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Publications

Journal Article Review Ppublish 56 citations

PubMed: 38831182 DOI: 10.1007/s11357-024-01194-0

Linking peripheral atherosclerosis to blood-brain barrier disruption: elucidating its role as a manifestation of cerebral small vessel disease in vascular cognitive impairment.

Geroscience 46(6):6511-6536

Authors: Ádám Nyúl-Tóth, Roland Patai, Anna Csiszar, Anna Ungvari, Rafal Gulej, Peter Mukli, Andriy Yabluchanskiy, Zoltan Benyo, Peter Sotonyi, Calin I Prodan, Eric M Liotta, Peter Toth, Fanny Elahi, Péter Barsi, Pál Maurovich-Horvat, Farzaneh A Sorond, Stefano Tarantini, Zoltan Ungvari

Affiliations

  • Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
  • Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
  • Department of Public Health, Semmelweis University, Semmelweis University, Budapest, Hungary.
  • Stephenson Cancer Center, University of Oklahoma, Oklahoma City, OK, USA.
  • Department of Public Health, Semmelweis University, Semmelweis University, Budapest, Hungary.
  • Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
  • Doctoral College/Department of Public Health, International Training Program in Geroscience, Semmelweis University, Budapest, Hungary.
  • Institute of Translational Medicine, Semmelweis University, 1094, Budapest, Hungary.
  • Cerebrovascular and Neurocognitive Disorders Research Group, HUN-REN, Semmelweis University, 1094, Budapest, Hungary.
  • Department of Vascular and Endovascular Surgery, Heart and Vascular Centre, Semmelweis University, 1122, Budapest, Hungary.
  • Veterans Affairs Medical Center, Oklahoma City, OK, USA.
  • Department of Neurology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
  • Department of Neurology, Division of Stroke and Neurocritical Care, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
  • Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA. Department of Public Health, Semmelweis University, Semmelweis University, Budapest, Hungary. Department of Neurosurgery, Medical School, University of Pecs, Pecs, Hungary. Neurotrauma Research Group, Szentagothai Research Centre, University of Pecs, Pecs, Hungary. ELKH-PTE Clinical Neuroscience MR Research Group, University of Pecs, Pecs, Hungary.
  • Departments of Neurology and Neuroscience Ronald M. Loeb Center for Alzheimer's Disease Friedman Brain Institute Icahn School of Medicine at Mount Sinai, New York, NY, USA.
  • James J. Peters VA Medical Center, Bronx, NY, USA.
  • ELKH-SE Cardiovascular Imaging Research Group, Department of Radiology, Medical Imaging Centre, Semmelweis University, Budapest, Hungary.
  • Vascular Cognitive Impairment, Neurodegeneration and Healthy Brain Aging Program, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA. Oklahoma Center for Geroscience and Healthy Brain Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA. Stephenson Cancer Center, University of Oklahoma, Oklahoma City, OK, USA. Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA. Doctoral College/Department of Public Health, International Training Program in Geroscience, Semmelweis University, Budapest, Hungary.

Abstract

Aging plays a pivotal role in the pathogenesis of cerebral small vessel disease (CSVD), contributing to the onset and progression of vascular cognitive impairment and dementia (VCID). In older adults, CSVD often leads to significant pathological outcomes, including blood-brain barrier (BBB) disruption, which in turn triggers neuroinflammation and white matter damage. This damage is frequently observed as white matter hyperintensities (WMHs) in neuroimaging studies. There is mounting evidence that older adults with atherosclerotic vascular diseases, such as peripheral artery disease, ischemic heart disease, and carotid artery stenosis, face a heightened risk of developing CSVD and VCID. This review explores the complex relationship between peripheral atherosclerosis, the pathogenesis of CSVD, and BBB disruption. It explores the continuum of vascular aging, emphasizing the shared pathomechanisms that underlie atherosclerosis in large arteries and BBB disruption in the cerebral microcirculation, exacerbating both CSVD and VCID. By reviewing current evidence, this paper discusses the impact of endothelial dysfunction, cellular senescence, inflammation, and oxidative stress on vascular and neurovascular health. This review aims to enhance understanding of these complex interactions and advocate for integrated approaches to manage vascular health, thereby mitigating the risk and progression of CSVD and VCID.

MeSH

White Matter, Blood-Brain Barrier, Myocardial Ischemia, Blood, Aging, Brain, Cognitive Dysfunction, Arteries, Aged, Cognition Disorders, Atherosclerosis, Cerebral Small Vessel Diseases, Vascular Health

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