Comparative evaluation of 5.0 T and 3.0 T time-of-flight magnetic resonance angiography in assessing collateral circulation in moyamoya angiopathy

Introduction

Moyamoya angiopathy (MMA) is a chronic cerebrovascular disorder marked by progressive narrowing or occlusion of the intracranial internal carotid artery (ICA) and its proximal branches, accompanied by the formation of a basal collateral network (1-3). MMA refers to the radiological criteria of the angiopathy without referring to the underlying cause, which can be classified into two categories: moyamoya disease (MMD), when it occurs as an idiopathic condition, and moyamoya syndrome, when it is associated with acquired conditions. The etiology and natural progression of MMA remain largely unknown, and its clinical manifestations vary. The cerebral collateral circulatory system compensates for impaired cerebral blood flow by establishing alternative vascular pathways when the primary arteries are compromised. Disease progression in MMA reflects both the occlusion of principal intracranial arteries and the development of collateral circulation. Studies have suggested that the status of collateral circulation is closely linked to clinical outcomes in ischemic stroke patients (4-6), and it may affect therapeutic results in acute ischemic stroke patients (6). However, limited research has focused on assessing this collateral system in MMA patients using magnetic resonance imaging (MRI).

Time-of-flight magnetic resonance angiography (TOF MRA) is a widely recognized noninvasive diagnostic tool. Conventional angiography is unnecessary when MRA identifies ICA occlusion and moyamoya vessels (MMVs) (7). However, 3.0 T TOF MRA may lack the precision needed to evaluate collateral circulation in MMA (8). The introduction of an ultra-high field (UHF) magnetic resonance (MR) system, such as 7.0 T, offers superior signal-to-noise ratios (SNRs) and extended T1 relaxation times compared to 3.0 T systems, resulting in enhanced image quality, particularly for small arteries (9-11). Nonetheless, the depiction of the internal carotid siphon and distal segments of basilar artery on 7.0 T TOF MRA is constrained by higher B1 inhomogeneity and more pronounced signal loss at UHF strengths.

The 5.0 T MRI system, a recent development in clinical research, has shown imaging quality comparable to 7.0 T while surpassing that of 3.0 T (12). Despite this, there are limited studies comparing the evaluation of the leptomeningeal system between 3.0 T MRI and UHF MRI. In this cross-sectional observational study, we systematically compared collateral circulation using 5.0 T and 3.0 T TOF MRA in patients with MMA, aiming to demonstrate the superior efficacy of 5.0 T TOF MRA in collateral assessment. We present this article in accordance with the STROBE reporting checklist (available at https://cdt.amegroups.com/article/view/10.21037/cdt-2025-6/rc).

Methods

Participants

The cross-sectional observation research was sourced from a prospectively collected 5.0 T MRI database of patients with MMA. Between March 2023 and April 2024, 34 consecutive patients with MMA referred to Peking Union Medical College Hospital and Beijing Hospital underwent 5.0 T TOF MRA and were invited to additionally undergo 3.0 T TOF MRA with informed consent. Patients were excluded if they had previously undergone extracranial-to-intracranial bypass surgery before the examination (n=3) or the interval between 3.0 T and 5.0 T examination exceeded one week (n=2). A total of 8 patients were further excluded due to poor image quality. Finally, 21 patients were included in the analysis, among whom 8 underwent digital subtraction angiography (DSA). The study adhered to the Declaration of Helsinki and its subsequent amendments and was approved by the Institutional Ethics Committee for Human Research at Peking Union Medical College Hospital (No. K3147). Informed consent was obtained from all participants.

The diagnosis of MMA was radiological, based on DSA or 3.0 T TOF MRA, according to the guidelines (1,13,14): (I) stenosis or occlusion at the terminal portion of the ICA and/or at the proximal portion of the anterior cerebral artery (ACA) and/or the middle cerebral artery (MCA); (II) presence of an abnormal arteriolar network in the vicinity of the steno-occlusive lesions.

