Noninvasive methods to monitor intracranial pressure : Current Opinion in Neurology

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NEURO-OPHTHALMOLOGY: Edited by Valérie Biousse

Noninvasive methods to monitor intracranial pressure

Dattilo, Michael

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Current Opinion in Neurology 36(1):p 1-9, February 2023. | DOI: 10.1097/WCO.0000000000001126
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Abstract

INTRODUCTION

Intracranial pressure (ICP) is determined by the production rate and outflow facility of cerebrospinal fluid (CSF) [1–4]; decreased outflow or increased production leads to elevated ICP and increased outflow or decreased production leads to decreased ICP. Since alterations in ICP are implicated in the pathogenesis of a number of life-threatening and vision-threatening conditions, such as traumatic brain injury (TBI) [5–8], certain forms of meningitis [9,10], large hemispheric ischemic strokes [11,12], subdural/epidural/intracerebral hemorrhages [13,14], and idiopathic intracranial hypertension (IIH) [15–19], measurement of ICP is necessary and common [20]. However, all current methods used clinically to measure ICP are invasive and require direct CSF access [21]. Although lumbar puncture is the least invasive procedure to measure ICP, it still carries the risk of significant side effects, such as site pain, low-tension headaches, chronic CSF leaks requiring further intervention, infections, neurologic dysfunction, and brainstem herniation [21–27]. In addition, lumbar puncture is contraindicated in certain conditions [28,29], including the presence of intracranial space-occupying lesions, Arnold-Chiari malformation, coagulopathies, and skin infections at the puncture site, making ICP determination more challenging in these cases.

Accordingly, there is a large body of literature proposing a number of noninvasive modalities to measure ICP [21,30–38] to complement and, in some cases, supplant the use of invasive measurement of ICP. The development of accurate, reproducible, objective, and portable noninvasive modalities to measure and monitor ICP has the potential to dramatically change the management of certain diseases, such as low-tension glaucoma, IIH, and acute TBI. 

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NONINVASIVE METHODS TO MEASURE INTRACRANIAL PRESSURE

There are two main categories of noninvasive methods to measure ICP, those that rely on changes in ocular structures, such as changes in optic nerve sheath diameter, retinal venous pulsations, and choroidal thickness; and those that utilize changes in nonocular structures, such as otoacoustic emissions, tympanic membrane displacement (TMD), changes in skull compliance, and transcranial Doppler ultrasound.

METHODS BASED ON CHANGES IN NONOCULAR STRUCTURES

Otoacoustic emissions

Distortion product otoacoustic emissions (DPOAEs), low-intensity sounds generated from the cochlea in response to two tones of specific frequency [39], were initially developed as a test of auditory function [40]. However, DPOAEs have been proposed as a noninvasive method to assess ICP based upon changes in sound transmission due to ICP-related changes in pressure on the stapes [41,42].

In a recent study, Loiselle et al.[42], reported that changes in DPOAEs were linearly correlated with ICP above 3 mmHg. However, ICP was not directly assessed; the correlation between ICP and changes in DPOAEs was based on adapted data from Lindén et al.[43] and interpolated with the authors’ DPOAE phase shift data. In addition, due to ‘subject specific offset,’ DPOAE data had to be normalized for each patient, suggesting a prominent component of interindividual variability. Indeed, interindividual variability is a common limitation cited in publications regarding DPOAE and is likely responsible for the widely varying reported correlations between ICP and DPOAEs [44–46].

Tympanic membrane displacement

Similar to otoacoustic emissions, TMD attempts to leverage changes in auricular structures as a biomarker for ICP. TMD during reflex or induced contraction of the stapes, as detected by a transducer placed in the outer ear, is an indirect measure of perilymphatic pressure, which is influenced by ICP [35,47,48].

Although several studies have shown a significant relationship between evoked TMD and invasively obtained ICP [35,48–50], several other studies noted high intersubject variability in the TMD measurements, questioning the clinical utility of TMD to measure ICP [35,49,51–53]. However, a 2018 study by Sharif et al.[52] suggested that some of the variability in TMD measurements may be related to an increased vascular pulse amplitude; a large pulse amplitude was associated with increased variability in evoked TMD. Therefore, accounting for the pulse amplitude may improve the reliability of the evoked TMD measurements. Although a ‘corrected’ evoked TMD may be a reliable indicator of ICP status, further studies are necessary to determine if a ‘corrected’ evoked TMD better correlates with invasively obtained ICP measurements than uncorrected evoked TMD. Currently, TMD is not widely used clinically as a noninvasive method to detect or monitor ICP due to large intersubject variability and prior reports of a variable correlation with invasively obtained ICP [48,51,52,54].

