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Trans-Ocular Brain Impedance Indices Predict Pressure Reactivity Index Changes in a Porcine Model of Hypotension and Cerebral Autoregulation Perturbation

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Abstract

Background

Cerebrovascular autoregulation (CA) is a protective mechanism that enables the cerebral vasculature to automodulate tone in response to changes in cerebral perfusion pressure to ensure constant levels of cerebral blood flow (CBF) and oxygen delivery. CA can be impaired after neurological injury and contributes to secondary brain injury. In this study, we report novel impedance indices using trans-ocular brain impedance (TOBI) during controlled systemic hemorrhage and hypotension to assess CA in comparison with pressure reactivity index (PRx).

Methods

Yorkshire swine were instrumented to record intracranial pressure (ICP), mean arterial pressure (MAP), and CBF. TOBI was recorded using electrocardiographic electrodes placed on the closed eyelids. Impedance changes (dz) were recorded in response to introducing an alternating current (0.4 mA) through the electrodes. MAP, ICP, and CBF were also measured. Animals were subjected to a controlled hemorrhage to remove 30–40% of each animal’s total blood volume over 25–35 min. Hemorrhage was titrated to reach an MAP of approximately 35 mm Hg and end-tidal carbon dioxide above 28 mm Hg. PRx was calculated as a moving Pearson correlation between MAP and ICP. TOBI indices were calculated as the amplitude of the respiratory-induced changes in dz. DZx was calculated as a moving Pearson correlation between dz and MAP. TOBI indices (dz and DZx) were compared with hemodynamic indicators and PRx.

Results

dz was shown to be highly correlated with MAP, ICP, cerebral perfusion pressure, and CBF (r =  − 0.823, − 0.723, − 0.813, and − 0.726), respectively (p < 0.0001). During hemorrhage, cerebral perfusion pressure and CBF had a mean percent decrease (standard deviation) from baseline of − 54.2% (12.5%) and − 28.3% (14.7%), respectively, whereas dz increased by 277% (268%). Receiver operator characteristics and precision-recall curves demonstrated high predictive performance of DZx when compared with PRx with an area under the curve above 0.82 and 0.89 for receiver operator characteristic and precision-recall curves, respectively, with high sensitivity and positive predictive power.

Conclusions

TOBI indices appear to track changes in PRx and hemodynamics that affect CA during hemorrhage-induced hypotension. TOBI may offer a suitable, less invasive surrogate to PRx for monitoring and assessing CA.

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Acknowledgements

The authors would like to thank Katelyn Murphy and the Michigan Center for Integrative Research in Critical Care for their technical support.

Author information

Authors and Affiliations

  1. Department of Emergency Medicine, University of Michigan, Ann Arbor, MI, USA

    Mohamad H. Tiba, Brendan M. McCracken, Danielle C. Leander, Carmen I. Colmenero Mahmood, Nicholas L. Greer & Kevin R. Ward

  2. Michigan Center for Integrative Research in Critical Care (MCIRCC), University of Michigan, Ann Arbor, MI, USA

    Mohamad H. Tiba, Brendan M. McCracken, Danielle C. Leander, Carmen I. Colmenero Mahmood, Nicholas L. Greer, Paul Picton, Craig A. Williamson & Kevin R. Ward

  3. Department of Anesthesiology, University of Michigan, Ann Arbor, MI, USA

    Paul Picton

  4. Department of Neurological Surgery, University of Michigan, Ann Arbor, MI, USA

    Craig A. Williamson

  5. Department of Neurology, University of Michigan, Ann Arbor, MI, USA

    Craig A. Williamson

  6. Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, USA

    Kevin R. Ward

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  1. Mohamad H. Tiba
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MT, BM, DL, CCM, and NG. The first draft of the manuscript was written by MT, BM and KW. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mohamad H. Tiba.

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Source of Support

This study was supported by a grant from the Department of Defense (#W81XWH-18-1-0005).

Conflict of interest

Dr. Tiba and Dr. Ward report grants from Department of Defense, during the conduct of the study; In addition, Dr. Tiba and Dr. Ward have a patent 16/613,707 pending which is assigned to the University of Michigan. The technology has been licensed from the University of Michigan to New Vital Signs, Inc. Dr. Ward has equity in the company. Dr. Williamson reports grants from Department of Defense, during the conduct of the study. Dr. Picton, Mr. McCracken, Ms. Leander, Ms. Colmenero Mahmood, and Mr. Greer have nothing to disclose.

Ethical approval

All procedures outlined in this study adhere to the principles stated in the eighth edition of the Guide for the Care and Use of Laboratory Animals and were approved by the University of Michigan’s Institutional Animal Care and Use Committee.

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Tiba, M.H., McCracken, B.M., Leander, D.C. et al. Trans-Ocular Brain Impedance Indices Predict Pressure Reactivity Index Changes in a Porcine Model of Hypotension and Cerebral Autoregulation Perturbation. Neurocrit Care 36, 139–147 (2022). https://doi.org/10.1007/s12028-021-01272-7

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