cardiac-gated intracranial balloon pump and swine model of cerebral edema. In the present experiment they measured elastance at 4 points along the cardiac cycle—early systole, peak systole, mid-diastole, and end diastole—by using rapid balloon inflation to 1 ml over an ICP range of 10–30 mm Hg.

RESULTS

The authors studied 7 swine with increasing cerebral edema. Intracranial elastance rose progressively with increasing ICP. Peak-systolic and end-diastolic elastance demonstrated the most consistent rise in elastance as ICP increased. Cardiac-gated elastance measurements had markedly lower variance within swine compared with non–cardiac-gated measures. The slope of the ICP–elastance curve differed between swine. At ICP between 20 and 25 mm Hg, elastance varied between 8.7 and 15.8 mm Hg/ml, indicating that ICP alone cannot accurately predict intracranial elastance.

CONCLUSIONS

Measuring intracranial elastance in a cardiac-gated manner is feasible and may offer an improved precision of measure. The authors’ preliminary data suggest that because elastance values may vary at similar ICP levels, ICP alone may not necessarily best reflect the state of intracranial volume reserve capacity. Paired ICP–elastance measurements may offer benefit as an adjunct “early warning monitor” alerting to the risk of untoward ICP elevation in brain-injured patients that is induced by small increases in intracranial volume.

ABBREVIATIONS ICP = intracranial pressure; PV = pressure-volume; TBI = traumatic brain injury.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Guy Rosenthal: Hadassah-Hebrew University Medical Center, Kiryat Hadassah, Jerusalem, Israel. rosenthalg@hadassah.org.il.

INCLUDE WHEN CITING Published online June 5, 2020; DOI: 10.3171/2020.3.JNS193262.

Disclosures Prof. Barnea and Dr. Doron are listed as inventors on a patent of the intracranial cardiac-gated balloon pump used in this work. Prof. Barnea is the founder and CEO of Syncath Neuroscience. Drs. Nossek, Rosenthal, and Stocchetti serve as scientific advisors on the medical advisory board for Syncath, Ltd.

  • 1

    Kellie G. An account of the appearance observed in the dissection of two or three individuals presumed to have perished in the storm of the third and whose bodies were discovered in the vicinity of Leith on the morning of the fourth November 1821, with some reflections on the pathology of the brain. Trans Med Chir Soc Edinb. 1824;I:84169.

    • Search Google Scholar
    • Export Citation
  • 2

    Monro A. Observations on the Structure and Function of the Nervous System. Creech & Johnston; 1783.

  • 3

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

    • Search Google Scholar
    • Export Citation
  • 4

    Marmarou A, Shulman K, LaMorgese J. Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg. 1975;43(5):523534.

    • Search Google Scholar
    • Export Citation
  • 5

    Marmarou A, Shulman K, Rosende RM. A nonlinear analysis of the cerebrospinal fluid system and intracranial pressure dynamics. J Neurosurg. 1978;48(3):332344.

    • Search Google Scholar
    • Export Citation
  • 6

    Miller JD, Garibi J, Pickard JD. Induced changes of cerebrospinal fluid volume. Effects during continuous monitoring of ventricular fluid pressure. Arch Neurol. 1973;28(4):265269.

    • Search Google Scholar
    • Export Citation
  • 7

    Miller JD, Garibi J. Intracranial volume/pressure relationships during continuous monitoring of ventricular fluid pressure. In: Brock M, Dietz H, eds. Intracranial Pressure. Springer; 1972:270274.

    • Search Google Scholar
    • Export Citation
  • 8

    Miller JD. Volume and pressure in the craniospinal axis. Clin Neurosurg. 1975;22:76105.

  • 9

    Miller JD, Pickard JD. Intracranial volume pressure studies in patients with head injury. Injury. 1974;5(3):265268.

  • 10

    Hase U, Reulen HJ, Meinig G, Schürmann K. The influence of the decompressive operation on the intracranial pressure and the pressure-volume relation in patients with severe head injuries. Acta Neurochir (Wien). 1978;45(1-2):113.

    • Search Google Scholar
    • Export Citation
  • 11

    Sullivan HG, Miller JD, Griffith RL III, Becker DP. CSF pressure-volume dynamics in neurosurgical patients: a preliminary evaluation in six patients. Surg Neurol. 1978;9(1):4754.

    • Search Google Scholar
    • Export Citation
  • 12

    Sullivan HG, Miller JD, Griffith RL III, Bolous versus steady-state infusion for determination of CSF outflow resistance. Ann Neurol. 1979;5(3):228238.

