The value of whole-brain CT perfusion imaging combined with dynamic CT angiography in the evaluation of pial collateral circulation with middle cerebral artery occlusion

Abstract

BACKGROUND:

Middle cerebral artery (MCA) occlusion is extremely common, especially unilateral artery, which can result in a significant incidence of cerebral infarction.

OBJECTIVE:

To assess the value of whole-brain computed tomography perfusion (CTP) imaging combined with dynamic CT angiography (dCTA) in the evaluation of pial collateral circulation in patients with MCA occlusion.

METHODS:

Whole-brain CTP and dCTA images were acquired in 58 patients with unilateral MCA occlusion. All patients were divided into three groups according to the American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) collateral score (by CTA). The CTP parameters were analysed, including relative cerebral blood flow (rCBF), relative cerebral blood volume (rCBV), relative mean transit time (rMTT), and relative time to peak (rTTP). Patients were followed up with the modified Rankin scale (mRS). All cases in this study were confirmed by DSA.

RESULTS:

The CTP parameters of the MCA blood supply area on the affected side of patients with different degrees of stenosis were significantly different from those on the unaffected side. There are significant differences in the CTP parameters and openings of the Willis circle in patients with different degrees of stenosis. Significant differences were found in the number of patients with good prognosis.

CONCLUSIONS:

Whole-brain CT perfusion combined with dynamic CTA can structurally and functionally evaluate the establishment of pial collateral circulation and its effect on cerebral hemodynamic changes.

Keywords

CT perfusion dynamic CTA pial collateral circulation middle cerebral artery occlusion

1. Introduction

Ischemic cerebrovascular disease leads to high disability and mortality worldwide [1]. Intracranial vascular stenosis and occlusion are the major contributors to ischemic cerebral infarction [2, 3]. Middle cerebral artery (MCA) occlusion is extremely common, especially unilateral artery, which can result in a significant incidence of cerebral infarction [4, 5, 6].

The clinical characteristics and outcome of cerebral infarction vary strongly according to the degree of stenosis, ranging from large-scale infarction and severe sequelae to mild symptoms with a good prognosis [7, 8]. It mainly depends on the establishment of pial collateral circulation in the lesion area and the cerebral blood perfusion reserve [7, 8]. Changes in cerebral blood volume are associated with the effectiveness of collateral circulation supply [9], and good collaterals are incredibly important to improve recanalization rates [10, 11, 12, 13, 14]. Collateral vessel status is a determinant factor to predict the future hemispheric infarct area and clinical prognosis [14, 15, 16].

Digital subtraction angiography (DSA) is regarded as the criterion standard for visualizing the collateral circulation [17]. However, DSA examination is invasive, with risks including ionizing radiation exposure, iatrogenic arterial damage, as well as cerebral thromboembolism [18, 19]. Moreover, DSA is commonly used for endovascular treatment of acute stroke [20]. By comparison, cranial computed tomography angiography (CTA) has the advantages of noninvasive imaging, high spatiotemporal resolution, short scanning times, reliability and a wide availability [21]. CTA has emerged as a noninvasive alternative method to DSA, and it is often utilized in the assessment of cerebral collateral circulation [22, 23]. Single-phase CTA is only used for the visualization of cerebral circulation in the arterial phase [24], and it fails to capture the delayed collateral circulation enhancement [25]. Compared with single-phase CTA, dynamic CTA (dCTA) is a superior imaging technique for better evaluation of collateralization with high spatial and temporal resolution [26]. Dynamic CTA is derived from computed tomography perfusion (CTP) data set, and it can record the entire circulatory process as the iodine contrast agent flows from arteries to veins [17, 21]. In addition, dynamic CTA can evaluate the extent and the velocity of collateral vessel filling, which is increasingly investigated for assessment of collateral blood flow [17].

CT perfusion (CTP) technique may provide hemodynamic information of cerebral collateral circulation, by generating parametric maps of cerebral blood volume (CBV), cerebral blood flow (CBF), mean transit time (MTT), and time to peak (TTP) [27, 28]. CT-based perfusion offers advantages of a faster acquisition and wider availability [9, 29, 30]. CTP maps are more sensitive to evaluate the cerebrovascular reserve and the degree of cerebral ischemia quantitatively [28, 31]. It can successfully distinguish between hypoperfused tissue likely to infarct and ischemic tissue likely to recover [32, 33]. Moreover, with developments of imaging technique, whole-brain CT perfusion (WB-CTP) has been available, allowing clinicians to assess the whole brain perfusion status [3, 34].

