Evaluating intracranial artery dissection by using three-dimensional simultaneous non-contrast angiography and intra-plaque hemorrhage high-resolution magnetic resonance imaging: a retrospective study

Abstract

Background

There was no previous report on the three-dimensional simultaneous non-contrast angiography and intra-plaque hemorrhage (3D-SNAP) magnetic resonance imaging (MRI) sequence to diagnose intracranial artery dissection (IAD).

Purpose

To improve the diagnostic accuracy and guide the clinical treatment for IAD by elucidating its pathological features using 3D-SNAP MRI.

Material and Methods

From January 2015 to September 2018, 113 patients with suspected IAD were analyzed. They were divided into IAD and non-IAD groups according to the spontaneous coronary artery dissection (SCAD) criteria. All patients underwent 3D-SNAP, 3D-TOF, T2W imaging, 3D-PD, 3D-T1W-VISTA, and 3D-T1WCE) using 3.0-T MRI; clinical data were collected. The IAD imaging findings (intramural hematoma, double lumen, intimal flap, aneurysmal dilatation, stenosis, or occlusion) in every sequence were analyzed. Receiver operating characteristic (ROC) curve analysis was used to evaluate the diagnostic efficiency of each sequence.

Results

There was a significant difference in the probability of intramural hematoma, relative signal intensity of intramural hematoma, double lumen, stenosis, or occlusion signs on 3D-TOF, T2W, 3D-PD, 3D-T1W-VISTA, 3D-SNAP, and 3D-T1WCE sequences (P<0.05). The 3D-SNAP and 3D-T1WCE sequences were most sensitive for diagnosing intramural hematoma and displaying double-lumen signs, respectively. The diagnostic efficiency of the 3D-SNAP sequence combined with 3D-T1WCE was the highest (area under the curve [AUC] 0.966). The AUC value of the 3D-SNAP sequence (AUC 0.897) was slightly inferior to that of 3D-T1W enhancement (AUC 0.903).

Conclusion

3D-SNAP MRI is a non-invasive and effective method and had the greatest potential among those methods tested for improving the diagnostic accuracy for IAD.

Keywords

Intracranial artery dissection three-dimensional simultaneous non-contrast angiography and intra-plaque hemorrhage magnetic resonance imaging

Introduction

Intracranial artery dissection (IAD) is a condition whereby blood enters the vascular wall through the damaged endothelium of the intracranial artery, forming a true and false lumen in the vascular wall or spontaneous hematoma in the intracranial artery wall, and resulting in vascular stenosis, occlusion, or rupture (1). The incidence of IAD is approximately 1–1.5 per 100,000, which may lead to significant arterial stenosis, occlusion, pseudoaneurysm formation with subsequent hemodynamic, embolic infarction, and subarachnoid hemorrhage (2). IAD is a major cause for stroke in young and middle-aged people and often leads to the serious complications of ischemia and hemorrhage, accounting for 10%–25% of all strokes in young and middle-aged people (3,4). Neurological complications occur in over 80% of IAD cases in the first two weeks after the onset of clinical presentation (5,6). Therefore, an early and reliable diagnosis is important for performing early anticoagulation or antithrombotic treatment and reducing the risk of neurological complications.

IAD is typically diagnosed based on angiography findings including a double lumen, intramural hematoma, intimal flap, secondary artery dilatation, and pearl or string signs. A meta-analysis of 91 articles compared the performance of magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), and computed tomography angiography (CTA) with digital subtraction angiography (DSA) for the detection of carotid and vertebral artery dissection and found that the sensitivity and specificity of CTA and MRA were fairly similar for diagnosing IAD (7). At present, intraluminal imaging (DSA, CTA, and MRA) cannot reveal the direct signs of IAD clearly enough, and the detection rate is only 32%–50% (8). Although conventional lumen imaging (CTA, MRA, and DSA) can sensitively display the lumen of blood vessels, a limitation of these modalities is that they cannot differentiate pathological changes in vessel walls in IAD, because different pathologies may exhibit similar luminal presentation on conventional lumen imaging methods. Hence, IAD is apt to missed or misdiagnosed by conventional lumen imaging.

