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. 2013 Jun;3(2):74-83.
doi: 10.1089/ther.2013.0010.

Mild hypothermia reduces tissue plasminogen activator-related hemorrhage and blood brain barrier disruption after experimental stroke

Mild hypothermia reduces tissue plasminogen activator-related hemorrhage and blood brain barrier disruption after experimental stroke

Xian Nan Tang et al. Ther Hypothermia Temp Manag. 2013 Jun.

Abstract

Therapeutic hypothermia has shown neuroprotective promise, but whether it can be used to improve outcome in stroke has yet to be determined in patients. Recombinant tissue plasminogen activator (rt-PA) is only given to a minority of patients with acute ischemic stroke, and is not without risk, namely significant brain hemorrhage.We explored whether mild hypothermia, in combination with rt-PA, influences the safety of rt-PA. Mice were subjected to middle cerebral artery occlusion (MCAO) using a filament model, followed by 24 hours reperfusion.Two paradigms were studied. In the first paradigm, cooling and rt-PA treatment began at the same time upon reperfusion, whereas in the second paradigm, cooling began soon after ischemia onset, and rt-PA began after rewarming and upon reperfusion. Experimental groups included: tPA treatment at normothermia (37°C), rt-PA treatment at hypothermia (33°C), no rt-PA at normothermia, and no rt-PA treatment at hypothermia. Infarct size, neurological deficit scores, blood brain barrier (BBB) permeability, brain hemorrhage, and expression of endogenous tissue plasminogen activator (tPA) and its inhibitor, plasminogen activator inhibitor (PAI-1) were assessed. For both paradigms, hypothermia reduced infarct size and neurological deficits compared to normothermia, regardless of whether rt-PA was given. rt-PA treatment increased brain hemorrhage and BBB disruption compared to normothermia, and this was prevented by cooling. However, mortality was higher when rt-PA and cooling were administered at the same time, beginning 1–2 hours post MCAO. Endogenous tPA expression was reduced in hypothermic mice, whereas PAI-1 levels were unchanged by cooling. In the setting of rt-PA treatment, hypothermia reduces brain hemorrhage, and BBB disruption, suggesting that combination therapy with mild hypothermia and rt-PA appears safe.

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Figures

FIG. 1.
FIG. 1.
Diagrams showing the two experimental paradigms studied. In paradigm #1, animals underwent 1 hour middle cerebral artery occlusion (MCAO) followed by recombinant tissue plasminogen activator (rt-PA) treatment and cooling (simultaneous treatment). In paradigm #2, animals underwent 3 hours MCAO and 3 hours cooling following by rt-PA treatment at normothermia (staggered treatment).
FIG. 2.
FIG. 2.
Hypothermia decreased infarct size and improves neurological deficits. (A, B) Therapeutic cooling led to smaller infarct sizes in both paradigms, regardless of whether animals were give rt-PA. (C, D) Therapeutic cooling led to improved neurological deficit scores amongst animals that received cooling in paradigm #1. Nonsignificant trends were observed in paradigm #2. Numbers of animals included in the data presented are in parentheses. *p<0.05, NN, no rt-PA/normothermia; NH, no rt-PA/hypothermia; TN, rt-PA/normothermia; TH, rt-PA/hypothermia.
FIG. 3.
FIG. 3.
Thrombolysis increased cerebral hemorrhage after MCAO, and this was decreased by hypothermia. The left side of the figure shows representative gross brain sections of animals treated with rt-PA at normothermia (T+N) and rt-PA plus hypothermia (T+H) from paradigm #2. Graphs on the right side of the figure show hemorrhage scores for each paradigm. In each paradigm, rt-PA treatment at normothermia increased brain hemorrhage, and this was reduced by cooling. *p<0.05. Color images available online at www.liebertpub.com/ther
FIG. 4.
FIG. 4.
Hypothermia decreased blood brain barrier (BBB) disruption. The left side of the figure shows representative gross brain sections of animals perfused with Evan's blue dye (EBD) to delineate regions of BBB leakage. Shown are animals treated with rt-PA at normothermia (T+N) and rt-PA plus hypothermia (T+H) from paradigm #2. The graph in the upper right corner shows high correlation between a well established spectrophotometic method of estimating BBB leakage by measuring the amount of EBD in brain lysate (X-axis) and by computing blue areas on brain sections multiplied by the section thickness (Y-axis). The graph in the bottom right corner shows volumes of EBD extravasation normalized to infarct size (paradigm #2). Rt-PA treatment at normothermia (TN) increased the extent of EBD leakage compared to no rt-PA at normothermia (NN). Combined rt-PA at hypothermia (TH) reduced EBD leakage to levels similar to the NN group (*p<0.05). Color images available online at www.liebertpub.com/ther
FIG. 5.
FIG. 5.
Endogenous expression of rt-PA and plasminogen activator inhibitor (PAI-1), effect of hypothermia. (A) Immunostains of a brain from a normothermic animal not given rt-PA (NN), 24 hours after MCAO show that the majority of cells positive for endogenous rt-PA (red) are neurons (NeuN stain, green). (B) Immunostains of endogenous tPA and its endogenous inhibitor PAI-1 (plasminogen activator inhibitor-1) are shown from a normothermic animal (37C, NN group) and hypothermic animal (33C, NH group) after MCAO. Endogenous rt-PA (left panels) is markedly decreased in the hypothermia brain, whereas PAI-1 levels are not affected by cooling (right panels). (C) Western blots of ischemic (ipsi) and contralateral nonischemic (contra) brain samples are shown for hypothermic (33C) and normothermic (37C) animals not given rt-PA. Similar to patterns shown in the immunostains, Western blots show decreased rt-PA protein, but no differences in PAI-1 by hypothermia. Quantification of the blots show decreased endogenous tPA expression with hypothermia (HT) compared to normothermia (NT) in brains exposed to MCAO. No significant differences were observed for PAI-1. *p<0.01.

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