WB-CTP can be combined with CTA data for evaluating collaterals efficiently and effectively [3, 35, 36]. CTP and CTA can provide the functional assessment and the anatomic assessment of collateral circulation, respectively [37]. By conducting a retrospective study, Tan et al. [30] found that the combination of CTP and CTA afforded the pretty accurate assessment of occlusion location, infarct core, salvageable ischemic brain tissue, and collaterals among patients with suspected strokes. Furthermore, virtual CT perfusion datasets can be obtained by utilizing CTA information [38].

In this study, we hypothesized that WB-CTP imaging combined with dynamic CTA may comprehensively and accurately evaluate perfusion status and vascular conditions of pial collaterals in patients with unilateral MCA occlusion. To this end, we employed WB one-stop CTP imaging combined with dynamic CTA to evaluate the establishment of pial collateral circulation and its effect on hemodynamic changes in the blood supply area after unilateral MCA occlusion to provide references for clinical treatment options and prognosis evaluation.

2. Methods

2.1 Study design and population

The retrospective study was conducted in our hospital and was approved by our institutional research review board. Informed consent is not required because of the retrospective nature of the study. Patient anonymity was preserved.

Patients with ischemic cerebral infarction were retrospectively collected as the study subjects between January 2019 and August 2020. Patients were admitted to the Department of Neurology, Neurosurgery, and Department of Intervention in our hospital. All cases in this study were confirmed by DSA. Siemens Artis Zeego robot DSA was used for DSA inspection. The modified Seldinger technique was used to perform bilateral internal carotid artery and vertebrobasilar artery conventional angiography through femoral artery puncture and catheterization under local anesthesia. Thrombolysis or thrombectomy were performed on occluded vessels during operation.

Inclusion criteria: (1) patients with cerebral infarction due to unilateral MCA occlusion in the blood supply area, with confirmation by computed tomography (CT) or magnetic resonance imaging (MRI) examination; (2) complete whole-brain CTP raw datasets were acquired within 7 days after onset; (3) unilateral MCA M1 segment occlusion confirmed by dCTA; (4) patients were followed up after discharge for 10 days, 20 days, 30 days. Exclusion criteria: (1) patients with severe stenosis or occlusion in an internal carotid artery, anterior cerebral artery (ACA), posterior cerebral artery (PCA), and vertebrobasilar artery; (2) previous massive cerebral infarction and hemorrhage with severe sequelae and disability; (3) ischemic cerebral infarction caused by cerebrovascular malformations and arteritis; (4) severely damaged heart, lung, liver, and kidney functions.

A total of 58 patients were finally enrolled, including 32 males and 26 females. The ages ranged from 55 to 86 years, with a mean (SD) age of 68.29 (7.62) years. The main clinical symptoms of patients were hemiplegia, unilateral limb weakness, movement disorder, dizziness, headache, and slurred speech.

2.2 Clinical baseline data

The score of the National Institutes of Health Stroke Scale (NIHSS) [39] and the medical history of hypertension, diabetes mellitus, hyperlipidemia, coronary heart disease were recorded at admission. The modified Rankin scale (mRS) [40, 41] was employed to evaluate the patients’ prognosis at discharge and 10 days after discharge, 20 days after discharge, 30 days after discharge (they were followed up in the outpatient clinic or by telephone). MRS $\leqslant$ 2 was regarded as a good prognosis, and mRS $>$ 2 was regarded as a poor prognosis [39, 40].

2.3 CT examination protocol

All images were obtained on GE Revolution 256-detector spiral CT scanner (GE Healthcare, Waukesha, WI, USA). All patients were received a standard scanning protocol during the presentation, including non-contrast computed tomography (NCCT), whole-brain CT perfusion, single-phase CTA, and dynamic CTA.