High-resolution MRI (HR-MRI) can offer excellent visualization of the arterial wall and lumen, thus enabling the determination of the direct and indirect imaging findings of IAD. Wang et al. (9) reported that HR-MRI could display 61% of intramural hematoma, 50% of double-lumen sign, and 42% of intimal flap; however, the methodology is not sensitive enough to display intramural hematoma except for that in the subacute phase. Although susceptibility-weighted imaging (SWI) is a sensitive method for the diagnosis of intramural hematoma in IAD, the data obtained for the wall and lumen could not be distinguished adequately due to magnetic sensitive artifacts and slow blood flow, thus reducing the detection rate of IAD on SWI (10,11). High-resolution simultaneous non-contrast angiography and intra-plaque hemorrhage (SNAP) is a new technology that can simultaneously display the lumen, vessel wall, and intra-plaque hemorrhage (IPH) in a single acquisition due to suppression of blood flow signals (12). This technique has been widely used to assess IPH, plaque composition, and stenosis in cervical and intracranial atherosclerotic plaques (13,14). However, so far, few studies have evaluated intramural hematoma, double-lumen sign, intimal flap, and the indirect signs of IAD by using SNAP.

Thus, the aim of the present study was to apply 3D-SNAP to evaluate the direct and indirect signs of IAD. It was first application for the diagnosis of IAD. Furthermore, we compared the detection rate of IAD signs and diagnostic effectiveness for IAD between 3D-SNAP and other HR-MRI sequences to verify our hypothesis that 3D-SNAP can afford a good contrast among the true and false lumen, intramural hematoma, intimal flap, and secondary vessel change in IAD.

Material and Methods

Patients

The study was approved by the local Institutional Review Board. An informed consent form was signed by all participants. From January 2015 to September 2018, patients with suspected IAD in the Department of Neurology, Shaanxi Provincial People's Hospital, were evaluated. The patient inclusion criteria were as follows (15,16): (i) patients with neurological symptoms, such as dizziness, headache, ataxia, sensory and motor disorders, transient ischemic attack, and ischemic stroke; and (ii) patients with suspected IAD who had undergone DSA or CTA. The exclusion criteria were as follows: (i) poor image quality that could not be evaluated; (ii) a history of cerebral trauma and brain tumors; (iii) vasculitis and vascular malformations; and (iv) intracavitary treatment. A senior neurologist (JLG) made a definite diagnosis of IAD by imaging findings and clinical data, which required the following conditions (17): (i) any pathognomonic signs of dissection (double lumen, intimal flap, intramural hematoma, and intramural hematoma) were identified on CTA, DSA, MRA, or HR-MRI; (ii) patients with typical clinical symptoms (headache, neck pain, ischemia, subarachnoid hemorrhage, compression symptoms, etc.) or the possible pathological features of IAD disappeared after follow-up. The cases were divided into dissection and non-dissection groups. The patients underwent multiparameter HR-MRI including 3D time-of-flight (3D-TOF), T2-weighted (T2W) imaging, 3D-proton density (3D-PD), 3D-T1-weighted volumetric isotropic turbo spin-echo acquisition (3D-T1W-VISTA), and 3D-contrast-enhanced T1W imaging (3D-T1WCE), and 3D-SNAP within one week of DSA or CTA examination.

MRI protocol

MRI was performed with the patients in the supine position and a 16-channel head-neck coil was used with a Philips Ingenia 3.0-T MRI scanner (Ingenia, Philips Medical Systems, Best, The Netherlands). The HR-MRI protocols included 3D-SNAP, TOF-MRA, 3D-PD, 3D-T1W-VISTA, T2W imaging, and 3D-T1WCE imaging with perpendicular planes to the arterial course. T1WCE was performed following intravenous administration of gadoterate meglumine at a dose of 0.1 mmol/kg. The scan parameters for 3D-SNAP were as follows: TR/TE = 10/5 ms; field of view (FOV) = 200 × 170 mm²; acquisition matrix = 400 × 340; image resolution = 0.5 × 0.5 × 0.5 mm³; acceleration factor = 2; and slice thickness = 0.5 mm (no gap). The spatial resolution for other HR-MRI sequences were unified with 3D-SNAP. The total acquisition time was approximately 30 min.