Clinical data, including sex, age, and clinical manifestations, were recorded. For participants with clinical symptoms, we chose the symptomatic MMA hemisphere for analysis. A symptomatic MMA hemisphere was defined by either: (I) a history of recurrent transient ischemic attack, infarction, or hemorrhage, with or without corresponding MRI findings; (II) persistent neurological symptoms such as hemiparesis or sensory deficits. Headache, if not localized to one hemisphere, was attributed to both hemispheres. For participants without specific clinical symptoms, the more severely affected hemisphere was selected for analysis.

MRI acquisition

Both 3.0 T and 5.0 T TOF MRA were performed without contrast. A 5.0 T MRI system was used (uMR Jupiter, United Imaging Healthcare, Shanghai, China) equipped with a two-channel transmit and 48-channel receiver head coil. Scanning parameters for the 5.0 T TOF MRA included the following: Repetition time (TR)/echo time (TE) 19.5 ms/3.8 ms; flip angle 15; field of view (FOV) 230×200 mm²; acquisition time 80.4–103.8 s; slice thickness 0.6 mm; and pixel size of 0.6×0.6 mm² (0.3 mm³ isotropic after interpolation).

3.0 T TOF MRA images were collected using a 3.0 T MRI scanner (uMR 790, United Imaging Healthcare, China). The scanning parameters included the following: TR/TE 19.5 ms/4.5 ms; flip angle 15°; FOV 230×200 mm²; acquisition time 133.7–163.0 s; slice thickness 0.6 mm; and pixel size of 0.6×0.6 mm².

DSA acquisition

DSA was conducted using a standard protocol on a biplane system. Frontal and lateral views were captured following the injection of a 4–12 mL bolus of iodinated contrast agent at a rate of 2–6 mL/s into each internal carotid and vertebral artery, with a 1-second delay incorporated before initiating the injection process.

Image analysis

All images were manually reviewed to ensure accuracy and avoid potential misinterpretations caused by image quality. To ensure consistency in collateral assessment, transverse and lateral views of maximum intensity projection (MIP) images and raw MRA images were evaluated, with other MIP image angles used as references.

Qualitative evaluation

Participants who underwent DSA had their arterial visualization assessed using DSA findings as the reference standard. The assessment focused on terminal ICAs, distal MCAs, MMV, and leptomeningeal collaterals from the posterior circulation, employing a 0–4 scale (Table 1), and was conducted by two radiologists. Their qualitative evaluations were individually recorded.

Quantitative evaluation

The collateral circulation was further assessed by semi-quantitative grading score based on the TOF MRA images, including the visibility of MMVs and leptomeningeal anastomosis (LMA) from the posterior cerebral artery (PCA). The grading score was determined as described below:

• Based on a 3.0 T MRI study (7), the MMV area score evaluated the visibility of MMVs. Scores range from 0 to 5, encompassing five regions: the basal ganglion, anterior communicating artery, MCA-ICA tip, posterior communicating artery (PCoA)-PCA, and basilar artery tip areas (Figure 1).
• The LMA from PCA was evaluated using the LMA score, based on the anatomy extent of pial collateral blood from the PCA. As defined in a previous DSA study (6), the leptomeningeal system scores evaluate three components of the collateral networks: (i) the anastomosis from the PCA to the ACA was assessed. Anastomosis to the cortical border zone between the ACA and PCA territories was scored 1 (Figure 2A), whereas anastomosis over the central sulcus via the posterior pericallosal artery was scored 2 (Figure 2B); (ii) the anastomosis of the anterior temporal branch of the PCA to the temporal branch of the MCA was scored 1 (Figure 3A); (iii) for PCA to MCA anastomosis, a score of 1 was given for extensions in superficial vessels only (Figure 3B), a score of 2 for extensions into the Sylvian fissure (Figure 3C), and a score of 3 for extensions reaching the occlusion (Figure 3D). The leptomeningeal system score is the total of the 3 components mentioned earlier, with a score of 0 assigned for the absence of LMAs.

