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Spatiotemporal correlations between blood-brain barrier permeability and apparent diffusion coefficient in a rat model of ischemic stroke.

Taheri S, Candelario-Jalil E, Estrada EY, Rosenberg GA - PLoS ONE (2009)

Bottom Line: We found significant increases in BBB leakage and reduction in ADC values between 3 and 48 h of reperfusion.We observed a pattern of lesion evolution where the extent of initial ischemic injury reflected by ADC abnormalities determines vascular integrity.Our results suggest that regions with vasogenic edema alone are not likely to develop low ADC by 48 h and may undergo recovery.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of New Mexico, Health Sciences Center, Albuquerque, NM, USA.

ABSTRACT
Variations in apparent diffusion coefficient of water (ADC) and blood-brain barrier (BBB) permeability after ischemia have been suggested, though the correlation between ADC alterations and BBB opening remains to be studied. We hypothesized that there are correlations between the alteration of ADC and BBB permeability. Rats were subjected to 2 h of transient middle cerebral artery occlusion and studied at 3 and 48 h of reperfusion, which are crucial times of BBB opening. BBB permeability and ADC values were measured by dynamic contrast-enhanced MRI and diffusion-weighted imaging, respectively. Temporal and spatial analyses of the evolution of BBB permeability and ADC alteration in cortical and subcortical regions were conducted along with the correlation between ADC and BBB permeability data. We found significant increases in BBB leakage and reduction in ADC values between 3 and 48 h of reperfusion. We identified three MR tissue signature models: high K(i) and low ADC, high K(i) and normal ADC, and normal K(i) and low ADC. Over time, areas with normal K(i) and low ADC transformed into areas with high K(i). We observed a pattern of lesion evolution where the extent of initial ischemic injury reflected by ADC abnormalities determines vascular integrity. Our results suggest that regions with vasogenic edema alone are not likely to develop low ADC by 48 h and may undergo recovery.

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Cumulative spatiotemporal distribution of BBB permeability for cerebral cortex and subcortex (Panels A and B).Statistical analysis of raw data presented in A and B was performed by calculating the area of leakage for each brain region with Ki values higher than 0.001 ml/g-min. As shown in panel C and D, BBB permeability changes at 48 h were significantly higher than at 3 h. The vertical axis shows the frequency of pixels with different Ki values (shown in the horizontal axis).
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pone-0006597-g002: Cumulative spatiotemporal distribution of BBB permeability for cerebral cortex and subcortex (Panels A and B).Statistical analysis of raw data presented in A and B was performed by calculating the area of leakage for each brain region with Ki values higher than 0.001 ml/g-min. As shown in panel C and D, BBB permeability changes at 48 h were significantly higher than at 3 h. The vertical axis shows the frequency of pixels with different Ki values (shown in the horizontal axis).

Mentions: The spatiotemporal distribution of BBB permeability for cerebral cortex and subcortical areas is presented in Fig. 2. The BBB permeability at 3 h of reperfusion is not as high as the permeability at 48 h for both cerebral cortex and subcortical areas, as shown by the area under the curve (Fig. 2A and 2B). There was a marked increase in the percentage of pixels with Ki higher than 0.001 ml/g-min between 3 and 48 h of recirculation (24.5% at 3 h vs. 68.4% at 48 h for cerebral cortex, p<0.0001, χ2 test; and 17% at 3 h vs. 64.2% at 48 h for the subcortical regions, p<0.0001, χ2 test). In a rat model of focal cerebral ischemia, it has been previously shown that Ki values higher than 0.001 ml/g-min are abnormal [27]. We calculated the area of leakage by multiplying the number of pixels with Ki values higher than 0.001 ml/g-min by the pixel size. Quantitative data shown in Fig. 2C indicate that there is a statistically significant (p<0.01) increase in the area of leakage in the ipsilateral cortex and subcortex between 3 and 48 h of reperfusion. For each brain region, we calculated the median of Ki values for ipsilateral (stroke) and contralateral side and found a significant increase in the BBB permeability values between the ischemic and contralateral side at a given time point (Fig. 2D). However, a significant increase (p<0.03) in the Ki values was only found for the subcortex between 3 and 48 h of reperfusion. There was a trend toward an increase in the Ki values at 48 h with respect to 3 h in the cerebral cortex, but this increase did not reach statistical significance (Fig. 2D).