Image postprocessing and analysis

All raw data were imported into a Philips MR WorkSpace postprocessing workstation to generate axial, coronal, and sagittal views, minimum density projection, and curved planar reconstruction to observe the imaging characteristics of IAD. Before analyzing 3D-SNAP and other multi-parameter HR-MRI (3D-T1WCE, 3D-T1W-VISTA, 3D-PD, TOF-MRA and T2W imaging) data, experienced neuroradiologists (XZ and LCL, with five years of experience in HR-MRI of the arterial wall) were trained to observe the direct and indirect signs of IAD. A double-blind observation of the direct and indirect features of IAD was performed on multiparameter HR images in the IAD and non-IAD groups. The characteristics of direct signs were defined as follows. The intimal flap sign was defined as a visible linear signal crossing the arterial lumen and extending to the artery side wall on any serial image (8). The double-lumen sign was defined as true and false lumens with different flow velocities in the lumen of the artery (18). Intramural hematoma was defined as intramural filling of hematoma signal without vascular flow (19). The relative signal intensity of intramural hematoma was 1.3 times higher than that for the normal brainstem or temporal lobe on the same level on fat-suppression T1W imaging or PD or SNAP sequences (20,21). The indirect signs were defined as follows. Aneurysmal dilatation was defined as a visual increase of 1.5 times in the diameter relative to the adjacent normal vessel diameter (22). The pearl and string sign was defined as eccentric aneurysmal dilatation accompanied by proximal and distal vascular lumen stenosis (23). The direct and indirect signs of suspected IAD were observed separately by two experienced neuroradiologists on 3D-SNAP and HR imaging scans, who were blinded to the clinical information. The detection rate and diagnostic efficiency of direct and indirect signs of IAD were compared on 3D-SNAP and HR imaging scans. When the evaluations of IAD signs was inconsistent between the two experienced neuroradiologists, a senior neuroimaging doctor (XLZ) made the final decision.

Statistical analysis

All data were analyzed using SPSS version 22.0 (IBM, Armonk, NY, USA). The counting data were expressed as number (%), and quantitative data were expressed as mean ± standard deviation. The basic clinical data and imaging features of each sequence in the IAD and non-IAD groups were compared using the chi-square test, exact probability method, ANOVA, and independent-sample t-test according to different conditions. Kappa analysis was used to evaluate the consistency between the observation results of the two physicians (Kappa value > 0.75 was considered an indicator of high consistency). The effectiveness of 3D-SNAP, TOF-MRA, T2W imaging, 3D-PD, 3D-T1W-VISTA, and 3D-T1WCE in identifying the signs diagnosis of IAD were evaluated by receiver operating characteristic (ROC) curve analysis. All tests were two-tailed, and P < 0.05 was considered statistically significant.

Results

Clinical data

The present study enrolled 113 patients who were divided into the dissection (n = 38) and non-dissection (n = 75) groups. The clinical data of the IAD and non-IAD groups are presented in Table 2. The main clinical symptoms of patients with dissection of arteries were headache and neck pain, dizziness, weakness, ataxia, transient ischemic attack, and ischemic stroke. Eleven cases involved dissection of the intracranial segment of the internal carotid artery, two involved middle cerebral artery dissection, nine involved vertebral artery dissection, and 16 involved basilar artery dissection. Seven cases of arterial dissection were initially diagnosed on DSA (three cases showed the pearl-and-string sign, while four cases showed a double-lumen sign with an intimal flap), 14 cases of arterial dissection were initially diagnosed on CTA (double lumen, intramural hematoma, intimal flap), and 17 cases of dissection were diagnosed after follow-up CTA reexamination. The non-dissection group included 67 cases of intracranial atherosclerosis and eight cases with an intracranial aneurysm, and the main clinical symptoms of 67 patients were dizziness, headache, transient ischemic attack, sensory or motor disorders, and ischemic stroke.

Table 1.

Clinical data in the intracranial artery dissection (IAD) group and the non-IAD group.

