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Vasoconstriction and Impairment of Neurovascular Coupling after Subarachnoid Hemorrhage: a Descriptive Analysis of Retinal Changes

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Abstract

Impaired cerebral autoregulation and neurovascular coupling (NVC) contribute to delayed cerebral ischemia after subarachnoid hemorrhage (SAH). Retinal vessel analysis (RVA) allows non-invasive assessment of vessel dimension and NVC hereby demonstrating a predictive value in the context of various neurovascular diseases. Using RVA as a translational approach, we aimed to assess the retinal vessels in patients with SAH. RVA was performed prospectively in 24 patients with acute SAH (group A: day 5–14), in 11 patients 3 months after ictus (group B: day 90 ± 35), and in 35 age-matched healthy controls (group C). Data was acquired using a Retinal Vessel Analyzer (Imedos Systems UG, Jena) for examination of retinal vessel dimension and NVC using flicker-light excitation. Diameter of retinal vessels—central retinal arteriolar and venular equivalent—was significantly reduced in the acute phase (p < 0.001) with gradual improvement in group B (p < 0.05). Arterial NVC of group A was significantly impaired with diminished dilatation (p < 0.001) and reduced area under the curve (p < 0.01) when compared to group C. Group B showed persistent prolonged latency of arterial dilation (p < 0.05). Venous NVC was significantly delayed after SAH compared to group C (A p < 0.001; B p < 0.05). To our knowledge, this is the first clinical study to document retinal vasoconstriction and impairment of NVC in patients with SAH. Using non-invasive RVA as a translational approach, characteristic patterns of compromise were detected for the arterial and venous compartment of the neurovascular unit in a time-dependent fashion. Recruitment will continue to facilitate a correlation analysis with clinical course and outcome.

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Acknowledgements

The authors are grateful to Mrs. Jasmin Dell’Anna and Professor Klaus Rademacher (Faculty of Medical Engineering, Helmholtz-Institute for Biomedical Engineering, RWTH Aachen University) for supporting the constructional set up of the imaging device.

Funding

CC was supported by the START-Program of the Faculty of Medicine (RWTH Aachen University) and by the Foundation of Neurosurgical Research (German Society of Neurosurgery, 2016). WA was supported by funding from the German Society of Neurointensive and Emergency Medicine (Junior research award 2017).

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Author notes

  1. Catharina Conzen and Walid Albanna contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, RWTH Aachen University, Pauwelsstr. 30, 52074, Aachen, Germany

    Catharina Conzen, Walid Albanna, Miriam Weiss, Charlotte Zäske, Hans Clusmann & Gerrit Alexander Schubert

  2. Department of Ophthalmology, RWTH Aachen University, Aachen, Germany

    David Kürten

  3. IMEDOS Systems UG, Jena, Germany

    Walthard Vilser

  4. Department of Medical Engineering and Technomathematics, FH Aachen University of Applied Sciences, Aachen, Germany

    Konstantin Kotliar

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  1. Catharina Conzen
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Correspondence to Gerrit Alexander Schubert.

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Conflict of Interest

IMEDOS Systems provided the Retinal Vessel Analyzer for research purposes only. WV is affiliated to IMEDOS Systems as the company’s CEO. WV did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

The other authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Conzen, C., Albanna, W., Weiss, M. et al. Vasoconstriction and Impairment of Neurovascular Coupling after Subarachnoid Hemorrhage: a Descriptive Analysis of Retinal Changes. Transl. Stroke Res. 9, 284–293 (2018). https://doi.org/10.1007/s12975-017-0585-8

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