Waveform Morphology as a Surrogate for ICP Monitoring: A Comparison Between an Invasive and a Noninvasive Method

Fabiano Moulin de Moraes, Eva Rocha, Felipe Chaves Duarte Barros, Flávio Geraldo Rezende Freitas, Maramelia Miranda, Raul Alberto Valiente, João Brainer Clares de Andrade, Feres Eduardo Aparecido Chaddad Neto, Gisele Sampaio Silva, Fabiano Moulin de Moraes, Eva Rocha, Felipe Chaves Duarte Barros, Flávio Geraldo Rezende Freitas, Maramelia Miranda, Raul Alberto Valiente, João Brainer Clares de Andrade, Feres Eduardo Aparecido Chaddad Neto, Gisele Sampaio Silva

Abstract

Background: Although the placement of an intraventricular catheter remains the gold standard technique for measuring intracranial pressure (ICP), the method has several limitations. Therefore, noninvasive alternatives to ICP (ICPni) measurement are of great interest. The main objective of this study was to compare the correlation and agreement of wave morphology between ICP (standard intraventricular ICP monitoring) and a new ICPni monitor in patients admitted with stroke. The second objective was to estimate the discrimination of the noninvasive method to detect intracranial hypertension.

Methods: We prospectively collected data of adults admitted to an intensive care unit with subarachnoid hemorrhage, intracerebral hemorrhage, or ischemic stroke in whom an invasive ICP monitor was placed. Measurements were simultaneously collected from two parameters [time-to-peak (TTP) and the ratio regarding the second and first peak of the ICP wave (P2/P1 ratio)] of ICP and ICPni wave morphology monitors (Brain4care). Intracranial hypertension was defined as an invasively measured sustained ICP > 20 mm Hg for at least 5 min.

Results: We studied 18 patients (subarachnoid hemorrhage = 14; intracerebral hemorrhage = 3; ischemic stroke = 1) on 60 occasions with a median age of 52 ± 14.3 years. A total of 197,400 waves (2495 min) from both ICP (standard ICP monitoring) and the ICPni monitor were sliced into 1-min-long segments, and we determined TTP and the P2/P1 ratio from the mean pulse. The median invasively measured ICP was 13 (9.8-16.2) mm Hg, and intracranial hypertension was present on 18 occasions (30%). The correlation and agreement between invasive and noninvasive methods for wave morphology were strong for the P2/P1 ratio and moderate for TTP using categoric (κ agreement 88.1% and 71.3%, respectively) and continuous (intraclass correlation coefficient 0.831 and 0.584, respectively) measures. There was a moderate but significant correlation with the mean ICP value (P2/P1 ratio r = 0.427; TTP r = 0.353; p < 0.001 for all) between noninvasive and invasive techniques. The areas under the curve to estimate intracranial hypertension were 0.786 [95% confidence interval (CI) 0.72-0.93] for the P2/P1 ratio and 0.694 (95% CI 0.60-0.74) for TTP.

Conclusions: The new ICPni wave morphology monitor showed a good agreement with the standard invasive method and an acceptable discriminatory power to detect intracranial hypertension. Clinical trial registration Trial registration: NCT05121155.

Keywords: Brain trauma; Intracranial pressure wave morphology; Neurointensive care unit; Noninvasive intracranial pressure monitor; Stroke.

Conflict of interest statement

None.

© 2022. Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society.

Figures

Fig. 1
Fig. 1
Demonstration of Brain4care technology: position of the sensor and the elastic band on the patient’s head and the monitor showing the intracranial pressure waves
Fig. 2
Fig. 2
Inclusion and exclusion criteria for patients in the study. B4C Brain4care monitor, BD brain dead, EVD external ventricular drainage, ICPi invasive intracranial pressure monitor
Fig. 3
Fig. 3
Bland–Altman plots for mean P2/P1 ratio (a) and mean TTP (b) between ICPi and B4c. B4C Brain4care monitor, ICPi invasive intracranial pressure monitor, TTP time-to-peak
Fig. 4
Fig. 4
Distribution of B4c values (mean P2/P1 ratio and TTP) concerning IH. B4C Brain4care monitor, ICPi invasive intracranial pressure monitor, IH intracranial hypertension, TTP time-to-peak
Fig. 5
Fig. 5
ROC curves of the morphological variables of B4c referring to mean ICP greater than 20 mm Hg. a Curve referring to P2/P1 ratio B4c (AUC: 0.786). b Curve referring to TTP B4c (AUC:0.694). AUC area under the curve, B4c Brain4care monitor, ICP intracranial pressure, ROC receiver operating characteristic, TTP time-to-peak