Groups	IAD (n = 38)	Non-IAD (n = 75)	P value
Age (years)	37.4 ± 14.6	55.8 ± 9.5	<0.001
Sex (M/F)	22/16	33/42	0.163
Headache and neck pain (yes/no)	11/27	8/67	0.014
Ataxia (yes/no)	6/32	13/62	0.836
Subarachnoid hemorrhage (yes/no)	4/34	12/63	0.572
Systolic pressure (mmHg)	122.5 ± 28.9	137.1 ± 42.4	0.44
Diastolic pressure (mmHg)	79.2 ± 22.3	88.6 ± 35.8	0.27
Diabetes	6/15.8	17/22.7	0.391
Smoking	7/18.4	11/14.7	0.606
Interval time from onset to examination (h)	161.0 ± 42.4	122.5 ± 53.3	<0.01

Values are given as n or mean ± SD.

Table 2.

Comparison of the IAD findings among all HR-MRI sequences.

Signs/Sequences	TOF-MRA	T2W	3D-PD	3D-T1-VISTA	3D-SNAP	T1WCE	P value
Intramural hematoma	14 (36.8)	5 (15.2)	7 (22.6)	15 (39.5)	18 (47.4)	12 (31.6)	0.01
Intramural hematoma relative signal intensity	1.45 ± 0.43	0.75 ± 0.27	0.99 ± 0.26	1.62 ± 0.47	1.88 ± 0.28	1.56 ± 0.31	0.01
Double lumen	14 (36.8)	7 (18.4)	16 (42.1)	15 (39.5)	20 (52.6)	25 (65.8)	0.013
Intimal flap	10 (26.3)	11 (28.9)	18 (47.4)	17 (44.7)	16 (42.1)	21 (55.3)	0.083
Aneurysmal	15 (39.5)	20 (52.6)	25 (65.8)	22 (57.9)	18 (47.4)	24 (63.2)	0.111
Stenosis or occlusion	11 (28.9)	16 (42.1)	25 (65.8)	24 (63.2)	22 (57.9)	20 (52.6)	0.011

Values are given as n (%) or mean ± SD.

3D, three-dimensional; IAD, intracranial artery dissection; MRA, magnetic resonance angiography; PD, proton density; SNAP, simultaneous non-contrast angiography and intra-plaque; T1WCE, contrast-enhanced T1-weighted; T2W, T2-weighted; TOF, time of flight.

Inter-observer consistency

The inter-observer agreement of two senior doctors was evaluated for all direct signs (double-lumen sign, intramural hematoma, intimal flap) and indirect signs of IAD (aneurysmal dilatation, stenosis, or occlusion) in 3D-SNAP and other multiparameter HR-MRI. The Kappa values were as follows: K_{double lumen} = 0.892; K_{intramural hematoma} = 0.923; K_{intimal flap} = 0.931; and K_{indirect sign} = 0.955, suggesting substantial agreement between the two observers.

Characteristics and detection rates of direct signs of IAD on 3D-SNAP MRI and other multiparameter HR-MRI

In the majority of cases, the true lumen showed a low signal and was small, while the pseudolumen was large on all the sequences (Fig. 1). Intramural hematoma (n = 18) in the acute and subacute phase showed moderate and obviously homogeneous hyper-intensity on 3D-SNAP (Figs. 2 and 3), and showed iso/hypo-intensity on 3D-PD and T2W imaging. Intramural hematoma in the acute phase showed iso-intensity, and its subacute phase showed high signal on 3D-T1W-VISTA, MRA, and 3D-T1WCE (Fig. 2). The relative signal intensity of intramural hematoma on 3D-SNAP was higher than that on the other sequences. Only 20 cases of IAD showed a double-lumen sign on 3D-SNAP, false lumen showed a low signal (n = 3) and slightly hyper-intensity (n = 12), while five cases showed an inhomogeneous high signal for a false lumen with thrombosis. False lumen showed significant hyper-intensity on 3D-T1WCE (n = 15), while false lumen with thrombosis showed inhomogeneous contrast, and showed hypo-intensity (n = 10). False lumen showed iso/hypo-intensity on the source of TOF-MRA (n = 14). Five cases showed inhomogeneous hyper-intensity for a false lumen with thrombosis, and 11 cases showed a low signal on 3D-PD. Seven cases showed inhomogeneous iso/hypo-intensity on T2W imaging. Twenty-one cases of IAD showed an intimal flap, in which the intimal flap showed moderate and obviously enhancement on 3D-T1WCE and linear iso-intensity on the other sequences in the lumen (Fig. 1). Comparison of the IAD findings (direct or indirect signs) among all HR-MRI sequences is shown in Table 2. The detection rates for IAD direct findings were compared between 3D-SNAP and other HR-MRI sequences (P < 0.05). 3D-SNAP was the most sensitive method to detect intramural hematoma, while 3D-T1WCE was the most sensitive method for identifying the double-lumen sign. There was no significant difference in the detection rates of aneurysmal dilatation in the HR-MRI sequences (P = 0.111), while there was a significant difference in the detection rates of stenosis or occlusion in the HR-MRI sequences.

