Correlation Between Apelin and Collateral Circulation in Patients with Middle Cerebral Artery Occlusion and Moyamoya Disease

Figures & data

Table 1 Univariate Analysis of Control, MMD, and MCA Occlusion Groups

Parameters	Controls (29)	MMD Group (68)	MCA Occlusion Group (25)	P-value
Age, years^b	51.00±10.50	46.66±9.65	53.24±12.16	0.009
Sex, male (n, %)^c	15 (51.7)	26 (38.2)	19 (76)	0.005
BMI, kg/m^2a	24.44±3.39	24.93±3.10	25.64±3.32	0.476
SBP (mmHg)^a	133.10±18.53	136.25±16.58	144.84±17.94	0.050
DBP (mmHg)^a	80.38±9.09	84.97±9.25	88.48±9.58	0.006
Smoke (n, %)^c	7 (24.1)	5 (7.4)	11 (44)	<0.001
Drunk (n, %)^c	6 (20.7)	5 (7.4)	8 (32)	0.010
Stroke type (n, %, ischemic)^c	0	44 (64.7)	25 (100)	0.001
Stroke history (n, %)^c	0	33 (48.5)	7 (28)	0.078
Total cholesterol (mg/dL)^a	4.33±0.72	4.07±1.09	3.77±1.31	0.077
Triglyceride (mg/dL)^a	2.06±1.80	1.27±0.50	1.27±0.96	0.194
LDL-cholesterol (mg/dL)^a	2.59±0.76	2.42±0.82	1.99±1.00	0.285
Lipoprotein a (mmol/L)^a	279.26±249.06	270.84±251.37	356.91±227.37	0.165
Blood glucose (mmol/L)^a	5.20±0.97	4.79±0.70	5.83±1.23	0.002
Homocysteine (µmol/L)^a	12.17±5.23	10.00±4.00	12.25±5.93	0.911
Apelin-13 (pg/mL)^b	32.15±28.14	271.15±137.85	155.18±105.73	0.000
Apelin-17 (ng/dL)^b	60.99±63.13	196.78±75.82	139.04±60.74	0.000
Apelin-36 (ng/dL)^b	354.05±244.14	957.80±481.28	727.11±250.39	0.000
NO (nmol/L)^b	41.02±36.08	113.21±135.18	112.59±105.53	0.000
VEGF (pg/mL)^b		195.48±405.12	166.81±161.39	0.840
Aspirin treatment (%)^c	1 (3.4)	7 (10.3)	2 (8)	0.531
Clopidogrel treatment (%)^c	0 (0)	2 (2.9)	2 (8)	0.251
Atorvastatin (%)^c	1 (3.4)	7 (10.3)	2 (8)	0.531
NHISS^b	0.14±0.58	1.40±3.61	4.40±3.74	0.000
Remarks: 34 (50%) moyamoya disease patients had middle cerebral artery occlusion; all patients in the MCA occlusion group had middle artery occlusion.

Notes: Continuous data conform to normal distribution are presented with mean±SD marked as “^a”, and abnormal distribution data are presented as median±IQR (interquartile range), which is marked as “^b”, the counting data of said frequency and percentage marked as “^c”.

BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; NO, nitric oxide; MMD, moyamoya disease; MCA, middle cerebral artery; NHISS, National Institutes of Health Stroke Scale.

Figure 1 Plasma apelin-13, apelin-17, apelin-36, and serum NO and VEGF levels in patients with moyamoya disease (MMD) or middle cerebral artery occlusion and healthy controls.

Table 2 Multivariate Binary Logistics Regression Analysis of MMD and MCA Occlusion Groups, MMD Group Was Used as a Reference

Parameters	Quartiles	P-value	OR	Odds Ratio (95% CI)
Age		0.022	1.129	1.018–1.252
Sex (male)		0.650	1.600	0.211–12.130
Smoke (yes)		0.078	0.092	0.006–1.313
Drunk (yes)		0.734	1.566	0.117–20.866
SBP		0.846	0.996	0.962–1.042
Blood glucose	3.83–4.37	0.151
	4.38–4.91	0.026	0.037	0.002–0.672
	4.92–5.46	0.460	0.371	0.027–5.141
	5.47–9.81	0.130	0.171	0.018–1.679
Apelin-13	42.02–130.106	0.021
	130.107–214.971	0.004	61.582	3.762–1007.960
	214.972–314.971	0.023	28.775	1.594–519.556
	314.972–694.64	0.785	1.504	0.080–28.141
Apelin-17	58.34–121.940	0.411
	121.941–172.320	0.479	2.542	0.192–33.558
	172.321–231.590	0.394	0.269	0.013–5.518
	231.591–426.51	0.582	0.465	0.030–7.107
Apelin-36	196.86–577.810	0.106
	577.811–805.640	0.619	2.383	0.078–72.877
	805.641–1135.710	0.405	4.269	0.140–130.222
	1135.711–2631.11	0.035	43.659	1.310–1454.824

Notes: The regression model was adjusted by age, sex, smoke, drunk, blood glucose, SBP. We divided continuous variables into four intervals according to the quartile method, the results showed that apelin-13 in MMD was higher in the MCA occlusion group, and the age of the MCA occlusion group was significantly higher than that of the MMD group.

Abbreviation: SBP, systolic blood pressure.

Figure 2 Receiver operating characteristic (ROC) curve analyses of apelin-13 (A) and age (B) as predictors of moyamoya disease (MMD) from middle cerebral artery occlusion.

Figure 3 Linear regression analysis of Apelin levels among different grades in the MMD group. As described above, all MMD patients were divided into three levels, and linear regression was performed on apelin-13, apelin-17, and apelin-36 levels. Through a pairwise comparison between the three groups, the results show that apelin-13, apelin-17, and apelin-36 levels increased as the grades rose without exception (***P<0.001, 95% CI of OR are shown inside brackets).

Figure 4 Three DSA images of the included patients with MMD. The compensation gradually improves from left to right (from Grade I to Grade III).