Patients underwent an unenhanced brain CT scan (120 kV, automatic mAs, rotation time 1.0 second, maximum pitch 0.8 mm). The CTP scan (rotation time 0.3 seconds, maximum pitch 0.5 mm, collimation 0.625 mm) was started 5 seconds after injection of 40 ml contrast agent (Iopamidol 370 mg/mL) at a flow rate of 5 ml/second, followed by a bolus of 30 ml saline at 5 ml/sec. Tube voltage and tube current were 80 kV and 150 mAs, respectively. The whole-brain CTP data were acquired with cranial-caudal coverage. One scan was acquired 1.5 seconds. 30 continuous dynamic scans were performed to obtain 30 sets of volume data. The total scan time was 60 seconds. All CTP data reconstructed with a slice thickness of 2.5 mm were converted into 5 mm thick slices. Single-phase CTA was performed from the aortic arch to the vertex using spiral CT scanning, with a 120 kV tube voltage, 150 mAs, 0.5-seconds rotation time, 0.6 mm pitch. Another 50 mL of contrast agent (Iopamidol 370 mg/mL) was injected into the cubital vein, followed by a bolus of 30 mL saline, both with a flow rate of 5 mL/second. The original slice thickness was 0.625 mm, and the reconstruction slice thickness was 1 mm. Appropriate radiation protection was provided.

Two experienced neuro-radiologists (each with $>$ 10 years of experience) were responsible for assessing the whole-brain CTP and CTA images, who were blinded to the clinical data. After reviewing the images independently, consensus judgment was determined.

2.4 CTP image postprocessing and analysis

The CTP raw data was transferred to a multimodality workstation (GE Advantage 4.7; GE Healthcare) equipped with a CT perfusion software package (GE’s Perfusion 4D Neuro, GE Healthcare) for image postprocessing. The singular value decomposition and the delay-invariant deconvolution algorithm was used to calculate cerebral perfusion parameters. In order to generate the time-density curve (TDC), the middle cerebral artery and the superior sagittal sinus were selected as the inflow artery and the outflow vein, respectively. When the contrast agent passed through the brain tissue, CBF, CBV, MTT and TTP perfusion maps were automatically created according to the time density curve (TDC) obtained. The maximum level of abnormal perfusion was selected. The radiologists manually delineated the regions of interest (ROI), avoiding large vessels, in the entire MCA blood supply area on the affected side, including the parietal lobe, the temporal lobe, the internal capsule, the thalamus as well as a portion of the frontal lobe. We calculated mean values of CBF, CBV, TTP and MTT within each of the defined ROIs. The corresponding perfusion parameters on the unaffected side (control side) were further measured by the mirroring method. By dividing the values of the affected side by the corresponding values of the unaffected side, the relative CBF (rCBF), relative CBV (rCBV), relative MTT (rMTT) and relative TTP (rTTP) were obtained (Fig. 1).

Figure 1.

A 52-year-old man with the M1 segment occlusion of the left MCA. a–d are the images selected in the CTA. a and c are the volume rendering (VR) images, b and d are the maximum intensity projection (MIPï¼‰images. The figures show the occlusion in the M1 segment of the left MCA, pial collateral compensatory vessels, few pial collateral vessel formations of the affected side before the venous phase, increases in collateral vessels in the venous and delayed phases, some delayed developments in images, moderate collateral circulation compensation, and no development of left venous sinus of the patient. The patient had a good prognosis at 10 days after discharge, 20 days after discharge, 30 days after discharge (mRS $\leqslant$ 2). e–h are CTP images with CBF, CBV, MTT, and TTP. e are CTP images with CBF, f are CTP images with CBV, g are CTP images with MTT, h are CTP images with TTP. The CBF in the MCA blood supply area on the affected side was decreased, the CBV of the central part of the lesion was decreased, the peripheral CBV was increased, MTT and TTP were prolonged, and the ROI was the whole MCA blood supply area on the affected side.

2.5 Dynamic CTA image processing and analysis

Postprocessing of CTA data was performed on a dedicated computer workstation (GE AW 4.7 workstation, GE Healthcare). The CTA image processing was made including motion correction, four-dimensional (4D) noise reduction and automated bone removal. We created the maximal intensity projection (MIP) images, multiplanar reconstruction (MPR) images, volume rendering (VR) images and shaded surface display (SSD) images. From the CTA raw datasets, we reconstructed the dynamic CTA images to analyse the blood flow in a noninvasive way. Vasculopathy and compensatory collateral blood vessels were further displayed by continuous dynamic playback and frame-by-frame display mode. The Circle of Willis was evaluated. We recorded the number of patients with anterior and posterior traffic artery openings on the affected side.