Fig. 1.

A 57-year-old man with weakness of lower limbs and speech disorder for seven days. (a) TOF-MRA: the basilar artery was locally dilated and inhomogeneous signal (arrows). (b) The source image of TOF-MRA, the pseudolumen was large and showed low signal (arrows), true lumen showed slightly hyper-intensity (triangle). (c) 3D-PD: the basilar artery was fusiform dilated. (d, g) T1W imaging: true lumen showed hypo-intensity (triangle) and false lumen showed iso-intensity signal (arrows). (e, h) T1WCE: false lumen showed significant hyper-intensity (arrows), true lumen showed hypo-intensity (triangle), intimal flap showed obviously enhancement (dashed arrows). (f) T2W imaging: false lumen and true lumen showed low signal, intimal flap showed linear iso-intensity in the lumen (dashed arrows). (i) 3D-SNAP: true lumen showed hypo-intensity (triangle) and the pseudolumen showed moderate hyper-intensity (arrows), intimal flap depicted linear mild hyper-intensity. MRA, magnetic resonance angiography; PD, proton density; SNAP, simultaneous non-contrast angiography and intra-plaque; T1W, T1-weighted; T1WCE, contrast-enhanced T1-weighted; T2W, T2-weighted; TOF, time of flight.

Fig. 2.

A 43-year-old man presenting with dizziness and unstable gait for six days. (a) TOF-MRA showed a pearl-and-string sign in the basilar artery. (b) The wall showed thickening and lumen showed narrowing in the basilar artery on 3D-PD (arrows). An intramural hematoma showed hyper-intensity (arrows) and lumen showed narrowing in the basilar artery on T1W imaging (c, f) and 3D-SNAP (h). (e) T2W imaging: an intramural hematoma showed iso/hypo-intensity. (d, g) T1WCE: an intramural hematoma had no enhancement (arrows). MRA, magnetic resonance angiography; PD, proton density; SNAP, simultaneous non-contrast angiography and intra-plaque; T1W, T1-weighted; T1WCE, contrast-enhanced T1-weighted; T2W, T2-weighted; TOF, time of flight.

Fig. 3.

A 53-year-old man presenting with occipital pain and nausea for 1 day. No significant lesion is seen on (a) TOF-MRA, the source image of (b) MRA, (c) 3D-PD, (d, f) T1W imaging, and (e) T2W imaging. (g) T1WCE: intramural hematoma had no enhancement (arrows) and showed moderate linear enhancement (triangle). (h) 3D-SNAP: intramural hematoma showed moderate homogeneous hyper-intensity (arrows). MRA, magnetic resonance angiography; PD, proton density; SNAP, simultaneous non-contrast angiography and intra-plaque; T1W, T1-weighted; T1WCE, contrast-enhanced T1-weighted; T2W, T2-weighted; TOF, time of flight.

Fig. 4.

The effectiveness of every sequence in identifying signs and combined diagnosis of intracranial arterial dissection by receiver operating characteristic (ROC) curve.

Comparison of 3D-SNAP and multiparameter HR-MRI in the diagnosis of IAD

A total of 38 cases of IAD were confirmed, of which one case was not detected by 3D-SNAP and HR-MRI. The area under the curve of single sequences was in the following order: 3D-T1WCE > 3D-SNAP > 3D-T1W-VISTA > 3D-PD > TOF-MRA > T2W imaging. The diagnostic efficiency of 3D-SNAP combined with 3D-T1WCE was the highest (Fig. 4 and Table 3).

Table 3.

Sensitivity and specificity of all sequences in detecting IAD.