References

    1. Fried HI, Nathan BR, Rowe AS, Zabramski JM, Andaluz N, Bhimraj A, et al. The insertion and management of external ventricular drains: an evidence-based consensus statement: a statement for healthcare professionals from the neurocritical care society. Neurocrit Care. 2016;24(1):61–81. doi: 10.1007/s12028-015-0224-8.
    1. Srinivasan VM, O’Neill BR, Jho D, Whiting DM, Oh MY. The history of external ventricular drainage: historical vignette. J Neurosurg. 2014;120(1):228–236. doi: 10.3171/2013.6.JNS121577.
    1. Helbok R, Olson DW, Le Roux P, Vespa P, Menon DK, Vespa P, et al. Intracranial pressure and cerebral perfusion pressure monitoring in non-TBI patients: special considerations. Neurocrit Care. 2014;21(2):85–94. doi: 10.1007/s12028-014-0040-6.
    1. 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(3):473–491. doi: 10.1007/s12028-016-0258-6.
    1. Zacchetti L, Magnoni S, Di Corte F, Zanier ER, Stocchetti N. Accuracy of intracranial pressure monitoring: systematic review and meta-analysis. Crit Care. 2015;19(1):1–8. doi: 10.1186/s13054-015-1137-9.
    1. de Moraes FM, Silva GS. Noninvasive intracranial pressure monitoring methods: a critical review. Arq Neuropsiquiatr. 2021;79(5):437–446. doi: 10.1590/0004-282x-anp-2020-0300.
    1. Vinciguerra L, Bösel J. Noninvasive neuromonitoring: current utility in subarachnoid hemorrhage, traumatic brain injury, and stroke. Neurocrit Care. 2017;27(1):122–140. doi: 10.1007/s12028-016-0361-8.
    1. Harary M, Dolmans RGF, Gormley WB. Intracranial pressure monitoring—review and avenues for development. Sensors (Switzerland) 2018;18(2):3–7. doi: 10.3390/s18020465.
    1. Sonig A, Jumah F, Raju B, Patel NV, Gupta G, Nanda A. The historical evolution of intracranial pressure monitoring. World Neurosurg. 2020;138:491–497. doi: 10.1016/j.wneu.2020.03.028.
    1. Pitlyk PJ, Piantanida TPPD. Noninvasive intracranial pressure monitoring. Neurosurgery. 1985;17:581–584. doi: 10.1227/00006123-198510000-00008.
    1. Xy LW. Deformation of skull bone as intracranial pressure changing. Afr J Biotechnol. 2009;8:745–750.
    1. Mascarenhas S, Vilela GHF, Carlotti C, Damiano LEG, Seluque W, Colli B, et al. The new ICP minimally invasive method shows that the monro-kellie doctrine is not valid. Acta Neurochir Suppl. 2012;114:117–120. doi: 10.1007/978-3-7091-0956-4_21.
    1. Mascarenhas SVG. Noninvasive intracranian pressure system. United States; Patent No. WO/2013/041973., 2013.
    1. Fan JY, Kirkness C, Vicini P, Burr RMP. Intracranial pressure waveform morphology and intracranial adaptive capacity. Am J Crit Care. 2008;6:545–556. doi: 10.4037/ajcc2008.17.6.545.
    1. Cabella B, Vilela GHF, Mascarenhas S, Czosnyka M, Smielewski P, Dias C, et al. Validation of a new noninvasive intracranial pressure monitoring method by direct comparison with an invasive technique. Acta Neurochir Suppl. 2016;122:93–96. doi: 10.1007/978-3-319-22533-3_18.
    1. Kasprowicz M, Lalou DA, Czosnyka M, Garnett M, Czosnyka Z. Intracranial pressure, its components and cerebrospinal fluid pressure–volume compensation. Acta Neurol Scand. 2016;134(3):168–180. doi: 10.1111/ane.12541.
    1. Gomes I, Shibaki J, Padua B, Silva F, Gonçalves T, Spavieri-Junior DL, Frigieri G, Mascarenhas SDC. Comparison of waveforms between noninvasive and invasive monitoring of intracranial pressure. Acta Neurochir Suppl. 2021;131:135–140. doi: 10.1007/978-3-030-59436-7_28.
    1. Brasil S, Taccone FS, Wayhs Y, Tomazini BM, Annoni F, Fonseca S, et al. brain sciences cerebral hemodynamics and intracranial compliance impairment in critically Ill COVID-19 patients: a pilot study. Brain Sciences. 2021;11:874. doi: 10.3390/brainsci11070874.
    1. Frigieri G, Andrade RAP, Wang CC, Spavieri D, Lopes L, Brunelli R, et al. Analysis of a minimally invasive intracranial pressure signals during infusion at the subarachnoid spinal space of pigs. Acta Neurochir Suppl. 2018;126:75–77. doi: 10.1007/978-3-319-65798-1_16.
    1. 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. 2008;30(1):34–40. doi: 10.1016/j.medengphy.2007.01.005.
