Visualization of cortical neoangiogenesis after combined revascularization surgery in moyamoya disease using silent MRA

Abstract

Purpose: To investigate postsurgical indirect cortical neoangiogenesis in patients with moyamoya disease (MMD) using silent magnetic resonance angiography (MRA).

Methods: We studied 44 patients with MMD (63 hemispheres) who were previously revascularized with combined bypass surgery (23 and 40 hemispheres in pediatric and adult patients, respectively). They underwent follow-up for postoperative bypass patency using time-of-flight (TOF)-MRA and silent MRA between January 2022 and December 2023. The mean duration from surgery to MRA was 8.5 years (range, 1.2-22.3 years). Two observers independently rated the revascularization as follows: 0 (near-complete signal loss or no signal); 1, poor (slightly visible donor arteries); 2, good (acceptable revascularization around the brain surface); and 3, excellent (good quality of revascularization with perfusion from the cortical surface into the middle cerebral artery).

Results: Silent MRA visualized indirect bypass significantly better than TOF-MRA (2.6 ± 0.7 and 1.4 ± 0.8) (P < 0.01). In silent MRA, the mean score of indirect bypass was significantly higher than that of direct bypass (2.6 ± 0.7 and 1.7 ± 1.0; P < 0.01) and indicated good indirect bypass development in both children and adults (91.3% and 85.0%; score ≥ 2). Children exhibited a higher rate of excellent indirect bypass patency than adults (73.9% and 55.0%; score 3). Poor bypass development in indirect bypass (8 hemispheres, mean age: 35.5 ± 17.5 years, mean follow-up period: 11.3 years) was significantly observed in male patients (P < 0.01).

Conclusion: Silent MRA enables better precision in postsurgical visualization of indirect cortical neoangiogenesis during long-term follow-up and reveals indirect bypass development even in adult patients.

Keywords: Cortical neoangiogenesis; Indirect bypass; Moyamoya disease; Silent MRA; UTE-MRA.

Fig. 1

Grading score of postsurgical bypass patency on a four-point scale. (A) Grade 0, not visible (near-complete signal loss or no signal of donor arteries; white arrow); (B) grade 1, poor (slightly visible donor arteries; white arrows); (C) grade 2, good (acceptable revascularization around the brain surface; white dotted circle); (D) grade 3 in indirect bypass, excellent (good quality of revascularization with perfusion from the cortical surface into the middle cerebral artery; white dotted circle); and (E) grade 3 in direct bypass (white arrows)

Fig. 2

Representative MRA images of pediatric patients in long-term follow-up. A 14-year-old girl, who had previously suffered from transient ischemic attack, was treated with combined direct and indirect bypass (superficial temporal artery [STA]–middle cerebral artery [MCA] single anastomosis with encephalomyosynangiosis [EMS] and encephalodurosynangiosis [EDS]) for both hemispheres. Fourteen years after bypass surgery, follow-up (A) silent MRA and (B) TOF-MRA were performed. (A) Based on silent MRA, the scores of the two observers were 2.5 for direct bypass and 3 for indirect bypass on the right side and 1 for direct bypass and 3 for indirect bypass on the left side (white dotted circles). (B) Based on TOF-MRA, the scores of the two observers were 1 for direct bypass and 1.5 for indirect bypass on the right side and 2 for direct bypass and 2 for indirect bypass on the left side (white dotted circles). An 8-year-old girl, who had previously suffered from epilepsy, was treated with combined direct and indirect bypass (STA-MCA single anastomosis with EMS and EDS) for both hemispheres. Twenty-two years after bypass surgery, follow-up (C) silent MRA and (D) TOF-MRA were performed. (C) Based on silent MRA, the scores of the two observers were 2.5 for direct bypass and 3 for indirect bypass on the right side and 1 for direct bypass and 3 for indirect bypass on the left side (white dotted circles). (D) Based on TOF-MRA, the scores of the two observers were 1.5 for direct bypass and 0.5 for indirect bypass on the right side and 1.5 for direct bypass and 0 for indirect bypass on the left side (white dotted circles)

Fig. 3

Representative MRA images of adult patients in long-term follow-up. A 51-year-old woman, who had previously suffered from cerebral infarction, was treated with combined direct and indirect bypass (superficial temporal artery [STA]–middle cerebral artery [MCA] single anastomosis with encephalomyosynangiosis [EMS] and encephalodurosynangiosis [EDS]) for both hemispheres. Fourteen years after bypass surgery, follow-up (A) silent MRA and (B) TOF-MRA were performed. (A) Based on silent MRA, the scores of the two observers were 1 for direct bypass and 3 for indirect bypass on the right side and 1 for direct bypass and 3 for indirect bypass on the left side (white dotted circles). (B) Based on TOF-MRA, the scores of the two observers were 0.5 for direct bypass and 2.5 for indirect bypass on the right side and 1 for direct bypass and 0 for indirect bypass on the left side (white dotted circles). A 41-year-old woman, who had previously suffered from cerebral infarction, was treated with combined direct and indirect bypass (right STA-MCA single anastomosis with EMS and EDS). Twenty-two years after bypass surgery, follow-up (C) silent MRA and (D) TOF-MRA were performed. (C) Based on silent MRA, the mean scores of the two observers were 2.5 for direct bypass and 3 for indirect bypass (white dotted circle). (D) Based on TOF-MRA, the scores of the two observers were 1.5 for direct bypass and 1 for indirect bypass (white dotted circle)

Fig. 4

Representative MRA images of patients with poor indirect bypass development. (A) A 49-year-old man, who had previously suffered from cerebral infarction, was treated with combined direct and indirect bypass (right superficial temporal artery [STA]–middle cerebral artery [MCA] single anastomosis with encephalomyosynangiosis [EMS] and encephalodurosynangiosis [EDS]). Two years after bypass surgery, follow-up silent magnetic resonance angiography (MRA) was performed. The mean scores of the two observers were 1.5 for direct bypass and 0 for indirect bypass (white arrows). (B) A 39-year-old man, who had previously suffered from cerebral infarction, was treated with combined direct and indirect bypass (STA-MCA single anastomosis with EMS and EDS). Seventeen years after bypass surgery, follow-up silent MRA was performed. The scores of the two observers were 0 for direct bypass and 0 for indirect bypass on the right side (white arrow) and 2.5 for direct bypass and 1 for indirect bypass on the left side