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      Dissociation of Cerebral Blood Flow and Femoral Artery Blood Pressure Pulsatility After Cardiac Arrest and Resuscitation in a Rodent Model: Implications for Neurological Recovery

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          Abstract

          Background

          Impaired neurological function affects 85% to 90% of cardiac arrest ( CA) survivors. Pulsatile blood flow may play an important role in neurological recovery after CA. Cerebral blood flow ( CBF) pulsatility immediately, during, and after CA and resuscitation has not been investigated. We characterized the effects of asphyxial CA on short‐term (<2 hours after CA) CBF and femoral arterial blood pressure ( ABP) pulsatility and studied their relationship to cerebrovascular resistance ( CVR) and short‐term neuroelectrical recovery.

          Methods and Results

          Male rats underwent asphyxial CA followed by cardiopulmonary resuscitation. A multimodal platform combining laser speckle imaging, ABP, and electroencephalography to monitor CBF, peripheral blood pressure, and brain electrophysiology, respectively, was used. CBF and ABP pulsatility and CVR were assessed during baseline, CA, and multiple time points after resuscitation. Neuroelectrical recovery, a surrogate for neurological outcome, was assessed using quantitative electroencephalography 90 minutes after resuscitation. We found that CBF pulsatility differs significantly from baseline at all experimental time points with sustained deficits during the 2 hours of postresuscitation monitoring, whereas ABP pulsatility was relatively unaffected. Alterations in CBF pulsatility were inversely correlated with changes in CVR, but ABP pulsatility had no association to CVR. Interestingly, despite small changes in ABP pulsatility, higher ABP pulsatility was associated with worse neuroelectrical recovery, whereas CBF pulsatility had no association.

          Conclusions

          Our results reveal, for the first time, that CBF pulsatility and CVR are significantly altered in the short‐term postresuscitation period after CA. Nevertheless, higher ABP pulsatility appears to be inversely associated with neuroelectrical recovery, possibly caused by impaired cerebral autoregulation and/or more severe global cerebral ischemia.

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          Most cited references52

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          Arterial stiffness, pressure and flow pulsatility and brain structure and function: the Age, Gene/Environment Susceptibility--Reykjavik study.

          Gary F Mitchell, Mark van Buchem, Sigurdur Sigurdsson … (2011)
          Aortic stiffness increases with age and vascular risk factor exposure and is associated with increased risk for structural and functional abnormalities in the brain. High ambient flow and low impedance are thought to sensitize the cerebral microcirculation to harmful effects of excessive pressure and flow pulsatility. However, haemodynamic mechanisms contributing to structural brain lesions and cognitive impairment in the presence of high aortic stiffness remain unclear. We hypothesized that disproportionate stiffening of the proximal aorta as compared with the carotid arteries reduces wave reflection at this important interface and thereby facilitates transmission of excessive pulsatile energy into the cerebral microcirculation, leading to microvascular damage and impaired function. To assess this hypothesis, we evaluated carotid pressure and flow, carotid-femoral pulse wave velocity, brain magnetic resonance images and cognitive scores in participants in the community-based Age, Gene/Environment Susceptibility--Reykjavik study who had no history of stroke, transient ischaemic attack or dementia (n = 668, 378 females, 69-93 years of age). Aortic characteristic impedance was assessed in a random subset (n = 422) and the reflection coefficient at the aorta-carotid interface was computed. Carotid flow pulsatility index was negatively related to the aorta-carotid reflection coefficient (R = -0.66, P<0.001). Carotid pulse pressure, pulsatility index and carotid-femoral pulse wave velocity were each associated with increased risk for silent subcortical infarcts (hazard ratios of 1.62-1.71 per standard deviation, P<0.002). Carotid-femoral pulse wave velocity was associated with higher white matter hyperintensity volume (0.108 ± 0.045 SD/SD, P = 0.018). Pulsatility index was associated with lower whole brain (-0.127 ± 0.037 SD/SD, P<0.001), grey matter (-0.079 ± 0.038 SD/SD, P = 0.038) and white matter (-0.128 ± 0.039 SD/SD, P<0.001) volumes. Carotid-femoral pulse wave velocity (-0.095 ± 0.043 SD/SD, P = 0.028) and carotid pulse pressure (-0.114 ± 0.045 SD/SD, P = 0.013) were associated with lower memory scores. Pulsatility index was associated with lower memory scores (-0.165 ± 0.039 SD/SD, P<0.001), slower processing speed (-0.118 ± 0.033 SD/SD, P<0.001) and worse performance on tests assessing executive function (-0.155 ± 0.041 SD/SD, P<0.001). When magnetic resonance imaging measures (grey and white matter volumes, white matter hyperintensity volumes and prevalent subcortical infarcts) were included in cognitive models, haemodynamic associations were attenuated or no longer significant, consistent with the hypothesis that increased aortic stiffness and excessive flow pulsatility damage the microcirculation, leading to quantifiable tissue damage and reduced cognitive performance. Marked stiffening of the aorta is associated with reduced wave reflection at the interface between carotid and aorta, transmission of excessive flow pulsatility into the brain, microvascular structural brain damage and lower scores in various cognitive domains.
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            Increased cerebral arterial pulsatility in patients with leukoaraiosis: arterial stiffness enhances transmission of aortic pulsatility.

