Transition to Collateral Flow After Arterial Occlusion Predisposes to Cerebral Venous Steal

Department of Anesthesiology, New York Hospital Queens, Flushing, NY, USA.
Stroke (Impact Factor: 5.72). 02/2012; 43(2):575-9. DOI: 10.1161/STROKEAHA.111.635037
Source: PubMed

ABSTRACT Stroke-related tissue pressure increase in the core and penumbra determines regional cerebral perfusion pressure (rCPP) defined as a difference between local inflow pressure and venous or tissue pressure, whichever is higher. We previously showed that venous pressure reduction below the pressure in the core causes blood flow diversion-cerebral venous steal. Now we investigated how transition to collateral circulation after complete arterial occlusion affects rCPP distribution.
We modified parallel Starling resistor model to simulate transition to collateral inflow after complete main stem occlusion. We decreased venous pressure from the arterial pressure to zero and investigated how arterial and venous pressure elevation augments rCPP.
When core pressure exceeded venous, rCPP=inflow pressure in the core. Venous pressure decrease from arterial pressure to pressure in the core caused smaller inflow pressure to drop augmenting rCPP. Further drop of venous pressure decreased rCPP in the core but augmented rCPP in penumbra. After transition to collateral circulation, lowering venous pressure below pressure in the penumbra further decreased rCPP and collaterals themselves became a pathway for steal. Venous pressure level at which rCPP in the core becomes zero we termed the "point of no reflow." Transition from direct to collateral circulation resulted in decreased inflow pressure, decreased rCPP, and a shift of point of no reflow to higher venous loading values. Arterial pressure augmentation increased rCPP, but only after venous pressure exceeded point of no reflow.
In the presence of tissue pressure gradients, transition to collateral flow predisposes to venous steal (collateral failure), which may be reversed by venous pressure augmentation.

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Available from: Osvaldas Pranevicius, Sep 28, 2015
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    • "In the large multicenter Warfarin-Aspirin Symptomatic Intracranial Disease trial, in subjects with stenoses of 70% to 99% the presence of more extensive collaterals lowered the risk of subsequent territorial stroke by B4-to 6-fold (Liebeskind et al, 2011). While collateral perfusion beyond an occlusion aids recanalization (Liebeskind, 2009a), it is nonetheless the case that revascularization strategies designed to open an occluded artery (i.e., recanalization ) may not necessarily result in effective parenchymal reperfusion (Liebeskind, 2010a) owing to the presence of resistance to downstream flow mediated by microcirculatory obstruction, endothelial injury (Barber et al, 2004), or dynamic changes in the venous circulation (Pranevicius et al, 2012). Although recanalization of occluded vessels in stroke patients leads to higher CT-perfusion indices of reperfusion (e.g., cerebral blood volume and mean transit time), even in patients without recanalization those with good collateral flow have higher reperfusion indices than those with poor collateral flow (Soares et al, 2010). "
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    ABSTRACT: Recent human imaging studies indicate that reduced blood flow through pial collateral vessels (‘collateral failure’) is associated with late infarct expansion despite stable arterial occlusion. The cause for ‘collateral failure’ is unknown. We recently showed that intracranial pressure (ICP) rises dramatically but transiently 24 hours after even minor experimental stroke. We hypothesized that ICP elevation would reduce collateral blood flow. First, we investigated the regulation of flow through collateral vessels and the penetrating arterioles arising from them during stroke reperfusion. Wistar rats were subjected to intraluminal middle cerebral artery (MCA) occlusion (MCAo). Individual pial collateral and associated penetrating arteriole blood flow was quantified using fluorescent microspheres. Baseline bidirectional flow changed to MCA-directed flow and increased by 450% immediately after MCAo. Collateral diameter changed minimally. Second, we determined the effect of ICP elevation on collateral and watershed penetrating arteriole flow. Intracranial pressure was artificially raised in stepwise increments during MCAo. The ICP increase was strongly correlated with collateral and penetrating arteriole flow reductions. Changes in collateral flow post-stroke appear to be primarily driven by the pressure drop across the collateral vessel, not vessel diameter. The ICP elevation reduces cerebral perfusion pressure and collateral flow, and is the possible explanation for ‘collateral failure’ in stroke-in-progression.
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