Combined Perfusion and Permeability Imaging Reveals Different Pathophysiologic Tissue Responses After Successful Thrombectomy

Abstract

Despite successful recanalization of large-vessel occlusions in acute ischemic stroke, individual patients profit to a varying degree. Dynamic susceptibility-weighted perfusion and dynamic T1-weighted contrast-enhanced blood-brain barrier permeability imaging may help to determine secondary stroke injury and predict clinical outcome. We prospectively performed perfusion and permeability imaging in 38 patients within 24 h after successful mechanical thrombectomy of an occlusion of the middle cerebral artery M1 segment. Perfusion alterations were evaluated on cerebral blood flow maps, blood-brain barrier disruption (BBBD) visually and quantitatively on ktrans maps and hemorrhagic transformation on susceptibility-weighted images. Visual BBBD within the DWI lesion corresponded to a median ktrans elevation (IQR) of 0.77 (0.41–1.4) min−1 and was found in all 7 cases of hypoperfusion (100%), in 10 of 16 cases of hyperperfusion (63%), and in only three of 13 cases with unaffected perfusion (23%). BBBD was significantly associated with hemorrhagic transformation (p < 0.001). While BBBD alone was not a predictor of clinical outcome at 3 months (positive predictive value (PPV) = 0.8 [0.56–0.94]), hypoperfusion occurred more often in patients with unfavorable clinical outcome (PPV = 0.43 [0.10–0.82]) compared to hyperperfusion (PPV = 0.93 [0.68–1.0]) or unaffected perfusion (PPV = 1.0 [0.75–1.0]). We show that combined perfusion and permeability imaging reveals distinct infarct signatures after recanalization, indicating the severity of prior ischemic damage. It assists in predicting clinical outcome and may identify patients at risk of stroke progression.

Post‐stroke blood–brain barrier disruption predicts poor outcome in patients enrolled in the ACTION study

“…BBPI has previously been applied retrospectively to clinical trial data looking at acute stroke treatments; 10 however, this is the first time it has been applied to a dataset from a clinical trial aimed at treating post-stroke inflammation. Prior studies have found post-stroke hypoperfusion to be associated with poor functional outcome, 14 as it was in our study; however, in the current study, BBB disruption was associated with outcome independent of the degree of reperfusion. BBB imaging when used in early time windows has been used to assess the risk of hemorrhagic transformation.…”

Seizures and epilepsy in patients with ischaemic stroke

“…Using MRI techniques, the occurrence of BBB disruption in acute ischaemic stroke has been increasingly investigated, particularly with regard to associated demographic and clinical factors, the impact of reperfusion therapies, and the prognostic relevance of BBB dysfunction for predicting haemorrhagic transformation and clinical outcomes after stroke [101]. For the assessment of BBB disruption in the setting of acute stroke, perfusionweighted imaging (PWI) is a particularly useful technique that can easily be incorporated into a standardised stroke imaging protocol and has been widely used [102][103][104][105]. The PWI approach that has traditionally been applied to the investigation of pathological changes in BBB permeability is dynamic contrast-enhanced imaging (DCE, often referred to as permeability imaging) and considers differences in the pre-and post-contrast T1-weighted images [102].…”

“…For the assessment of BBB disruption in the setting of acute stroke, perfusionweighted imaging (PWI) is a particularly useful technique that can easily be incorporated into a standardised stroke imaging protocol and has been widely used [102][103][104][105]. The PWI approach that has traditionally been applied to the investigation of pathological changes in BBB permeability is dynamic contrast-enhanced imaging (DCE, often referred to as permeability imaging) and considers differences in the pre-and post-contrast T1-weighted images [102]. However, bolus-tracking dynamic susceptibility contrast imaging (DSC), which is included in standardised clinical stroke imaging protocols for the assessment of tissue-at-risk and therapeutic decision-making at many stroke centres [106], can also be employed to investigate BBB damage in acute stroke [105,107], as the echoplanar imaging (EPI) sequences employed for DSC feature a mild T1-weighting in addition to being predominantly T2*-weighted [103,105].…”

“…However, patients exhibiting a cerebral perfusion deficit, such as in acute stroke, require an arrival time correction for DSC-based permeability imaging to control for altered blood flow effects before calculating the permeability signal [103,105]. Both the DCE-PWI and delay-corrected DSC-PWI techniques to assess BBB permeability have successfully been applied successfully to investigate pre-and post-treatment BBB leakage in previous studies, which demonstrated associations between BBB disruption and haemorrhagic transformation, parenchymal haemorrhage, and unfavourable clinical outcomes [102,104,105,107,108] (Fig. 4).…”

“…4). Furthermore, a high magnitude of BBB disruption correlates with the degree of hypoperfusion and is associated with poor collateral flow [102], whereas a favourable penumbral profile that predicts a favourable clinical outcome is associated with reduced BBB disruption [108]. As the clinical stroke severity influences the PSE risk, this suggests a link between BBB disruption and PSE.…”