    1. Nucci CG, De Bonis P, Mangiola A, Santini P, Sciandrone M, Risi A, et al. Intracranial pressure wave morphological classification: automated analysis and clinical validation. Acta Neurochir (Wien) 2016;158(3):581–588. doi: 10.1007/s00701-015-2672-5.
    1. Teichmann D, Lynch JC, Heldt T. Distortion of the intracranial pressure waveform by extraventricular drainage system. IEEE Trans Biomed Eng. 2021;68(5):1646–1657. doi: 10.1109/TBME.2020.3036283.
    1. Portella G, Cormio M, Citerio G, Contant C, Kiening K, Enblad P, et al. Continuous cerebral compliance monitoring in severe head injury: Its relationship with intracranial pressure and cerebral perfusion pressure. Acta Neurochir (Wien) 2005;147(7):707–713. doi: 10.1007/s00701-005-0537-z.
    1. Carrera E, Kim DJ, Castellani G, Zweifel C, Czosnyka Z, Kasparowicz M, et al. What shapes pulse amplitude of intracranial pressure? J Neurotrauma. 2010;27(2):317–324. doi: 10.1089/neu.2009.0951.
    1. Eide PK. The correlation between pulsatile intracranial pressure and indices of intracranial pressure–volume reserve capacity: results from ventricular infusion testing. J Neurosurg. 2016;125(6):1493–1503. doi: 10.3171/2015.11.JNS151529.
    1. Avezaat CJJ, Van Eijndhoven JHM, Wyper DJ. Cerebrospinal fluid pulse pressure and intracranial volume–pressure relationships. J Neurol Neurosurg Psychiatry. 1979;42(8):687–700. doi: 10.1136/jnnp.42.8.687.
    1. Cardoso ER, Rowan JO, Galbraith S. Analysis of the cerebrospinal fluid pulse wave in intracranial pressure. J Neurosurg. 1983;59(5):817–821. doi: 10.3171/jns.1983.59.5.0817.
    1. Kazimierska A, Kasprowicz M, Czosnyka M, Placek MM, Baledent O, Smielewski P, et al. Compliance of the cerebrospinal space: comparison of three methods. Acta Neurochir (Wien) 2021;163:1979–1989. doi: 10.1007/s00701-021-04834-y.
    1. Eide PK, Bentsen G, Sorteberg AG, Marthinsen PB, Stubhaug A, Sorteberg W. A randomized and blinded single-center trial comparing the effect of intracranial pressure and intracranial pressure wave amplitude-guided intensive care management on early clinical state and 12-month outcome in patients with aneurysmal subarachnoid hemo. Neurosurgery. 2011;69(5):1105–1115. doi: 10.1227/NEU.0b013e318227e0e1.
    1. Bellner J, Romner B, Reinstrup P, Kristiansson K-A, Ryding E, Brandt L. Transcranial Doppler sonography pulsatility index (PI) reflects intracranial pressure (ICP) Surg Neurol. 2004;62:45–51. doi: 10.1016/j.surneu.2003.12.007.
    1. De Riva N, Budohoski KP, Smielewski P, Kasprowicz M, Zweifel C, Steiner LA, et al. Transcranial Doppler pulsatility index: What it is and what it isn’t. Neurocrit Care. 2012;17(1):58–66. doi: 10.1007/s12028-012-9672-6.
    1. Behrens A, Lenfeldt N, Ambarki K, Malm J, Eklund A, Koskinen LO. Transcranial Doppler pulsatility index: Not an accurate method to assess intracranial pressure. Neurosurgery. 2010;66(6):1050–1057. doi: 10.1227/01.NEU.0000369519.35932.F2.
    1. Zweifel C, Czosnyka M, Carrera E, Deriva N, Pickard JD, Smielewski P. Reliability of the blood flow velocity pulsatility index for assessment of intracranial and cerebral perfusion pressures in head-injured patients. Neurosurgery. 2012;71(4):853–861. doi: 10.1227/NEU.0b013e3182675b42.
    1. Robba C, Robba C, Pozzebon S, Moro B, Vincent JL, Creteur J, et al. Multimodal non-invasive assessment of intracranial hypertension: an observational study. Crit Care. 2020;24(1):1–10. doi: 10.1186/s13054-020-03105-z.
    1. Kim DJ, Czosnyka Z, Kasprowicz M, Smieleweski P, Baledent O, Guerguerian AM, et al. Continuous monitoring of the Monro–Kellie doctrine: Is it possible? J Neurotrauma. 2012;29(7):1354–1363. doi: 10.1089/neu.2011.2018.
    1. Hall A, O’Kane R. The best marker for guiding the clinical management of patients with raised intracranial pressure—the RAP index or the mean pulse amplitude? Acta Neurochir (Wien) 2016;158(10):1997–2009. doi: 10.1007/s00701-016-2932-z.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever