The use of noninvasive measurements of intracranial pressure in patients with traumatic brain injury: a narrative review

Faria, Bárbara Caroline Dias; Sacramento, Luiz Gustavo Guimarães; Queiroz, André Vitor Rocha; Leite, Fernanda de Andrade Dias; Oliveira, Henrique Lacerda Lage Lopes de; Kimura, Thais Yuki; Faleiro, Rodrigo Moreira

doi:10.1055/s-0043-1764411

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Arquivos de Neuro-Psiquiatria

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View and Review • Arq. Neuro-Psiquiatr. 81 (6) • June 2023 • https://doi.org/10.1055/s-0043-1764411 copy

The use of noninvasive measurements of intracranial pressure in patients with traumatic brain injury: a narrative review

Avaliação não invasiva da pressão intracraniana em pacientes com traumatismo cranioencefálico: uma revisão narrativa

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Background

The most frequent cause of death in neurosurgical patients is due to the increase in intracranial pressure (ICP); consequently, adequate monitoring of this parameter is extremely important.

Objectives

In this study, we aimed to analyze the accuracy of noninvasive measurement methods for intracranial hypertension (IH) in patients with traumatic brain injury (TBI).

Methods

The data were obtained from the PubMed database, using the following terms: intracranial pressure, noninvasive, monitoring, assessment, and measurement. The selected articles date from 1980 to 2021, all of which were observational studies or clinical trials, in English and specifying ICP measurement in TBI. At the end of the selection, 21 articles were included in this review.

Results

The optic nerve sheath diameter (ONSD), pupillometry, transcranial doppler (TCD), multimodal combination, brain compliance using ICP waveform (ICPW), HeadSense, and Visual flash evoked pressure (FVEP) were analyzed. Pupillometry was not found to correlate with ICP, while HeadSense monitor and the FVEP method appear to have good correlation, but sensitivity and specificity data are not available. The ONSD and TCD methods showed good-to-moderate accuracy on invasive ICP values and potential to detect IH in most studies. Furthermore, multimodal combination may reduce the error possibility related to each technique. Finally, ICPW showed good accuracy to ICP values, but this analysis included TBI and non-TBI patients in the same sample.

Conclusions

Noninvasive ICP monitoring methods may be used in the near future to guide TBI patients’ management.

Keywords
Brain Injuries, Traumatic; Intracranial Pressure; Intracranial Hypertension

