Asymmetrically hypointense veins on T2*w imaging and susceptibility-weighted imaging in ischemic stroke

Table 1 Publications using T2*w sequences

Ref.	n	Field strength	Occluded vessel	Time from onset	Validation method	Results
Hermier et al[7]	49	1.5 T	Anterior circulation	6 h	DWI; DSC-MRI	AVV obvious in 8/49, moderate in 15/49 patients, inter- and intra-observer reliability r > 0.9; Correlated with higher baseline NIHSS, larger DWI and PWI lesions, worse outcome, intracranial haemorrhage and more severe hemodynamic impairment
Liebeskind et al[8]	91	NS	MCA	NS	MRA; DWI	Hypointense vessels in or adjacent to the infarct in 40/91 patients
Liebeskind et al[9]	83	NS	MCA	Median 2 d	MRA	Unilateral hypointensity of the basal vein of Rosenthal was noted in 27/83 patients on the side of the occlusion
Hermier et al[10]	48	1.5 T	NS	6 h	DWI; DSC-MRI	AVLV present in 17/48 patients, within TTP lesion, not concordant with DWI lesion; No impact on clinical status and final stroke volume
Seo et al[11]	20	3 T	ICA, MCA	6 h	DSC-MRI; DWI	HVS present in 13/20 patients. Patients with asymmetrical HVS had better NIHSS improvement (8.1 ± 5.7 vs 2 ± 4.2)
Sohn et al[12]	86	NS	ICA, MCA	12 h	DSC-MRI; DWI	Present in 59/86 patients; HypoTCV associated with large perfusion defect, but low cholesterol and haemoglobin level may obscure its visibility
Ha et al[13]	22	3 T	MCA	6 h	DSA	Present in 7/22 patients. Patients with HLV showed larger baseline NIHSS (16.9 ± 3.4 vs 11.7 ± 5.3) and major improvement (≥ 8 points) was observed more often. It corresponded with delayed venous wash-out on DSA
Morita et al[14]	24	3 T	ICA, MCA	12 h	DWI; FAIR	CVS present in all patients, BS present in 23/24 patients, good interobserver agreement (κ = 0.7). Area defined by CVS/BS similar to hypoperfused area
Harada et al[15]	24	3 T	NS	12 h	FAIR; DWI	κ for cortical and deep vessel signs 0.84 and 0.72, respectively
Ha et al[16]	35	NS	MCA	6 h	DSC-MRI; DWI; DSA	HLV present in 12/35 patients. Patients with HLV had larger NIHSS improvement at 7 d (6.5 ± 4.6 d vs 0.5 ± 6.7 d) and bigger TTP-DWI mismatch. HLV corresponded with delayed venous wash-out
Kaya et al[17]	20	3 T	Large arteries	3 h	DWI; DSC-MRI	Present in all patients. Very good correlation of RMHV with final infarct (r = 0.91) and MTT/rCBV lesion (r = 0.96); very high interobserver correlation (ICC = 0.99)
Kinoshita et al[18]	NS (case series)	1.5 T	NS	NS	15O-PET	Enhanced venous contrast (hypointensity and enlargement of veins), ipsilateral corresponding increased OEF
Harada et al[19]	33	3 T	ICA, MCA	3 h	FAIR; DWI	IschV present in 79% (κ = 0.83); Not correlated with worse outcome
Tada et al[20]	2	3 T	MCA (stenosis)	NS	DWI; DSC-MRI; 123I-IMP SPECT	Area defined by ischemic signs was similar to area of hypoperfusion on MRI and SPECT
Rosso et al[21]	60	3 T	Anterior circulation	6 h	DWI; MRI	VTV present in 58.3% (κ = 0.895), correlated with larger infarcts and haemorrhage but not with baseline or follow-up NIHSS
Ryoo et al[22]	30	NS	ICA, MCA	6 h	Clinical	GRE vein present in 15/30 patients. Early neurological improvement (ΔNIHSS ≥ 8 or NIHSS ≤ 2 at 24 h) more frequently observed with GRE vein (8 patients vs 1 patients, P = 0.014)

NS: Not stated; ICA: Internal carotid artery; MCA: Middle cerebral artery; DWI: Diffusion-weighted image; DSC-MRI: Dynamic susceptibility-contrast magnetic resonance imaging; MRA: Magnetic resonance angiography; AVV: Abnormal visibility of transcerebral veins; PWI: Perfusion-weighted image; AVLV: Abnormal visualization of leptomeningeal vessels; TTP: Time to peak; CVS: Cerebral vasospasm; BS: Brush sign; HVS: Hyperintense vessel sign; HLV: Hypointense leptomeningeal vessels;