Figure 1 TOF MRA MIP image of a patient who presented with headache and was diagnosed with MMA. (A) 5.0 T TOF MRA MIP image shows that MMV are visible at the basal ganglion, anterior communicating artery, MCA-ICA tip, PCoA-PCA (arrowhead, MMV area score of 4). (B) MMVs cannot be clearly visible on 3.0 T TOF MRA of the same patient. ICA, internal carotid artery; MCA, middle cerebral artery; MIP, maximum intensity projection; MMA, moyamoya angiopathy; MMV, moyamoya vessels; PCA, posterior cerebral artery; PCoA, posterior communicating artery; TOF MRA, time of flight magnetic resonance angiography.

Figure 2 Leptomeningeal collateral from the PCA to the ACA territory. (A) The anastomosis (parieto-occipital branch of the PCA→ACA) extending to the cortical border zone between the ACA and PCA territory was assigned a score of 1 (arrowhead), and (B) the anastomosis over the central sulcus via the posterior pericallosal artery was scored 2 (arrowhead), which would be confirmed by raw MRA images. ACA, anterior cerebral artery; MRA, magnetic resonance angiography; PCA, posterior cerebral artery.

Figure 3 Leptomeningeal collateral from the PCA to the MCA territory. (A) The anastomoses of the anterior temporal branches of PCA to MCA was scored 1 (arrowhead). (B-D) Parieto-occipital PCA anastomoses to MCA. (B) A score of 1 was assigned if the anastomoses extended in superficial vessels only (arrowhead). (C) A score of 2 was assigned if the anastomoses extended into the Sylvian fissure (arrowhead). (D) A score of 3 was assigned if the anastomoses up to the occlusion (arrowhead). MCA, middle cerebral artery; PCA, posterior cerebral artery.

Each set of TOF MRA images was independently reviewed by two radiologists. The radiologists remained uninformed about the field strength and clinical indicators post data collection. If discrepancies arose between the two radiologists, the score was determined by them reaching a consensus. For the participants who underwent DSA, the number of hemispheres demonstrating each component of MMVs and LMA collateral circulation pattern was evaluated using DSA, 5.0 T TOF MRA and 3.0 T TOF MRA. The sensitivity of detecting each component of MMVs and LMA on 3.0 T/5.0 T TOF MRA was assessed using DSA findings as the gold standard reference.

Statistical analysis

Scores of vessel visualization for the two observers were compared separately between 3.0 T and 5.0 T TOF MRA using the Wilcoxon matched-pair signed-rank test. Comparative analysis of MMV area scores and LMA scores between 3.0 T and 5.0 T TOF MRA was executed using the Wilcoxon matched-pair signed-rank test. Weighted κ value was used to evaluate the interrater agreement in MMV area score and LMA score. All analyses were conducted with SPSS software, version 29.0 (IBM Corp., Armonk, NY, USA). A P value less than 0.05 was deemed statistically significant.

Results

Participant characteristics

A total of 21 participants with 29 hemispheres were analyzed in this study. Of these, 11 (52.4%) were males. The mean age was 36 years (range, 18–57 years). Weakness and/or numbness of limbs was the predominant major clinical symptom affecting 12 (57.1%) participants. There were two participants who did not exhibit specific clinical symptoms (Table 2).

Qualitative evaluation of visualization of arteries

A total of 10 hemispheres of 8 participants were included. The vessel visualization scores are summarized in Table 3. The visualization scores of terminal ICAs did not significantly differ between 5.0 T and 3.0 T TOF MRA for both observers. However, the 5.0 T TOF angiography provided superior visualization scores for distal MCAs, MMV, and LMA collaterals compared to the 3.0 T TOF MRA (P<0.05 for both observers).

Comparison of MMV area scores between 3.0 T and 5.0 T TOF MRA

The MMV area score for 3.0 T MRA ranged from 0 to 5 [median 2, interquartile range (IQR), 1–3], and the MMV area score for 5.0 T MRA spanned from 1 to 5 (median 3, IQR, 3–5) (Table S1). MMV area scores of 5.0 T TOF MRA were significantly higher than those of its 3.0 T counterpart (z=4.41, P<0.001). DSA confirmed that certain MMVs were detectable via 5.0 T TOF MRA but not by 3.0 T TOF MRA (Figure 4). For those participants who underwent DSA, 5.0 T TOF MRA showed higher sensitivity than 3.0 T TOF MRA for each component of MMVs (Table S2).