Author	Study design	Sample of TBI patients	Noninvasive ICP monitoring method	Summary of findings
Raffiz et al., 2017¹1 Raffi z M, Abdullah JM. Optic nerve sheath diameter measurement: a means of detecting raised ICP in adult traumatic and non-traumatic neurosurgical patients. Am J Emerg Med 2017;35(01): 150-153	Prospective observational study	41	ONSD	– ONSD values and ICP: r = 0.820; p = 0.01. – Including TBI and non-TBI groups: AUC of 0.964 (CI 95% 0.921–1.0) – Best cutoff point: 5.205 mm with 95.8% sensitivity and 80.4% specificity – Sensitivity and specificity of 5.47 mm in TBI group were higher than in non-TBI group (94.4% vs 83.3% and 95.2% vs 93.3%)
Singer et al., 2021²2 Singer KE, Wallen TE, Jalbert T, et al. Efficacy of Noninvasive Technologies in Triaging Traumatic Brain Injury and Correlating With Intracranial Pressure: A Prospective Study. J Surg Res 2021; 262:27-37	Prospective observational study	135P	ONSD Pupillometry TCD	ONSD – ONSD differs significantly bilaterally between mild TBI, non-TBI, and severe TBI on postinjury days 2 and 3 – ONSD was not found to correlate with ICP. Pupillometry – Significant bilaterally percent changes in pupil diameters (p < 0.01), constriction velocity (p < 0.01) and dilatation velocity (p < 0.01) on postinjury days 1 and 2 – Values obtained from dynamic changes of pupil reliably differentiated severe TBI from mild brain injuries on postinjury days 2 and 3. – Pupillometry values and ICP: p > 0.05 TCD – Middle cerebral artery (MCA) peak systolic velocity, MCA flow velocity and common carotid artery flow velocity showed a statistically significant correlation with ICP in severe TBI patients
Maissan et al., 2015¹²12 Maissan IM, Dirven PJ, Haitsma IK, Hoeks SE, Gommers D, Stolker RJ. Ultrasonographic measured optic nerve sheath diameter as an accurate and quick monitor for changes in intracranial pressure. J Neurosurg 2015;123(03):743-747	Prospective observational study	18	ONSD	– ONSD values and ICP: R2 = 0.80 – Cutoff point ≥ 5.00 mm: sensitivity = 94% and specificity = 98% – AUC 0.99 (0.97–1.00) was found for detection of IH
Strumwasser et al., 2011¹³13 Strumwasser A, Kwan RO, Yeung L, et al. Sonographic optic nerve sheath diameter as an estimate of intracranial pressure in adult trauma. J Surg Res 2011;170(02):265-271	Prospective observational study	10	ONSD	ONSD values and ICP in unilateral (R2 = 0.45, p < 0.01) and bilateral (R2 = 0.21, p = 0.01) lesions. AUC = 0.36; p = 0.01 Sensitivity was 36%, specificity 38%, PPV 40%, the NPV 16% and the accuracy for estimating ICP with the ONSD was 37%.
Rajajee et al., 2011⁴4 Rajajee V, Vanaman M, Fletcher JJ, Jacobs TL. Optic nerve ultra-sound for the detection of raised intracranial pressure. Neurocrit Care 2011;15(03):506-515	Prospective observational study	65	ONSD	– Optimal cutoff point of 4.8 mm: sensitivity = 96% (91–99%) and specificity = 94% (92–96%). – AUC = 0.98 (CI 5 A% 0.96–0.99; p < 0.96–0.99; p < 0.0001 for AUC = 0.5)
Soldatos et al., 2008⁹9 Soldatos T, Karakitsos D, Chatzimichail K, Papathanasiou M, Gouliamos A, Karabinis A. Optic nerve sonography in the diagnostic evaluation of adult brain injury. Crit Care 2008;12(03):R67	Prospective observational study	76	ONSD	ONSD and ICPi values: r = 0.68; p = 0.002 Best cutoff point: 5.7 mm – sensitivity = 74,1% and specificity = 100% ONSD and estimated ICP (eICP): o Severe brain injury: 6.1 ± 0.7 mm and 26.2 ± 8.7 mmHg, respectively; p < 0.0001 o Moderate brain injury: 4, 2 ± 1.2 mm and 12.0 ± 3.6 mmHg o Control patients: 3.6 ± 0.6 mm and 10.3 ± 3.1 mmHg – Strong correlation between the values of ONSD, eICP (r = 0.80, p < 0.0001) and the neuroimaging scale (r = 0.82, p < 0.001)
Stevens et al., 2019¹⁰10 Stevens AR, Su Z, Toman E, Belli A, Davies D. Optical pupillometry in traumatic brain injury: neurological pupil index and its relationship with intracranial pressure through significant event analysis. Brain Inj 2019;33(08):1032-1038	Prospective observational study	41	Pupillometry	– Pupillometry and ICP: OR 3.36; (95% CI 0.93–13.53; p = 0.07) – Decrease in the pupil reactivity may indicate a raised ICP
Cardim et al., 2020¹⁶16 Cardim D, Robba C, Czosnyka M, et al. Noninvasive Intracranial Pressure Estimation With Transcranial Doppler: A Prospective Observational Study. J Neurosurg Anesthesiol 2020;32(04): 349-353	Prospective observational study	100	TCD	ICPtcd and IPCi: r = - 0.17; p = 0.097
Rasulo et al., 2017¹⁵15 Moraes FM, Silva GS. Noninvasive intracranial pressure monitoring methods: a critical review. Arq Neuropsiquiatr 2021;79(05): 437-446[Accessed 20 September 2022], pp. 437-446. Wu J, He W, Chen W, Zhu L. Research on simulation and experiment of noninvasive intracranial pressure monitoring based on acoustoelasticity effects. Med Devices (Auckl). 2013;6:123-131	Prospective observational study	20	TCD	– AUC of 0.96 (0.898–1.00), with an estimated best threshold at ICPi of 24.8 mmHg (corresponding a sensitivity of 100% and specificity of 91.2% of the ICPtcd detection of IH)
Robba et al., 2017⁶6 Robba C, Cardim D, Tajsic T, et al. Ultrasound non-invasive measurement of intracranial pressure in neurointensive care: A prospective observational study. PLoS Med 2017;14(07): e1002356	Prospective observational study	41	ONSD TCD	ONSD – ONSD and ICP: r = 0.76; p < 0.05 – AUC of 0.91 (0.88–0.95) to detect cases with IH TCD – Straight sinus FVsv and ICP: r = 0.72; p < 0.05 – Combined ONSD and FVsv: r = 0.78; AUC for prediction of ICP 20 mm Hg was 0.93