Sequence	AUC	95% CI	Sensitivity	Specificity
3D-T1WCE	0.903	0.833–0.973	0.868	0.937
3D-SNAP	0.897	0.829–0.966	0.895	0.90
3D-PD	0.818	0.725–0.911	0.711	0.925
3D-T1W-VISTA	0.845	0.760–0.930	0.789	0.90
T2W	0.771	0.669–0.874	0.605	0.937
TOF-MRA	0.766	0.666–0.866	0.658	0.875
3D-SNAP +T1WCE	0.966	0.928–1	0.916	0.942

3D, three-dimensional; AUC, area under the curve; CI, confidence interval; IAD, intracranial artery dissection; MRA, magnetic resonance angiography; PD, proton density; SNAP, simultaneous non-contrast angiography and intra-plaque; T1W-VISTA, T1-weighted volumetric isotropic turbo spin-echo acquisition; T1WCE, contrast-enhanced T1-weighted; T2W, T2-weighted; TOF, time of flight.

Discussion

The present study used 3D-SNAP to evaluate the direct and indirect signs of IAD. Our results showed that the intramural hematoma sign was the most sensitive sign on 3D-SNAP, and the signal intensity of intramural hematoma was significantly higher than that of other HR-MRI sequences. The 3D-SNAP sequence also showed obvious advantages for the detection of other direct and indirect signs of IAD. Its diagnostic efficiency in IAD was just slightly lower than that of 3D-T1WCE.

The 3D-SNAP technology involved a one-time acquisition of intravascular and hemorrhage information in the vascular wall by phase-sensitive reconstruction (24). Previous studies (25) demonstrated that the SNAP sequence could sensitively display hemorrhage in atherosclerotic plaques and could increase the signal intensity of IPH by 35% in comparison with other HR-MRI sequences. Intramural hematoma or pseudolumen thrombosis is known to be one of the pathologies of IAD. Therefore, we speculated that 3D-SNAP could also sensitively detect intramural hematoma signs of IAD. The results also confirmed our hypothesis. Our findings showed that 3D-SNAP was the most sensitive and specific sequence among the non-contrast technique to diagnose IAD. This was related to the presence of paramagnetic substances such as endogenous natural contrast agent in intramural hematoma or pseudolumen thrombus, and the suppression of blood flow signals in the true lumen of IAD (14). These factors were responsible for the excellent contrast between the wall and lumen of the blood vessel.

Intramural hematoma, double lumen, and intimal flap signs were important signs for diagnosing IAD. With the popularization of high-field MRI and the application of HR-MRI in intracranial vascular diseases, the detection rate of direct signs of IAD has increased significantly (26). The present study showed that the detection rate of intramural hematoma in IAD by 3D-SNAP technology was significantly higher than those of other imaging sequences. The relative signal intensity of intramural hematoma was also higher than those of other sequences. This was consistent with the findings by Wang et al. (25). They found that 3D-SNAP could improve the contrast of the IPH-wall of intramural plaques in comparison with other imaging methods (25). A previous study (21,27) also demonstrated that 3D-SNAP was a sensitive and reliable technique to detect IPH with histopathological confirmation. The true lumen blood flow velocity is high and has flow void effect, the black blood sequence (3D-PD, T2W imaging, 3D-T1W imaging, and 3D-SNAP) showed low signal, while the bright blood sequence (TOF-MRA) showed high signal. The blood flow velocity of false lumen was slow, which was easy to form turbulence and stagnation, the black blood sequence showed iso-low signal or slightly hyper-intensity, bright blood sequence signal was lower than true lumen, while false lumen with thrombosis showed inhomogeneous signal. At present, the reported detection rate of intramural hematoma, intimal flap, and double lumen are low in conventional MR diagnosis of intramural arterial dissection (9,18,28). Therefore, 3D-SNAP could greatly improve the detection rate of direct or indirect signs of IAD and provide evidence for the diagnosis of intracranial artery dissection.