Neuroimaging (MRI and computerized tomography)

Radiographic findings, such as a dilated and expanded partially empty/empty sella turcica, a dilated perioptic CSF space, increased vertical tortuosity of the optic nerves, and cerebellar tonsillar descent, are commonly seen in patients with increased ICP [55,56,57▪,58]. However, some of these findings are also relatively common in the general population [59]; a partially empty sella turcica has been reported in up to 33% of MRI scans performed in the general population [60▪]. In addition to radiographic findings of increased ICP being present in the general population, another potential limitation of using radiographic findings as an indicator of ICP is the persistence of some of these findings long after normalization of ICP [55], suggesting that MRI findings may not be an ideal method to detect elevated ICP or to assess a response to treatment.

However, a recent publication using displacement encoding with stimulated echoes (DENSE) MRI, an MRI technique highly sensitive to brain motion, has suggested that DENSE MRI analysis of pontine displacement may be better able to qualitatively assess ICP than standard MRI scans/sequences and it may even be able to provide a quantitative assessment of ICP [61]. Patients with elevated ICP were found to have a smaller pontine displacement prior to lumbar puncture than following lumbar puncture [61]. In addition, postlumbar puncture patients had statistically similar pontine displacements to control patients [61]. Therefore, the use of specialized sequencing protocols [61,62], such as the DENSE MRI protocol, may increase the utility of neuroimaging studies in ICP assessment. However, due to cost and access to scanners, it is unlikely that neuroimaging studies will be commonly used clinically to measure ICP, and it would be impractical to use neuroimaging studies for serial ICP assessments.

Near-infrared spectroscopy

Near-infrared spectroscopy (NIRS), which uses near-infrared light (700–1000 nm) to penetrate superficial layers of the head, has been developed as a clinical tool to monitor brain oxygenation [63]. Since brain oxygenation demand changes with changes in brain metabolic state, and changes in ICP alter brain metabolism and cerebral perfusion pressure [64,65], it is believed that brain oxygenation changes can be used as a biomarker for ICP. On the contrary, multiple studies have produced either conflicting results or have failed to show a correlation between invasively obtained ICP and changes in NIRS [66,67]. Therefore, it is unlikely that NIRS will be a clinically useful tool to assess or monitor alterations in ICP.

Electroencephalogram

Similar to NIRS, which detects brain oxygenation changes due to altered brain metabolism, electroencephalography may be able to detect changes in neuronal activity related to changes in brain metabolism. Since brain metabolism is altered by changes in ICP [64], electroencephalography may potentially be useful to measure or monitor ICP [68,69]. Significantly, in a small cohort of patients with TBI or subarachnoid hemorrhage, electroencephalogram (EEG) changes preceded ICP changes, suggesting that EEG changes can be used to predict ICP changes [70]. From a practical perspective, this information could be useful therapeutically, allowing a treatment window for providers to intervene prior to the development of ICP changes. However, it is not clear from the available data if there is a large enough delay between EEG changes and ICP changes to significantly alter patient management [70]. Although EEG changes, such as generalized rhythmic delta activity and attenuation of fast activity, have been reported to correlate with changes in ICP [71], EEG changes have not been shown to provide a quantitative assessment of ICP, limiting its clinical utility as a noninvasive biomarker to monitor ICP.

Skull elasticity

Although it is generally assumed that deformations in the skull due to changes in ICP do not occur after fontanelle closure, animal studies have shown that minute deformations in the skull occur due to changes in ICP and that these deformations positively correlate with changes in ICP [72]. Recently, this technology has been applied to humans, where very small variations in skull volume due to ICP pulsations were detected by a noninvasive electric resistance extensometer placed on the scalp at the temporoparietal transition [73–75,76▪▪,77]. The skull deformations are transformed into ICP waveforms in real time, which have been shown to correlate well with invasively obtained ICP waveforms [78]. However, in its present state, this technology has not been quantitatively correlated with ICP status. In addition, there is some inter-individual variability in the magnitude of waveform pattern changes due to changes in ICP. Although a promising noninvasive method to monitor ICP, further validation and calibration of this technique is necessary before it can be considered a viable alternative to invasively obtained ICP.