            Michela Simoni, Sara Mazzucco, Wilhelm Kuker … (2012)
            Arterial stiffening reduces damping of the arterial waveform and hence increases pulsatility of cerebral blood flow, potentially damaging small vessels. In the absence of previous studies in patients with recent transient ischemic attack or stroke, we determined the associations between leukoaraiosis and aortic and middle cerebral artery stiffness and pulsatility. Patients were recruited from the Oxford Vascular Study within 6 weeks of a transient ischemic attack or minor stroke. Leukoaraiosis was categorized on MRI by 2 independent observers with the Fazekas and age-related white matter change scales. Middle cerebral artery (MCA) stiffness (transit time) and pulsatility (Gosling's index: MCA-PI) were measured with transcranial ultrasound and aortic pulse wave velocity and aortic systolic, diastolic, and pulse pressure with applanation tonometry (Sphygmocor). In 100 patients, MCA-PI was significantly greater in patients with leukoaraiosis (0.91 versus 0.73, P<0.0001). Severity of leukoaraiosis was associated with MCA-PI and aortic pulse wave velocity (Fazekas: χ(2)=0.39, MCA-PI P=0.01, aortic pulse wave velocity P=0.06; age-related white matter change: χ(2)=0.38, MCA-PI P=0.015; aortic pulse wave velocity P=0.026) for periventricular and deep white matter lesions independent of aortic systolic blood pressure, diastolic blood pressure, and pulse pressure and MCA transit time with MCA-PI independent of age. In a multivariate model (r(2)=0.68, P<0.0001), MCA-PI was independently associated with aortic pulse wave velocity (P=0.016) and aortic pulse pressure (P<0.0001) and inversely associated with aortic diastolic blood pressure (P<0.0001) and MCA transit time (P=0.001). MCA pulsatility was the strongest physiological correlate of leukoaraiosis, independent of age, and was dependent on aortic diastolic blood pressure and pulse pressure and aortic and MCA stiffness, supporting the hypothesis that large artery stiffening results in increased arterial pulsatility with transmission to the cerebral small vessels resulting in leukoaraiosis.
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              Using a common average reference to improve cortical neuron recordings from microelectrode arrays.