Spatiotemporal correlations between blood-brain barrier permeability and apparent diffusion coefficient in a rat model of ischemic stroke.

Taheri S, Candelario-Jalil E, Estrada EY, Rosenberg GA - PLoS ONE (2009)

Cumulative spatiotemporal distribution of BBB permeability for cerebral cortex and subcortex (Panels A and B).Statistical analysis of raw data presented in A and B was performed by calculating the area of leakage for each brain region with Ki values higher than 0.001 ml/g-min. As shown in panel C and D, BBB permeability changes at 48 h were significantly higher than at 3 h. The vertical axis shows the frequency of pixels with different Ki values (shown in the horizontal axis).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2719093&req=5

pone-0006597-g002: Cumulative spatiotemporal distribution of BBB permeability for cerebral cortex and subcortex (Panels A and B).Statistical analysis of raw data presented in A and B was performed by calculating the area of leakage for each brain region with Ki values higher than 0.001 ml/g-min. As shown in panel C and D, BBB permeability changes at 48 h were significantly higher than at 3 h. The vertical axis shows the frequency of pixels with different Ki values (shown in the horizontal axis).
Mentions: The spatiotemporal distribution of BBB permeability for cerebral cortex and subcortical areas is presented in Fig. 2. The BBB permeability at 3 h of reperfusion is not as high as the permeability at 48 h for both cerebral cortex and subcortical areas, as shown by the area under the curve (Fig. 2A and 2B). There was a marked increase in the percentage of pixels with Ki higher than 0.001 ml/g-min between 3 and 48 h of recirculation (24.5% at 3 h vs. 68.4% at 48 h for cerebral cortex, p<0.0001, χ2 test; and 17% at 3 h vs. 64.2% at 48 h for the subcortical regions, p<0.0001, χ2 test). In a rat model of focal cerebral ischemia, it has been previously shown that Ki values higher than 0.001 ml/g-min are abnormal [27]. We calculated the area of leakage by multiplying the number of pixels with Ki values higher than 0.001 ml/g-min by the pixel size. Quantitative data shown in Fig. 2C indicate that there is a statistically significant (p<0.01) increase in the area of leakage in the ipsilateral cortex and subcortex between 3 and 48 h of reperfusion. For each brain region, we calculated the median of Ki values for ipsilateral (stroke) and contralateral side and found a significant increase in the BBB permeability values between the ischemic and contralateral side at a given time point (Fig. 2D). However, a significant increase (p<0.03) in the Ki values was only found for the subcortex between 3 and 48 h of reperfusion. There was a trend toward an increase in the Ki values at 48 h with respect to 3 h in the cerebral cortex, but this increase did not reach statistical significance (Fig. 2D).

Bottom Line: We found significant increases in BBB leakage and reduction in ADC values between 3 and 48 h of reperfusion.We observed a pattern of lesion evolution where the extent of initial ischemic injury reflected by ADC abnormalities determines vascular integrity.Our results suggest that regions with vasogenic edema alone are not likely to develop low ADC by 48 h and may undergo recovery.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of New Mexico, Health Sciences Center, Albuquerque, NM, USA.

ABSTRACT
Variations in apparent diffusion coefficient of water (ADC) and blood-brain barrier (BBB) permeability after ischemia have been suggested, though the correlation between ADC alterations and BBB opening remains to be studied. We hypothesized that there are correlations between the alteration of ADC and BBB permeability. Rats were subjected to 2 h of transient middle cerebral artery occlusion and studied at 3 and 48 h of reperfusion, which are crucial times of BBB opening. BBB permeability and ADC values were measured by dynamic contrast-enhanced MRI and diffusion-weighted imaging, respectively. Temporal and spatial analyses of the evolution of BBB permeability and ADC alteration in cortical and subcortical regions were conducted along with the correlation between ADC and BBB permeability data. We found significant increases in BBB leakage and reduction in ADC values between 3 and 48 h of reperfusion. We identified three MR tissue signature models: high K(i) and low ADC, high K(i) and normal ADC, and normal K(i) and low ADC. Over time, areas with normal K(i) and low ADC transformed into areas with high K(i). We observed a pattern of lesion evolution where the extent of initial ischemic injury reflected by ADC abnormalities determines vascular integrity. Our results suggest that regions with vasogenic edema alone are not likely to develop low ADC by 48 h and may undergo recovery.

Show MeSH
Related in: MedlinePlus