¹⁵O-PET: Oxygen-15 positron emission tomography; CT: Computed tomography; HypoTCV: Hypointense transcerebral or cortical veins; FAIR: Flow sensitive alternating inversion recovery;

¹²³I-IMP SPECT: Iodine-123 iodoamphetamine single-photon emission computed tomography; DSA: Digital subtraction angiography; NIHSS: National Institute of Health Stroke Score; RMHV: Region of multiple hypointense vessels; MTT: Mean transit time; rCBV: Relative cerebral blood volume; ICC: Intraclass correlation; OEF: Oxygen extraction fraction; VTV: Visibility of the transcerebral veins; GRE: Gradient-echo.

Table 2 Publications using susceptibility-weighted imaging and combining T2*w imaging and susceptibility-weighted imaging

Ref.	n	Field strength	Occluded vessel	Time from onset	Validation method	Results
Ida[23]	62	1.5 T	NS	24 h	DSC-MRI; DWI	IVC were noted in 77.4%, agreement with perfusion defect in all patients
Tong et al[24]	1	NS	MCA	3 d	ADC	Prominent asymmetric medullary veins exceeding the area of the DWI lesion
Mittal et al[25]	1	1.5 T	MCA	2 h	DWI; DSC-MRI	Prominently hypointense cortical veins exceeding the area of the DWI lesion, similar to PWI lesion
Santhosh et al[26]	1	1.5 T	MCA	NS	DWI	Prominent veins exceeding the area of the DWI lesion
Tsui et al[27]	1	NS	MCA	NS	DWI	Prominent hypointense veins exceeding the area of the DWI lesion
Christoforidis et al[28]	6	3 T	MCA	NS	DSC-MRI; DWI	MHV were noted within the MTT lesion while they absent within the DWI lesion
Hingwala et al[29]	1	NS	MCA	NS	DWI	Prominent veins exceeding the area of the DWI lesion
Huisman et al[30]	1	NS	MCA	NS	ADC/DWI	Prominent intramedullary veins exceeding the area of the DWI lesion
Mittal et al[31]	2	1.5 T	MCA	NS	ADC/DWI; DSC-MRI	Prominent hypointense veins exceeding the area of the DWI lesion, similar to PWI lesion
Yen et al[32]	1	NS	MCA	4 d	DWI; DSC-MRI	Prominent venous hypointensities exceeding the area of the DWI lesion, similar to PWI lesion
Kesavadas et al[33]	2	NS	MCA	NS	DSC-MRI; ADC/DWI	Prominent veins exceeding the area of the DWI lesion, similar to PWI lesion
Park et al[34]	82	NS	ICA, MCA	3 d	DSC-MRI; DWI	MHV visible in 73/82 patients, excellent agreement with TTP maps
Lin et al[35]	53	NS	ICA, MCA	12 h	Traditional MRI	Hypointense transmedullary veins predisposed to worse outcome (OR = 2.2)
Meoded et al[36]	2	NS	MCA, ACA	NS	Conventional MRI; DWI	Prominent intramedullary veins were noted within the DWI lesion. In one case prominent sulcal veins matched the area of infarct growth.
Gasparotti et al[37]	1	1.5 T	ICA	NS	DWI; DSC-MRI	SWI lesion exceeded DWI lesion and matched MTT lesion
Yamashita et al[38]	30	3 T	MCA	7 d	DWI; FAIR	Increased venous contrast in 22/30 patients, area similar to hypoperfused tissue
Huang et al[39]	44	3 T	MCA	2 d	DWI; MRA; CT	Prominent veins present in 15/44 patients; Not correlated with haemorrhage or outcome
Kao et al[40]	15	1.5 T	MCA	18 h	DWI; DSC-MRI	MTT-DWI and SWI-DWI mismatch similar to predict infarct growth
Tsai et al[41]	49	NS	NS	3.5-8.5 h	MRI; Clinical	Presence of hypointense veins in all patients with worse outcome and haemorrhagic complications
Meoded et al[42]	8	NS	NS	72 h	DWI	DWI > SWI mismatch found in 1/15 affected regions
Park et al[43]	9	NS	TIA	NS	DWI; DSC-MRI; MRA	4/9 patients with DWI negative TIA showed asymmetric hypointense vessels, in accordance with perfusion deficit and stenosed/occluded vessel
Fujioka et al[44]	1	NS	ICA	10 h	MRI	SWI lesion exceeding DWI lesion matured into infarction
Verschuuren et al[45]	1	NS	MCA, ACA	NS	ADC; CT	SWI lesion exceeding ADC lesion matured into infarction on CT
Meoded et al[46]	1	1.5 T	MCA, PCA	NS	T2; ADC	SWI lesion matches ADC lesion; Mismatch also noted, indicating critical perfusion
Baik et al[47]	19	1.5 Tand 3 T	ICA, MCA, BA	Median 2.5 h	DWI	Prominent veins present in affected territory which disappeared after recanalization (10/10 patients); After recanalization within DWI lesion: Equally prominent in 10/19 patients, small DWI lesions, good clinical outcome (7 d NIHSS median 3.5, 90 d mRS median 0) indicating normalisation; Less prominent in 5/19 patients, large DWI lesions, poor clinical outcome (7 d NIHSS median 13, 90 d mRS median 4) indicating futile reperfusion; Mixed in 4/19 patients, medium DWI lesions, relatively poor outcome (7d NIHSS median 13, 90 d mRS median 2)
Tsai[48]	59	NS	NS	NS	Imaging; Clinical	34 patients improved or stable (clinical, imaging), 25 worse; SWI correlated with poor prognosis
Sohn et al1 [49]	65	NS	Anterior circulation	12 h	Perfusion MRI	Asymmetrical HVS in 98% (SWI) and 74% (T2*w)

