Hypoxemia increases blood-brain barrier permeability during extreme apnea in humans

Author:

Bailey Damian M1ORCID,Bain Anthony R2,Hoiland Ryan L34,Barak Otto F56,Drvis Ivan7,Hirtz Christophe8,Lehmann Sylvain8,Marchi Nicola9,Janigro Damir1011,MacLeod David B12,Ainslie Philip N113,Dujic Zeljko5

Affiliation:

1. Neurovascular Research Laboratory, Faculty of Life Sciences and Education, University of South Wales, University of South Wales, Glamorgan, UK

2. Faculty of Human Kinetics, University of Windsor, Windsor, ON, Canada

3. Department of Anaesthesiology, Pharmacology and Therapeutics, Vancouver General Hospital, University of British Columbia, Vancouver, BC, Canada

4. Department of Cellular and Physiological Sciences, Faculty of Medicine, University of British Columbia, Vancouver, BC, Canada

5. School of Medicine, University of Split, Split, Croatia

6. Faculty of Medicine, University of Novi Sad, Serbia

7. School of Kinesiology, University of Zagreb, Zagreb, Croatia

8. LBPC-PPC, University of Montpellier, Institute of Regenerative Medicine-Biotherapy IRMB, Centre Hospitalier Universitaire de Montpellier, INSERM, Montpellier, France

9. Institute of Functional Genomics, University of Montpellier, Montpellier, France

10. Department of Physiology, Case Western Reserve University, Cleveland, OH, USA

11. FloTBI, Cleveland, OH, USA

12. Department of Anesthesiology, Duke University Medical Center, Durham, NC, USA

13. Center for Heart Lung and Vascular Health, University of British Columbia, Kelowna, British Columbia, Canada

Abstract

Voluntary asphyxia imposed by static apnea challenges blood-brain barrier (BBB) integrity in humans through transient extremes of hypertension, hypoxemia and hypercapnia. In the present study, ten ultra-elite breath-hold divers performed two maximal dry apneas preceded by normoxic normoventilation (NX: severe hypoxemia and hypercapnia) and hyperoxic hyperventilation (HX: absence of hypoxemia with exacerbating hypercapnia) with measurements obtained before and immediately after apnea. Transcerebral exchange of NVU proteins (ELISA, Single Molecule Array) were calculated as the product of global cerebral blood flow (gCBF, duplex ultrasound) and radial arterial to internal jugular venous concentration gradients. Apnea duration increased from 5 m 6 s in NX to 15 m 59 s in HX ( P = <0.001) resulting in marked elevations in gCBF and venous S100B, glial fibrillary acidic protein, ubiquitin carboxy-terminal hydrolase-L1 and total tau (all P < 0.05 vs. baseline). This culminated in net cerebral output reflecting mildly increased BBB permeability and increased neuronal-gliovascular reactivity that was more pronounced in NX due to more severe systemic and intracranial hypertension ( P < 0.05 vs. HX). These findings identify the hemodynamic stress to which the apneic brain is exposed, highlighting the critical contribution of hypoxemia and not just hypercapnia to BBB disruption.

Publisher

SAGE Publications

Subject

Cardiology and Cardiovascular Medicine,Neurology (clinical),Neurology

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