Carotid Artery Stenting and Blood–Brain Barrier Permeability in Subjects with Chronic Carotid Artery Stenosis

Abstract

Failure of the blood-brain barrier (BBB) is a critical event in the development and progression of diseases such as acute ischemic stroke, chronic ischemia or small vessels disease that affect the central nervous system. It is not known whether BBB breakdown in subjects with chronic carotid artery stenosis can be restrained with postoperative recovery of cerebral perfusion. The aim of the study was to assess the short-term effect of internal carotid artery stenting on basic perfusion parameters and permeability surface area-product (PS) in such a population. Forty subjects (23 males) with stenosis of >70% within a single internal carotid artery and neurological symptoms who underwent a carotid artery stenting procedure were investigated. Differences in the following computed tomography perfusion (CTP) parameters were compared before and after surgery: global cerebral blood flow (CBF), cerebral blood volume (CBV), mean transit time (MTT), time to peak (TTP) and PS. PS acquired by CTP is used to measure the permeability of the BBB to contrast material. In all baseline cases, the CBF and CBV values were low, while MTT and TTP were high on both the ipsi- and contralateral sides compared to reference values. PS was approximately twice the normal value. CBF was higher (+6.14%), while MTT was lower (−9.34%) on the contralateral than on the ipsilateral side. All perfusion parameters improved after stenting on both the ipsilateral (CBF +22.66%; CBV +18.98%; MTT −16.09%, TTP −7.62%) and contralateral (CBF +22.27%, CBV +19.72%, MTT −14.65%, TTP −7.46%) sides. PS decreased by almost half: ipsilateral −48.11%, contralateral −45.19%. The decline in BBB permeability was symmetrical on the ipsi- and contralateral sides to the stenosis. Augmented BBB permeability can be controlled by surgical intervention in humans.

Computed tomography indicators of cerebral microperfusion improve long term after carotid stenting in symptomatic patients

“…Consequently, carotid artery stenting effects are not only limited to CBF improvement but also encompassed in a wide range of modifications to the ischaemic status of the brain. This study confirms our earlier results demonstrating that the carotid artery stenting and subsequent reperfusion diminish the BBB permeability (Szarmach et al, 2017). In addition, we show that it has a long term effect.…”

“…In neoplasms, inflammatory/infectious states, ischaemia, and neurodegenerative diseases, the BBB is impaired, and the diffusion of fluid, blood or contrast molecules into the extravascular space is augmented (Jain et al, 2008;Topakian et al, 2010;Avsenik et al, 2015). PS was higher in the investigated sample when compared to the control subjects, indicating BBB impairment and enhanced permeability (Szarmach et al, 2017).…”

“…Several authors had reported CBF and MTT improvements in the early postinterventional phase (ranging from one day to a few weeks) after either carotid endarterectomy or stenting (Niesen et al, 2004;Gaudiello et al, 2008;Tavares et al, 2010;Ding et al, 2016;Szarmach et al, 2017). In turn, CBV assessed shortly (from one day to a few weeks) after the mentioned procedures either did not change (Matsubara et al, 2009;Tavares et al, 2010) or had increased (Kawai et al, 2014;Piñero et al, 2014;Ding et al, 2016;Szarmach et al, 2017). Only Trojanowska and others (Trojanowska et al, 2006) reported the perfusion parameter improvement in both hemispheres (CBF increase, MTT and CBV decline) that persisted 6 months after carotid artery stenting.…”

“…Our CT perfusion technique has been previously described in detail (Szarmach et al, 2016;Szarmach et al, 2017;Szarmach et al, 2018). Briefly, all CT examinations were performed with the use of the same scanner (64-MDct Light Speed VCT XT, GE Healthcare Technologies, Wisconsin, USA).…”

“…Our perfusion application offers two different models of evaluation: the "neuro brain stroke" and the "neuro brain tumour". The first mode applies the maximal slope method (Fiorella et al, 2004;Szarmach et al, 2016;Szarmach et al, 2017) for measurement of CBF, CBV, MTT or TTP, while the second one calculates microvascular permeability (PS) and the fractional blood volume based on the Johnson and Wilson model (St Lawrence & Lee, 1998a;St Lawrence & Lee, 1998b).…”