    • Search Google Scholar
    • Export Citation
  • 13

    Heldt T, Zoerle T, Teichmann D, Stocchetti N. Intracranial pressure and intracranial elastance monitoring in neurocritical care. Annu Rev Biomed Eng. 2019;21:523549.

    • Search Google Scholar
    • Export Citation
  • 14

    Ramirez de Noriega F, Manley GT, Moscovici S, A swine model of intracellular cerebral edema – cerebral physiology and intracranial compliance. J Clin Neurosci. 2018;58:192199.

    • Search Google Scholar
    • Export Citation
  • 15

    Doron O, Or T, Battino L, Cerebral blood flow augmentation using a cardiac-gated intracranial pulsating balloon pump in a swine model of elevated ICP. J Neurosurg. 2020;132(5):16061615.

    • Search Google Scholar
    • Export Citation
  • 16

    Leech P, Miller JD. Intracranial volume–pressure relationships during experimental brain compression in primates. 1. Pressure responses to changes in ventricular volume. J Neurol Neurosurg Psychiatry. 1974;37(10):10931098.

    • Search Google Scholar
    • Export Citation
  • 17

    Stocchetti N, Mattioli C, Mainini P, Clinical use of cerebral elastance and intracranial dynamics measurements. Article in Italian. Minerva Anestesiol. 1993;59(1-2):19.

    • Search Google Scholar
    • Export Citation
  • 18

    Abdullah J, Zamzuri I, Awang S, Preliminary report on Spiegelberg pre and post-operative monitoring of severe head-injured patients who received decompressive craniectomy. Acta Neurochir Suppl. 2005;95:311314.

    • Search Google Scholar
    • Export Citation
  • 19

    Piper I, Spiegelberg A, Whittle I, A comparative study of the Spiegelberg compliance device with a manual volume-injection method: a clinical evaluation in patients with hydrocephalus. Br J Neurosurg. 1999;13(6):581586.

    • Search Google Scholar
    • Export Citation
  • 20

    Yau YH, Piper IR, Contant C, Assessment of different data representations and averaging methods on the Spiegelberg compliance device. Acta Neurochir Suppl. 2005;95:289292.

    • Search Google Scholar
    • Export Citation
  • 21

    Anile C, Portnoy HD, Branch C. Intracranial compliance is time-dependent. Neurosurgery. 1987;20(3):389395.

  • 22

    Bratton SL, Chestnut RM, Ghajar J, Guidelines for the management of severe traumatic brain injury. VIII. Intracranial pressure thresholds. J Neurotrauma. 2007;24(suppl 1):S55S58. Published correction appears in J Neurotrauma. 2008;25(3):276–278.

    • Search Google Scholar
    • Export Citation
  • 23

    Carney N, Totten AM, O’Reilly C, Guidelines for the Management of Severe Traumatic Brain Injury, Fourth Edition. Neurosurgery. 2017;80(1):615.

    • Search Google Scholar
    • Export Citation
  • 24

    Hutchinson PJ, Kolias AG, Timofeev IS, Trial of decompressive craniectomy for traumatic intracranial hypertension. N Engl J Med. 2016;375(12):11191130.

    • Search Google Scholar
    • Export Citation
  • 25

    Lazaridis C, DeSantis SM, Smielewski P, Patient-specific thresholds of intracranial pressure in severe traumatic brain injury. J Neurosurg. 2014;120(4):893900.

    • Search Google Scholar
    • Export Citation
  • 26

    Sheth KN, Stein DM, Aarabi B, Intracranial pressure dose and outcome in traumatic brain injury. Neurocrit Care. 2013;18(1):2632.

  • 27

    Vik A, Nag T, Fredriksli OA, Relationship of “dose” of intracranial hypertension to outcome in severe traumatic brain injury. J Neurosurg. 2008;109(4):678684.

    • Search Google Scholar
    • Export Citation
  • 28

    Chesnut R, Videtta W, Vespa P, Le Roux P. Intracranial pressure monitoring: fundamental considerations and rationale for monitoring. Neurocrit Care. 2014;21(suppl 2):S64S84.

    • Search Google Scholar
    • Export Citation
  • 29

    Chesnut RM. A conceptual approach to managing severe traumatic brain injury in a time of uncertainty. Ann N Y Acad Sci. 2015;1345:99107.

    • Search Google Scholar
    • Export Citation
  • 30

    Di Rocco C, Pettorossi VE, Caldarelli M, Experimental hydrocephalus following mechanical increment of intraventricular pulse pressure. Experientia. 1977;33(11):14701472.

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 467 467 296
Full Text Views 46 46 24
PDF Downloads 36 36 26
EPUB Downloads 0 0 0