Leptomeningeal collaterals regulate reperfusion in ischemic stroke and rescue the brain from futile recanalization.
Nadine Felizitas BinderMohamad El AmkiChaim GlückWilliam MiddlehamAnna Maria ReussAdrien BertoloPatrick ThurnerThomas DeffieuxChryso LambrideRobert EppHannah-Lea HandelsmannPhilipp BaumgartnerCyrille OrsetPhilipp BethgeZsolt KulcsarAdriano AguzziMickael TanterFranca SchmidDenis VivienMatthias Tasso WyssAndreas LuftMichael WellerBruno WeberSusanne WegenerPublished in: Neuron (2024)
Recanalization is the mainstay of ischemic stroke treatment. However, even with timely clot removal, many stroke patients recover poorly. Leptomeningeal collaterals (LMCs) are pial anastomotic vessels with yet-unknown functions. We applied laser speckle imaging, ultrafast ultrasound, and two-photon microscopy in a thrombin-based mouse model of stroke and fibrinolytic treatment to show that LMCs maintain cerebral autoregulation and allow for gradual reperfusion, resulting in small infarcts. In mice with poor LMCs, distal arterial segments collapse, and deleterious hyperemia causes hemorrhage and mortality after recanalization. In silico analyses confirm the relevance of LMCs for preserving perfusion in the ischemic region. Accordingly, in stroke patients with poor collaterals undergoing thrombectomy, rapid reperfusion resulted in hemorrhagic transformation and unfavorable recovery. Thus, we identify LMCs as key components regulating reperfusion and preventing futile recanalization after stroke. Future therapeutic interventions should aim to enhance collateral function, allowing for beneficial reperfusion after stroke.
Keyphrases
- cerebral ischemia
- subarachnoid hemorrhage
- brain injury
- blood brain barrier
- acute ischemic stroke
- acute myocardial infarction
- atrial fibrillation
- middle cerebral artery
- mouse model
- endovascular treatment
- high resolution
- magnetic resonance imaging
- cerebrospinal fluid
- metabolic syndrome
- computed tomography
- high throughput
- type diabetes
- magnetic resonance
- current status
- high speed
- molecular docking
- ischemia reperfusion injury
- multiple sclerosis
- white matter
- optical coherence tomography
- minimally invasive
- oxidative stress
- mass spectrometry