The present study showed that 3D-T1WCE enhancement had the highest diagnostic efficiency and was the most sensitive method to detect the double lumen of IAD. The combination of 3D-SNAP and 3D-T1WCE showed higher diagnostic efficiency. Studies have shown that 3D-T1W-VISTA offered advantages in displaying the intramural hematoma of subacute IAD (27,29). However, it also shows limitations in displaying acute and chronic intramural hematoma as well as 3D-PD, 3D-T1W, TOF-MRA, and T2W imaging (29 –31). The possible reason why intramural hematoma show iso/hypo-intensity in these sequences is that the red blood cells are intact, the deoxygenated hemoglobin is diamagnetic, and the magnetic field is not uniform inside and outside the red blood cells in the acute phase of the intramural hematoma. Moreover, the scope for the use of contrast agents is limited in patients with renal insufficiency, pregnancy, and allergies. The image spatial resolution and contrast signal-to-noise ratio were also reduced on T1W enhancement due to the first-pass effect. Therefore, the non-invasive and non-contrast agent in 3D-SNAP technology plays an important role in allowing evaluation of the characteristics of IAD when the scope for application of contrast agent was limited. In addition, 3D-SNAP can also dynamically observe the changes of the wall and lumen of IAD, which was helpful in understanding the natural history and healing process, and providing more evidence for clinical personal treatment.

Most studies have shown that IAD is one of the important causes of stroke in young and middle-aged people, which can cause headache, ischemic symptoms, subarachnoid hemorrhage, and compressive symptoms (2,3,5). This study showed that patients with IAD were younger than those with other arterial diseases. However, the interval from onset to examination was longer than that in other intracranial arterial diseases, which may be due to the atypical and mild symptoms in most patients. Therefore, patients with suspected IAD should be examined by HR-MRI in time, which can ensure early definite diagnosis, early treatment, and fewer complications.

The present study also had several limitations. First, the small sample size and lack of information regarding the stages of IAD might have resulted in some bias. The sample size should be enlarged and observation of characteristics of IAD in different stages should be performed in future studies. Second, we did not determine the contrast between imaging characteristics and pathologic results in IAD. In the future, animal models should be used in contrast and longitudinal follow-up studies to assess IAD histological and high-resolution MRI features, which might elucidate the pathophysiological dynamic changes caused by IAD on 3D-SNAP imaging to further understanding pathological basis of IAD.

In conclusion, 3D-SNAP is a non-invasive and effective method that shows great potential and promise in evaluation of IAD. The popularization of 3D-SNAP will improve the diagnosis rate of IAD, and this technique has the potential to become the primary option for evaluating the high-risk factors of stroke caused by IAD, especially in patients with suspected IAD with limited use of contrast agent.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Key Research and Development Program of Shaanxi Province of China (2018ZDXM-SF-038).

ORCID iD

Xiaoling Zhang

References

Uhl

Schmid-Elsaesser

Steiger

HJ.

Ruptured intracranial dissecting aneurysms: management considerations with a focus on surgical and endovascular techniques to preserve arterial continuity. Acta Neurochir (Wien) 2003; 145:1073–1083.

Giroud

Fayolle

Andre

, et al. Incidence of internal carotid artery dissection in the community of Dijon. J Neurol Neurosurg Psychiatry 1994; 57:1443.

Schievink

WI.

Spontaneous dissection of the carotid and vertebral arteries. N Engl J Med 2001; 344:898–906.

Schievink

Mokri

O’Fallon

WM.

Recurrent spontaneous cervical-artery dissection. N Engl J Med 1994; 330:393–397.

Beletsky

Nadareishvili

Lynch

, et al. Cervical Arterial Dissection: Time for a Therapeutic Trial? Stroke 2003; 34:2856–2860.

Biousse

D’Anglejan-Chatillon

Touboul

, et al. Time Course of Symptoms in Extracranial Carotid Artery Dissections A Series of 80 Patients. Stroke 1995; 26:235–239.

Provenzale

Sarikaya

Comparison of test performance characteristics of MRI, MR angiography, and CT angiography in the diagnosis of carotid and vertebral artery dissection: a review of the medical literature. AJR Am J Roentgenol 2009; 193:1167–1174.

Han

Rim

Lee

, et al. Feasibility of high-resolution MR imaging for the diagnosis of intracranial vertebrobasilar artery dissection. Eur Radiol 2014; 24:3017–3024.

Wang

Lou

, et al. Imaging investigation of intracranial arterial dissecting aneurysms by using 3T high-resolution MRI and DSA: from the interventional neuroradiologists’ view. Acta Neurochir (Wien) 2014; 156:515–525.

10.

