Elevated intracranial pressure and reversible eye-tracking changes detected while viewing a film clip

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OBJECTIVE

The precise threshold differentiating normal and elevated intracranial pressure (ICP) is variable among individuals. In the context of several pathophysiological conditions, elevated ICP leads to abnormalities in global cerebral functioning and impacts the function of cranial nerves (CNs), either or both of which may contribute to ocular dysmotility. The purpose of this study was to assess the impact of elevated ICP on eye-tracking performed while patients were watching a short film clip.

METHODS

Awake patients requiring placement of an ICP monitor for clinical purposes underwent eye tracking while watching a 220-second continuously playing video moving around the perimeter of a viewing monitor. Pupil position was recorded at 500 Hz and metrics associated with each eye individually and both eyes together were calculated. Linear regression with generalized estimating equations was performed to test the association of eye-tracking metrics with changes in ICP.

RESULTS

Eye tracking was performed at ICP levels ranging from −3 to 30 mm Hg in 23 patients (12 women, 11 men, mean age 46.8 years) on 55 separate occasions. Eye-tracking measures correlating with CN function linearly decreased with increasing ICP (p < 0.001). Measures for CN VI were most prominently affected. The area under the curve (AUC) for eye-tracking metrics to discriminate between ICP < 12 and ≥ 12 mm Hg was 0.798. To discriminate an ICP < 15 from ≥ 15 mm Hg the AUC was 0.833, and to discriminate ICP < 20 from ≥ 20 mm Hg the AUC was 0.889.

CONCLUSIONS

Increasingly elevated ICP was associated with increasingly abnormal eye tracking detected while patients were watching a short film clip. These results suggest that eye tracking may be used as a noninvasive, automatable means to quantitate the physiological impact of elevated ICP, which has clinical application for assessment of shunt malfunction, pseudotumor cerebri, concussion, and prevention of second-impact syndrome.

ABBREVIATIONS AUC = area under the curve; CN = cranial nerve; EVD = external ventricular drain; GEE = generalized estimating equation; ICP = intracranial pressure; ROC = receiver operating characteristic; SAH = subarachnoid hemorrhage.

Article Information

Correspondence Uzma Samadani, Department of Neurosurgery, Hennepin County Medical Center and University of Minnesota, 701 Park Ave. S, PL.610, Minneapolis, MN 55415. email: uzma.samadani@hcmed.org.

INCLUDE WHEN CITING Published online June 2, 2017; DOI: 10.3171/2016.12.JNS161265.

Disclosures Dr. Samadani has been issued a patent describing the technology used in this paper. The ICP patent which has been issued is jointly owned by New York University (NYU) and the Veterans Administration (VA). Other patents related to this work are owned by NYU, the VA, and the Hennepin County Medical Center (HCMC) and are licensed to Oculogica Inc., a company in which Dr. Samadani, NYU, the VA, and HCMC have an equity interest. She also discloses support from Abbott Diagnostic Labs and Integra, Inc., for a non–study-related clinical or research effort that she oversees. Dr. Kondziolka discloses support from Brainlab for a non–study-related clinical or research effort that he oversees.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Charts showing that as the ICP increases, the area of the box plot decreases, suggesting impaired ocular motility at higher ICPs. The area of the eye-tracking scatterplot (box plot) is charted against the ICP in 23 patients undergoing 55 eye-tracking sessions. Each symbol represents an individual patient, with lines connecting the occasions on which each patient was tracked at a different ICP. Patients who were only tracked once do not have lines. Panel A represents the mean area in the left eye, and panel B is of the mean area in the right eye. Figure is available in color online only.

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    Case 1. Eye tracking is impaired at elevated ICP and recovers as the patient recovers clinically. Serial eye tracking was performed in a 45-year-old woman who sustained an SAH. A: The first eye-tracking session was at an ICP of 5 mm Hg and demonstrated normal metrics. B: The second session was at an ICP of 10 mm Hg and tracking was impaired. C: The third trial was after clinical and radiographic recovery from hydrocephalus and removal of ventriculostomy. It demonstrated normal metrics. Figure is available in color online only.

  • View in gallery

    Case 2. Eye tracking is impaired at elevated ICP and recovers as the patient recovers clinically. Serial eye tracking was performed in a 46-year-old woman who sustained an SAH. A: The first eye-tracking session was performed at an ICP of 3 mm Hg and demonstrated normal metrics. B: The second trial was at an ICP of 9 mm Hg and tracking was impaired. C: The third trial was performed after placement of a shunt to treat hydrocephalus and resolution of clinical symptoms. It demonstrated normal metrics. Figure is available in color online only.

  • View in gallery

    Case 3. Eye tracking is impaired at elevated ICP and recovers as the patient recovers clinically. Serial eye tracking was performed in a 55-year-old woman who sustained an SAH. A: The first eye-tracking session was at an ICP of 8 mm Hg and demonstrated normal metrics. B: The second trial was at an ICP of 10 mm Hg. The third trial was at an ICP of 8 mm Hg, and was again normal (not shown). C: The last eye-tracking session was performed after clinical and radiographic recovery from hydrocephalus and removal of ventriculostomy. It demonstrated normal metrics. Figure is available in color online only.

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