Transcranial Doppler ultrasound

Ultrasound is readily available and commonly used in emergency departments and in intensive care units as a noninvasive tool to screen patients for internal injuries after trauma (E-FAST; extended focused assessment with sonography in trauma) [79,80] and to monitor complications arising from intracranial injuries, such as cerebral artery vasospasm [81–83]. Several parameters of transcranial Doppler (TCD) ultrasound, such as cerebral blood flow velocity (CBV), pulsatility index, and the ability to measure the diameter of the optic nerve sheath (discussed in a later section), have been studied as noninvasive biomarkers of ICP [84–86]. Although several early studies and a few recent studies have shown a strong correlation between TCD and ICP [87], a number of studies have shown varying correlations between TCD-determined ICP and invasively obtained ICP or have failed to show a correlation [84,88–91].

In a study of 16 patients with IIH, there was a significant reduction in middle cerebral artery mean flow velocities following lumbar puncture, while there was no significant change in pulsatility index in the middle cerebral artery, the basilar artery, or the vertebral artery following lumbar puncture [86]. In contrast, in a study of 100 TBI patients who had invasive intracranial monitoring, TCD diastolic flow velocities were unable to reliably detect ICP above 20 mmHg; the reported sensitivity and specificity for detecting ICP at least 20 mmHg was 0% and 74.4%, respectively [92]. Similarly, in a study of 262 patients with acute brain injury (TBI, subarachnoid hemorrhage, intracranial hemorrhage, or ischemic stroke), TCD (based on a determination of flow velocities and mean arterial pressure) was able to rule out elevated ICP (ICP > 22; negative predictive value of 95.6%), however, it was unable to reliably detect elevated ICP (ICP > 22; a positive predictive value of 23.0%) [85].

Although there have been conflicting data regarding the correlation between CBV or pulsatility index and ICP, a recent study using two-depth TCD to compare the flow velocity in the extracranial and intracranial portions of the ophthalmic artery has shown a strong correlation with invasively obtained ICP [93▪▪]. Continuous noninvasively obtained ICP using two-depth TCD of the ophthalmic artery over a 1-h period showed a very strong correlation with invasively obtained ICP (correlation coefficient of 0.94) [93▪▪]. The TCD-predicted ICP changes closely mimicked the real-time changes in ICP over the 1-h period [93▪▪]. Therefore, while TCD-derived pulsatility index or CBV does not appear to consistently correlate with ICP, two-depth TCD has the potential to be a useful noninvasive method to measure and monitor ICP.

METHODS BASED ON CHANGES IN OCULAR STRUCTURES

Optic nerve sheath diameter

Optic nerve sheath diameter (ONSD) is a widely studied noninvasive method for determining ICP and is commonly measured by orbital ultrasound, however, MRI and computerized tomography (CT) have also been used to measure the ONSD. Indeed, a PubMed search for ‘optic nerve sheath diameter intracranial pressure’ yielded over 150 articles in 2021 and 2022.

A number of recent studies have shown a good correlation between ONSD and invasively obtained ICP [84,87,91,94–97]. For example, a recent study showed that measurement of the ONSD 3 mm posterior to the globe in patients with IIH predicted elevated ICP with good sensitivity and specificity (97% sensitivity and 100% specificity) [98]. In addition, a prospective study in patients undergoing lumbar puncture in a general hospital in China reported that ONSD was significantly different between patients with intracranial hypotension (ICP ≤ 60-mm water), control patients, and patients with intracranial hypertension (ICP > 200-mm water) [99▪]. In addition, a strong correlation was reported between ONSDs and lumbar puncture obtained ICP (r = 0.952 for all patients included in the study and r = 0.871 for patients with elevated ICP) [99▪]. Although a few recent studies have failed to show a strong relationship between ONSD and ICP in both pediatric and adult patients [88,100–102], based on the large amount of data suggesting that ONSD can be used to determine ICP, ONSD measurement may be a useful clinical tool to estimate and potentially measure ICP.

However, several significant limitations of ultrasound-determined ONSD exist, which can dramatically alter ONSD measurements, potentially limiting its usefulness as a noninvasive biomarker for ICP. These limitations include ultrasound probe choice, nonstandardized ultrasound gain settings, not having standardized protocols regarding in which planes to obtain ultrasound images, and operator experience [103–109]. Although using MRI or CT scans to measure ONSD eliminates some of these limitations, the expense, time (MRI), availability, and exposure to radiation (CT scan), make MRI-determined or CT-determined ONSD measurements less ideal and less useful methods to measure or serially monitor changes in ICP [110,111].