Collaterals were assessed with the CTA-based modified American Society of Interventional and Therapeutic Neuroradiology/Society of Interventional Radiology (ASITN/SIR) Collateral Flow Grading System [42]. The distal pial collateral circulation of the blood vessel with MCA occlusion was graded, and they were compared with the image of the blood vessel on the unaffected side. These grades included: 0 $=$ there was no or only very few visible pial collaterals on the ischemic site in any phase; 1 $=$ part of the collateral circulation could be seen in the ischemic site until the late venous phase; 2 $=$ part of the collateral circulation could be seen in the ischemic site before the venous phase; 3 $=$ complete collateral circulation could be seen in the ischemic site at the late venous phase; 4 $=$ complete collateral circulation of the ischemic site could be seen before the venous phase. Grade 3 to 4 were regarded as good collateral circulation (group A), grade 2 as moderate (group B), and grade 0 to 1 as poor (group C) [43].

2.6 Statistical analysis

IBM SPSS 19.0 software (SPSS, Armonk, NY, USA) was used for statistical analysis. The measurement data were tested for normality. The normally distributed variables were expressed as the means $\pm$ standard deviation ( $M\pm SD$ ). We employed the paired t-tests to compare the differences in the CTP parameters of MCA blood supply area between the affected side and unaffected side among groups A, B, and C. In addition, we analysed differences in CTP parameters (rCBF, rCBV, rMTT, rTTP) of pial collateral circulation, the number of the openings of the Willis circle, the clinical baseline data, and the prognosis in the three groups. For measurement data with homogeneity of variance, one-way analysis of variance (ANOVA) was used, and for measurement data with heterogeneity of variance, the Welch test was used. The least significant difference (LSD) test was employed for pairwise comparison, and the $\chi^{2}$ test was used for count data. $P<$ 0.05 indicates statistically significant.

3. Results

3.1 Study population

Table 1 shows the baseline characteristics and clinical information of the study population. There was significant difference in age, NIHSS score, and hypertension history at admission among the three groups ( $p<$ 0.05). There was significant difference in the history of diabetes mellitus, hyperlipidemia, coronary heart disease among the three groups ( $p>$ 0.05).

Table 1
Baseline characteristics of the study population

Characteristics	Group A ( $n=$ 19)	Group B ( $n=$ 21)	Group C ( $n=$ 18)	$F/\chi^{2}$ value	$p$ value
Age (years)	63.82 $\pm$ 6.40	68.09 $\pm$ 7.01	76.83 $\pm$ 8.22	15.546	0.000 ${}^{\ast\ast\ast}$
Admission NIHSS	2.64 $\pm$ 1.89	8.00 $\pm$ 2.19	12.01 $\pm$ 3.94	53.138	0.000 ${}^{\ast\ast\ast}$
Hypertension	11 (57.89%)	18 (85.71%)	17 (94.44%)	8.348	0.015 ${}^{\ast}$
Diabetes mellitus	8 (42.10%)	6 (28.57%)	5 (27.78%)	1.123	0.570
Hyperlipidemia	8 (42.10%)	5 (23.81%)	7 (38.89%)	1.702	0.427
Coronary heart disease	5 (26.32%)	4 (19.05%)	5 (27.78%)	0.477	0.788

${}^{\ast}p<$ 0.05; ${}^{\ast\ast\ast}p<$ 0.001. NIHSS, National Institutes of Health Stroke Scale; data are expressed as mean $\pm$ SD, and $n$ (%); SD, standard deviations.

Table 2

Comparison of prognosis measured with mRS among the three groups

Follow-up	Group A ( $n=$ 19)	Group B ( $n=$ 21)	$F/\chi^{2}$ value	$p$ value
mRS $\leqslant$ 2 at discharge	17 (89.47%)	7 (33.33%)	31.384	0.000 ${}^{\ast\ast\ast}$
mRS $\leqslant$ 2 at 10 days after discharge	17 (89.47%)	9 (42.86%)	29.971	0.000 ${}^{\ast\ast\ast}$
mRS $\leqslant$ 2 at 20 days after discharge	18 (94.73%)	9 (42.86%)	33.523	0.000 ${}^{\ast\ast\ast}$
mRS $\leqslant$ 2 at 30 days after discharge	18 (94.73%)	10 (47.62%)	33.229	0.000 ${}^{\ast\ast\ast}$

${}^{\ast\ast\ast}p<$ 0.001. mRS, modified Rankin scale; data are expressed as $n$ (%).