Cardim et al., 2016¹⁷17 Cardim D, Robba C, Donnelly J, et al. Prospective Study on Noninvasive Assessment of Intracranial Pressure in Traumatic Brain-Injured Patients: Comparison of Four Methods. J Neurotrauma 2016;33(08):792-802	Prospective observational study	40	TCD	− ICPtcd pulsatility index: o The best correlation with iICP, including spontaneous changes in ICP > 7 mmHg (R = 0.61) o The best efficacy for ICP dynamics monitoring
Schmidt et al., 2005⁷7 Schmidt B, Bocklisch SF, Pässler M, Czosnyka M, Schwarze JJ, Klingelhöfer J. Fuzzy pattern classification of hemodynamic data can be used to determine noninvasive intracranial pressure. Acta Neurochir Suppl (Wien) 2005;95:345-349	Prospective observational study	103	TCD	− FV and ABP comparative parameters could infer the ICP with a median absolute difference of 5.7 mmHg when compared to the invasive method.
Ragauskas et al., 20053	Prospective observational study	57	TCD	− The difference in the ICP when comparing the 2 methods was 0.939 mmHg, suggesting the effectiveness of the noninvasive method.
Schmidt et al., 2003⁸8 Schmidt B, Czosnyka M, Raabe A, et al. Adaptive noninvasive assessment of intracranial pressure and cerebral autoregulation. Stroke 2003;34(01):84-89	Prospective observational study	145	TCD	– Mx and nMx: r = 0.90; p < 0.001. – PRx and nPRx: r = 0.62; p < 0.001. – The sensitivity of nMx to estimate Mx was 0.92, the specificity of Mx was 0.79 and the fuzzy values were 0.97 and 0.92. – The sensitivity of nPRx to estimate PRx was 0.61 and its specificity was 0.67. – ABP and FV signals cannot be evaluated alone to estimate nICP.
Czosnyka et al., 1998¹⁸18 Czosnyka M, Matta BF, Smielewski P, Kirkpatrick PJ, Pickard JD. Cerebral perfusion pressure in head-injured patients: a noninva-sive assessment using transcranial Doppler ultrasonography. J Neurosurg 1998;88(05):802-808	Prospective observational study	96	TCD	– PPV of 94% for the detection of a low CPP (60 mmHg), with r = 0.73 – Estimation error of less than 10 mmHg in 71% of the cases.
Mursch et al., 1995¹⁹19 Mursch K, Vogelsang JP, Zimmerer B, Ludwig HC, Behnke J, Markakis E. Bedside measurement of the third ventricle’s diameter during episodes of arising intracranial pressure after head trauma. Using transcranial real-time sonography for a non-invasive examination of intracranial compensation mechanisms. Acta Neurochir (Wien) 1995;1371-2, discussion 23-2419-23	Prospective observational study	28	TCD	– Reductions in diameter were observed: 0.3 to 1.1 mm when there was an increase in ICP. – The relationship between this drop and ICP was not specifically analyzed
Klingelhöfer et al., 1987²⁰20 Klingelhöfer J, Conrad B, Benecke R, Sander D. Intracranial flow patterns at increasing intracranial pressure. Klin Wochenschr 1987;65(12):542-545	Prospective observational study	5	TCD	– Changes in the ICP significantly influenced flow patterns – TCD is a useful noninvasive method for gathering information regarding the development of ICP. – The study did not correlate in detail changes in flow patterns and ICP.
Herklots et al., 2017²¹21 Herklots MW, Moudrous W, Oldenbeuving A, et al. Prospective Evaluation of Noninvasive HeadSense Intracranial Pressure Monitor in Traumatic Brain Injury Patients Undergoing Invasive Intracranial Pressure Monitoring. World Neurosurg 2017; 106:557-562	Prospective observational study	14	HeadSense monitor	– HeadSense and ICPi: r = 0.604; p < 0.001 – Sensitivity and specificity data were not presented in the study
Zhao et al., 2005¹¹11 Zhao YL, Zhou JY, Zhu GH. Clinical experience with the noninvasive ICP monitoring system. Acta Neurochir Suppl (Wien) 2005; 95:351-355	Prospective observational study	16	FVEP	– FVEP and ICP: r = 0.97 – No significant difference between the results from noninvasive and ICPi examinations – Sensibility and specificity data were not analyzed in this study
Brasil et al., 2021²⁶26 Brasil S, Solla DJF, Nogueira RC, Teixeira MJ, Malbouisson LMS, Paiva WDS. A Novel Noninvasive Technique for Intracranial Pressure Waveform Monitoring in Critical Care. J Pers Med 2021;11(12):1302	Prospective observational study	21	Brain compliance using ICPW (B4C monitor)	– B4C sensor measurements and ICP: P2/P1 ratio (r = 0.72) and TTP (r = 0.85) – The B4C P2/P1 ratio threshold of ≥ 1.1 resulted in AUC 0.77 (0.62–0.92), p < 0.001, sensitivity 0.88, specificity 0.60) to detect IH
Robba et al., 2020¹⁴14 Robba C, Pozzebon S, Moro B, Vincent JL, Creteur J, Taccone FS. Multimodal non-invasive assessment of intracranial hypertension: an observational study. Crit Care 2020;24(01):379	Prospective observational study	30	ONSD PI eICP using TCD NPI using pupillometry	ONSD – AUC of 0.78 (0.62–0.95) to detect IH – Cutoff point of ONSD > 5.3 mm: sensitivity = 67% and specificity = 73% PI – AUC of 0.79 (0.63–0.96) to detect IH – Cutoff point of PI > 1.10: sensitivity = 61% and specificity = 80% eICP using TCD – AUC of 0.83 (CI 0.69–0.98) to detect IH – Cutoff point was eICP > 20 mmHg: sensitivity = 67% and specificity = 87%. NPI – AUC was 0.61 (95% CI 0.49-0.83) to detect IH – Cut-off point of NPI < 4.0: sensitivity = 61% and specificity = 73% COMBINED METHODS – All four methods: AUC 0.91 (0.80–1.00) to detect IH – ONSD with eICP using TCD: AUC 0.92 (0.81–1.00)

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[1] Address for correspondence Bárbara Caroline Dias Faria (email: barbaradiascf@gmail.com).