¹Publication combining T2*w imaging and susceptibility-weighted imaging. NS: Not stated; ICA: Internal carotid artery; MCA: Middle cerebral artery; ACA: Anterior cerebral artery; ADC: Apparent diffusion coefficient; BA: Basilar artery; FAIR: Flow sensitive alternating inversion recovery; MRA: Magnetic resonance angiography; CT: Computed tomography; PCA: Posterior cerebral artery; IVC: Increased vessel contrast; TIA: Transient ischemic attack; DWI: Diffusion-weighted image; PWI: Perfusion-weighted image; MTT: Mean transit time; DSC-MRI: Dynamic susceptibility-contrast magnetic resonance imaging; NIHSS: National Institute of Health Stroke Score; mRS: Modified ranking scal; SWI: Susceptibility-weighted imaging; HVS: Hypointense vessel sign; MHV: Multiple hypointense vessels.

Table 3 Comparison of publications using T2*w imaging and susceptibility-weighted imaging n (%)

	T2*w imagingpublications (patients)	SWIpublications (patients)
Number of publications	17 (692)1	27 (518)1
Presence of vessel signs	54%	81%
	16 (668)	21 (334)
Interrater agreement	κ = 0.7 to > 0.9 and ICC = 0.99	-
	6 (210)
Reliability assessment	r = 0.92-0.96	-
	1 (20)
Occluded vessel
Anterior circulation	12 (598)1	22 (331)1
Large arteries	1 (20)	-
Critical MCA stenosis	1 (2)	-
TIA	-	1 (9)
BA	-	1 (1)2
NS	3 (72)3	4 (178)
Time from onset
≤ 6 h	9 (317)	2 (18)4
> 6 h	5 (282)	12 (364)1
3.5-8.5 h	-	1 (49)
NS	3 (93)3	13 (87)
Outcome
Worse outcome	1 (49)	3 (161)
Better NIHSS improvement	4 (107)	-
Better outcome with normalisation	-	1 (19)
No correlation	3 (141)	1 (44)
Validation method
DSC-MRI	7 (260)	10 (181)
FAIR	3 (81)	1 (30)
Conventional MRI	3 (234)	11 (242)
15O-PET	1 (NS)	-
DSA	1 (22)	-
Field strength
1.5 T	3 (97)	7 (83)
3 T	8 (205)	3 (80)
NS	6 (390)13	17 (355)15

¹Including one publication using T2*w imaging and susceptibility-weighted imaging (SWI) (Sohn et al[49]), thus the total number of studies and patients differs from the one stated in the main text;

²Including one patient with occluded BA (Baik et al[47]);

³Number of subjects not stated (Kinoshita et al[18]);

⁴Including 17 patients ≤ 6 h and 2 patients > 6 h (Baik et al[47]);

⁵Including those who used 1.5 T and 3 T (Baik et al[47]). NS: Not stated; ICA: Internal carotid artery; MCA: Middle cerebral artery; BA: Basilar artery; TIA: Transient ischemic attack; DSC-MRI: dynamic susceptibility-contrast magnetic resonance imaging; FAIR: Flow sensitive alternating inversion recovery;

¹⁵O-PET: Oxygen-15 positron emission tomography; DSA: Digital subtraction angiography; NIHSS: National Institute of Health Stroke Score.