3.2 CTA-based pial collateral circulation grouping and prognosis

Satisfactory CTA images were obtained in all 58 patients (Fig. 1). Table 2 shows the comparison of prognosis measured with mRS at discharge and 10 days after discharge and 20 days after discharge and 30 days after discharge among three groups. Significant differences were found in the number of patients with good prognosis among the three groups ( $p<$ 0.01). The prognosis of patients in group A were significantly better than those in groups B and C. Of the 19 patients in group A, 18 had a good prognosis at discharge, and one patient with a previous history of cerebral infarction had a poor prognosis at discharge. However, the prognosis was good 10 days after discharge, 20 days after discharge, 30 days after discharge (the follow-up). Of the 21 patients in group B, 9 had a good prognosis, and 12 had a poor prognosis at discharge. At 10 days after discharge, 20 days after discharge, 30 days after discharge, symptoms had improved in most patients, 14 patients had a good prognosis, and 7 patients still had a poor prognosis. There were 18 patients in group C, of whom three had hemorrhage after infarction, and the prognosis was poor at discharge and at 10 days after discharge, 20 days after discharge, 30 days after discharge.

Table 3
Comparison of the CTP parameters between the affected side and unaffected side among the three groups

	Group A ( $n=$ 19)				Group B ( $n=$ 21)				Group C ( $n=$ 18)
	CBF	CBV	MTT	TTP	CBF	CBV	MTT	TTP	CBF	CBV	MTT	TTP
Affected side	51.12 $\pm$ 4.79	4.17 $\pm$ 0.30	5.21 $\pm$ 0.67	14.80 $\pm$ 0.78	42.29 $\pm$ 8.39	3.27 $\pm$ 0.61	6.51 $\pm$ 1.50	15.24 $\pm$ 1.98	26.78 $\pm$ 7.62	2.11 $\pm$ 039	6.84 $\pm$ 0.83	16.75 $\pm$ 3.13
Unaffected side	58.23 $\pm$ 4.72	3.25 $\pm$ 0.45	3.35 $\pm$ 0.27	10.31 $\pm$ 1.16	54.08 $\pm$ 6.68	3.34 $\pm$ 0.31	3.94 $\pm$ 0.49	11.51 $\pm$ 1.43	60.96 $\pm$ 8.20	3.19 $\pm$ 0.78	3.51 $\pm$ 0.44	11.26 $\pm$ 1.40
$t$ value	4.612	$-$ 7.422	$-$ 11.239	$-$ 13.967	5.037	0.436	$-$ 7.467	$-$ 6.997	12.957	5.227	$-$ 15.060	$-$ 6.796
$p$ value	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.666	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$	0.000 ${}^{\ast\ast\ast}$

${}^{\ast\ast\ast}p<$ 0.001. CBF, cerebral blood flow; CBV, cerebral blood volume; MTT, mean transit time; TTP, time to peak. CBF (ml $\cdot$ 100ml ${}^{-1}\cdot$ min ${}^{-1}$ ), CBV (ml/100ml), TTP (s), MTT (s); data are expressed as mean $\pm$ SD; SD, standard deviations.

3.3 Comparison of the CTP parameters between the affected side and the uninfected side among the three groups

Among all these patients with MCA occlusion, abnormal perfusion in the MCA blood supply area corresponding to clinical symptoms were visible on WB-CTP images, while the perfusion on the control side was essentially normal (Fig. 1). As shown in Table 3, in group A, the CTP parameters of the MCA blood supply area on the affected side were significantly different from those on the unaffected side, including slightly decreased CBF, slightly increased CBV, and prolonged MTT and TTP ( $p<$ 0.01). In group B, the CBF was decreased and MTT and TTP prolonged on the affected side, with statistically significant differences ( $p<$ 0.01), while the difference in CBV was not statistically significant ( $p>$ 0.05). In group C, CBF and CBV on the affected side were significantly decreased, MTT and TTP were significantly prolonged, and the differences were statistically significant ( $p<$ 0.01).