              K. Anderson, N Langhals, K. Ludwig … (2009)
              In this study, we propose and evaluate a technique known as common average referencing (CAR) to generate a more ideal reference electrode for microelectrode recordings. CAR is a computationally simple technique, and therefore amenable to both on-chip and real-time applications. CAR is commonly used in EEG, where it is necessary to identify small signal sources in very noisy recordings. To study the efficacy of common average referencing, we compared CAR to both referencing with a stainless steel bone-screw and a single microelectrode site. Data consisted of in vivo chronic recordings in anesthetized Sprague-Dawley rats drawn from prior studies, as well as previously unpublished data. By combining the data from multiple studies, we generated and analyzed one of the more comprehensive chronic neural recording datasets to date. Reference types were compared in terms of noise level, signal-to-noise ratio, and number of neurons recorded across days. Common average referencing was found to drastically outperform standard types of electrical referencing, reducing noise by >30%. As a result of the reduced noise floor, arrays referenced to a CAR yielded almost 60% more discernible neural units than traditional methods of electrical referencing. CAR should impart similar benefits to other microelectrode recording technologies-for example, chemical sensing-where similar differential recording concepts apply. In addition, we provide a mathematical justification for CAR using Gauss-Markov theorem and therefore help place the application of CAR into a theoretical context.
              Article 0 comments Cited 111 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Yama Akbari: yakbari@uci.edu
                Bernard Choi: choib@uci.edu
                Journal
                Journal ID (nlm-ta): J Am Heart Assoc
                Journal ID (iso-abbrev): J Am Heart Assoc
                Journal ID (doi): 10.1002/(ISSN)2047-9980
                Journal ID (publisher-id): JAH3
                Journal ID (hwp): ahaoa
                Title: Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Electronic): 2047-9980
                Publication date (Electronic): 04 January 2020
                Publication date Collection: 07 January 2020
                Volume: 9
                Issue: 1 ( doiID: 10.1002/jah3.v9.1 )
                Electronic Location Identifier: e012691
                Affiliations
                [ 1 ] Beckman Laser Institute and Medical Clinic Irvine CA
                [ 2 ] Department of Biomedical Engineering University of California Irvine CA
                [ 3 ] Department of Neurology University of California Irvine CA
                [ 4 ] Department of Surgery University of California Irvine CA
                [ 5 ] Edwards Lifesciences Center for Advanced Cardiovascular Technology Irvine CA
                [ 6 ] University of California, Irvine Irvine CA
                Author notes
                [*] [* ] Correspondence to: Bernard Choi, PhD, 1002 Health Sciences Rd E, Irvine, CA 92612. E‐mail: choib@ 123456uci.edu and Yama Akbari, MD, PhD, 2113 Gillespie Neuroscience Research Facility, 837 Health Sciences Rd, Irvine, CA 92697. E‐mail: yakbari@ 123456uci.edu
                Article
                Publisher ID: JAH34707
                DOI: 10.1161/JAHA.119.012691
                PMC ID: 6988151
                PubMed ID: 31902319
                SO-VID: 29afb3ce-8f75-4b9a-89ba-c8970e591148
                Copyright © © 2020 The Authors. Published on behalf of the American Heart Association, Inc., by Wiley.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                Date received : 09 April 2019
                Date accepted : 15 November 2019
                Page count
                Figures: 6, Tables: 2, Pages: 21, Words: 10267
                Funding
                Funded by: Arnold and Mabel Beckman Foundation , open-funder-registry 10.13039/100000997;
                Funded by: Roneet Carmell Memorial Endowment Fund
                Funded by: National Institutes of Health , open-funder-registry 10.13039/100000002;
                Award ID: P41EB015890
                Award ID: TL1TR001415‐01
                Award ID: R21 EB024793
                Award ID: 5KL2TR001416
                Award ID: UL1 TR001414
                Funded by: National Science Foundation Graduate Research Fellowship Program , open-funder-registry 10.13039/100000001;
                Award ID: DGE‐1321846
                Funded by: National Center for Research Resources , open-funder-registry 10.13039/100000097;
                Funded by: National Center for Advancing Translational Sciences , open-funder-registry 10.13039/100006108;
                Categories
                Subject: Original Research
                Subject: Original Research
                Subject: Resuscitation Science
                Custom metadata
                source-schema-version-number 2.0
                cover-date 07 January 2020
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.4 mode:remove_FC converted:06.01.2020

                ScienceOpen disciplines: Cardiovascular Medicine
                Keywords: cardiac arrest,cerebral autoregulation,cerebral blood flow,electroencephalography,laser speckle imaging,perfusion,pulsatile,imaging,blood pressure,cardiopulmonary arrest,cardiopulmonary resuscitation and emergency cardiac care,hemodynamics
                Data availability:
                ScienceOpen disciplines: Cardiovascular Medicine
                Keywords: cardiac arrest, cerebral autoregulation, cerebral blood flow, electroencephalography, laser speckle imaging, perfusion, pulsatile, imaging, blood pressure, cardiopulmonary arrest, cardiopulmonary resuscitation and emergency cardiac care, hemodynamics

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