Cerebral small vessel disease pathology in COVID-19 patients: A systematic review

Cameron D Owens; Camila Bonin Pinto; Sam Detwiler; Peter Mukli; Anna Peterfi; Zsofia Szarvas; Jordan R Hoffmeister; Juliette Galindo; Jila Noori; Angelia C Kirkpatrick; Tarun W Dasari; Judith James; Stefano Tarantini; Anna Csiszar; Zoltan Ungvari; Calin I Prodan; Andriy Yabluchanskiy

doi:10.1016/j.arr.2023.101962

Cerebral small vessel disease pathology in COVID-19 patients: A systematic review

Ageing Res Rev. 2023 Jul:88:101962. doi: 10.1016/j.arr.2023.101962. Epub 2023 May 22.

Authors

Cameron D Owens¹, Camila Bonin Pinto¹, Sam Detwiler¹, Peter Mukli², Anna Peterfi², Zsofia Szarvas², Jordan R Hoffmeister³, Juliette Galindo³, Jila Noori⁴, Angelia C Kirkpatrick⁵, Tarun W Dasari⁶, Judith James⁷, Stefano Tarantini⁸, Anna Csiszar², Zoltan Ungvari⁹, Calin I Prodan¹⁰, Andriy Yabluchanskiy¹¹

Affiliations

¹ Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
² Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; International Training Program in Geroscience, Doctoral School of Basic and Translational Medicine/Departments of Public Health, Translational Medicine and Physiology, Semmelweis University, Budapest, Hungary.
³ Department of Psychiatry and Behavioral Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
⁴ Dean McGee Eye Institute, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
⁵ Cardiovascular Section, Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Veterans Affairs Medical Center, Oklahoma City, OK, USA.
⁶ Cardiovascular Section, Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
⁷ Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Arthritis & Clinical Immunology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA; Department of Internal Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Department of Pathology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
⁸ Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; International Training Program in Geroscience, Doctoral School of Basic and Translational Medicine/Departments of Public Health, Translational Medicine and Physiology, Semmelweis University, Budapest, Hungary; The Peggy and Charles Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
⁹ Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; International Training Program in Geroscience, Doctoral School of Basic and Translational Medicine/Departments of Public Health, Translational Medicine and Physiology, Semmelweis University, Budapest, Hungary; Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
¹⁰ Veterans Affairs Medical Center, Oklahoma City, OK, USA; Department of Neurology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
¹¹ Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; The Peggy and Charles Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA; Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA. Electronic address: andriy-yabluchanskiy@ouhsc.edu.

Abstract

Cerebral small vessel disease (CSVD) is the leading cause of vascular cognitive impairment and is associated with COVID-19. However, contributing factors that often accompany CSVD pathology in COVID-19 patients may influence the incidence of cerebrovascular complications. Thus, a mechanism linking COVID-19 and CSVD has yet to be uncovered and differentiated from age-related comorbidities (i.e., hypertension), and medical interventions during acute infection. We aimed to evaluate CSVD in acute and recovered COVID-19 patients and to differentiate COVID-19-related cerebrovascular pathology from the above-mentioned contributing factors by assessing the localization of microbleeds and ischemic lesions/infarctions in the cerebrum, cerebellum, and brainstem. A systematic search was performed in December 2022 on PubMed, Web of Science, and Embase using a pre-established search criterion related to history of, or active COVID-19 with CSVD pathology in adults. From a pool of 161 studies, 59 met eligibility criteria and were included. Microbleeds and ischemic lesions had a strong predilection for the corpus callosum and subcortical/deep white matter in COVID-19 patients, suggesting a distinct CSVD pathology. These findings have important implications for clinical practice and biomedical research as COVID-19 may independently, and through exacerbation of age-related mechanisms, contribute to increased incidence of CSVD.

Keywords: Aging; COVID-19; Cerebral small vessel disease; Cognitive impairment.

Publication types

Systematic Review
Review
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural

MeSH terms

COVID-19* / complications
COVID-19* / epidemiology
Cerebral Hemorrhage / complications
Cerebral Hemorrhage / epidemiology
Cerebral Hemorrhage / pathology
Cerebral Small Vessel Diseases* / complications
Humans
Hypertension* / pathology
Magnetic Resonance Imaging
White Matter* / pathology

Abstract

Publication types

MeSH terms

Grants and funding