Restoration of oscillatory shear stress in humans activates an endothelial protective genetic program and prevents DVT
Sravanthi Bandla, Matthew Nicholas Montoya Rush, Sarbani Ghosh, SreeLakshmy Suresh, Abhishek Jain, Varun Puri, John D Welsh, Mark L. Kahn, Gary Marklin, Jennifer M Leonard, Grace Martin Niziolek, Isaiah R Turnbull, Mark Houston HoofnagleDeep vein thrombosis (DVT) is a major cause of morbidity and mortality in critically ill patients. DVT clots typically form in the sinus of the deep venous valves and are strongly associated with immobility and reduced venous flow. Physical activity alters venous blood flow, generating frequent periods of recirculatory flow and oscillatory shear stress (OSS) at venous valves. Endothelial sensing of OSS stimulates expression of a potent antithrombotic endothelial phenotype within the valve sinus, but the phenotype may be lost during prolonged immobility. To test whether restoring OSS-signaling in immobile subjects could prevent thrombosis, we applied rapid cycling compression devices (RCDs) unilaterally to brain-dead organ donors (BDOD), a clinically relevant translational model of critical illness. In healthy subjects, vascular ultrasound showed that RCDs recapitulate valve sinus recirculatory flow comparable to muscular activity. Additionally, in BDOD subjects, we found that RCD treatment caused significantly more valve sinus recirculatory flow compared to currently used sequential compression devices (SCDs). In BDOD, prolonged RCD therapy increased expression of OSS-regulated genes (FoxC2, Prox1) and suppressed adhesion molecules (P-selectin, CCL2). Further, RCD treatment reduced DVT and microthrombus formation in BDOD subjects compared to standard anticoagulation alone. Randomized comparisons with SCDs revealed no systemic biomarker differences, indicating that RCD effects were localized to valve endothelium. These results extend our previous findings by identifying endothelial shear-dependent signaling in response to OSS as a critical mediator of DVT molecular pathology and establishing targeted hemodynamic modulation as a potential strategy in a novel model of human critical illness.