Impaired cerebrovascular reactivity correlates with reduced retinal vessel density in patients with carotid artery stenosis: Cross-sectional, single center study

Rita Magyar-Stang; Lilla István; Hanga Pál; Borbála Csányi; Anna Gaál; Zsuzsanna Mihály; Zsófia Czinege; Péter Sótonyi; Horváth Tamás; Akos Koller; Dániel Bereczki; Illés Kovács; Róbert Debreczeni

doi:10.1371/journal.pone.0291521

Impaired cerebrovascular reactivity correlates with reduced retinal vessel density in patients with carotid artery stenosis: Cross-sectional, single center study

PLoS One. 2023 Sep 14;18(9):e0291521. doi: 10.1371/journal.pone.0291521. eCollection 2023.

Authors

Rita Magyar-Stang^{1

2}, Lilla István³, Hanga Pál^{1

2}, Borbála Csányi⁴, Anna Gaál⁴, Zsuzsanna Mihály⁵, Zsófia Czinege⁵, Péter Sótonyi⁵, Horváth Tamás⁶, Akos Koller^{6

7

8}, Dániel Bereczki¹, Illés Kovács^{3

9

10}, Róbert Debreczeni¹

Affiliations

¹ Department of Neurology, Semmelweis University, Budapest, Hungary.
² Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, Hungary.
³ Department of Ophthalmology, Semmelweis University, Budapest, Hungary.
⁴ Faculty of Medicine, Semmelweis University, Budapest, Hungary.
⁵ Department of Vascular and Endovascular Surgery, Semmelweis University, Budapest, Hungary.
⁶ Research Center for Sport Physiology, Hungarian University of Sports Science, Budapest, Hungary.
⁷ Department of Morphology&Physiology, Faculty of Health Sciences, and Translational Medicine Institute, Faculty of Medicine, and ELKH-SE, Cerebrovascular and Neurocognitive Disorders Research Group, Semmelweis University, Budapest, Hungary.
⁸ Department of Physiology, New York Medical College, Valhalla, NY, United States of America.
⁹ Department of Ophthalmology, Weill Cornell Medical College, New York, NY, United States of America.
¹⁰ Department of Clinical Ophthalmology, Semmelweis University, Budapest, Hungary.

Abstract

Background: The cerebral and retinal circulation systems are developmentally, anatomically, and physiologically interconnected. Thus, we hypothesized that hypoperfusion due to atherosclerotic stenosis of the internal carotid artery (ICA) can result in disturbances of both cerebral and retinal microcirculations. We aimed to characterize parameters indicating cerebrovascular reactivity (CVR) and retinal microvascular density in patients with ICA stenosis, and assess if there is correlation between them.

Methods: In this cross-sectional study the middle cerebral artery (MCA) blood flow velocity was measured by transcranial Doppler (TCD) and, simultaneously, continuous non-invasive arterial blood pressure measurement was performed on the radial artery by applanation tonometry. CVR was assessed based on the response to the common carotid artery compression (CCC) test. The transient hyperemic response ratio (THRR) and cerebral arterial resistance transient hyperemic response ratio (CAR-THRR) were calculated. Optical coherence tomography angiography (OCTA) was used to determine vessel density (VD) on the papilla whole image for all (VDP-WIall) and for small vessels (VDP-WIsmall). The same was done in the peripapillary region: all (VDPPall), and small (VDPPsmall) vessels. The VD of superficial (VDMspf) and deep (VDMdeep) macula was also determined. Significance was accepted when p<0.05.

Results: Twenty-four ICA stenotic patients were evaluated. Both CVR and retinal VD were characterized. There was a significant, negative correlation between CAR-THRR (median = -0.40) and VDPPsmall vessels (median = 52%), as well as between VDPPall vessels (median = 58%), and similar correlation between CAR-THRR and VDP-WIsmall (median = 49.5%) and between VDP-WIall (median = 55%).

Conclusion: The significant correlation between impaired cerebrovascular reactivity and retinal vessel density in patients with ICA stenosis suggests a common mechanism of action. We propose that the combined use of these diagnostic tools (TCD and OCTA) helps to better identify patients with increased ischemic or other cerebrovascular risks.

Copyright: © 2023 Magyar-Stang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Carotid Artery, Common
Carotid Stenosis* / diagnostic imaging
Constriction, Pathologic
Cross-Sectional Studies
Humans
Hyperemia*
Retinal Vessels / diagnostic imaging

Grants and funding

The study was supported by the National Office for Research, Development and Innovation (Project no. NKFIK129277 ("Evaluation of cerebrovascular events in patients with occlusive carotid artery disorders based on morphological and hemodynamic features") has been implemented with the support provided by the Ministry of Innovation and Technology of Hungary from the National Research, Development, and Innovation Fund. AK: NKFI-1 K OTKA 132596 K-19, TKP2021-EGA-37 of MIT of Hungary-NRDI TKP2021-EGA funding and HAS/MTA Post-Covid 2021-34. DB: Ministry of Innovation and Technology of Hungary from the National Research, Development and Innovation Fund (Grant No: TKP2021-EGA/TKP2021-NVA/TKP2021-NKTA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.