Table 4
Comparison of CTP parameters and openings of the Willis circle among the three groups

Parameter	Group A ( $n=$ 19)	Group B ( $n=$ 21)	Group C ( $n=$ 18)	$F/\chi^{2}$ value	$P$ value
rCBF	1.07 $\pm$ 0.12	0.69 $\pm$ 0.15	0.41 $\pm$ 0.10	130.878	0.000 ${}^{\ast\ast\ast}$
rCBV	1.07 $\pm$ 0.10	1.00 $\pm$ 0.11	0.50 $\pm$ 0.10	167.494	0.000 ${}^{\ast\ast\ast}$
rMTT	1.68 $\pm$ 0.31	1.78 $\pm$ 0.28	1.94 $\pm$ 0.13	4.806	0.012 ${}^{\ast}$
rTTP	1.31 $\pm$ 0.20	1.41 $\pm$ 0.09	1.47 $\pm$ 0.14	5.194	0.009 ${}^{\ast\ast}$
Opening of the Willis Circle	15 (78.95%)	14 (66.67%)	6 (33.33%)	8.587	0.014 ${}^{\ast}$

${}^{\ast}p<$ 0.05; ${}^{\ast\ast}p<$ 0.01; ${}^{\ast\ast\ast}p<$ 0.001. rCBF, relative cerebral blood flow; rCBV, relative cerebral blood volume; rMTT, relative mean transit time; rTTP, relative time to peak; CBF (ml $\cdot$ 100 ml ${}^{-1}\cdot$ min ${}^{-1}$ ), CBV (ml/100ml), TTP (s), MTT (s); data are expressed as mean $\pm$ SD, and $n$ (%); SD, standard deviations.

3.4 Comparison of CTP parameters and openings of the Willis circle among the three groups

As shown in Table 4, significant differences were found in the CTP parameters (rCBF, rCBV, rMTT, and rTTP) among the three groups (all $p<$ 0.05). The value of rCBF and rCBV in group A were significantly increased than those in group B and C (all $p<$ 0.01). On the contrary, the value of rMTT and rTTP in group C were significantly increased than those in group A and B (all $p<$ 0.05). There were 15, 14, and 6 patients with the openings of the Willis circle in groups A, B, and C, respectively. The differences in the openings of the Willis circle among the three groups were statistically significant ( $p<$ 0.05). Furthermore, the ratio of the cases with the openings of the Willis circle in groups A, B, and C decreased sequentially.

4. Discussion

The establishment of good collateral circulation can effectively improve the blood perfusion of the brain tissue in the ischemic penumbra, prolong the survival time of ischemic brain tissue, extend the treatment time window, reduce the final number and volume of lesions of cerebral infarction, and improve the patient’s prognosis [44, 45]. When MCA is severely stenosed or occluded, collateral circulation is first established between the pial vascular anastomosis and the ipsilateral ACA and PCA. Furthermore, new capillaries are formed, so that the ischemic brain tissue is compensated with different degrees of blood perfusion [46]. A comprehensive and systematic evaluation of the degree of collateral circulation compensation is of great significance to the individualized treatment options and prognostic evaluation of patients with MCA occlusion-induced cerebral infarction.

4.1 Advantages of CTA and CTP in collateral circulation evaluation

The imaging evaluation of collateral circulation is divided into structural and functional evaluations [43]. In the structural evaluation, DSA is the gold standard, but it is an invasive examination with some postoperative complications, resulting in limited clinical use [47]. CTA is still widely used in the evaluation of pial collateral circulation after MCA occlusion. CTA can record the entire process of contrast agent flowing from the arteries to veins, dynamically observe the morphology and blood flow of the whole brain, better display diseased vessels and collateral compensatory vessels, improve the accuracy of the evaluation of pial collateral circulation, and display the morphology and pathological changes in cerebral venous vessels [48, 49]. CTP is mainly used in the function evaluation [27, 28]. WB-CTP can quickly and effectively evaluate the blood perfusion and circulatory reserve in brain tissue and is of great significance in diagnosing acute cerebral infarction and ischemic penumbra [3, 34]. For patients with unilateral MCA occlusion, CTP can provide the location, scope, and extent of lesions, and it can reflect the blood perfusion produced by the pial collateral circulation and new capillaries. In addition, CTP data can be directly processed to obtain dCTA images, which avoids repeated examination and reduces radiation dose.