Figure 4 A patient who performed transient weakness of right limbs. DSA revealed MMV (A,B, red arrows). MMV at the basal ganglion are also detected on 5.0 T MRA (D, red arrows), whereas 3.0 T MRA cannot reveal the anastomoses (C). DSA, digital subtraction angiography; MMV, moyamoya vessel; MRA, magnetic resonance angiography.

Comparison of the LMA scores between 3.0 T and 5.0 T TOF MRA

The LMA score for 3.0 T MRA ranged from 0 to 6 (median 1, IQR, 0–2.75). Conversely, the score for 5.0 T MRA ranged from 0 to 6 (median 2, IQR, 1.25–3.00) (Table S1). The leptomeningeal system scores of 5.0 T TOF MRA were significantly higher than those of its 3.0 T counterpart (z=3.72, P<0.001). LMA was not detected in 8 hemispheres on 3.0 T TOF MRA. However, 6 of these (75.0%) were shown to have LMA when assessed with 5.0 T TOF MRA. DSA confirmed that some leptomeningeal collateral vessels are detectable via 5.0 T TOF MRA but not by 3.0 T TOF MRA (Figure 5). For those participants who underwent DSA, 5.0 T TOF MRA showed higher sensitivity than 3.0 T TOF MRA for all components of LMA (Table S2).

Figure 5 A patient who experienced weakness of bilateral limbs. DSA revealed parieto-occipital PCA anastomoses to the MCA (A and B, arrow). It can also be detected on 5.0 T MRA (C, arrow), whereas 3.0 T MRA cannot reveal the anastomoses. DSA, digital subtraction angiography; MCA, middle cerebral artery; MRA, magnetic resonance angiography; PCA, posterior cerebral artery.

Inter-observer agreements of the MMV area scores and LMA scores

Interobserver agreements in MMV area scores and LMA scores were good for both 3.0 T and 5.0 T imaging (all weighted κ values >0.6), as shown in Table 4.

Discussion

In our study, 5.0 T TOF MRA demonstrated superior detection capabilities, revealing a clearer visualization of MMV and LMA compared to 3.0 T TOF MRA. Radiological evaluations indicated that 5.0 T images portrayed MMV and LMA branches with significantly better clarity than 3.0 T images, highlighting the potential of 5.0 T in offering a comprehensive assessment of the abnormal vascular networks in MMA patients.

TOF MRA has become a cornerstone diagnostic tool for MMA, owing to its advantages over DSA. These benefits include non-invasiveness, no need for contrast media, zero radiation exposure, and their ability to detect other crucial findings, such as infarctions, hemorrhages, and cerebral atrophy (15,16). Nevertheless, the capabilities of 3.0 T MRA might be limited when it comes to accurately evaluating the abnormal collateral circulation in MMD (8,17). Theoretically, UHF MRA enhances SNR, allowing for high-resolution imaging and better blood-tissue contrast compared to 3.0 T MRA. Specifically, 7.0 T has demonstrated heightened sensitivity to slow-flowing blood in smaller vessels with the right acquisition parameters (18-22). However, 7.0 T MRA faces challenges when depicting areas such as the carotid siphon and basilar arteries (21), primarily due to signal loss from radio frequency (RF) inhomogeneities, potentially limiting its assessment capabilities for MMV. The introduction of the 5.0 T MRI system, apt for whole-body examinations (23), seems to bridge this gap. Previous study has highlighted that 5.0 T MRI, being an intermediate magnetic field strength, offers superior B1+ field homogeneity, reduced RF energy deposition, and fewer specific absorption rate (SAR)-related safety concerns than 7.0 T MRI, while still significantly outperforming 3.0 T MRI in terms of SNR (24). Our study accentuates the advantages of 5.0 T’s elevated magnetic field strength, resulting in a superior depiction of collateral circulation compared to 3.0 T.