Kim

Choi

Koo

, et al. Intramural Hematoma Detection by Susceptibility-Weighted Imaging in Intracranial Vertebral Artery Dissection. Cerebrovasc Dis 2013; 36:292–298.

11.

Haacke

Mittal

, et al. Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR Am J Neuroradiol 2009; 30:19–30.

12.

Huang

R J

Zhu

, et al. Simultaneous non-contrast angiography and intraplaque haemorrhage (SNAP) imaging for cervical artery dissections. Clin Radiol 2019; 74:e1–7.

13.

Mittal

Neelavalli

, et al. Susceptibility-weighted imaging: technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol 2009; 30:232–252.

14.

Jung

Kim

Choi

, et al. Quantitative analysis using high-resolution 3 T MRI in acute intracranial artery dissection. J Neuroimaging 2016; 26:612–617.

15.

Rodallec

Marteau

Gerber

, et al. Craniocervical arterial dissection: spectrum of imaging findings and differential diagnosis. Radiographics 2008; 28:1711–1728.

16.

Arnold

Bousser

Fahrni

, et al. Vertebral artery dissection: presenting findings and predictors of outcome. Stroke 2006; 37:2499–2503.

17.

Tsukahara

Minematsu

Overview of Spontaneous Cervicocephalic Arterial Dissection in Japan.

Acta Neurochir Suppl 2010; 107:35–40.

18.

Hunter

Santosh

Teasdale

, et al. High-resolution double inversion recovery black-blood imaging of cervical artery dissection using 3T MR imaging. AJNR Am J Neuroradiol 2012; 33:E133–137.

19.

Drapkin

AJ.

The double lumen: a pathognomonic angiographic sign of arterial dissection?

Neuroradiology 2000; 42:203–205.

20.

Gao

, et al. Middle cerebral artery intraplaque hemorrhage: prevalence and clinical relevance. Ann Neurol 2012; 71:195–198.

21.

Wang

Guan

Yamada

, et al. In Vivo Validation of Simultaneous Non-Contrast Angiography and intraPlaque Hemorrhage (SNAP) Magnetic Resonance Angiography: An Intracranial Artery Study. PLoS One 2016; 11:e0149130.

22.

Varnava

Mills

Davies

MJ.

Relationship between coronary artery remodeling and plaque vulnerability. Circulation 2002; 105:939–943.

23.

Nakatsuka

Mizuno

Three-Dimensional Computed Tomographic Angiography in Four Patients with Dissecting Aneurysms of the Vertebrobasilar System. Acta Neurochir (Wien) 2000; 142:995–1001.

24.

Wang

Börnert

Zhao

, et al. Simultaneous noncontrast angiography and intraplaque hemorrhage (SNAP) imaging for carotid atherosclerotic disease evaluation. Magn Reson Med 2013; 69:337–345.

25.

Wang

Ferguson

Balu

, et al. Improved carotid intraplaque hemorrhage imaging using a slab-selective phase-sensitive inversion-recovery (SPI) sequence. Magn Reson Med 2010; 64:1332–1340.

26.

Tohru

Natural course of intracranial arterial dissections. J Neurosurg 2011; 14:1037–1044.

27.

Chen

Wong

Lam

WWM

, et al. High signal on T1 sequence of magnetic resonance imaging confirmed to be intraplaque haemorrhage by histology in middle cerebral artery. Int J Stroke 2014; 9:E19.

28.

Ahn

Kim

Suh

, et al. Spontaneous symptomatic intracranial vertebrobasilar dissection: initial and follow-up imaging findings. Radiology 2012; 264:196–202.

29.

Oppenheim

Naggara

Touzé

, et al. High-resolution MR imaging of the cervical arterial wall: what the radiologist needs to know. Radiographics 2009; 29:1413–1431.

30.

Habs

Pfefferkorn

Cyran

, et al. Age determination of vessel wall hematoma in spontaneous cervical artery dissection: A multi-sequence 3T Cardiovascular Magnetic resonance study. J Cardiovasc Magn Reson 2011; 13:76.

31.

Kim

Shin

Kim

, et al. Added Value of 3D Proton-Density Weighted Images in Diagnosis of Intracranial Arterial Dissection. PLoS One 2016; 11:e0166929.