Venous ophthalmodynamometry

Venous ophthalmodynamometry (ODM) measures central retinal vein (CRV) pressure by determining the force necessary to collapse the CRV; the force necessary to collapse the CRV is equal to the sum of the intraocular pressure (IOP) and a variable force applied externally to the globe [112,113]. Since the CRV is exposed to and influenced by ICP as it leaves the globe and travels within the substance of the optic nerve, CRV pressure is believed to be a useful biomarker for ICP [112]. Although this theory was first proposed in 1925 [114], it was not formally studied until 2000, when Firsching et al.[115] showed a good correlation between ODM and invasively obtained ICP measurements. Although most early reports suffered from several limitations, such as a variable correlation between CRV pressure and ICP and using estimated IOP rather than true IOP during ODM, Firsching et al.[116] have shown that, due to advances in technique and technology, the sensitivity and specificity of detecting elevated ICP with ODM can be as high as 84.2% and 92.8%, respectively. However, the study did not attempt to quantitatively correlate CRV pressures with ICP. In addition, patients with papilledema were excluded from the study because the effect of papilledema on CRV pressure was unclear [116]. Since ODM may not be able to be reliably performed in patients with papilledema, a common consequence of elevated ICP, ODM may have limited utility as a noninvasive method to measure ICP.

Spontaneous retinal venous pulsations

Similar to CRV pressure, spontaneous retinal venous pulsations (SRVPs), pulsations of the CRV on or near the optic disc, have also been reported to be affected by changes in ICP and may be a useful biomarker to noninvasively determine ICP [117,118]. SRVPs are reported to occur in ∼75–80% of normal patients when detected ophthalmoscopically, however, newer technology, such as imaging the pulsations with video recordings or with optical coherence tomography (OCT), has shown that SRVPs occur in more than 95% of people with normal ICP and IOP [119].

SRVPs have long been used as a qualitative indicator of ICP, with venous pulsations diminishing or disappearing in patients with elevated ICP. Indeed, acute loss of SRVPs due to an experimentally induced increase in ICP has been confirmed in animal models, showing that changes in SRVPs occur quickly following changes in ICP [120▪]. Similarly, in a recent study of SRVPs in a para-primate animal model, alterations in ICP and IOP were found to acutely alter SRVP presence and SRVP amplitude [121]. A higher IOP was necessary to elicit SRVPs at higher ICPs than at lower ICPs and SRVPs had smaller amplitudes at high ICPs than at lower ICPs [121]. These data demonstrate multiple effects of changes in ICP on SRVPs and suggest that the relationship between SRVPs, IOP, and ICP is not straightforward. Similar findings were reported in a 2019 study by D’Antona et al.[122], where larger SRVP amplitudes were found in patients with lower ICP compared to patients with higher ICP. Although these studies demonstrate a correlation between SRVPs and ICP and suggest that SRVPs may be useful biomarkers for ICP, more work in this area is needed to determine if SRVPs can quantitatively measure ICP and before measurement of SRVPs can potentially be developed as a noninvasive method to determine ICP.

Pupillometry

Automated infrared pupillometry provides accurate quantitative measurements of iris function. A neurological pupil index (NPI) is determined by comparing automated pupillometry measurements to a normative model of iris function [123]. Multiple studies have shown that lower NPI values, which indicate abnormal iris function, correlate with a higher ICP [123–126], potentially making the NPI a valuable screening tool to rapidly detect an abnormal ICP. In addition, sustained low NPI values have been shown to be predictive of poor clinical outcomes in patients with severe TBI [127,128]. However, the NPI is not currently able to provide quantitative information about ICP, and several studies have reported that the NPI does not reliably detect changes in ICP, limiting its utility as a clinical tool to measure ICP or to monitor changes in ICP [123,129,130].

Visual evoked potential

Visual evoked potentials (VEPs), electrical potentials extracted from EEG recordings using signal averaging, are used to assess the integrity of the visual pathways from the optic nerves to the occipital cortex [131]. Therefore, any process that affects the integrity of the visual system can affect VEPs, such as myelin plaques from multiple sclerosis, compression of the anterior visual pathways from space-occupying lesions or hydrocephalus, or from cerebral cortical injuries [131].

