Standardized MR Perfusion Scoring System for Evaluation of Sequential Perfusion Changes and Surgical Outcome of Moyamoya Disease

Y.-H. Lin; M.-F. Kuo; C.-J. Lu; C.-W. Lee; S.-H. Yang; Y.-C. Huang; H.-M. Liu; Y.-F. Chen

doi:10.3174/ajnr.A5945

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Fig 1.
Serial changes in 3 levels in standardized TTP maps of an 18-year-old female patient with MMD. Preoperatively (A) and 1 (B) and 3 (C) months after left temporal EDAS and frontal EPS and a 6-month map after a right-sided operation (D). Preoperative maps show large areas of prolonged TTP in the anterior cerebral artery and MCA territories bilaterally (A). Areas of normalized TTP near the craniotomy site (arrows: temporal EDAS; arrowheads: frontal EPS) are shown in the 1-month postoperative map (B) and are enlarged in the 3-month map (C). The contralateral hemisphere shows simultaneous improvement. After a subsequent right-sided operation, the right cerebrum shows increased areas of TTP normalization. The final maps show only small areas of TTP prolongation at the bilateral medial cerebrum (D).
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Fig 2.
TTP scoring system. We counted and totaled 14 cortical regions in 3 levels of cerebral hemispheres: ganglionic level (A), ventricular roof level (B), and high convexity (C). Each level is approximately 2 cm apart. An area of blue larger than one-half of 1 region is counted as 1 point, otherwise, it is counted as 0 points. The total TTP score of 1 hemisphere ranges from 0 to 14 points: 4, 8, and 2 for the anterior cerebral artery, MCA, and posterior cerebral artery areas, respectively.
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Fig 3.
Line chart revealing postoperative sequential changes of TTP score improvement. In both pediatric and adult groups, the score improvements are most robust at 0–3 months followed by 3–6 months and reach a plateau at the 6-month follow-up. Our adult group has more score improvement than the pediatric group, probably related to more severe preoperative disease status.
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Fig 4.
Scatter diagram indicating that the preoperative TTP score is inversely correlated with the TTP score improvement after the operation.

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Table 1:

Patient demographic and clinical data

	Pediatric Patients (n = 24)	Adult Patients (n = 20)
Age (mean) (yr)	9.21 ± 3.59	32.4 ± 10.94
Sex (male) (No.) (%)	16 (67)	3 (15)
Clinical presentation (No.) (%)
Focal neurologic symptoms	17 (71)	13 (65)
Seizure	3 (13)	4 (20)
Headache	5 (21)	3 (15)
Infarction	9 (38)	14 (70)
Hemorrhage	0 (0)	1 (5)
Comorbidities (No.) (%)^{^a}	3 (8)	0 (0)

↵a There were 2 patients with neurofibromatosis type 1 and 1 patient with systemic lupus erythematosus.

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Table 2:

Pre- and postoperative radiologic characteristics

	Pediatric Hemispheres (n = 41)	Adult Hemispheres (n = 34)
Preoperative Suzuki stage (No.) (%)
I	1 (2)	0 (0)
II	7 (17)	5 (15)
III	18 (44)	11 (32)
IV	12 (29)	10 (29)
V	3 (7)	3 (9)
VI	0 (0)	5 (15)
Preoperative TTP score (points) (mean)	7.34 ± 3.90	4.88 ± 3.24
Additional EPS (No.) (%)	15 (36)	30 (88)
Periprocedural infarction (No.) (%)	0 (0)	3 (9)
Duration of follow-up (mean) (mo)	38.00 ± 16.57	29.85 ± 5.11
Progressive PCA disease (No.) (%)	3 (7)	0 (0)
Recurrent stroke during follow-up (No.) (%)^{^a}	3 (7)	0 (0)

Note:—PCA indicates posterior cerebral artery.
↵a Between 2 operations: 2 on the nonoperated side, 1 in the PCA territory on the operated side.

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Table 3:

Postoperative Matsushima grading and TTP score improvement (6 months after the operation) indicating that TTP score improvement is correlated with Matsushima grading

	Pediatric		Adult
	No. of Hemispheres (%)	Score Improvement (Mean)	No. of Hemispheres (%)	Score Improvement (Mean)
Matsushima grade
A	17 (52)	5.94 ± 3.72	10 (44)	7.40 ± 2.37
B	10 (30)	3.50 ± 2.83	9 (39)	6.00 ± 2.96
C	6 (18)	0.17 ± 1.17	4 (17)	3.50 ± 4.73
Unknown^{^a}	8	4.13 ± 2.62	11	5.73 ± 2.69

↵a The patients did not undergo postoperative catheter angiography.

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Table 4:

Linear mixed regression model analyses of predictors for postoperative 6-month TTP score improvement^{^a}

Variable	Univariable		Multivariable
Variable	Coefficient (SD)	P Value^{^b}	Coefficient (SD)	P Value^{^b}
Age	0.92 (0.40)	.03	−0.28 (0.24)	.26
Sex (male)	−2.47 (0.76)	.002	−0.51 (0.44)	.26
Preoperative TTP score	−3.03 (0.19)	<.001	−2.93 (0.21)	<.001
Additional EPS^{^c}	3.03 (0.75)	<.001	0.58 (0.47)	.21

↵a Linear mixed regression model with random intercepts and standardized age and preoperative TTP scores were used.
↵b P values were obtained with the Wald test.
↵c EPS to the hypoperfusion area at frontal or parietal regions in addition to temporal EDAS in the same procedure.