In a related study, the ability of 5.0 T MRA to visualize small arterial branches was found comparable to that of 7.0 T MRA, and distinctly superior to the 3.0 T MRA (12). This underscores the potential of the 5.0 T MRA as a balanced solution that meets both clinical needs and technical feasibility. To the best of our understanding, our study is pioneering in its comparison of 5.0 T and 3.0 T TOF MRA for patients with MMA. Our findings indicated that the depiction of MMV and LMA branches on 5.0 T images surpassed those on 3.0 T, resonating with earlier studies conducted on 7.0 T (9-11).

Our study revealed that LMA collaterals and MMVs were better visualized with 5.0 T TOF MRA than they were with 3.0 T TOF MRA. Previous studies have highlighted the significance of LMA collaterals from the posterior circulation in patients with MMD (25-27). Changes in posterior circulation correlate with the distribution and extent of cerebral infarction (27). PCA involvement is associated with higher incidence of perioperative complications (28), suggesting that the significance of LMA collaterals from the posterior circulation may play an important role in the maintenance of cerebral perfusion. MMV is also an important part of the collaterals. The rupture of fragile, dilated MMVs may lead to intracranial hemorrhage (29). 5.0 T TOF MRA is valuable for assessing these vessels, providing crucial imaging insights into the cerebrovascular event risk in MMA patients.

A prior DSA study formulated an MMD collateral grading system (6), suggesting that ischemic MMD patients with severe ischemic symptoms tend to exhibit fair or poor collateral status. Such patients, especially those with poor collateral status, were found to be at a higher risk of subsequent strokes and had a less favorable prognosis (6). Our study affirmed that 5.0 T TOF MRA offered a clearer visualization of MMV and LMA collaterals than did 3.0 T TOF MRA, hinting at the potential of 5.0 T MRI in assessing hemodynamic status, and aiding therapeutic decision-making for MMA patients.

This research has some inherent limitations. The limited sample size sample size might have led to false-negative outcomes. This study did not include patients with certain clinical symptoms, such as cognitive impairment and seizures, and the relationship between the clinical symptoms and collateral circulation status remains unclarified. Secondly, since DSA is an invasive examination, whether to perform DSA was cautiously determined by the clinician with the agreement of the patients, so not all patients performed DSA in this study. Thirdly, although the readers were blinded to the field strength, the discernible differences in image quality between 5.0 T and 3.0 T images might have influenced their evaluations. Fourthly, since the components of the duro-cortical system are too complex to generalize and classify on TOF MRA, the transdural anastomosis, which also play important roles in MMA, was not analyzed in this study. Finally, the difference in coil systems stemming from technological advancements might have impacted the perceived improvement in image quality, obscuring the genuine benefits derived solely from the increased magnetic field strength.

Conclusions

This study underscores the advantages of the 5.0 T TOF MRA over its 3.0 T counterpart in assessing collateral circulation of MMA patients. The 5.0 T MRA revealed a clearer visualization of MMV and LMA compared to 3.0 T TOF MRA. Such enhanced capabilities offer the potential for a more comprehensive assessment of MMA’s abnormal vascular networks. Although the research points to the promising capabilities of the 5.0 T MRI system, the findings also indicate the need for further studies with larger sample sizes and controlled parameters to corroborate the results and harness the full diagnostic potential of this advanced imaging technology.

Acknowledgments

The authors thank the Theranostics and Translational Research Center, National Infrastructures for Translational Medicine, Institute of Clinical Medicine, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences for supporting the study.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://cdt.amegroups.com/article/view/10.21037/cdt-2025-6/rc

Data Sharing Statement: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-2025-6/dss

Peer Review File: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-2025-6/prf

Funding: This study was supported by the National Natural Science Foundation of China (No. 82325026), the Major International (Regional) Joint Research Project of National Natural Science Foundation of China (No. 82020108018), the Beijing Natural Science Foundation (No. Z210013) and National High Level Hospital Clinical Research Funding (No. 2022-PUMCH-B-027).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cdt.amegroups.com/article/view/10.21037/cdt-2025-6/coif). K.X. and Y.Y. are employees of United Imaging Healthcare. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the ethics committee of Peking Union Medical College Hospital (No. K3147) and informed consent was taken from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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