In the 1980s, York et al.[132] reported a good relationship between elevated ICP and a shift in the latency of the N2 wave, which occurs at approximately 70 ms and corresponds to cortical potentials. Based on this work, VEPs were further studied as a potential noninvasive method to measure ICP. However, several studies found that VEPs did not change significantly in patients with elevated ICP; that there was a wide range of VEP latencies, amplitudes, and waveforms in normal subjects; and that there was a large variability over time in individual subjects, questioning the utility of VEPs as a noninvasive biomarker for ICP [133,134].

More recent studies have looked at pattern reversal VEPs in patients with craniosynostosis and at sustained giant pattern VEPs (VEP amplitudes that exceeded the upper 97th percentile of VEP amplitudes) as markers of elevated ICP [133,135]. Similar to prior VEP studies, pattern reversal VEPs or sustained giant pattern VEPs were not found to be reliable indicators of elevated ICP [135]. Pattern reversal VEPs were shown to have a sensitivity for elevated ICP that ranged between 58.3 and 70.6% [133] and sustained giant pattern VEPs incorrectly suggested elevated ICP in at least 20% of pediatric patients [135]. Therefore, it is unlikely that changes in VEP can be used to reliably detect changes in ICP and even less likely that it can provide a quantitative measurement of ICP.

Optical coherence tomography changes

OCT is a noninvasive modality that can image the retina, optic nerve, and choroid with a resolution approaching that of histological sections [136]. Given the high resolution of OCT, certain structural characteristics of the optic nerve head and surrounding retina, such as the peripapillary retinal nerve fiber layer thickness, the size of Bruch's membrane opening (the opening that surrounds the optic nerve), the angle of Bruch's membrane, and the subfoveal choroidal thickness, can be clearly visualized and measured [137–141]. Changes in these structures have been suggested as biomarkers for ICP.

Although most studies using OCT have shown a qualitative correlation with ICP, some recent studies have suggested that OCT can be used to quantitatively determine ICP. In a recent study of 104 patients with IIH, optic nerve head central thickness showed a modest correlation with lumbar puncture-obtained ICP (correlation coefficients for the right and left eye were 0.21 and 0.28 at baseline and were 0.46 and 0.46 at a 24-month follow-up, respectively) [142]. There was no correlation between ICP and retinal nerve fiber layer thickness, ganglion cell layer thickness, or macular volume changes [142]. However, a study of 22 patients with IIH showed that the subfoveal choroidal thickness was significantly higher (258.22 ± 33.9 μm) in IIH patients than in control subjects (228.04 ± 7.94 μm) [140]. In addition, subfoveal choroidal thickness was positively correlated with ICP obtained by lumbar puncture (correlation coefficient of 0.851) [139]. Although this study demonstrated a good correlation between subfoveal choroidal thickness and ICP, spectral domain OCT was used for choroidal thickness measurements. A stronger correlation may be possible with the use of enhanced depth imaging spectral domain OCT, which can more accurately delineate the transition between choroid and sclera.

Although some studies support the use of OCT as a quantitative biomarker for invasively obtained ICP, all OCT studies assess structural changes in the retina and peripapillary regions which may not readily change in response to ICP-lowering treatments [140]. Therefore, OCT may have limited utility as a noninvasive biomarker for invasively obtained ICP.

CONCLUSION

Multiple biomarkers have been developed as potential noninvasive methods to determine and monitor ICP. Although none of these noninvasive methods are in routine clinical use due to concerns about their accuracy, several of the noninvasive biomarkers, such as skull elasticity, specialized MRI sequences, two-depth TCD, ONSD measurement, and subfoveal choroidal thickness, have shown strong correlations with invasively obtained ICP. Therefore, it is possible that further technology developed around these biomarkers may be able to produce rapid, accurate, reliable, and portable noninvasive devices to measure and monitor ICP. Development of such devices would allow ICP determination to become more commonplace, potentially supplanting the use of invasively obtained ICP measurement in certain clinical situations, and could significantly change how diseases such as IIH, glaucoma, and acute TBI are managed.

Acknowledgements

None.

Financial support and sponsorship

MD is supported in part by a departmental grant from the Research to Prevent Blindness, by NIH/NEI core grant P30-EY06360 (Department of Ophthalmology, Emory University School of Medicine), by a University Research Committee pilot grant (Emory University School of Medicine), and by a North American Neuro-Ophthalmology Society pilot grant.

Conflicts of interest

There are no conflicts of interest.

REFERENCES AND RECOMMENDED READING

Papers of particular interest, published within the annual period of review, have been highlighted as:

▪ of special interest

▪▪ of outstanding interest

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Keywords:

cerebrospinal fluid; intracranial pressure; noninvasive

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