4.2 Application of CTA combined with CTP in collateral circulation evaluation of patients with unilateral MCA occlusion

In this study, we divided patients into three groups (A, B and C) based on the score of pial collateral circulation by CTA. We analysed the differences in perfusion parameters between the affected side and the unaffected side of each group. There were significant differences in the CTP parameters between the affected side and unaffected side in group A and C. In group A, CBF was slightly decreased, CBV was increased, and MTT and TTP were prolonged on the affected side. This finding suggests that CBV increased despite blood flow decreased slightly and perfusion delayed after MCA occlusion. Because most of the lesion area was compensated by pial collateral circulation and capillaries, and the brain tissue in the lesion area was fully perfused, reducing brain cellular damage. In group C, CBF and CBV were significantly decreased, and MTT and TTP were significantly prolonged on the affected side. It indicated a poor prognosis, if the microcirculation disorder in the lesion area was significantly worsened, the cerebral blood perfusion and collateral circulation were poorly compensated, brain cell necrosis was increased, and the risk of hemorrhage outcome was increased [50]. In group B, CBF was decreased, MTT and TTP were prolonged on the affected side, and the difference in CBV was not statistically significant, indicating that the blood flow of the patients in this group was decreased and the perfusion delayed. However, CBV on the affected side may be slightly decreased, normal or slightly increased, and there was still some CBV compensatory reserve in the lesion area. Timely and effective treatments can save more surviving brain tissue and improve clinical outcomes. In group B, the prognosis of most patients was further improved at 30 days after discharge.

For the comparison of perfusion parameters among the three groups, the differences in rCBF and rCBV among groups and the pairwise comparisons were statistically significant, and the rCBF and rCBV in groups A, B, and C decreased sequentially. Better collateral circulation compensation correlated with better cerebral blood perfusion in the lesion area, higher CBV reserve, and longer survival time of the brain tissue in the lesion area, thus reducing the final infarct volume. Worse collateral circulation compensation was correlated with lower cerebral blood perfusion in the lesion area, lower CBV reserve, higher degree of cerebral ischemia and hypoxia, and a larger scope and degree of cerebral infarction [7]. The differences in rMTT and rTTP among groups were statistically significant, and there was no statistically significant difference between groups A and B. MTT and TTP are sensitive indicators to distinguish abnormal brain tissue perfusion and can provide information on abnormal perfusion range. Therefore, this study used the pseudocolor images of TTP to determine the maximum abnormal perfusion level and outline the ROI. The compensation degree of brain tissue blood flow and the evaluation of circulatory reserve mainly depend on CBF and CBV [7, 51]. The opening of the Circle of Willis, age and the NIHSS score at admission were significantly different among the three groups, and the pairwise comparisons were also significantly different, which is consistent with previous studies [52, 53]. The opening of the Circle of Willis was positively correlated with the formation of pial collateral circulation, and the larger the age and higher the NIHSS score on admission, the poorer the compensation of pial collateral circulation. The clinical history in this study had little effect on the grouping of the pial collateral circulation, and some of them were different from previous studies [32, 54, 55]. This may be due to the small sample size and the failure to fully reflect the patient’s medical history.

4.3 Limitations of this study

There are limitations in this study. First, the study results may prone to selection bias, because this was a retrospective study. Second, only patients with unilateral MCA occlusion were considered. The situation of multivascular lesions needs further study. Third, the sample size of cases retrospectively included was relatively small, which may limit its application. Further larger prospective studies are needed to implement in future.

5. Conclusions

This study demonstrated that whole-brain one-stop CTP imaging combined with dynamic CTA can comprehensively evaluate the establishment of pial collateral circulation and blood perfusion reserve in the lesion area, for patients with unilateral middle cerebral artery occlusion. These findings facilitate the formulation of treatment plans and prognostic evaluation.

Footnotes

Conflict of interest

None to report.

Ethical approval and informed consent

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Declaration of Helsinki and its later amendments. This study was approved by the institutional research board. Informed consent was waived because of the retrospective nature of the study with pre-existing data.

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The value of whole-brain CT perfusion imaging combined with dynamic CT angiography in the evaluation of pial collateral circulation with middle cerebral artery occlusion

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

2.1 Study design and population

2.2 Clinical baseline data

2.3 CT examination protocol

2.4 CTP image postprocessing and analysis

2.6 Statistical analysis

3. Results

3.1 Study population

Table 1 Baseline characteristics of the study population

Table 3 Comparison of the CTP parameters between the affected side and unaffected side among the three groups

Table 4 Comparison of CTP parameters and openings of the Willis circle among the three groups

4. Discussion

4.1 Advantages of CTA and CTP in collateral circulation evaluation

4.2 Application of CTA combined with CTP in collateral circulation evaluation of patients with unilateral MCA occlusion

4.3 Limitations of this study

5. Conclusions

Footnotes

Conflict of interest

Ethical approval and informed consent

References

Table 1
Baseline characteristics of the study population

Table 3
Comparison of the CTP parameters between the affected side and unaffected side among the three groups

Table 4
Comparison of CTP parameters and openings of the Willis circle among the three groups